AN INTEGRATIVE APPROACH TO SOCIAL LEARNING AND BEHAVIORALTRADITIONS IN PRIMATES
A collection of 30 years of research work (1979 to 2009)

Michael A. Huffman
Section of Social Systems Evolution
Primate Research Institute, Kyoto University
Kanrin 41-2, Inuyama
Aichi Prefecture, Japan 484-8506
Email: huffman@pri.kyoto-u.ac.jp

Jean-Baptiste Leca
Section of Social Systems Evolution
Primate Research Institute, Kyoto University
Kanrin 41-2, Inuyama
Aichi Prefecture, Japan 484-8506
Email: jbtleca@yahoo.com

Charmalie A. D. Nahallage
Department of Sociology and Anthropology
University of Sri Jayewardenepura
Gangodawila, Nugegoda, Sri Lanka
Tp. 94112802207
Email: charmalie2@hotmail.com

C.A.D. Nahallage, J.-B. Leca, and M.A. Huffman (Ubud, Bali, Indonesia, August 2008)

About the authors

Michael A. Huffman earned an MSc (1985) and a D.Sc. (1989) from the Department of
Zoology, Kyoto University under the direction of Professors Junichiro Itani and Toshisaa
Nishida (who joined the laboratory ca. 1987). He started his primatological career in 1979 as
an undergraduate, with work on female mate choice and partner preference in Japanesemacaques (the topic of his graduate degrees). Huffman is now an associate professor at thePrimate Research Institute of Kyoto University. His research experience covers a wide rangeof species including chimpanzees in East Africa (Tanzania, Uganda) and in captivity (Japan,
Italy) as well as macaques in Japan, Bali, Sri Lanka and India. He has published on a wide
range of topics spanning from reproduction and sexual behavior, parasite ecology, social
learning and primate self-medication. Jean-Baptiste and Charmalie are his two key
collaborators in the current work on stone handling, joining his laboratory as a post doc andgraduate student, respectively.

Jean-Baptiste Leca earned a Ph.D. in Ethology (2002) from the University Louis Pasteur,
Strasbourg, France, and was a Post-Doctoral Fellow at the Primate Research Institute, Kyoto
University for 4 years between 2003-2004 and 2008-2009. His research explores the
biological, social, and ecological foundations of behavioral traditions in non-human primates.
More specifically, he is interested in the determinants of behavioral innovations as well as theconstraints on their diffusion and long-term maintenance within social groups. Among thevarious traditional behaviors reported in Japanese macaques, he mainly focuses on stone
handling behavior in multiple troops across Japan. From 2003, he has been taking an
integrative approach to studying stone handling through the combination of comparative,
longitudinal, and experimental methods. Recently, he also provided an update about themaintenance of the fish-eating behavior in the Japanese macaques living on Koshima Islet,
and reported the first case of dental flossing behavior by a Japanese macaque at Arashiyama.

Charmalie A.D. Nahallage, earned a Ph.D. in Primatology (2008) from the Primate
Research Institute, Kyoto University, Kyoto, Japan, and now is a senior faculty member at
the Department of Sociology and Anthropology, University of Sri Jayewardenepura, Sri
Lanka. Her initial research was to explore the effects of biological and environmental factors
for the maintenance of a behavioral tradition in a social group. Later by long term research
she was able to demonstrate the acquisition and development process of a behavioral tradition
by socially biased learning. Then she shifted to compare the interspecies difference in thesame traditional behavior using three macaque species performing it, namely Japanesemacaques, rhesus and long-tailed macaques. Currently she is analyzing the grip patterns ofobject manipulation in Japanese macaques.

About this document
The following compilation of scientific research articles is the result of the first 30 years offruitful collaborations from people of different nations, backgrounds, interests and cultures.
We believe that these collaborations have provided new insights into the understanding of theappearance, diffusion, and long-term maintenance of behavioral traditions in monkeys, aswell as some of the underlying social learning mechanisms involved in the evolution ofprimate culture.
In the quest for cultural versus alternative explanations of behavioral variation within andbetween groups of the same species, there has been a heated conceptual and methodologicaldebate among field and laboratory researchers. According to the environmental conditions ofstudy, the species attributes, and the behavioral domain under investigation, the questions
addressed and the methods used to answer them vary considerably. However, when
considered alone, each of them has its limitations and even flaws. An integrative approach
could then compensate for this shortcoming. By addressing the influence of environmental,socio-demographic, developmental, and phylogenetic constraints on the emergence,
diffusion, and maintenance of behavioral traditions in the genus Macaca, a major part of thepresent research aims at contributing to this ongoing debate.
Among the various behavioral innovations and traditions reported in Japanese macaques(Macaca fuscata), stone handling (SH) is a form of solitary object play consisting of the noninstrumental manipulation of stones by performing various behavioral patterns, such as
gathering stones into a pile, clacking stones together, or repeatedly pounding a stone on asubstrate. We used a standardized observation procedure to systematically compare thecontext of occurrence, frequency and form of SH in 10 troops of Japanese macaques. Morespecifically, we compared four captive troops housed at the Kyoto University Primate
Research Institute and Japan Monkey Centre, Inuyama, and six free-ranging provisioned
troops living at four geographically isolated field sites in Japan, namely Arashiyama (Kyoto
Prefecture), Koshima (Miyazaki Prefecture), Shodoshima (Kagawa Prefecture), andTakasakiyama (Oita Prefecture). Recently, we extended our comparison to five additional
field sites in Japan, namely Funakoshiyama (Hyogo Prefecture), Katsuyama (Okayama
Prefecture), Minoo (Osaka Prefecture), Miyajima (Hiroshima Prefecture), and Tsubaki(Wakayama Prefecture). We also extended our comparison of SH to two other macaquespecies, namely rhesus macaques, M. mulatta (one captive group housed at Kyoto University
Primate Research Institute) and long-tailed macaques, M. fascicularis (one free-ranging
provisioned troop in the Sacred Monkey Forest Sanctuary, Padangtegal, Ubud, Bali,
Indonesia). We collected longitudinal data on the appearance, early diffusion, and long-term
maintenance of SH within one free-ranging group of Japanese macaques and acrossgenerations at several points in time over a 30-year period. In the semi-controlled conditionsof an outdoor enclosure, we focused on mother-infants dyads, and evaluated the influence ofearly exposure to environmental and social stimuli in the acquisition of SH during the first six
months of life. We conducted field experiments to test the effect of SH artefacts (e.g., piles ofstones left on the ground by previous stone handlers) on the subsequent performance of SH.
The combination of the comparative, longitudinal, and experimental approaches to studying
SH behavior allowed 1) to establish the comprehensive repertoire of 45 SH patterns inJapanese macaques, 2) to reveal substantial variation in SH between troops, referred to as SH
cultures, 3) to show a geographic distribution of clear troop-dependent clusters of SH variants
suggestive of the notion of cultural zones, based on inter-troop observation and possiblymales transferring SH patterns when migrating from one troop to another, 4) to rule out
simple alternative explanations for such behavioral variability, such as genetic determinantsor some obvious environmental differences, 5) to indicate that group size and composition inage classes, as well as group spatial cohesion may impact the prevalence of SH, 6) to provide
evidence for the role of social factors in the acquisition of the behavior and the maintenanceof the tradition, which may involve not only direct social influences through the observation
by naïve infants of their mothers as SH demonstrators, but also indirect social inputs throughthe stimulating effect of SH artefacts, 7) to interpret some intra-group variability in theperformance of SH patterns from the viewpoint of developmental constraints, 8) to show thatin several troops, this behavioral tradition has reached its transformation phase, with anincrease in the SH repertoire and an expansion of the contexts in which SH is practiced, also
referred to as “ratchet effect” or “cumulative culture”, 9) to argue that food provisioning byhumans may be a key factor in the innovation and transformation phases of the SH tradition,and 10) to discuss the role of phylogenetic constraints and behavioral predispositions in theevolution of the SH culture in the genus Macaca.
In sum, our integrative approach to SH emphasizes both the product (via the comparative
method to assess which differences are observed in the form of behaviors) and themechanisms (via the longitudinal and experimental methods to determine which specificprocesses are involved in producing such differences) of the cultural phenomenon. SH isprobably the longest studied and best-documented cultural behavior in monkeys to date. The
methodology we used and the findings we obtained may have implications for various fields,
including anthropology, psychology, ecology, ethology, and evolutionary biology. We draw
an overall picture of rich cultural diversity in a particular type of object-play behavior in
macaques, and suggest that multiple factors should be jointly considered to identify thesources of behavioral variation in animals. Our comprehensive dataset provides valuable
empirical information to test predictions and fit models generated from theories about the roleof cultural processes in human evolution. Our findings will contribute to the understanding of
the biological foundations of non-human primate culture and the role behavioral traditions
might have played in the emergence of hominid material culture through stone-tool
technology (for stone-tool use in macaques, see also Malaivijitnond et al., 2007: Am. J.
Primatol. 69, 227-233 and Gumert et al., 2009: Am. J. Primatol. 71, 594-608).
In addition to this major focus on SH behavior, we also studied, in Japanese macaques, fisheating behavior on Koshima island, and dental flossing behavior at Arashiyama, as well as
leaf swallowing behavior in chimpanzees (Pan troglodytes). We addressed the determinantsof behavioral innovations and the constraints on their diffusion and maintenance within socialgroups of primates. Many new behaviors have been reported to appear in primate troops, butwere either idiosyncratic, or independently adopted by very few individuals, or theirperformance was restricted to a small class of the population, and for some reason, they neverwidely spread within the group by social means to become traditions. We used longitudinal,
cross-sectional, and experimental data to explore the history, describe the propagation, andassess the current prevalence of these behaviors at the group-level. We examined the factorsthat may have favored these innovations, including the environmental context, the individual
characteristics of the innovator, and the structural and functional aspects of the behavior.
Group size, kinship, and dominance are socio-demographic factors that are likely to limit theopportunities for any group member to observe the innovator, and thus constrain the diffusion
or maintenance of these potential candidates for behavioral traditions. We discussed the roleof the conformity process in the cultural transmission of behavioral variants. Identifying thedeterminants of innovations and the constraints on their diffusion within social groups of
non-human primates is of special interest to understanding cultural evolution in hominids.
The research articles compiled in this document were ordered chronologically by year of
publication, and then alphabetically by name of the first author. Related and complementary
information, including additional theoretical background, methodological materials, maps ofthe field sites, galleries of pictures, the pdf files of most articles, and the curriculum vitae of
the authors, can be found online at the following address:
http://www.primatecultures-stonehandling.pri.kyoto-u.ac.jp/
This work would not have been possible without the contribution of many people who helped
in many ways during the course of our research. We wish to thank the researchers, students,
staff, and friends who provided permission to work, support, assistance, and valuable specificinformation about the history, demography and environmental conditions of the troops at thedifferent study sites and general information from other field sites. We are grateful to thefollowing people in Japan: S. Asaba, J. Hashiguchi, T. Kawashima, S. Kobatake, and S.
Tamada (Iwatayama Monkey Park, Arashiyama), S. Hanamura (Kyoto University Laboratoryof Human Evolution Studies), F. Kanchi and T. Suzumura (Koshima Field Station), H. Kurita(Takasakiyama Natural Zoo), M. Matsubara, T. Matsuzawa, A. Mori, Rizaldi, H. Takemoto,and K. Watanabe (Kyoto University Primate Research Institute), M. Nakamura and Y.
Takenoshita (Japan Monkey Centre), and M. Shimada (Teikyo University of Science andTechnology). We also thank our Balinese colleagues from Udayana University’s Primate
Research Center, Denpasar, and more particularly A. Rompis, G. Soma, and N. Wandia. For
her major participation in different stages of the research, including logistic assistance,
contribution to data collection, entering, and analysis, as well as insightful comments during
manuscript writing, we sincerely thank N. Gunst (University of Georgia, USA). For fruitful
discussion and for providing us with longitudinal data on the Arashiyama-E troop, we thankP.L. Vasey (University of Lethbridge, Canada). For occasional assistance with data collection,
we thank K.J. Petrzelkova (Academy of Sciences of the Czech Republic), M. Sakakibara and
T. Harasaki (Gifu University, Japan), N. Tworoski (University of Minnesota, USA), and B.
Detta and R. Manullang (Udayana University, Bali, Indonesia). We thank A. Jacobs(University of Strasbourg, France) for designing the website. JB is indebted to the Enomoto
family for generously providing him with logistic assistance at Arashiyama during his study
periods.
The authors' work was funded by: a Grant-In-Aid for scientific research (No. 1907421 to
M.A. Huffman) sponsored by Ministry of Education, Science, Sports and Culture, Japan, by a
Lavoisier postdoctoral Grant, Ministère des Affaires Etrangères, France and a JSPS (Japan
Society for the Promotion of Science) postdoctoral fellowship to J.-B. Leca (No. 07421), a
scholarship from the Japanese Ministry of Education, Science and Culture for graduate
studies in Japan to C.A.D. Nahallage, and by travel funds from the HOPE Project, a core-tocore program sponsored by JSPS to these three researchers.
The printing of this document was made possible through research funds provided to M.A.
Huffman (Grant-In-Aid for scientific research, No. 1907421, sponsored by Ministry of
Education, Science, Sports and Culture, Japan). Any mistakes or omissions are solely our
responsibility.
Michael A. Huffman, Jean-Baptiste Leca, and Charmalie A.D. Nahallage, Inuyama, Japan,
December 7, 2009

Every study has a beginning, and this is ours
M. A. Huffman
After the first semester of my freshman year as an undergraduate at Ft. Lewis College,
Durango Colorado, I arrived in Japan in early February 1978 for what was supposed to be a
3-month study abroad program between my university and the Kansai University of Foreign
Language Studies (Kansai Gaidai), Hirakata, Osaka. I stayed on until August 1980. Througha fateful chain of events, starting with an introduction from the Dean of Student Affairs at
Kansai Gaidai, I met with Dr. Masao Kawai at the Primate Research Institute, Kyoto
University (KU) and his colleague in Kyoto, Dr. Junichiro Itani, in the Laboratory of Physical
Anthropology, Department of Zoology (KU). In my heart I was convinced after my meetingwith Itani sensei that Japan was where I was meant to be and that this was the place to study
primates. Itani sensei invited me to attend the lab’s seminar every Friday and introduced me
to Yukio Takahata, who was then just finishing his MSc research on the reproductive biology
and socio-sexual behavior of the Arashiyama Japanese macaques.
My observations of the Arashiyama B troop first began on August 2, 1979. Every Friday
after seminar, I went to Arashiyama, and slept up on the mountain several days a week for the
next 12 months. During my introduction to Japanese society and the society of Japanesemacaques, I was befriended by so many distinguished primatologists in Japan, and indeed
from around the world that came to visit Professor Itani in the laboratory of Human
Evolution. Their friendships lasting to this day and the tireless guidance offered along theway had an important impact on my life and my thinking. I reluctantly left Japan in Augustof 1980, stopping off in Kenya for a few weeks to observe baboons at Gilgil with Fred
Berkovitch and his wife Denise.

Mike Huffman (22 yrs.) at Arashiyam in the early summer of 1980
Back in the US and totally reverse culture shocked, I spent the next two and a half years inColorado finishing up my undergraduate degree, thinking of nothing but returning as quickly
as possible to resume my research at Arashiyama and to continue with my life in Japan. I
received word in the summer of 1983 that I was granted a Japanese Government scholarshipfor graduate studies at Kyoto University. I quit a part-time job at a Japanese restaurant,
Arigatou, in Durango, and prepared for the big adventure.

October 1983, Iwatayama Monkey Park, Arashiyama
On my first day back in Kyoto after reporting to Itani sensei, now my official graduate
advisor, I took the bus and local train from Kyoto University to the Hankyu Arashiayama
Railways station and rushed up to the provisioning grounds on top of Iwatayama. It had been
three long years back in the US, finishing up my undergraduate degree. I had long waited forthis day to come, working over-time back in Colorado to finish up my Bachelor of Science
degree at Ft. Lewis College, Durango.
I climbed up the mountain with great anticipation, eager to see how my friends, both humanand monkey, had been in my absence. I first greeted ‘Encho san’ (Nobuo Asaba, Director of
the Park) and caught up on the latest news on the mountain. He had been like a second
father, treating me like family, and providing every kind of support in my study of theJapanese monkeys. He allowed me to live up on Iwatayama in the small building he hadconstructed as an office and meeting place for the Arashiyama Natural History Society.
Every few weeks he would say “Mike san, your looking a bit thin, we need to go get you
something good to eat!” Working to support myself, I was on a tight budget. I becamefamous for discovering and eating good things that the monkeys ate in the forest as well as
the fresh fruits and vegetables that Encho san and his staff gave to the monkeys. During mystay in 1979, I would usually spend four consecutive days a week up on the mountain. Mostof the time waking up before the monkeys arrived at first light, going to bed late in the night
after having followed the monkeys to their sleeping sites, sometimes returning again later inthe evening to see what they did at night, and pouring over the literature Encho san had
accumulated on research work done at Arashiyama since 1954.
Now back again on the mountain in 1983, nothing much had changed during my absence.
The adult monkeys I had spent many hours with in 1979 had gotten a little older, some had
died or migrated out of the troop, but of course there were many new young faces that I had
to learn before starting up observations again.
It was time for the 12:00 feeding. Encho san and I were talking in his office about futureplans for my research, what the monkeys had been up to etc… Suddenly a curious loudbanging sound coming from the metal roof above us caught my attention. Curious, I rushed
outside to see what was going on. Many young monkeys were up on the roof with handfulsof stones, rubbing them across the metal surface, gathering them together and scattering them
about again. I had never observed the monkeys up on the roof with stones like this at
Arashiyama before, and so I asked Encho san when this had started. He said that he wasaware of this behavior for at least the two years (started to be noticeable sometime in 1981).
He added that it had became particularly more noticeable after he dumped a large pile ofstones on the side of the provisioning grounds, that had been left over from some trail repairs
he had made.
After thinking about all this for a bit, I suddenly remembered a curious observation I had
made during my first stay, of a young female playing with stones at the feeding site one day
in December of 1979. Excited about the prospects of having possibly witnessed the start of a
new cultural behavior for Japanese macaques I returned to the lab that afternoon and told
Itani sensei what I had seen and heard at Arashiyama. He was very interested andencouraged me to look into it in more detail. A few days latter, after I had un-packed all mybooks and field notes, I found the field diary, in which I recorded in more detail that day’s
events from my field notes. I then went through my photo and slide files and found a pictureof the young female in action!

Field Diary entry: December 7 1979, Iwatayama Monkey Park, Arashiyama Kyoto
A few minutes after the 12:00 feeding time: My attention is drawn to a young individual out
in the center of the feeding site, a few minutes after the group is provisioned with wheat andsoy beans. The 3-year old female, Glance 6476 is stacking and rearranging blocks of stones.
I am struck by this human infant-like behavior. I quickly take a few photos then continue towatch her.

Glance 6476 (Arashiyama, December 7, 1979)
She scatters the block like stones around with open hands, and scoops them together into apile. I find it interesting that these stones could not have been collected from the immediatearea because the feeding grounds were routinely swept clean of all debris (feces, liter etc.)
after each feeding time for the tourist traffic. The rocks were deliberately gathered andbrought to the center of the feeding site by this female from the forest at the edge of theprovisioning ground. At one point when she was disturbed by other monkeys she picked up
as many stones as possible, holding them against her chest with her arms and some clutchedin both hands, she then moved off to a location about 5 meters away.
I picked up the remaining stones and brought them to her to see what she would do. She
quickly took them, mixed them in with the other stones, and continued to play.
Two weeks after this first observation of stone handling in 1979, I traveled down to Kyushu
on December 22 to spend New Years in Kagoshima Prefecture at the home of a friend (myfuture wife). Along the way, we stopped at the Takasakiyama Monkey Park, in Beppu (Oita
Prefecture, northern Kyushu), famous as one of the earliest study sites of Japanese macaques
by Junichiro Itani and colleagues. We stayed there for two days. Talking with park
employees I learned that they too had seen monkeys handling stones for the first time in1979. I was intrigued as to how this could happen. After I returned to Arashiyama on
January 5 1980, I kept my eyes peeled for more incidences of this behavior. However, during
the course of my entire study of the troop between August 1979 and August 1980 I saw stone
handling only this one time.
Back to the future: Fall 1983 onward. My main topic of research at Arashiyama for mymasters and doctorate was a study of female mate choice and partner preference in theJapanese macaques. This was a continuation of one of my study topics in 1979. My main
focus of observations was mating activity of the troop, and this meant that my observations ofstone handling couldn’t start in earnest until the early spring of 1984, after the end of themating season.
In December of 1984, Duane Quiatt, a professor from the University of Colorado’s DenverCampus came to visit me in Japan. We had met in Colorado when I was an undergraduate
and he was quite interested in observing the behavior of Japanese macaques since he had also
observed rhesus monkeys on Cayo Santiago of the cost of Puerto Rico. We spent several
weeks together observing the monkeys at Arashiyama. We also traveled to observe stone
handling at Takasakiyama with Itani sensei, and then traveled on to Yakushima to see thesub-species Macaca fuscata yakui. Duane was the first to join me in the study of stone
handling and together we began to conceptualize some of the implications for the long-term
study of this behavior.
At the time, little did I know what and were this was going to lead to. These opportune
events and guidance from senior colleagues at the beginning of my career set the stage for avery productive study that had led us on a study that has lasted now for more than 30 years.
Most of the early work I did alone, but it is clear to me that the real advances began after
collaboration with others. The first census of 1990 at Arashiyama was possible with the helpof Ms. Connie Cagampang, an under-graduate from Berkley who came for the summer toassist in data collection and data entry. She volunteered her time in exchange for theopportunity to see if primatology was what she wanted to pursue for her graduate studies.
She was a great help, and a source of motivation to systematically observe every individual in
the troop. She went on to study law. She will certainly make more money!
Many advances in our understanding of this behavior and its implications for the study ofsocial learning and culture in animals have been made in the last few years, thanks to thebeautiful collaborations with my two junior colleagues and co-compilers of this document JB
and Charmalie. It is through the tireless efforts that we own our understanding of the detailsof transmission, social learning and cultural variation between sites of stone handlingbehavior.

Junichiro Itani and Mike Huffman, co-chairing a satellite symposium on Culture
as part of the 1990 IPS Congress in Kyoto, JapanTABLE OF CONTENTS

Huffman MA. 1984. Stone-play of Macaca fuscata in Arashiyama B troop: Transmission of a
non-adaptive behavior. Journal of Human Evolution, 13 (8): 725-735.
……..........1
Huffman MA, Quiatt D. 1986. Stone handling by Japanese macaques (Macaca fuscata):
Implications for tool use of stones. Primates, 27 (4): 413-423.
……........12
Quiatt D, Huffman MA. 1993. On home bases, nesting sites, activity centers, and new
analytic perspectives. Current Anthropology, 34 (1): 68-70.
……........23
Huffman MA. 1996. Acquisition of innovative cultural behaviors in non-human primates: A
case study of stone handling, a socially transmitted behavior in Japanese macaques. In:
Galef B Jr, Heyes C, editors. Social Learning in Animals: The Roots of Culture. Orlando:
Academic Press. p 267-289.
……........27
Huffman MA, Hirata S. 2003. Biological and ecological foundations of primate behavioral
tradition. In: Fragaszy DM, Perry S, editors. The biology of tradition: Models andevidence. Cambridge: Cambridge University Press. p 267-296.
……........50
Huffman MA, Hirata S. 2004. An experimental study of leaf swallowing in captive
chimpanzees: insights into the origin of a self-medicative behavior and the role of social
learning. Primates, 45 (2): 113-118. DOI 10.1007/s10329-003-0065-5.
……........80
Leca JB, Gunst N, Watanabe K, Huffman MA. 2007. A new case of fish-eating in Japanesemacaques: Implications for social constraints on the diffusion of feeding innovation.
American Journal of Primatology, 69 (7): 821-828. DOI: 10.1002/ajp.20401.
……........86
Leca JB, Gunst N, Huffman MA. 2007. Japanese macaque cultures: Inter- and intra-troop
behavioural variability of stone handling patterns across 10 troops. Behaviour, 144 (3):251-281. DOI: 10.1163/156853907780425712.
……........94
Leca JB, Gunst N, Huffman MA. 2007. Age-related differences in the performance, diffusion,and maintenance of stone handling, a behavioral tradition in Japanese macaques. Journalof Human Evolution 53 (6): 691-708. DOI:10.1016/j.jhevol.2007.05.009.
……......125
Nahallage CAD, Huffman MA. 2007. Age-specific functions of stone handling, a solitaryobject play behavior, in Japanese macaques (Macaca fuscata). American Journal ofPrimatology, 69 (3): 267-281. DOI: 10.1002/ajp.20348.
……......143

Nahallage CAD, Huffman MA. 2007. Acquisition and development of stone handlingbehavior in infant Japanese macaques. Behaviour, 144 (10): 1193-1215. DOI:
10.1163/156853907781890959.
……......158
Huffman MA, Nahallage CAD, Leca JB. 2008. Cultured monkeys, social learning cast in
stones. Current Directions in Psychological Science, 17 (6): 410-414.
……......181
Leca JB, Gunst N, Huffman MA. 2008. Of stones and monkeys: Testing ecologicalconstraints on stone handling, a behavioral tradition in Japanese macaques. American
Journal of Physical Anthropology, 135 (2): 233-244. DOI: 10.1002/ajpa.20726.
……......186
Leca JB, Gunst N, Huffman MA. 2008. Food provisioning and stone handling tradition in
Japanese macaques: a comparative study of ten troops. American Journal of Primatology,
70 (8): 803-813. DOI: 10.1002/ajp.20551.
……......198
Leca JB, Nahallage CAD, Gunst N, Huffman MA. 2008. Stone-throwing by Japanesemacaques: form and functional aspects of a group-specific behavioral tradition. Journal of
Human Evolution, 55 (6): 989-998. DOI: 10.1016/j.jhevol.2008.06.004.
……......209
Nahallage CAD, Huffman MA. 2008. Environmental and social factors associated with theoccurrence of stone-handling behavior in a captive troop of Macaca fuscata. International
Journal of Primatology, 29 (3): 795-806. DOI: 10.1007/s10764-008-9268-3.
……......219
Nahallage CAD, Huffman MA. 2008. Comparison of stone handling behavior in two
macaque species: Implications for the role of phylogeny and environment in primate
cultural variation. American Journal of Primatology, 70 (12): 1124-1132. DOI:
10.1002/ajp.20610.
……......231
Huffman MA, Leca JB, Nahallage CAD. In press. Cultured Japanese macaques – A multidisciplinary approach to stone handling behavior and its implications for the evolution of
behavioral traditions in non-human primates. In: N. Nakagawa, M. Nakamichi & H.
Sugiura (eds). The Japanese macaques. Springer, Tokyo.
……......240
Leca JB, Gunst N, Huffman MA. In press. The first case of dental flossing by a Japanesemacaque (Macaca fuscata): implications for the determinants of behavioral innovationand the constraints on social transmission. Primates. DOI: 10.1007/s10329-009-0159-9(Accepted in June 2009).
……......257

Leca JB, Gunst N, Huffman MA. In press. Indirect social influence in the maintenance of thestone handling tradition in Japanese macaques (Macaca fuscata). Animal Behaviour.
DOI: 10.1016/j.anbehav.2009.09.035 (Accepted in September 2009).
……......267
Leca JB, Gunst N, Huffman MA. In press. Principles and levels of laterality in unimanual andbimanual stone handling patterns by Japanese macaques. Journal of Human Evolution.
DOI: 10.1016/j.jhevol.2009.09.005 (Accepted in September 2009).
……......277
Manuscripts in review (not reported in this document)
Leca JB, Gunst N, Huffman MA. In review. Complexity in object manipulation by Japanesemacaques: a cross-sectional analysis of manual coordination in stone handling patterns.
Journal of Comparative Psychology.
Huffman MA, Spiezio C, Sgaravatti A, Leca JB. In review. Spontaneous emergence andcultural conformity of two variants of leaf swallowing behaviour in two groups of captive
chimpanzees (Pan troglodytes). Animal Cognition.

Michael A. Huffman
Laboratory of Human Evolution
Studies, Kyoto University, Faculty of
Science, Kita Shirogawa,Oiwake-cho, Sakyo-ku, Kyoto,
Japan 606"
Received 22July 1984 andaccepted 24 August 1984

Keywords: MacacaJi*scala,stone-play, non-adaptive
behavior, tradition, hominid
evolution.

Stone-Play of Macaca fuscata in Arashiyama
B Troop: Transmission of a Non-adaptive
Behavior
Stone-play, a directly non-adaptive behavior, was observed in thefree-ranging Arashiyama B troop ofJapanese macaques near Kyoto,Japan.
Stone-play was classified into eight types characterized by gathering,picking up, scattering about, rolling in hands, rubbing in hands, clacking,carrying, or cuddling, of stones. The behavior, first observed in 1979,
spread throughout 49% (n = 236) of the troop by 1984. Infants andjuveniles of both sexes accounted for 80% (n = 92), while the remaining
20% were young adult males (6) and females (6) or adult females (11).
Unlike other reported cases of novel cultural behaviors, this non-adaptive
behavior initially diffused among younger individuals and was then latertransmitted in form of tradition from these individuals to their offspring or
younger sibs and playmates.

1. I n t r o d u c t i o n
The acquisition and transmission of new behaviors in Japanese macaques (Macacafuscala)have been well documented (Itani & Nishimura, 1973). These behaviors all share incommon a relation to feeding and are thus positively reinforced by tile direct benefits
acquired through its practice. The acquisition of stone-play, which involves the collecting,scattering, or carrying of stones, cannot be explained in these terms. Stone-play is not themeans to an end in which apparent benefits are acquired. This article describes stone-play
behavior and its transmission in the Japanese macaques of Arashiyama. The significanceof this phenomenon in Japanese macaques and its implications for the study of hominid
cultural evolution are discussed.
2. M e t h o d a n d Materials
Japanese macaques have been provisioned and studied since 1954 at the I w a t a y a m aNatural Park, Arashiyama, J a p a n . (Baldwin el at., 1980; Koyama, 1967; Takahata, 1982).
The following observations were made during two periods (July 1979-September 1980 andNovember 1983-June 1984) on the Arashiyama B troop (Figure 1). Ad libitum observations
were recorded with pen and note pad, occasionally supplemented with VHS video
recording.
3. O b s e r v a t i o n s

Description of Behavior
The sizes of a sample of 43 stones used in play, ranged from 11 m m • 11 mm • 1I m mweighing about 2 g to 110 m m • 110 m m x 70 mm~ weighing 730 g. The mean measure of
the three dimensions (arbitrarily determined) gives the size of an ordinary stone used inplay as: 44 m m X 31 m m • 20 mm.
Stone-play was most predictably observed on clear, warm days and less frequently on
rainy days. The number of players appeared to be fewer on overcast days. Stone-play could
be most predictably observed after the provisioning of wheat and corn, a time when most
Journal of Human Evolution (1984) 13, 725-735
0047-2484/84/080725 + 11 $03.00/0

9 1984 Academic Press Inc. (London) Limited

1

726

M. A. HUFFMAN

Figm'e 1. M a p of J a p a n and location of primate study sites.

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km

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Arashiyarni@_
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individuals are engaged in resting, grooming, or social play. Individuals seen stone-playing
after feeding always had their cheeks filled with grain and showed no signs of distress or any
emotional expression. Likewise, individuals stone-playing at other times of the day
appeared calm while in the play activity. Individuals stone-played at or away from thefeeding station.
Stone-play was classified into eight basic types.

Gathering: several stones (2-20) are collected, gathered into a pile or separate piles.
These separate piles are formed when the individual picks up several stones, puts themdown and collects new stones (see below). Similar collecting and carrying of sticks or
peanut shells at the same time is also observed a m o n g certain individuals.
Pick up: one to several (5-7) stones are picked up and held in one hand. T h e stones are
dropped and the procedure is repeated; the same stones are picked up, new stones are
picked up from the same area, or new stones are picked up elsewhere.

Scatter about: stones which have been collected and placed in ti'ont of oneself are scatteredabout on the ground with open palm(s) in a circular or side-to-side sweeping motion[Figure 2(a)].
Roll in hands: one or two stones are picked up, and with an opposing directionalm o v e m e n t of the forearms, rolled about rapidly between the hands.

Rubbing stones: two stones are collected, holding one in each hand, and rapidly rubbed
against each other. Sometimes a smaller stone is held with one or both hands and rubbed
on a larger stationary stone or similar flat object in a torward and backward motion.

2

3

Figure 2. (a) I n d i v i d u a l s c a t t e r i n g several stones about. (b) I n d i v i d u a l
cuddling several stones in both hands.

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728

M.A. HUFFMAN

Clacking: two stones are collected, h o l d i n g one in each hand, a n d r a p i d l y struck together
p r o d u c i n g a clacking noise.
Carrying: stones (1-3) are picked u p and carried. T h e stones are not m a n i p u l a t e d in any
p a r t i c u l a r fashion, b u t instead are held close to the body with a h a n d or foot.
Cuddling: usually one large stone, b u t sometimes several smaller stones are picked up andheld closely to the b o d y [Figure 2(b)]. T h e stone is carried a r o u n d frequently when an
i n d i v i d u a l changes resting positions, b u t usually the i n d i v i d u a l j u s t sits in one placeholding the stone. In such situations the i n d i v i d u a l is sometimes seen in social
interaction with others, i.e., grooming, huddling, etc. Cuddling usually follows m o r e
active types o f s t o n e - p l a y behavior.
S t o n e - p l a y lasts from 30 seconds to over 20 minutes at a time with frequent periods ofrest or change in p l a y type. T h e s e b e h a v i o r a l types are p e r f o r m e d i n d i v i d u a l l y orsequentially. T h e o b s e r v e d relative frequencies of the above behaviors are given in T a b l e 1.
T h e d a t a is taken from 17 d a y s of observation. T h e following excerpt fi'om tield notes
exemplifies the sequential p e r f o r m a n c e of stone-play behaviors in an eight-year-old,
B1-596475.
April 3, 1984. 10:42, B1-596475 is in brush below teeding grounds. Pick up, rubbing stones,
gathering. 10 : 46'33"-: 51 '26", she changes positions, pick up, rubbing stones. 10 : 51 '26"- : 52'12",
stops and grooms own leg. 10 : 5 2 ' 2 8 " : 58'28". Carrying,pick up, carrying, rubbing stones. She stops
several times and looks toward me. I act as if my attention were focused elsewhere and she
resumes stone-play. 10:58'43"-:59'31", B1-596475 moves across the slope carrying several
stones with her. She sets the stones down in front of her and begins to feed offa'small clump ofgrass. 10 : 59'31"- 11:00'32", she moves in between small brush isolated t?om other monkeys
and the observer. Gathering, pick up, 11: 00'32"-:00'47", B1-596475 moves out into open andfeeds on grass. 11:00'47"-:02'30", pick up, scatter about, rubbing stones, gathering.
11 : 02'30"-: 05' 18", feeding on grass frequently pausing to groom herself. 11 : 05' 18"-: 05'40",
Pick up, gathering. 11 : 05'40"-: 06'24", B1-596475 feeds on grass then moves out in open area andsits with others. Her three year old male offspring B 1-59647580 approaches and both walk off'.
W h e n engaged in stone-play, others' attention was often d r a w n a n d one's stones wereoccasionally stolen. W h e n a p p r o a c h e d , an i n d i v i d u a l would pick up as m a n y stones as hecould c a r r y a n d run o f f b i p e d a l l y or t r i p e d a l l y , to resume play elsewhere. Stones left behind
were often picked up by the i n d i v i d u a l who a p p r o a c h e d , or by other individuals n e a r b y
who in t u r n would begin to play with the stones. In o t h e r instances, s t o n e - p l a y i n g
Table 1

Observed frequencies of stone-play behavior at Arashiyama

Behavior

Frequency (n = 391)

Gathering
Pick-up
Scatter about
Roll in hands
Rubbing stones
Clacking
Carrying
Cuddling
Data collected during 17 days from 169 instances.

4

42
91
83
39
34
7
78
17

TRANSMISSION OF N O N - A D A P T I V E

729

BEHAVIOR

individuals would be displaced and the intruder would begin to play with the stones,
Occasionally an infant or juvenile would be approached by several playmates initiatingchase or a wrestling bout. In some instances such individual would evade his playmatesand resume stone-play. In other instances the individual ceases stone-play and joins in playwith others.
In general, stone-play is a solitary activity with individuals spaced at least 1-3 m apart,but occasionally two to four individuals (mother-infant, siblings, playmates) would sit side
by side while playing. Stone-play was also seen in social interactions where the playing
individual was being groomed, would intermittently groom, or sit next to someone else
briefly. Individuals would also forage off the surrounding vegetation.

Diffusion
Until 7 December 1979, stone-play was never seen at Arashiyama. The first individual
discovered to display this behavior was G1-6476, then three years old. She was seen
scat!ering about, picking up and carrying stones in the open space of the feeding area. By
November 1983, stone-play occurred frequently (Table 1).
It is difficult to determine exactly to what extent stone-play behavior has spreadthroughout the troop, since it is impossible to test each individual for the acquisition of this
spontaneous behavior. However, a general picture can be drawn fi-om observations. Figure
3 shows the extent of observed diffusion. A total of 115 (49%) individuals were seen to
exhibit stone-play behavior. O f these individuals, 92 (80%) were born between 1980 and
1983, after this play was first innovated. The remaining 20% was composed of six young
adult males (4"5-8-5 yr), six young adult females (3"5-4"5 yr) and 11 adult females (5+ yr).
Frequently observed individuals not seen to exhibit stone-play behavior represented
24% (n = 57) of the troop. These individuals were all seven years or older. The remaining
Figure 3. Histogram of Arashiyama
B troop. Blackareas represent number of individuals seen to exhibit
stone-play behavior.

d
g

50

20
Male
n = 105

5

I0

I0

20
Female
n=lSI

50

730

M.A. HUFFMAN

unaccounted for individuals (62) all under 10 years of age, have not directly been observed
to play with stones or are peripheral individuals seldom seen with the troop.
The first individual seen to exhibit stone-play, G1-6476, was the only individual of her
age in the troop seen to exhibit this behavior during the second observation period. Threeolder females, G 1-6775 and G 1-6774 of the same Glance lineage group, and B t-596475,
were the only members of the troop older than G1-6476 seen to exhibit this behavior. In theacquisition of stone-play, like that of potato-washing or wheat-washing, observed on
Koshima islet (Kawai, 1965), both age and positive nature of the individual appear to berelated factors. These three females probably acquired this behavior as early as 1979,
suggesting that older individuals do not acquire this behavior.
Although it is unknown which one of the four females originated this stone-play
behavior, it is likely that she was a m e m b e r of the Glance (G1) lineage group. Figure 4
shows the Glance lineage members seen to exhibit stone-play.

Figure 4. Glance lineage group.
I~, ~: individuals seen to exhibit
stone-play behavior.

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No individuals over 10 years old were seen to exhibit stone-play behavior. In 28 out of 39
mother-offspring units (in which the mother was older than 10 years and the offspring wereyounger than six years), one or more offspring stone-played. This suggests that stone-play
was transmitted at least partially between sibs. There were six mothers, 10 years or
younger, seen to exhibit stone-play; G1-6774, G1-6775, B1-596475 (mentioned above),
Op-7078 and Mo-5978. In all of these cases, all of their offspring born before 1984 wereseen to exhibit stone-play. During the 1984 birth season, infants were born to B1-596475,
G1-6474, and for the first time Op-626878. These females were all seen to stone-playwithin two to five days after giving birth. On 1 July, 12:59 B1-596475 was seenstone-playing white her infant sat to the side. The infant approached and sat down in frontof her. As B 1-596475 began grooming the infant, it started to grasp, rub, and try to lift astone its mother had previously been using. The above observations suggest that the
behavior was also transmitted from mother to offspring. Non-sib playmates were seenstone-playing together, suggesting that transmission may also occur through thesechannels.

6

TRANSMISSION OF N O N - A D A P T I V E B E H A V I O R

731

4. D i s c u s s i o n

The above observations, as in the studies on the transmission of sweet-potato-washing,wheat-washing, and other cultural behaviors (Kawai, 1965; Itani & Nishimura, 1973),
show that play in innovative, young, and frequently female individuals can be responsible
for the initiation of new cultural behaviors into the troop. Frisch (1977) points out that play
is a very important element in the occurrence of inventive behavior. He states thatinventions are not the product of necessity, rewarded by food, mating, or status, but are
rather the byproduct of play.
The manipulation of stones appears to be a relatively unreported phenomenon in
macaques. A few brief descriptions of stone manipulation have been reported for enclosed
groups of Japanese macaques, including methodical manipulation, tossing, and carrying
among infants and juveniles, throwing as a form of display in young adult males, and use asa grooming tool on her infant by one adult female (Eaton, 1972; Candland, 1978, 1981).
Similar behaviors can arise independently among spacially separated groups of the same
species because they share a common capacity to perform the behaviors (see Figure 1). In
J a n u a r y of 1979 and 1984, stone-play was observed at Takasakiyama and is believed tohave started almost at the same time as at Arashiyama (Huff'man, unpublished data).
Stone-gathering was observed also at T a k a g o y a m a (troop 1) in 1974 while the troop wasstill being provisioned (Hiraiwa, 1975). The stone-play described by Hiraiwa is equivalent
to five behavioral types; gathering, cuddling, pick up, rubbing stones, and roll in hand, reported
here. Hiraiwa reports that, at that time stone-gathering was observed at a frequency of 15
times in nine out of 31 days. Compared with Arashiyama, the frequency of occurrence waslow (Table 1). At Takagoyama, stone-play was seen in individuals up to three years of age.
No adults were seen to stone-play at that time. At present stone-play is infrequently seen ina few individuals at T a k a g o y a m a after provisioning has been abandoned (T. Fujita, pets.
comm.). Aside from stone-play, other peculiar behaviors like this can be found in several
different troops. The following are examples. Snowball construction by enclosed J a p a n e s emonkeys captured near Hiroshima and now in Oregon was reported by Eaton (1972). This
novel behavior can also be observed among the free-ranging Japanese monkeys of
Shiga-kogen (Figure 1), J a p a n (N. Okayasu, pets. comm.). Sweet-potato-washing
behavior at Koshima reported by Kawai (1965) has been observed among a few individualmonkeys at Takasakiyama and Arashiyama (Huffman, unpublished data).
Although the relationship between feeding and stone-play is not yet fully understood, theindividuals involved clearly distinguish food objects from play objects. Except a few
infants, stones were never seen to be put either in the mouth or up to the nose like
provisioned or unfamiliar food objects.
Because of an overpopulation problem in provisioned troops, the volume of daily rations
was decreased gradually over a few years in several areas including Takasakiyama,
Takagoyama, and Arashiyama. The initial effect this may have had on the behavior ofindividuals in these troops is unknown. However, with the exception of T a k a g o y a m a atwhich provisioning has been abandoned all together, the amount of daily rations has notbeen further decreased in the last four to five years at Takasakiyama and at least six years
at Arashiyama. At Arashiyama rations are widely distributed throughout the feeding area
insuring that the lower ranking individuals have equal access. The most representative ageclass of stone-players, one to four years of age, have not experienced any change inprovisioned rations.

7

732

M.A. HUFFMAN

Behavior similar to stone-play has been observed at Arashiyama before provisioning wasstarted in 1955. Betbre provisioning of the troop at the present location, the monkeys
inhabited an area further west along the Katsura river. According to Eiji Oota, a naturalist
and educator in the area, there were several citris trees of the species Poncirus trifoliata in thetroop's old range. The round fruit, about 4 cm in diameter is hard and was rarely eaten by
the monkeys (Murata & Hazama, 1968). Oota (pers. comm.), who has watched the troop
since 1948, saw the monkeys collecting, carrying, and scattering about the fallen fruits, butrarely did they attempt to eat it. After provisioning at Arashiyama similar behavior with
provisioned food has not been reported.
The behavior described in this article is considered to be a form of object-play in
Candland's (1978) terminology. Stone-play is a motor activity rather than a sensory
activity and the behavior occurs under low arousal conditions. Solitary or object-play inadults of other free-ranging macaques have not been reported. As for the documentation of
adult play in free-ranging macaques there is little (Brueggeman, 1978; Caine & Mitchell,1979). At Arashiyama however, in adults both solitary and social play were observed in theform of stone-play. In general adult stone-play at Arashiyama consists of more complex
movement and manipulation of stones (e.g., clacking and rubbing stones), than younger
individuals, and occasionally included the collecting and rubbing of sticks. This greater
complexity can possibly be attributed to two factors: (1) experience and (2) greater
neuro-motor development.
Menzel (1976) earlier reported that free-ranging Japanese macaques at Takasakiyama,
Katsuyama, and Minoo, J a p a n , showed indifference to objects in their environment otherthan food (Figure 1). He stated that object manipulation lasted no more than 30 seconds,
but that an object possessed by another individual becomes of more interest. At
Arashiyama, individual stone-play lasted for several minutes at a time. Unlike food, thcsestones have no survival value, yet they are a sought-after commodity; especially whenanother monkey is playing with them. A positive reinforcement tbr the continuation of suchplay might be considered to be its popularity value. An object or play with that object isvalued because it is desired by others. A similar phenomenon reported by Susan Isaacs inhuman children is discussed by Levi-Strauss (1969, pp. 85-86) in the context of theframework of social life with which universal institutions can be connected. The study ofsuch behaviors in non-human primates may also provide data for application in similar
studies.
There are m a n y similarities between the nature of the transmission of stone-play andother cultural behaviors studied previously. However, there appears to be a fundamental
difference in the direction of initial transmission. This is probably influenced by the natureof these behaviors. T h a t is, one is play related and the others are feeding related. Thus thesocial networks involved are different. These differences in transmission are schematized in
Figure 5.
As described by Kawai (1965), the initial direction of transmission of sweetpotato-washing, wheat-washing, and other cultural behaviors was from the young to theolder; predominantly infant-mother and secondly among sibs. Listed above as transmission phase (a), Kawai calls this the "period of individual propagation". Once theyounger individuals become older, the behavior is transmitted in the reverse direction.
Kawai says it is always transmitted from the mother to child, and refers to this phase as the"period of pre-cultural propagation".

8

TRANSMISSIO N OF N O N - A D A P T I V E B E H A V I O R

733

F{gure -5. Ghanqels of the tLansmission Qf (a) previ0us]y ~tudied ct~!tt!ral
behavior-s gnfl (b) smneq?lay.
Transmission phase

Transm ss an phase@,
Traditign phase

Traditioq phqse

(a)

(b!

Itani (1959) uses the term ~'tradition" as opposed to pr,0pagation, fbr the mother toinfant or older to younger channel of cultural behavior acquisition. Here this is called the
tradition phase. As was found in this study, behavior can be acquired by a young
individual regardless of whether or not its mother exhibits the behavior. The transmission
phase (b) of Figt~re ,5 represents thc channels in which stone-play is considered to havefollowed. Looking at Figure 3 it can be s,ee,n thai no individuals over 10 years of age
acquired the behavior. Initially, the behavior was transmitted between young females ofthe same Glance lineage and then to same age playmates of other lineages. The rate ofdiffusion increased greatly when younger sibs or other younger playmates and then finally
one's own offspring began to acquire the behavior.
In a test designed to analyze the process of novel behavior acquisinon, Itani 19581
discovered that the rate of acquisition of caramel-eating behavior was highest amongindividuals between one and three years of age. Similar results were obtained in the present
study. !tani found that by six months of age 70% of the infants had acquired the behavior.
In another study, Itani . Itani & Nishimura 1973 found that almost all the naturally
occurring foods eaten by the T a k a s a k i y a m a troop were acquired by infants in their firstyear.
The research on culture in non,human primates which began with the J a p a n e s emacaque, has ana, lyzed the transmission of behaviors relative to subsistence; m a n yconcerning the acquisition of new fbods (Kaw0~m~tura,, 1959, 1965; Itani, 1958), methods offeeding (Kawamura, 1954; Kawai, ]965), or the manufacture of tQols for use in foraging(Goodall, 1963; Nishida, !973; .S,,ugiyama, 1979). It has been gen,erMly thotlght th~tt these
new behaviors were acquired and transmitted because they were of direct benefit to theindividual. However, Imanishi (1952), who first suggested thc presence of ,culture in
n0n-human primates, did not limi~ cultural transmission to %daptive" behaviors on!y:Stone-play, reported here, can be said to demonstrate that even bch~tviors of no direct
benetit to the individual are subject to c~:fltural transmission. An area paid particular

9

734

~. A. HUFFMAN

attention to by Imanishi (1957a, b), that of troop oriented behaviors such as the traditionaltransmission of leadership or troop leading related behavior have not yet been investigated.
This topic should be given special attention in the future, collecting information fromseveral areas before coming to any conclusions.
Frish (1976) states that "culture replaces r a n d o m genetic mutation as the chief means bywhich the organism adapts itself to the environment". As shown here such behaviors do notnecessarily have to be of direct adaptive value to be passed on from generation to
generation. Sometimes even behaviors of apparent advantage or benefit fail to be
propagated throughout the group (Kawai, 1965). This suggests that perhaps the mode of
introduction (e.g., play) and the direct stimulus for the continuance of the behavior within agroup (e.g., popularity), m a y be as i m p o r t a n t as "intrinsic" or envisaged adaptive value
when considering the transmission of early hominid cultural behavior. W h e n fixed in agroup as tradition, what form the behavior takes after further individual accretion is also a
topic worthy of further investigation.
In order to fully comprehend the process of early hominid evolution, it is necessary tounderstand the mechanism and full potential of their culture. T h e study of the transmissionof learned behaviors such as stone-play by J a p a n e s e macaques m a y provide new insights
into understanding the process of early hominid cultural evolution.

I wish to give m y sincere thanks to Prof. J. Itani for his guidance and never-ending
encouragement. Also I thank H. Hayaki, H. Takasaki and the other members of our
L a b o r a t o r y of H u m a n Evolution Studies, for their critical advice, guidance, andenthusiasm. I am most deeply indepted to N. Asaba and R. Asaba of the I w a t a y a m aNatural Park for their kind assistance and friendship, making my work there most efficient.
This work was supported in part by a Grant-in-aid for Special Project Research on
Biological Aspects of Optimal Strategy and Social Structure from the J a p a n Ministry of
Education, Science, and Culture.

References

Baldwin, L. A. et al. (1980). Field research onJapanese monkeys:an historical, geographical, and bibliographicallisting. Primates 21(2), 268-301.
Breuggeman, J. A, (1978). The function ofaduh play in free-ranging Macaca mulatto. In (E. O. Smith, Ed.) Social
Play in Primates, pp. 169-191. New York: Academic Press.
Caine, N. & Mitchell, G. (1979). A review of play in the genus Macaca: social correlates. Primates21 (4), 535-546.
Candland, D. G. (1981). "Stone-Grooming" in Macacafuscata. AmericanJournal ofPrimatolo~ 1(4), 464-468.
Candland, D. G. et al. (1978). Object-Play: test of a categorized model by the genesis of object-play in Macaca
fuscata. In (E, O. Smith, Ed.) Social Play in Primates, pp. 259-296. New York: Academic Press.
Eaton, G. (1972). Snowball construction by a feral troop of Japanese macaques (Macacafuscata) living underseminatural conditions. Primates 13(4), 411-414.
Frisch, J. E. (1967). Inventive behavior in Japanese monkeys and its implications for our understanding ofhominid origins. In Akten des AnthropologischonKongresses Brno, pp. 91-94. Brno.
Frisch, J. E. (1977). Considerations of the Subcultural Behavior ofJapanese Macaques (Macacajizscata). In (T.
Kato, S. Nakao & T. Umesao, Eds) Keishitsu, Shinka, Reichorui, pp. 371-386. Tokyo: Chuokoronsha.
Goodall, J. (1963). Feeding behavior of wild chimpanzees: A preliminary report. Symposiumof the ZoologicalSocietyof London 10, 39-47.
Hiraiwa, M. (1975). Pebble-collecting behavior by juvenile Japanese monkeys. Monkey 19 (5-6), 24-25 (inJapanese).
Imanishi, K. (1952). Evolution of humanity. In Iman#hi Man. Tokyo: Mainichi-Shinbunsha (in Japanese).

10TRANSMISSION OF NON-ADAPTIVE BEHAVIOR

735!minishi~ K. (1957a). Problems in the study of Japanese monkeys. Shizen 12(2), 3-9 (in Japanese).
Iminishi, K. (1957b), Social behavior in Japanese monkeys, Macacajizscata. Psychologia !, 47-54.
Ita/ni, J. (1958). On the acqilisition and propagation of a new [ood habit in the troop 0fJa~panese monkeys at
Takasakiyama. Primates li 84-98 (iI~Japanese).
Itani, J. & Nishimura, A. (1973). The study ofinfrahuman culture in Japan: A review. In (E. W. Menzel, Ed.)
Precultural Primate Behavior, pp. 26-50. Basel: Karger.
Kawai, M. (I965), Newly acquDed pre-culture behavior of a natural troop of Japanese monkeys on Koshimaisland. Primates 6, i-30.
Kawamura, S. (l 954 i. On a new type of feeding habit which developed in a group of wild Japanese macaques.
Seibutsu Shinka 2 (1) (in japanese).
Kawamura, S. (1959). The procdss of sub-human culture propagation among Japanese macaques. Primates2,
43-60.
Kawamura, S. (1965). Sub-culture among Japanese macaques. In (S. Kawamura & J. Itani, Eds) Monkeys andApea~-Sociological Studies, pp. 237-289. Tokyo: Chuokoronsha (in Japanese).
Koyama, N. (1967). On dominance rank arid kinship of a wild Japanese monkey troop in Arashiyama. Primates8,
189-216.
Lfivi-Strauss, C. (1969). The Elementary Structurea of Kinship. Bosto!n: Beacon Press.
Menzel, E. W. (l 976). Responsiveness to olqjecti in free-ranging.Japanese monkeys. I n (J. S. Bruner, A. Jolly &K. Sylva, Eds) Play." Its Role in Developmentand Evolution, pp. 174-183. New York: Penguin Books.
Murata, G. & Hazama, N. (1968). Flora ofArashiyama, Kyoto, ar/d plant food ofJapanese rri0nkeys, lwatayama
Shizenshi Kenkyujo Chosa Kenkyu Hokoku 2, 1 56 (in Japanese).
Nishida, T. (1973). Ant-gathering behavior by the use of toots among wild chimpanzees &the Mahale mountains.
Journal oJ'Human Evolution 2, 357-370.
Sugiyama, Y. (1979). Tool-using and -malting behavior in wild chimpanzees at Bassou, Guinea. Primates20(4),5 l 3-524.
Takahata, u (1982). The socio-sexual behavior of Japanese monkeys. Zeitsehrifijizr Tierpsychologie89, 89-108.

11

PRIMATES, 27(4), 413--423, October 1986

413

Stone Handling by Japanese Macaques (Macacafuscata)"
Implications for Tool Use of Stone
MICHAEL A. HUFFMAN
Kyoto University
and DUANE QUIATT
University of Colorado at Denver
ABSTRACT. Stone-play, a newly innovated cultural behavior, has been observed among the freeranging Arashiyama B troop Japanese macaques near Kyoto, Japan since 1979. Conditions in which
the non-purposefu! handling of stones might possibly give rise to tool behavior are discussed. The
progression of this behavior is traced through three phases: transmission, tradition, and transformation. During the first two phases, through social learning, the behavior was established within thegroup as a regular item of their behavioral repertoire and was most frequently observed after eating
provisioned grain. In the third phase, observations suggest a "faddish" shift in the practice of certain
behavioral sub-types between 1984 and 1985. During this period young individuals increasingly
began to carry stones away from the feeding station, mixing stone manipulation with forage-feeding
activities in the forest. Observations suggest under such conditions, stone handling is likely to leadto the occasional use of stone as a tool. This conclusion probably can be applied to species otherthan Maeaca fuseata. Consideration of the eco-setting and social learning correlates of stone handling suggests how the instrumental use of stone might emerge from a tradition of non-instrumental
manipulation.
Key Words: Japanese macaque; Play; Diet and behavior; Tool behavior evolution; Cultural transmission.

INTRODUCTIONBENJAMIN B. BECK has suggested that "the most important set of determinants in theorigin of learned tool use...(may be) associative experience with objects in free play or nonproblem settings" (BECK, 1980). Prior familiarity with the material properties and relationsof objects in an animal's environment could increase the likelihood of their employment in a
problem setting; and, on a more basic level of likelihood, fortuitous reward of some patternof object manipulation requires at least that that pattern occur.
Experience with objects gained early in development may be essential to later proficient
instrumental manipulation (RUMBAUGH, 1970, cited by BECK, 1980). MENZEL, on the basisof experimental data drawn from comparisons of wild-born and lab-born chimpanzees, hassuggested that full realization of developmental potential for tool behavior depends on"early experience of a very general sort" (MENZEL et al., 1970; see also GOODALL, 1968).
However, "...Tool using ability does not lie in the hands alone, in the central nervous system
alone, or in the environment alone...but in some lucky interaction and isomorphic fit between them..." (MENZEL et al., 1970). As BECK has made clear (BECK, 1980), the relations
between experience, setting, learning and evolution of tool behavior are complex and interesting. The case of Japanese macaque stone handling provides a nice opportunity to examinesome of those relations.

12M.A. HUFFMAN& D. QUIATT

414

Collection and manipulation of small stones by provisioned Japanese macaques was firstreported at Takagoyama by HIRAIWA (1975). Stone handling was observed at Arashiyama
and Takasakiyama in 1979, and its popularity at those two sites increased through 1984.
Stone handling can be characterized, following CANDLAND'Sterminology, as a form of object
play (CANDLA~qDet al., 1978), with inventive variations transmitted in a context of social
facilitation and observational learning, individual repertoires influenced in part by matriline
and other associations (HuFFMAN, 1984). HUrFMAN compared the cultural transmission ofstone handling with that of feeding innovations well documented for Japanese macaques,e.g., sweet potato washing and wheat washing (KAwAI, 1965; HUFFMAN, 1984). Those behaviors are directly contingent on provisioning and presumably are directly reinforced byfood rewards--food which washing makes more palatable or easier to ingest. Stone play,however, appears to be self-rewarding, with no apparent instrumental function, at least in
its manifestation to date.
Stone play differs, too, from sweet potato washing and wheat washing in the manner of
its early diffusion. Once introduced, sweet potato washing and wheat washing were acquiredby older relatives of the innovator (in each case the same young female) as well as by agemates. Stone play, on the other hand, was first transmitted solely among peer playmates
aged 3-5 (HUFFMAN, 1984). At Arashiyama and Takasakiyama, where stone play continues
to be observed, the original players have grown to adulthood. Stone handling now is acquired
ordinarily a few months after birth by infants whose mothers handle stones. The behavior
is widely diffused at both sites, but so far there has been no evidence for its adoption by adults.
This tends to support our notion of it as a kind of play. However, since we are not in thispaper concerned with the question of what constitutes play, or how playper se may contributeto the transmission and evolution of behavior, we will keep to a more neutral terminology:
hence stone handling.
The behavior at issue involves repetitive manipulation of stone in a variety of ways (HUFFMAN distinguished eight subcategories in his 1984 paper, and we discuss changes in distribution of these, by age, in a later section). Stone handling is readily distinguishable in form andactivity context from the occasional pick up, examination, and discard of a stone or otherobject by a monkey or ape engaged in exploration. Stone handling is essentially a solitaryactivity; although young monkeys may compete for stones and steal them from one another,stones are not the focus of social play--as when possession of an unusual found object triggers reciprocal chase-and-seizure games--nor is the manipulation of stones incorporated
into social displays. In those features which involve collecting, scattering, and regroupingof stones, stone handling resembles the collection of inedible fruits, twigs, or leaves which isinfrequently described as behavior idiosyncratic to one or a few related individuals in a group(OOTA, pers. comm. cited by HUFFMAN, 1984; QUIATT, unpub, data on Macaca mulatta,
Cayo Santiago). What is perhaps most striking about stone handling by Japanese macaques,at Arashiyama and Takasakiyama, is the time and energy which individuals devote to it andits steady increase in popularity.
MATERIALS AND METHODSThis study was conducted on the Arashiyama B troop at the Iwatayama Natural Park,
Arashiyama, Japan, over three periods (by one or both of the authors); July 1979-September
1980 (M.A.H.), November 1983-June 1984 (M.A.H.; D.Q. in January), September 1984-

13

Stone Handling and Tool Use of Stone

415

February 1985 (M.A.H.). Observations were made ad libitum, by scan sampling and withVHS video. The feeding station area was scanned for stone playing individuals after eachfeeding when the behavior could most predictably be observed. In scan sampling, the area
was scanned only once during any given feeding, moving across the grounds in a set direction
to avoid sampling the same individual twice during the same sample session. Behavioral
sub-types were recorded and individuals identified by name or age.
THEORETICAL CONSIDERATIONS
We will consider stone handling from two perspectives: (1) from a general standpoint,
looking at this behavior as a kind of fad which, whatever its origins, can appear, flourish fora while, and then likely as not disappear again from the repertoire of a group; and (2) from aparticular historical standpoint, focusing on Arashiyama at the present moment, and onstone handling there as a cultural phenomenon with its own history of adoption and transmission-asking how the specific contexts of stone handling may have changed (as opposed
to what we will suggest is a conductive general context, provisioning with hard-coated grain
foods), whether there have been important changes in character and distribution of manipulative suhcategories, and, most important, whether there is any basis for predicting what
is likely to happen next. The views from these two standpoints overlap, bringing into relief
certain implications of Japanese macaque stone handling for the evolution of tool behavior.
THE GENERALPERSPECTIVE: STONE HANDLINGIN
RELATION TO TOOL BEHAVIORBEN BECK, in his comprehensive review of animal tool behavior (BECK, 1980), noted that
captive animals frequently are observed to use tools not just because they are frequently
observed but because, caged, provisioned, and with plenty of "free" time, they are likely tospend some of that time exploring their restricted habitat and whatever objects it may contain.
Thus, they are likely to become thoroughly familiar with the properties of those objects and,through random manipulation, to develop motor patterns some set of which may eventually
be rewarded by attainment of food and thereby reinforced in practice.
The importance of observation and repeated imitative practice for mastering even soseemingly simple an exercise as probing for termites is well documented (e.g., GOODALL,
1968; MCGREW, 1977; see also BARD& VAUCLAIR,1984). PARKERand GIBSON, in a discussion of the evolution of language and intelligence in early hominids, maintain that developmental acquisition of skills essential to the tool-using procedures which early hominids arelikely to have practiced must have required a long period of juvenile dependency (PARKER&
GIBSON, 1977). Similarly, LANCASTERand LANCASTER,speculating about the role and character of parental investment in early hominids, argue that "for early hominids, the evolutionof a protected period of juvenile dependency...could have led to major improvements intool-using and tool-making techniques even before any significant change in brain size ororganization, because of the creation of leisure time to be spent in play, object manipulation,and the development of skilled performances without a need to participate in the food quest"(LANCASTER& LANCASTER,1983).
We do not mistake Japanese macaques for early hominids, nor do we propose to develop
the parallel, implicit in LANCASTERand LANCASTER'Sdiscussion, between cages of captive

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M . A . HUFFMAN& D. QUIATT

animals and putative home bases of "central places" (IsAAc, 1971, 1983) of early huntergatherer hominids. It is important to keep in mind, too, that the evidence so far for tool-use
and tool-making by small-brained hominids prior to 2.6 million years ago comes strictlyfrom comparative primate behavior and comparative and functional anatomy, not from theearth. We especially want not to equate Japanese macaque stone handling with tool using.
But we agree with BECKthat "tool use, in terms of topography function, or causal dynamics,
dovetails imperceptibly with other categories of behavior," and it seems to us that frequent
handling of stones, if to employ a stone as a tool entails having some familiarity with theproperties of stone, must be likely to increase the probability of stone tool use being initiated within a group.
BECK'S comments on the random manipulation of objects by captive animals may yieldinsight into the occurrence of stone handling among Japanese macaques provisioned with
hard-coated grains--as at Arashiyama, Takasakiyama, and, for a time at least, Takagoyama. About the precise connection between provisioning and stone handling, in its original
occurrence and initial stages of adoption, we can only speculate. But, at least until recently,"stone-play could be most predictably observed after the provisioning of wheat and corn"(HUFrMAN, 1984), and monkeys seen handling stones typically are engaged simultaneously
in chewing grain from cheek pouches.
In nature, for Japanese macaques and indeed for most primates, foraging is a time-consuming whole-body activity. Collection and processing of natural foods involves a complex conjunction of integrated activities, reaching out, grasping, holding, plucking, chewing, moving
to a new position, etc., operations in which there would seem to be reinforced an accustomed
synchrony of mastication and other body movements, particularly arm and hand movements
directed toward manipulation of foodstuffs. Under provisioning and in close competition
with group associates, Japanese macaques collect food as rapidly as possible, with minimal
pre-ingestive processing. Time spent on internal processing of pouched grain foods far outweighs that devoted to collection and pre-processing.
It seems reasonable therefore to speculate that, since hard-coated grains require considerable processing subsequent to collection and pouching, monkeys so provisioned and engaged
in long bouts of a strenuous but not particularly preoccupying activity (chewing) might feela need to be "doing something" with their hands--grooming, for instance, or (once tradition
has made it a possibility) handling stones. From this standpoint, to suggest that stone handling may be self-rewarding is not to beg the question of cause but to raise the question
whether such a need, given a particular set of diet and foraging constraints, might not bephysiological.
Rather than speculate further about what it is that could make this repetitive, ritualized
manipulation of stones so popular an activity in the contexts in which it has been observed
and recorded, we will simply reemphasize the original connection with corn and wheat provisioning. In Takagoyama, where provisioning was discontinued in March of 1976, stone
handling is reported to be now much reduced in frequency (FuJITA, pers. comm. cited by
HUFFMAN,1984). While we lack the quantitative data needed to document thoroughly thisrise and fall in popularity, the history of stone handling at Takagoyama, as reported, is suggestive. Of course, it should not suggest anything like a necessary correlation with provisioning; we do not want to argue that stone handling can occur only in conjunction with
provisioning or that, once having been introduced into a group, it must then persist for as
long as provisioning is maintained.

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Stone Handling and Tool Use of Stone

417

At Takasakiyama there appears to have been, in recent months, a decline in the frequencyof stone handling bouts. If that decline should continue, it will seem reasonable to inquire
whether there may not have been concomitant persistent changes in the pattern of provisioning or in some context features associated with provisioning. However, as noted, featuresof stone handling which interest us mightily are its faddishness, the apparent lack of instrumental function, the disinclination of adults to adopt it, and the inventive variations inpatterns of display--there seems to be nothing "necessary" about this behavior, and, apartfrom the obvious fact that familiarity with an object in some sense must underlie its purposeful employment (SCHILLER, 1957), stone handling cannot be posited as a necessary precursor
to stone tool use.
It makes sense to look at the evolution of stone tool behavior in terms of a Markov progression. The coincidence of stone handling with provisioning, and, in particular, with provisioning of hard-coated cereal grains, suggests some distribution of probabilities for theoccurrence of stone handling in nature (assuming that stone handling can occur in nature)in correlation with a limited range of dietary circumstances. Similarly (and disregarding
dietary circumstances) it seems reasonable to assign higher probabilities of eventual tool use
to groups in which stone handling has come to be practiced on a regular basis.
Thus, what we see from the general standpoint is a kind of object play, weaving in and outof the manifest repertoire of a species' behavior, more likely to be in when certain dietsprevail and, when it is in, tending to increase the likelihood of stone tool use. This raises thequestion whether we can outline, without considering the specific purposes to which stone
tools will be put, some conditions in which stone handling could be expected to give rise totool behavior. To deal with this question, we will move to the historical particular standpoint
and look at one manifestation of stone handling--at Arashiyama--as a prolonged cultural
phenomenon with its own history of adoption, transmission, and change.
THE HISTORICALPERSPECTIVE: STONE HANDLING AT ARASHIYAMAHUFFMAN has outlined the diffusion of stone handling at Arashiyama from its first appearance in 1979 through the spring of 1984 (HUFFMAN, 1984; Fig. 1 below), breaking it into twophases, in part to facilitate comparison with previously studied diffusions of innovated behaviors (ITANI, 1958; KAWAMURA, 1959; KAWAI, 1965). The conventional distinction drawn
between "transmission" and "tradition" phases in the propagation of innovations seems to
us meaningful and illuminating. However, these terms connote a processual conservatism
which does not quite fit the case of stone handling (see below) and events at Arashiyama
suggest that it may prove useful, where stone handling is concerned, to recognize a third
phase.

RESULTS
TRANSMISSIONPHASE

The introduction and early dissemination of stone handling presumably is similar fromgroup to group in the character of its occurrence. A young monkey (at Arashiyama, Glance6476) collects and manipulates stones, does so again, and over time continues to repeat that
activity for increasingly extended periods. Sibs and unrelated playmates aged 3 or less16

M. A. HUFFMAN& D. QUIATT

418
FeedingInnovations

TRANSMISSION

Stone H a n d l i n g

PHASE

TRANSMISSIONTRADITION PHASE

PHASE

TRADITION PHASE

Fig. 1. Direction of transmission of feeding innovations and stone handling (after HUFFMAN, 1984).
Note the difference in the transmission phase between stone handling and previously studied innovations in feeding behavior.

observe and imitate the behavior. This repetitive, stereotypical manipulation of stones istransmitted initially to a network of spatial-interactional associates which is specific to theinnovator(s) and characteristic of the behavior context (i.e., play). As innovators grow older,their social networks are extended; younger sibs and new peer-associates become stone
handlers. Observational learning plays an important role, as in, e.g., chimpanzees (GoODALL,
1968) and forest baboons (Mandrillus sphinx, CAMBEFORT, 1981). The relation between social
facilitation and imitative learning in this process of transmission has been discussed by
CAMBEFOXT (1981); individual learning and cultural transmission of behavior have been
compared by NISHIDA (1986); and KURLAND and BECKEXMAN(1985) have remarked on thecomplexity of relations between accident, invention, and observational learning.
TRADITION PHASE
When female stone handlers reach reproductive maturity, as many now have at Arashiyama, a new phase is opened. In this tradition phase the rate of diffusion is approximately
equal to the birth rate: an infant will learn stone handling from mother, from an infant
playmate whose mother handles stones, or from an older sib who has learned stone handlingfrom a playmate. This observational learning occurs very early in development. Infants as
young as 3 weeks show interest in handling of stones--approaching, grasping at, mouthing,and picking up stones being handled by mothers (HUFFMAN,unpub, data from Spring 1985).
At this stage, as long as there are stones available, stone handling may persist as a tradition
within the group, though there can be no guarantee that it will persist. The case of Takagoyama suggests that persistence may be contingent on diet and foraging circumstances, whichis consistent with the view presented here. Stone handling at Takagoyama appears never to17Stone Handling and Tool Use of Stone

419

have reached a high frequency, a n d it is likely t h a t the tradition p h a s e h a d n o t been a t t a i n e dbefore p r o v i s i o n i n g was discontinued.
T h e m o n k e y s at A r a s h i y a m a are n o w in the tradition phase, with stone h a n d l i n g p r o p a g a t e d via o b s e r v a t i o n a l l e a r n i n g f r o m m o t h e r s to infants as well as laterally a m o n g p l a y m a t e s .
Currently, there are indications o f change which s h o u l d n o t o n l y strengthen the t r a d i t i o nbut, in t h e o r y at least, increase the l i k e l i h o o d o f stone t o o l use o c c u r r i n g as an indirect outcome of non-purposeful manipulation.
TRANSFORMATION PHASE
F o r at least some y o u n g individuals, practice a n d acquired familiarity with the p r o p e r t i e s
o f stones are likely to extend the r e p e r t o i r e o f m o t o r sequences e m p l o y e d in stone handling.
I n terms o f the g r o u p , this m e a n s a n a c c u m u l a t i o n o f variety available via o b s e r v a t i o n a llearning to new stone handlers. T h a t variety is available in practice p r i m a r i l y to 1- to 3-yearolds. O l d e r individuals do n o t seem as q u i c k to p i c k u p on change, b u t within t h a t y o u n g e r
a g e - g r o u p i n n o v a t i o n , exchange, a n d r e p l a c e m e n t o f m a n i p u l a t i v e p a t t e r n s a r e free-flowing.
This f a d d i s h cycling o f m o t o r activities is difficult to d o c u m e n t , m u c h less interpret. H o w ever, c o n t i n u e d o b s e r v a t i o n o f stone h a n d l i n g at A r a s h i y a m a has yielded a n u m b e r o f newb e h a v i o r a l sub-types, m o s t o f which so far a p p e a r to reflect b e h a v i o r p r e d o m i n a n t l y o f individuals b o r n since 1980. F u r t h e r m o r e , c o m p a r i s o n b y age o f subject o f observed stonep l a y b e h a v i o r s shows an interesting d i s t r i b u t i o n (Table 1): Gather, Pick-up, a n d Scatter,
categories representing w h a t m i g h t be called the generic p a t t e r n o f stone handling, are b r o a d ly d i s t r i b u t e d across age classes, while categories w h i c h reflect a m o r e specific attention to
one or two stones as well as to the activity at h a n d are limited a l m o s t exclusively to 1- to 3year-olds.
I n J a n u a r y 1984, when we spent two weeks v i d e o t a p i n g sequences o f stone handling, there
were h e a v y snowfalls at A r a s h i y a m a ; the m o n k e y s spent m o s t o f each d a y at the feedingstation, where on sunny days the t h a w was quicker a n d where f o o d a n d stones were plentiful.
T h e next winter (1984-1985), when there was a n a b u n d a n c e o f a c o r n s a n d no snow on theg r o u n d t h r o u g h J a n u a r y , the t r o o p spent less time at the feeding station a n d m o r e in thew o o d s . T a b l e 2 shows an interesting shift in b e h a v i o r frequencies f r o m 1984 to 1985 (becauses a m p l i n g p r o c e d u r e s were revised in 198 5, tests o f significance c a n n o t be applied, b u t p a t t e r n s
o f difference are n o t m u c h affected).

Table 1. Distribution by age and behavioral sub-type for stone handling sampled in the fall and winter of 1984-85.
Stone handlingYear of birth
sub-types
1984 1983 1982 1981 1980 1979 1978 1977 1976 1975 1974 Total
Gather
5
12
5
4
19
2
12
-1
1
-61
Pick-up
11
15
9
1
18
5
20
-3
4
-86
Scatter
2
15
11
8
4
4
12
--2
-58
Roll in hands
-3
2
1
.
.
.
.
.
.
.
6
Rub
23
41
11
6
1
-1
--2
-85
Clack
-2
1
.
.
.
.
.
.
.
.
3
Carry
11
24
9
4
-1
6
-1
--56
Cuddle
6
13
6
1
-1
.
.
.
.
.
27 (iV = 382)
Data collected during 113 days between September 22, 1984 and February 15, 1985 from 95 identified individuals.

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M . A . HUFFMAN& D. Qt:IATT

Table 2. Relative frequencies of stone handling sub-types compared for 1984 and 1985.
Stone handling sub-type
1984
1985
Gather.11.14
Pick-up.23.20
Scatter.21.14Roll in hands
.10
.03
Rub
.09
.27
Clack
.02
.02
Carry
.20
.14
Cuddle.04.05
1.00 (N -- 391)
.99 (N = 681)
Data was collected during 17 days from 169 instances in 1984 and 22 days from 204 instances in 1985.

Some behaviors--Gather, Pick-up, Clack, and Cuddle--show very little change in frequency. Gather and Pick-up of course are activities basic to stone manipulation and probably
should not be expected to change much. Other behaviors show marked change in frequency;
most outstanding is Rub, which appears to be the going fad (note however that certain individual "specialists" account for a high proportion of Rub bouts--HUFFMAN, unpub, data).
Carry, Clack, Cuddle, and Rub are behaviors displayed most frequently by young individuals(Table 1). In 1985, the youngest stone players showed an increased tendency to take stones
into the woods on leaving the provisioning station and to mix stone play with feeding. For
these troop members, the range of sites and situational contexts in which they practice stone
handling was significantly expanded. The expansion may be attributed in part to (or at leastis nicely correlated with) change in weather conditions and increased abundance of natural
foods (acorns).
Two incidents from the winter of 1985 will serve to illustrate the conjunction of activities
just noted. HUFFMAN observed a 3-year-old male, a life-long stone player, rubbing stones,
his mouth full of acorns after foraging in the woods. He rubbed stones together, paused,removed an acorn from his cheek pouch, took the shell part way off, rubbed the acorn against
one of the stones, and ate the now wholly shelled meat. In the second incident, a monkey wasreported to have rubbed a dirty sweet potato with a rock before eating it.
Note that we do not submit these as instances of tool use. In our view, their significancelies precisely in their ambiguity, in the fact that they cannot readily be categorized by formal
criteria (i.e., apart from assumptions as to cognition and intent). They return us to BECK'S
observation that tool use dovetails with other categories of behavior (BEck:, 1980). The
repetitive, stereotypical character of stone handling in its initial forms has been invaded bylability, and more and more at Arashiyama the m o t o r patterns of stone play are being integrated with those of other activities. Stone handling in its original manifestation was, and is,
an exercise which affords experience with the properties of stones. When stones are handledin conjunction with other materials, while feeding for instance, a basis is established for relating the properties of stone to those of other materials--for an understanding, in effect, andin terms of accumulated sensory experience, not just of the properties of things but of relationships between them.

SUMMARY AND CONCLUSIONS
Propositions about the importance of play and diet to animal tool behavior arise from19

Stone Handling and Tool Use of Stone421

the observation that there is an inverse relation between time spent foraging and time available for object play, and that playing with an object increases the likelihood of putting it to
instrumental use. That tool behavior is more common among captive animals than amongwild conspecifics may be explained largely by the fact that the former are provisioned andhave more time to explore their environment. As BEcK points out, captive animals are also
likely to come in contact with novel objects as well as atypical foods. He further states that,atypical foods may stimulate atypical feeding responses--so that, altogether, (1) provisioning
promotes the exploratory manipulation of objects; and (2) "object manipulation provides apool of behavioral variants which, if fortuitously reinforced, can become tool patterns"(BECK, 1980).
Our examination of stone handling by free-ranging but provisioned Japanese macaques
supports BECK'Sargument. Stones are encountered by monkeys foraging in nature (especiallywhen digging for subsurface food items), hence they cannot be considered novel objects
when they occur in numbers at a provisioning site. Nevertheless, that they do occur there in
numbers and in conjunction with novel foods (i.e., hard-coated grains) is atypical.
Whether or not such foods are seen as stimulating atypical feeding responses must depend
on what one considers typical for Macaca fuscata. Japanese macaques, like other forestdwelling macaque species, forage much of the time off the ground. This requires a greater
investment of both time and overall body activity in procurement and processing, prior topouching, than does picking up harvested grain cast on the ground. Conversely, the latter
requires a considerable amount of active processing subsequent to initial intake and pouching. It appears as if there is a systematic relation between prolonged chewing of grain and themanipulatory activities involved in grooming and stone handling.
Stone handling raises other interesting issues. As noted, stone play in its initial manifestation (i.e., in the transmission and tradition phases) involves a distinctive set of apparently
self-rewarding operations. They appear to be highly absorbing and, in that sense, self-contained, detached in their exercise from other more ordinary activities. To the extent that
it is coupled temporally with ingesting provisioned food, stone handling may be reinforcedby food gratification, and so likely to become habitual in development. However, it is difficult
for us to imagine how a specific operation might be fortuitously instrumental and selectively
rewarded. On the other hand, if at Arashiyama young animals continue to carry stones awayfrom the feeding station, and if stone handling continues to be integrated with other activities
in what we have called, perhaps prematurely a transformation phase, then it is easier to see
how the application of stone to another material could be rewarded and lead to the learningof tool use (HAMILTON, 1973; BECK, 1980). The food-rubbing incidents cited earlier suggest
how this might occur. Where quadrupedal monkeys are concerned, skeletal-muscular constraints associated with habitual posture and locomotion are likely to direct the effective
instrumental manipulation of stone to rubbing or scraping operations rather than to hammering.
It is important also, where tool behavior is concerned, to keep in mind the distinction
between learning and evolution. Manipulation and instrumental use of an object may belearned by individual animals and transmitted as a feature of culture over generations. Fromthe standpoint of biological evolution, what evolves is not tool behavior per se but the facility
for learning, neural coordination, and--in the unique case of hominids--complex anatomical accommodation to a niche which has been radically transformed by habitual conversionof various materials to objects of use. Though we anticipate that stone handling at Arashi-

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M.A. HUrrMAN & D. QUIATT

422

y a m a and T a k a s a k i y a m a is likely to give rise to the occasional use of stone as a tool, we ofcourse do not predict niche transformation and further evolution of tool behavior in thissense. The most likely outcome for stone handling at Arashiyama and Takasakiyama is
continued cultural transmission of the trait until some change in the environment, e.g., longterm food shortage (HAMILTON, et al., 1978, cited by BECK, 1980) or change in diet make it
maladaptive. Environmental opportunity is critical for behavioral evolution.
The affirmation of the importance of environmental opportunity seems to us an importantlesson to be gained from considering the context of stone handling in Japanese macaques.
It encourages us not to think of the invention of stone tools either as a serendipitous solution
to problems set by nature or as the automatic endpoint of a natural chain of events: noninstrumental manipulation of stones---~use of stones as tools--~manufacture of stone tools.
Manipulation of stones is, to begin with, an oddity of behavior for most primates. In thecase of Japanese macaques, it appears that only exceptional environmental circumstances
are likely to provide " r o o m " for non-instrumental manipulation of stones as a regular itemof daily behavior. Even where stones are handled daily, and where stone play has become apopular, time consuming feature of behavior, our observations indicate that it is unlikely
to give rise to instrumental manipulation until the material and some of the operations of
this behavioral fad have been integrated into other, more basic life activities. Integrationm a y be furthered by minor and temporary environmental changes (e.g., climatic variationfrom one year to the next, as witnessed at Arashiyama between 1984 and 1985); but, alternatively, change in the environment may tend to reduce or eliminate what might be called thesource behavior, the habit of non-instrumental handling of stone (as we suggest may havebeen the case at Takagoyama). Thus, stone handling could occur, disappear, and reoccur
any number of times as an apparently regular item of a group's manifest repertoire of behavior, culturally transmitted from generation to generation and even from group to group,and never once be practiced in a context providing fortuitous reward and shaping instrumental use. Handling stones on a regular basis of course increases the likelihood of fortuitous
reward, subsequent learning, and transformation to the next stage of instrumental use ofstones as tools. But even then the process is reversible, and furthermore, it is most unlikelythat a group of Japanese macaques or any species of monkey would progress to a stage oftool manufacture. Only long-term perpetuation of just the right conjunction of circumstances
could bring about the change of niche which we must have in mind when we think about
the evolution of stone tool manufacture from habitual use of stone as tools. Events at Arashiyama and Takasakiyama shed no light on this end result; however, they contribute tounderstanding of the process by suggesting how, in a specific eco-setting, free handling ofstone can give rise to instrumental use.

Acknowledgements. We thank Prof. J. ITANIfor support, encouragement, and a critique of the manuscript in draft. We are much in debt, too, to Mr. 2',1.ASABAand Mr. R. ASABA of Iwatayama Natural
Park for assistance, still more for friendship and hospitality.
REFERENCES

BARD,K. L. & J. VAUCLAIR,1984. The communicative context of object manipulation in ape andhuman adult-infant pairs. J. Human Evol., 13: 181-190.
BECK, B. B., 1980. Animal Tool Behavior: The Use and Manufacture of Tools by Animals. Garland,
Yew York.

21

Stone Handling and Tool Use of Stone

423

CAMBEREORT,V. P., 1981. A comparative study of culturally transmitted patterns of feeding habitsin the chacma baboon Papio ursinus and the vervet monkey Cercopithecus aethiops. Folia Primatol., 36: 243-263.
CANDLAND, ~D. K., J. A. FRENCH, • C. N. JOHNSON, 1978. Object-play: test of a categorized modelby the genesis of object play in Macacafuscata. In: Social Play in Primates, E. O. SMITH (ed.),Academic Press, New York, pp. 259-296.
GOODALL,J., 1968. The behaviour of free-living chimpanzees in the Gombe Stream Reserve. Anita.
Behav. Monogr., 1: 161-311.
HAMILTON,W., 1973. Life's Color Code. McGraw-Hill, New York.
, R. BUSKIRK, & W. BUSKIRK, 1978. Environmental developmental determinants of object
manipulation by chacma baboons (Papio ursinus) in two Southern African environments. J.
Human EvoL, 7: 205-216.
HIRAIWA, M., 1975. Pebble-collecting behavior by juvenile Japanese monkeys. Monkey, 19(5-6):
24-25. (in Japanese)
HUEFMAN, M. A., 1984. Stone-play of Macaca fuscata in Arashiyama B troop: transmission of a
non-adaptive behavior. J. Human Evol., 13 : 725-735.
ISAAC, G., 1971. The diet of early man: aspects of archaeological evidence from Lower and Middle
Pleistocene sites in Africa. Worm Arehaeol., 2: 278-299.
- - ,1983. Aspects of human evolution. In: Evolution from Molecules to Man, D. S. BENDALL(ed.), Cambridge Univ. Press, Cambridge, pp. 509-543.
ITANI, J., 1958. On the acquisition and propagation of a new food habit in the troop of Japanesemonkeys at Takasakiyama. Primates, 1: 84-98. (in Japanese). Translated into English forJapanese Monkeys, a Collection of Translations Selected by KINJI IMANISHI,S. A. ALTMANN(ed. & publ.).
KAWAI, M., 1965. Newly acquired pre-cultural behavior of the natural troop of Japanese monkeys
on Koshima islet. Primates, 6: 1-30.
KAWAMURA,S., 1959. The process of sub-human culture propagation among Japanese macaques.
Primates, 2: 43-60.
KURLAND,J. A. & S. J. ]~ECKERMAN,1985. Optimal foraging and hominid evolution: labor andreciprocity. Amer. Anthropol., 87: 73-93.
LANCASTER,J. B. & C. S. LANCASTER,1983. Parental investment: the hominid adaptation. In: How
Humans Adapt, a Biocultural Odyssey, D. J. ORTNER (ed.), Smithsonian Institution Press, Washington, D.C., pp. 33-56.
McGREw, W. C., 1977. Socialization and object manipulation of wild chimpanzees. In: Primate
Biosocial Development, S. CHEVALIER-SKOLNIKOEF• F. E. POIRIER (eds.), Garland, New York,
pp. 261-288.
MENZEL, JR., E. W., K. R. DAVENPORT, & C. M. ROGERS, 1970. The development of tool using inwild-born and restriction-reared chimpanzees. Folia Primatol., 12: 273-283.
NISHIDA, T., 1986. Learning and cultural transmission in non-human primates. In: Primate Societies,
D. CHENEY, L. LELAND, L. SEYFARTH,B. B. SMUTS, T. STRHUSAKER,& R. W. WRANGHAM(eds.),
Univ. of Chicago Press, Chicago. (in press)
PARKER,S. & K. GIBSON,1977. Object manipulation, tool use and sensorimotor intelligence as feeding adaptations in Cebus monkeys and great apes. J. Human Evol., 6: 623-641.
RUMaAUGH, D., 1970. Learning skills of anthropoids. In: Primate Behavior, VoL 1, L. ROSENBLUM(ed.), Aldine, New York, pp. 1-70.
SCHILLER,P. H., 1957. Innate motor action as a basis of learning. In: Instinctive Behavior, C. H.
SCHILLER (ed.), International Univ. Press, New York, pp. 264-287.
- - R e c e i v e d March 10, 1986; Accepted June 25, 1986
Authors' Names and Addresses: MICHAELA. HUFFMAN,Laboratory of Human Evolution Studies, Faculty of
Science, Kyoto University, Sakyo-ku, Kyoto, 606 Japan; DUANE QUIATT,Department of Anthropology, University of Colorado at Denver, 1100 14th Street, Denver, Colorado 80202, U.S.A.

22

On Home Bases, Nesting Sites, Activity Centers, and New Analytic Perspectives
Duane Quiatt; Michael A. Huffman
Current Anthropology, Vol. 34, No. 1. (Feb., 1993), pp. 68-70.
Stable URL:
http://links.jstor.org/sici?sici=0011-3204%28199302%2934%3A1%3C68%3AOHBNSA%3E2.0.CO%3B2-Y
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68 1 C U R R E N T A N T H R O P O L O G Y

cent discussions on Piltdown and Keith's possible
involvement (CA 33:243-93).
First, although it has often been regarded as a depiction of Keith's reconstruction of the Piltdown skull, oneof us (P.V.T.)has shown recently that the cover figure
represents the Piltdown I hominoid fragments superimposed on the outline of a modern English skull often
used by Keith for purposes of comparison (CA 33:28 I).
Secondly, a curious contradiction has emerged as to
the words embossed alongside it: "Piltdown Skull" according to Kennedy (p. 269), "Piltdown Fragments" according to Tobias (p. 281). Further researches by us on
the various editions and impressions of The Antiquity
have revealed that both of us were right, albeit in respectof different impressions of the first edition.
We have found that "Piltdown Skull" appeared on the
cover of the first impression of the first edition (October
1915 ) and "Piltdown Fragments" on the second (December 1915)~the third (February 1916)~and the fourth(March ~ g z o )as, well as on the second edition (January
1925).The change from "skull" to "fragments" was thus
effected between the first and the second impression of
the first edition.
The original wording was misleading and, as we haveseen, did indeed mislead some scholars. It is possiblethat Keith realised how misleading it was and instructed
his publishers, Williams and Norgate, Limited, tochange the cover for the second impression. Or a colleague might have pointed it out to him. Possibly a reviewer of the book might have drawn attention to it, but
this is the least likely, for there was a lapse of only twomonths between the first and the corrected second impression.
Postscript. Carmel Schrire has kindly drawn our attention to an American printing of the 1915 edition published by J. B. Lippincott. The cover bears the label "Piltdown Skull," and we assume it was based upon the first
impression published in England. We have been unable
to trace whether Lippincott published a second impression.

tivity and in free-ranging circumstances, both in provisioned groups and, for a short period of time, in one
unprovisioned one. In groups in which stone handling is
popular and culturally well-established, transmitted
over several generations, individuals may engage in thisnoninstrumental manipulation of stones on a regular basis and for long periods of time. Is Japanese macaquestone handling relevant at all to the use of stone implements by early hominids and the formation of sites resembling home bases or food-processing locations? Ourstudies of stone handling (Huffman 1984, Huffman and
Quiatt 1986, Derr and Quiatt 1992) incline us toward a
positive answer, and that inclination is reconfirmed byour reading of Sept's (CA33:187-208) response to thechallenge issued some years ago by Isaac: (1986:237):"Can we conceive of patterns of behavior and adaptationthat could lead to the formation of familiar-looking patterns of archaeological evidence, and yet which were behaviors unfamiliar to us in that they were structured
differently from recent and present-day human ones?"
Sept asks whether the accumulation from year to yearof remains from chimpanzee foraging and nest construction might not establish a physical pattern similar in its
local concentration to that which suggested to Isaac theuse of home bases by early hominids. To test her hunch
she looks at the accumulation of nest remains over a
two-year period of a small population of chimpanzees
on the Ishasha River (p. 195):

If the chimpanzees had left durable residues of their
manipulative activities wherever they constructed anest, for example, sites could have been buried andpreserved by the overbank sediments of the Ishasha
River. Such "sites" would not have formed as a result of home-base behavior or other communal activity patterns; they would have formed because
something about the local forest structure and composition-perhaps fruit density or canopy heightfavored frequent reuse of the locality for chimpanzee
nesting or feeding and debris accumulated there
through time.
Sept concludes that her research "supports argumentsthat early archaeological sites could have formed as byproducts of a system of subsistence and ranging very
different from a home-base or central-place foraging
system."Chimpanzees do not manufacture and use stone tools
in nature, but Sept (p. 204) wonders whether it is possible to "imagine a behavioral mechanism that could account for the occasional transport of stone or bone tofavorite patches of fruiting or nesting trees without invoking cooperative foraging and food sharing." The answer, of course, is yes. As Boesch and Boesch (1984)have
shown, chimpanzees carry nut-cracking stones up to
several hundred meters. It may be, as Potts (1984, 1987)
has argued, that some concentrations of stone artifacts
and bone in Bed I Olduvai represent tool caches, stone
having been transported to refuge areas in conjunction
with a scavenging pattern of subsistence. But it may be,
too, that the ancestors of those putative scavengers

On Home Bases, Nesting Sites,
Activity Centers, and New
Analytic Perspectives
D U A N E QUIATT A N D MICHAEL A. HUFFMAN

Department o f Anthropology and Sociology, Campus
Box 105, University o f Colorado at Denver, P.O. Box
1733 64, Denver, Colo. 80217-3364, U.S.A.lDepartment
of Zoology, Kyoto University, Sakyo 606, Kyoto,
Japan. 26 VIII 92

Japanese macaques have been observed to engage in"stone play" or "stone handling," carrying about andmanipulating stones in a variety of contexts both in cap24

Volume 3 4 , Number I , February 1 9 9 3 1 69

transported stone to the same or similar refuge areas forquite other purposes-for processing vegetal foods or,for that matter, for purposes not directly connected withfood processing.
The questions put by Isaac and now Sept need not andprobably should not be addressed solely from a chimpcentric perspective; stone handling by free-ranging Japanese macaques provides a challenging example of how
activities can combine to produce clumpings of artifacts
that would be unlikely subsequently to yield insights
about origins. Since stone play and stone transport became established as a daily practice of the younger generations of the Arashiyama and Takasakiyama troops(five in total), piles of stones have begun to accumulate
in certain areas of the forest surrounding the provisioning grounds. These "play stations," revisited daily,
are occasionally located near forest foraging sites, because the behavior is often intermixed with or followedby (but in no way directly related to) foraging for acorns,
grass, and leaves. Stones are transported from one station to another and deposited on stone slabs (fig. I ) at
the bases of large trees and sometimes even in trees.

FIG. I . Stones left on flat stone surface by
free-ranging stone handlerfs) at Takasakiyama,
lapan. (Photo Michael A. Huffman.)

25

Stones are occasionally modified, scratched, or chippedin handling, and recycling can produce.repeated modification.
McGrew and Moore take issue with Sept's rejectionof "referential models" on grounds, following Stanford
and Allen ( I99 I), that the distinction drawn by Tooby
and DeVore (1987) between "referential" and "conceptual" models "is artificial and misleading" (Moore, p.
199).McGrew adds (p. 198) that while "referential models have their drawbacks (no species is another species), . . . they have one big advantage: Living organisms
can provide us with both behaviour and artefacts, while
concepts supply neither." We agree strongly with bothobservations and would like to remind readers, further,that Stanford and Allen were critical not just of Tooby
and DeVore1s advocacy of "conceptual" over "referential" models but of what they saw as a return under new
banners to the unreconstructed ground of male-centric
huntinglscavenging.
As Stanford and Allen remind us, although male cooperation in the hunt and use of stone implements to procure andlor process meat may have had great adaptive
significance at some stage of human evolution, there islittle support for the notion that hominid culture can betraced t o a n original association of these two "historicaloccurrence^.^' Indeed, the one documented instance todate of tool-assisted predation on vertebrates by chimpanzees in the wild is the very recent observation at
Mahale of an adolescent female's using a modified
branch to capture a large adult squirrel hiding in a hole
in a tree (Huffman and Kalunde I 993). Chimpanzee tools
are virtually never used in conjunction with meat procurement, and although females may participate infrequently in hunting parties at Gombe and Mahale (in 4%
of hunts observed at Gombe [Goodall 19861)~females at
the Tai National Park, where stone and wooden hammers are used to crack nuts (as they are not in either
Gombe or Mahale), are both more active hunters (13%of all individuals observed hunting [Boesch and Boesch
19891) and more active nut-crackers, just as Gombe females are more active termiters (McGrew 1981). Tai females are more active sharers of meat than females atGombe, sharing with males as well as with offspring andother females. "Most food sharing among chimpanzees
involves plant foods shared between mother and infant(de Waal I 989, McGrew 198 I), and so models of humansocial evolution based on meat procurement may apply
only to a very recent stage" (Stanford and Allen 1991).
Just as it is heuristic now and then to decouple our
speculations about male cooperation, hunting (and scavenging), and tool use, so it may be heuristic to decouple
our thoughts concerning object manipulation and transport, tool use, and food procurement. The implicationof Sept's mapping of the physical residues of chimpanzee
behavior, expressed tentatively by Sept and morestrongly by various commentators, is that lithic remains
at early hominid sites may have been trans~ortedfor use
in processing vegetal rather than animal-foods. Lithic
raw materials found at sites located up to 10 km fromsource deposits need not have been transported there in70 1 C U R R E N T A N T H R O P O L O G Y"a single, goal-directed journey" (McGrew, p. 197).Tai
forest chimpanzees regularly transport stones over shortand not-so-short distances, and, as McGrew goes on tonote, repeated carrying "over decades, or centuries, ormillennia" may eventually have built up concentrationsof stones at sites some distance from their original
source. "This," says McGrew, "is a topic ripe for computer modelling, and specification of which 'by-productsof other behaviors' " (i.e.,behaviors other than hunting1
scavenging) may be required. We agree, and, since weagree too with McGrew, Moore, and Stanford and Allen
concerning the utility of "referential" models, we would
add only that it may be helpful, when considering those"by-products of other behaviors," to look at the behaviorof, for instance, Japanese macaques.

1986. Stone handling by
Japanese macaques (Macaca fuscata):Implications for tool useof stone. Primates 27:427-37.
H U F F M A N , M . A , , A N D M . S . K A L U N D E . 1993. Tool-assisted
predation of a squirrel by a female chimpanzee in the Mahale
Mountains. Primates. In press.
I S A A C , G . L. 1986. "Foundation stones: Early artifacts as indicators of activities and abilities," in Stone Age prehistory: Studies in memory of Charles McBurney. Edited by G. N. Bailey
and P. Callow, pp. 221-41. Cambridge: Cambridge University
Press.
M C G R E W , W . C. 1981. "The female chimpanzee as a human
evolutionary prototype," in Woman the gatherer. Edited by F.
Dahlberg, pp. 35-75. New Haven: Yale University Press.
-.
1992. Comment on: Was there no place like home? by
J. M. Sept. CURRENT ANTHROPOLOGY 33:197-98.
M O O R E , J . 1992. Comment on: Was there no place like home?
by J. M. Sept. CURRENT ANTHROPOLOGY 33:198-99.
P O T T S , R . 1984 "Hominid hunters? Problems of identifying theearliest hunterlgatherers," in Hominid evolution and community ecology: Prehistoric human adaptation in biological perspective. Edited by R. Foley, pp. 129-66. London: Academic
Press.
-.
1987. "Transportation of resources: Reconstructions ofearly hominid socioecology, a critique of primate models," inThe evolution of human behavior: Primate models. Edited by
W. G. Kinzey, pp. 28-47. Albany: State University of New
York Press.
S E P T , J. M . 1992. Was there no place like home? A new perspective on early hominid archaeological sites from the mapping of
chimpanzee nests. CURRENT ANTHROPOLOGY 33: 187-207.
S T A N F O R D , C. B., A N D J . S . A L L E N . 1991. On strategic storytelling: Current models of human behavioral evolution. CURRENT ANTHROPOLOGY 32: 58-61.
T O O B Y , J., A N D I. D E V O R E . 1987. "The reconstruction of hominid behavioral evolution through strategic modeling," in The
evolution of human behavior: Primate models. Edited by
W. G. Kinzey, pp. 183-238. Albany: State University of New
York Press.
H U F F M A N , M . A., A N D D . Q U I A T T .

References Cited
c., A N D H . B O E S C H . 1984 Mental map in wild chimpanzees: An analysis of hammer transports for nut cracking.
Primates z5:160-70.
-.
1989. Hunting behavior of wild chimpanzees in the Tai
National Park. American Journal of Physical Anthropology
78:547-73.
D E R R , s., A N D D. Q U I A T T . 1992. Japanese macaque stone handlers in the New World (abstract].American Journal of Physical Anthropology, suppl. 14:70.
D E W A A L , F . 1989. Food sharing and reciprocal obligations
among chimpanzees. Iournal of Human Evolution I 8:43 3-5 9.
G O O D A L L , J . 1986. The chimpanzees of Gombe: Patterns of behavior. Cambridge: Harvard University Press.
H U F F M A N , M. A . 1984 Stone-play of Macaca fuscata in Arashiyama B Troop: Transmission of a non-adaptive behavior.
Iournal of Human Evolution 13:725-35.
BOESCH,

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Primates (2004) 45:113–118
DOI 10.1007/s10329-003-0065-5

O R I GI N A L A R T IC L E

Michael A. Huﬀman Æ Satoshi Hirata

An experimental study of leaf swallowing in captive chimpanzees:
insights into the origin of a self-medicative behavior
and the role of social learning
Received: 8 August 2002 / Accepted: 17 October 2003 / Published online: 23 January 2004
Ó Japan Monkey Centre and Springer-Verlag 2004

wild from opportunistic feeding behavior and was later
passed down in the form of a self-medicative behavioral tradition.

Abstract Chimpanzees in the wild swallow the roughhispid leaves of certain plant species as a means ofphysically expelling intestinal parasites. A plant withsuch a leaf texture was introduced in 36 trial sessions toa captive group of 11 healthy adult chimpanzees toinvestigate the possible origin and acquisition of leaf
swallowing behavior. One male (housed separatelyfrom the group during testing) and one female, both
captive born, spontaneously exhibited the behavior on
their ﬁrst trial without prior opportunity to observe
others with this plant. Six other chimpanzees on theirﬁrst trial displayed a phobic response to these leaves
and rejected them entirely, while another two chewed
and swallowed the leaves in a normal way. Four individuals eventually exhibited the behavior, after having
approached and closely observed the leaf swallowing of
the ﬁrst female to exhibit the behavior in the group.
Four of the six individuals that initially avoided theleaves never overcame their phobia toward this plant
and were not in proximity to a chimpanzee performing
leaf swallowing during test sessions. Individuals born towild chimpanzee mothers were no more likely to perform the behavior than captive-reared group mates.
These results suggest that the acquisition of thisbehavior is based in part on a propensity to fold andswallow rough, hispid leaves, but that the acquisitionand spread of leaf swallowing within a group is likely
to be socially inﬂuenced. This study provides support
for the hypothesis that leaf swallowing originated in the

Keywords Feeding Æ Social tolerance Æ Behavioral
tradition Æ Self-medication

Introduction
Attention was ﬁrst brought to leaf swallowing behavior
by Wrangham and Nishida (1983) when they pointed
out the signiﬁcance of this ingestive behavior as unlikely
to be that of providing any nutritional value. They noticed a pattern for the occurrence of folded, undigested
leaves of Aspilia species in the dung of chimpanzees atboth Gombe and Mahale. Currently, leaf swallowing is
documented in the greatest detail in chimpanzees at four
study sites in East Africa (Mahale, Gombe, Kibale, andBudongo), where its use is associated with the expulsionof adult intestinal nematodes and or cestode proglottids(Wrangham 1995; Huﬀman et al. 1996; Huﬀman andCaton 2001). Leaf swallowing has since been noted tooccur in at least 22 social groups of chimpanzees,
bonobos, and lowland gorillas at 13 study sites across
Africa (Huﬀman 2001). The 34 diﬀerent plant species
selected at these sites vary in life form (herb, vine, shrub,
and tree), but they all share the common property of
being rough and hispid (Huﬀman 1997).
The widespread occurrence of leaf swallowing andthis universal criterion for selecting rough, bristly leaves
suggests a behavioral predisposition for leaf swallowing
in all African great apes. There is also evidence to suggest that transmission within the group occurs at least inpart by some form of social learning (Huﬀman and
Hirata 2003). Observations from the wild suggest that
individuals’ ﬁrst exposure to leaf swallowing and otherforms of self-medicative behavior occurs at an early age,
not when ill themselves, but by observing the behaviorof close family members or associates that are ill.

Electronic Supplementary Material Supplementary material isavailable in the online version of this article at http://dx.doi.org/
10.1007/s10329-003-0065-5
M. A. Huﬀman (&)
Primate Research Institute, Kyoto University,
41-2 Kanrin, Inuyama, Aichi 484-8506, Japan
E-mail: huﬀman@pri.kyoto-u.ac.jp
S. Hirata
Great Ape Research Institute,Hayashibara Biochemical Laboratories, Inc., Okayama, Japan

80

114

feeding behavior that is later molded over time throughfurther individual experience and association of its
practice with illness in other group members. To elucidate some of these important questions regarding the
intrinsic nature and acquisition process of leaf swallowing behavior, we conducted a study on a sociallyliving group of captive chimpanzees.

Chimpanzees as young as 1 year of age closely watch
this behavior and have been seen to attempt immediately
thereafter to perform it on their own with varied success,regardless of health condition (Huﬀman and Seifu 1989;
Huﬀman and Wrangham 1994). At this stage, it is most
likely treated as one more element of the mother’s foraging repertoire that engages the infant’s interest.
We do not expect that the behavior is ﬁrst acquired
because of any understanding of its self-medicative
function, rather, that the self-medicative aspects of use
are likely to be learned over time if the appropriate
selective forces (e.g. parasite infection) are present in the
habitat in question. A combination of learning thecontext of use from watching others and positive feedback from any perceived personal relief from physicaldiscomfort that leaf swallowing may assist in providing
the ingestor is predicted to occur. Presently, the detailsof this underlying mechanism and how long it takes toacquire the behavior in its self-medicative context is
unclear. It is extremely diﬃcult to collect such evidence
from the ﬁeld given that these traditions appear to bealready well established in all groups where leaf swallowing is known to occur (Huﬀman 2001). Furthermore,as the behavior itself occurs at low frequencies in thewild due to strong seasonality linked with periods ofparasite reinfection (Huﬀman et al. 1996; Huﬀman
1997), the acquisition process of the behavior by new
individuals is diﬃcult to follow precisely under natural
conditions.
There is a range of possibilities for how leaf swallowing behavior started and how individuals come toswallow leaves instead of simply chewing them. At one
extreme, animals may have an innate tendency to selectappropriate properties in plants when ill, so that the roleof social context is local enhancement. That is, naive
individuals may have their attention drawn to areas withplant species used by others (Huﬀman and Wrangham
1994). At the other extreme, animals may have a propensity to swallow certain items without chewing, but
due to unfamiliarity with rough bristly leaves in their
daily diet, must somehow learn that such leaves can beingested before they are able to learn about any possible
beneﬁt from doing so. Thus, initial acquisition by youngor naive individuals, like the proposed origin of thisbehavior itself, may occur in the context of opportunistic
Table 1 Leaf swallowing test
subjects at the Primate
Research Institute (PRI)a

Age at the time of experimentsin October 1997b
Artiﬁcial insemination, handrearedMethods
The study was conducted between 9 October and 11 November
1997 on a group of 11 (3 males, 8 females) adult chimpanzees usedin cognitive studies at Kyoto University’s Primate Research Institute in Inuyama, Japan (Table 1). Among the 6 individuals born inAfrica, all but 2 of the oldest (Gon, Puchi) were brought into
captivity and reared from the age of 1 year. The remaining 5
individuals were captive born and or human reared in Japan orEurope. The veterinary staﬀ routinely examines the chimpanzees.
None of the subjects displayed symptoms of parasite infection
during the study period.
From 1996 up to the time this study was conducted in 1997, thechimpanzees had daily access to an environmentally enriched
outdoor enclosure containing 63 species (390 individual plants) oftrees and shrubs, a ﬂowing stream, and an 8-m-high multi-tiered
tower (Ochiai and Matsuzawa 1998, 1999). Prior to the experiments
described below, their exposure to plants in the outdoor compound
was limited to these 63 known species and a few local grass species
that spontaneously took root. None of the plants in the compound
resembled the texture of plants used for leaf swallowing by chimpanzees in the wild.
The test plant species used in this study, Helianthus tuberosus(Compositae), was selected because the leaves are virtually identicalin texture to species such as Aspilia mossambicensis, Lippia plicata,and Ficus exasperata used by chimpanzees at Mahale, Gombe, andelsewhere. No member of the study group had been exposed to thisor other species resembling it in leaf texture prior to testing. H.
tuberosus grows semi-wild between June and November alongroadsides, in open lots, and in some gardens in the neighborhood of
the Institute. Fresh branches were collected within 20 min prior to
testing and placed in water to maintain their freshness. Native to
North America, H. tuberosus is a nontoxic plant whose leaf andstem are often used as cattle fodder. Introduced to Japan over
100 years ago, the tubers are a delicacy consumed by people insome rural areas of the country. The plant is known as ‘‘kiku imo’’in Japanese and ‘‘earth apple’’ in English.
In total, 36 trial sessions were conducted on the chimpanzee
colony, with a minimum of 3 sessions per individual. A branch of
29–40 cm in length with 18–40 leaves and occasionally 1–8 ﬂowers
was given to an individual, selected randomly over the study period. It was possible to call an individual chimpanzee to the wall of
the enclosure and drop a branch down to it from the observation

Name

Sex

Agea

Arrived at PRI(age at arrival)

Origin (date of birth)

Gon
Puchi
Reiko
Mari
Akira
Ai
Pendesa
Chloe
Popo
Reo
Pan

M
F
F
F
M
F
F
F
F
M
F

31
31
31
21
21
21
20
16
15
15
13

30.1.79 (12)30.1.79 (12)3.7.68 (1.6)
30.1.78 (1.5)
30.1.78 (1.5)
10.11.77 (1)12.11.79 (2.7)
28.1.85 (5)West Africa, pet in Japan (1966, month unknown)
West Africa, pet in Japan (1966, month unknown)
West Africa (December 1966)
West Africa (June 1976)
West Africa (June 1976)
West Africa (October 1976)
Japan Monkey Centre (2 February 1977)
Paris Zoo (13 December 1980)
PRIb (7 March 1982) daughter of Puchi–Gon
PRIb (18 May 1982) son of Reiko–Gon
PRIb (7 December 1983) daughter of Puchi–Gon

81

115
To independently verify our assessment of leaf swallowing in
the trial sessions, individuals were separated from the rest of thegroup when they were brought inside for the night and put singly
into a night sleeping room when day-to-day management andongoing research protocol allowed. The following morning, after
these individuals were rejoined with the group, feces in their
sleeping rooms were inspected.

point. Normally tests were conducted on individuals in a socialgroup setting in the outdoor enclosure (n=28) with all or mostmembers present. Three test sessions, however, were conductedwith a sub-group of 3 individuals in a smaller holding room; oneplant was introduced and the 3 interacted consecutively with thesame plant. During the entire study period, adult male Reo was
kept in a separate enclosure from the main group during the day,with occasional access to his mother or other female companions.
During testing Reo was always alone in all 3 of his trial sessions.
Due to the physical separation of his enclosure from the main
outdoor enclosure, Reo had no opportunity to see other individuals
during their sessions and vice versa. The old adult male Gon andadult female Pan were also tested alone on one occasion each.
None of the subjects had access to the test plant species outside ofthese trial sessions.
Observations were recorded by the authors using 8-mm video
and by handwritten notes. All feeding behaviors and behavioral
interactions between the focal animal and others in the groupwere recorded. To obtain complete behavioral sequences of a
subject’s response to the plant material and interactions withothers, observations were continued for 5 min after the focal
individual no longer possessed test plant material. There was nostealing or disruption by others while the plant was in the possession of the focal subject. Because it was impossible to retrieve aplant from the enclosure if it was abandoned or retrieved byanother, the behavior of the new possessor and interactions withall others was recorded as a new trial session. In eight cases, an
onlooker picked up all of the remaining plant material after theoriginal focal subject freely discarded it. Because of this, no plantmaterial was left in the enclosure after the end of the ﬁnal trial
session of any given day.

Results
Veriﬁcation of leaf swallowing behavior
Folding and swallowing of leaves became the major
mode of ingestion for 6 of the 11 individuals at somepoint during the study (Fig. 1). The behavior was similar
to that observed for chimpanzees in the wild (LS-Wild
ESM1, LS-Chloe ESM2), supporting the notion of a
species-wide propensity to perform this behavior inchimpanzees. Leaves were deliberately folded, using a
combination of lips, palate, and tongue, while a leaf still
attached to the stalk was slowly drawn into the mouth.
The behavior was distinct from normal feeding as
chewing action was overtly absent and the leaves weredeliberately put into the mouth one at a time. Of those 6
individuals that leaf swallowed, there was no signiﬁcantdiﬀerence in the number of African born (3/6) versus
captive born (3/5) subjects (Fisher’s exact test, twotailed, P=1.000, NS) to exhibit this behavior.
Results of the 11 next-morning follow-up dung
inspections are presented in Table 2. All individuals
selected for the follow-up inspections were observed

Fig. 1 Observed responses of chimpanzees in trial sessions withnovel plant stimuli (Helianthus tuberoses L.). Solid lines connecting
boxes denote putative social learning network between Chloe (leafswallowing ‘‘demonstrator’’) and individuals that ﬁrst displayed
leaf swallowing behavior in subsequent trial sessions

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Table 2 Results of dung
inspection the day after
individual observation sessions.
Underlined subjects wereobserved to swallow leaves
during the trial session

Date

Subject

Parts ingested the previous day

Contents of dung

10 October
14 October
15 October
16 October
18 October
18 October
22 October
22 October
23 October
24 October
24 October

Puchi
Chloe
Reiko
Chloe
Puchi
Mari
Pan
Puchi
Reiko
Mari
Reiko

Stalk, ﬂowers
Leaves, ﬂowers
Leaves, ﬂowers
Leaves, ﬂowers
Stalk, leaves, ﬂowers
Flowers, leaves
Stalk, leaves
Stalk bark, leaves, ﬂowers
Stalk bark, leaves, ﬂowers
Stalk, leaves
Stalk, leaves

No leaf trace
3 folded leaves
No leaf trace
10 leaves
2 leaf fragments
No trace
1 leafNo leaf trace
6 leaves
No leaf trace
6 leaves

swallowing during her 1st and 2nd trial sessions. This
group of females also approached and closely inspected
one another when leaves and other parts were being
eaten (Fig. 1), showing their mutually tolerant social
relationships. With the exception of Popo, these females
all subsequently exhibited leaf swallowing behavior
themselves for the ﬁrst time 2–9 days after having observed Chloe perform leaf swallowing behavior. During
this study, Chloe was the ﬁrst and only possible model ofleaf swallowing for these four females (Fig. 1). Chloe
approached closely and intently watched the ﬁrst instance of leaf swallowing exhibited by Reiko and Pan.
Due to other ongoing research Ai and Pendesa were
frequently absent when group-setting test sessions wereconducted in the outdoor enclosures. During ten sessions outdoors in which leaf swallowing was observed,
Ai was absent during seven and Pendesa during six
sessions. Akira, Gon, Ai, and Pendesa were never observed to approach and inspect the feeding behavior ofothers in the possession of H. tuberosus, whether they
were leaf swallowing or chewing leaves or other parts ofthe plant. These four individuals consistently rejected H.
tuberosus in all of their test sessions.

to have ingested some or all parts of the plant during thetest session in question. Eight of these cases were ofindividuals directly observed to exhibit leaf-swallowinglike behavior during the session. The following morning,in 6 of these 8 cases, dung was found to contain one tosix folded, nondigested H. tuberosus leaves. No whole orpartial undigested leaves were found in the 3 cases inwhich individuals were only observed to chew leaves andor other plant parts.
Individuals’ ﬁrst response to rough hispid leaves
The ﬁrst response to the leaves varied from individual toindividual. Chloe and Reo, two captive-born individuals, spontaneously displayed leaf-swallowing-likebehavior in their ﬁrst session without the beneﬁt ofobserving it in other group members. Chloe consistently
displayed this pattern as her major mode of ingestion
during all three of her test sessions. Mari also folded andswallowed a portion of the leaves on the branch given toher on her ﬁrst (and second) session. She did so after
having closely observed Chloe fold and swallow leaves
4 days earlier (Fig. 1).
The typical ﬁrst response to the plant for six otherindividuals was an almost phobic rejection of the roughhispid leaves (Akira, Pendesa, Ai, Gon, Puchi, and Pan).
Four of these individuals consistently rejected the entire
plant throughout the study, while the other two discarded all of the leaves but ate other plant parts (Pan,Puchi). In contrast, two other individuals, (Reiko andPopo) chewed and ate the leaves in their ﬁrst trial session. Popo continued to chew and eat leaves in all of her
subsequent sessions. She displayed no aversion whatsoever, rapidly consuming everything (Fig. 1).

Discussion
Possible modes of acquisition and the originof leaf swallowing
This is the ﬁrst ever attempt to investigate leaf swallowing under semi-controlled conditions. Bearing in
mind the limited sample size and management restraints
on observational procedure, some basic aspects of thenature of leaf swallowing and insights into the possiblemodes of acquisition of this behavior by chimpanzees
can be considered. The spontaneous performance of leaf
swallowing by two individuals during their ﬁrst trial, in
the absence of a leaf swallowing ‘‘demonstrator,’’ showsthat chimpanzees may have a propensity to fold andswallow rough hispid leaves. This supports evidence
from the wild that the behavior can emerge without inter-group social contact in geographically isolated populations or subspecies (sec. Huﬀman and Hirata 2003).
However, unlike their counterparts in the wild that often
exhibit this behavior when ill and/or infected with

Leaf swallowing and social interactions
among individuals during the trial session
Leaf swallowing was observed in 10 of the 31 trial sessions conducted in a group setting. Individuals in possession of H. tuberosus attracted the attention of othersin 5 of these sessions (Fig. 1). Puchi, Mari, Reiko, Pan,and Popo approached within close proximity (<1 m) to,and intently inspected, Chloe while she exhibited leaf

83

117

propensity for folding and swallowing of rough hispid
leaves is expected to be a shared trait of all African great
apes. It follows then that the self-medicative function ofleaf swallowing behavior must be a secondary adaptationof a feeding response brought about by leaf texture,raising the question as to how the self-medicative context
of leaf swallowing emerged independently across Africa.
Further reﬁned, noninvasive testing of captive chimpanzee groups naive to rough hispid leaves is being
planned. Similar controlled and noninvasive studies
regarding the acquisition process of leaf swallowing andother self-medication in the African great apes and otherprimates is strongly encouraged. Greater attention
should be paid to the social networks of group individuals to grasp greater detail of the possible mode(s) ofsocial learning involved in the transmission of such
behaviors within the group (e.g. White and Burgman
1990; Ginsberg and Young 1992; Coussi-Korbel andFragaszy 1995; Whitehead 1997). Such studies are expected to increase our understanding of the possible
origins of self-medicative behaviors and the role social
learning may play in their maintenance in nature.

parasites (Wrangham 1995; Huﬀman et al. 1996), these
captive individuals were parasite free and showed novisible signs of ill health when they performed the
behavior. From this we conclude that folding andswallowing of leaves is not an innate response to parasite
infection. Indeed, the initial response for more than halfof the subjects was a phobic avoidance of these leaves orthe entire plant. Our results support the current
hypothesis regarding the origin of leaf swallowing
behavior (Huﬀman and Wrangham 1994), which proposes it may have originated in the feeding context of anovel plant item. It is suggested here that the leaf’srough hispid texture encourages the peculiar mode ofingestion, that is, folding and swallowing leaves whole.
Our results also support observations in the wild thatthe acquisition and spread of leaf swallowing within agroup is at least in part socially inﬂuenced, rather thanbeing solely the product of individual trial-and-error
learning. It is clear that the behavior was not acquiredby every individual in this study via the same mode oflearning. Excluding Chloe and Reo, who seemingly acquired leaf swallowing behavior spontaneously, theother individuals that later exhibited the behavior may
indeed have used multiple modes of learning over theperiod of acquisition (sec. Visalberghi and Fragaszy1990). Among the individuals that eventually exhibitedthe behavior during our study, social tolerance among
them in the feeding context (sec. van Schaik et al. 1999)
is considered to have been an important facilitator of
exposure to leaf swallowing, and thus opportunities forsocial learning. As suggested for object manipulation in
Japanese macaques (Huﬀman and Quiatt 1986) andforaging-related tool-use acquisition in orangutans (vanSchaik 2003), here too, interpersonal social networks
and social tolerance could be important factors in thetransmission of leaf swallowing behavior. This is further
supported by the fact that those individuals that neverapproached and observed another chimpanzee leaf
swallowing never overcame their phobia of the plant’srough, hispid leaves. All individuals that eventuallyexhibited leaf swallowing behavior did so only after
having seen the behavior being exhibited by Chloe, theﬁrst individual in the social group observed to display
folding and swallowing of H. tuberosus leaves spontaneously.

Acknowledgements We wish to give our sincere thanks to Testuro
Matsuzawa, Professor of the Section of Language and Intelligence(PRI) and Professor Iver Iversen of Northern Florida State University, for their encouragement and support in conducting thisstudy. We are indebted to the primate health care staﬀ of theCenter for Human Evolution Modeling Research for their assistance and day-to-day care of the chimpanzees. The present research
was partially ﬁnanced by Grants 07102010, 12301006, and
10CE2005 from the Ministry of Education, Science, Sports, andCulture, Japan. We thank our anonymous referees and Jean-Baptiste Leca for their insightful comments and criticisms of themanuscript in its ﬁnal stages. Last but not least, we thank the
chimpanzees for their patience and cooperation, without which thisstudy would not have been possible.

References
Coussi-Korbel S, Fragaszy DM (1995) On the relationship betweensocial dynamics and social learning. Anim Behav 50:1441–1453
Ginsberg JR, Young TP (1992) Measuring association between
individuals or groups in behavioural studies. Anim Behav
44:377–379
Huﬀman MA (1997) Current evidence for self-medication in primates: a multidisciplinary perspective. Yearb Phys Anthropol
40:171–200
Huﬀman MA (2001) Self-medicative behavior in the African great
apes: an evolutionary perspective into the origins of human
traditional medicine. BioScience 51:651–661
Huﬀman MA, Caton JM (2001) Self-induced increase of gut
motility and the control of parasitic infections in wild chimpanzees. Int J Primatol 22:329–346
Huﬀman MA, Hirata S (2003) Biological and ecological foundations of primate behavioral traditions. In: Fragaszy DM, Perry
S (eds) The biology of tradition: models and evidence. Cambridge University Press, Cambridge, pp 267–296
Huﬀman MA, Quiatt D (1986) Stone handling by Japanese macaques (Macaca fuscata): implications for tool use of stone.
Primates 27:413–423
Huﬀman MA, Seifu M (1989) Observations on the illness andconsumption of a medicinal plant Vernonia amygdalina by awild chimpanzee in the Mahale Mountains, Tanzania. Primates
30:51–63

Future studies
Controlled studies of self-medicative behavior in parasitized organisms are rare and limited to mice (Vitazkova
et al. 2001) and invertebrates (Karban and English-Loeb1997). There are obvious ethical reasons why we chose
not to conduct a controlled study on chimpanzees in thecontext of parasite infection. We have shown here that
there are important things to be learned without suchinvasive methods. Given the fact that bonobos andlowland gorillas too are known to habitually exhibit leaf
swallowing behavior in the wild (Huﬀman 1997), the

84

118
Perry S (eds) The biology of tradition: models and evidence.
University of Cambridge Press, Cambridge, pp 297–328
Schaik CP van, Deaner RO, Merrill MY (1999) The conditions fortool use in primates: implications for the evolution of material
culture. J Hum Evol 36:719–741
Visalberghi E, Fragaszy DM (1990) Food washing behaviour intufted capuchin monkeys, Cebus apella, and crab eating macaques, Macaca fuscicularis. Anim Behav 40:829–836
Vitazkova SK, Long E, Paul A, Glendinning JI (2001) Mice suppress malaria infection by sampling ‘bitter’ chemotherapy
agent. Anim Behav 61:887–894
White FJ, Burgman MA (1990) Social organization of the pygmy
chimpanzee (Pan paniscus): multivariate analysis of intracommunity associations. Am J Phys Anthropol 83:193–201
Whitehead H (1997) Analysing animal social structure. Animal
Behav 53:1053–1067
Wrangham RW (1995) Relationship between chimpanzee leaf
swallowing to a tapeworm infection. Am J Primatol 37:297–303
Wrangham RW, Nishida T (1983) Aspilia spp. leaves: a puzzle in
the feeding behavior of wild chimpanzees. Primates 24:276–282

Huﬀman MA, Wrangham RW (1994) Diversity of medicinal plant
use by chimpanzees in the wild. In: Wrangham RW, McGrew
WC, deWaal FB, Heltne PG (eds) Chimpanzee cultures. Harvard University Press, Cambridge, Mass., pp 129–148
Huﬀman MA, Page JE, Sukhdeo MVK, Gotoh S, Kalunde MS,
Chandrasiri T, Towers GHN (1996) Leaf-swallowing by
chimpanzees: a behavioral adaptation for the control of strongyle nematode infections. Int J Primatol 72:475–503
Karban R, English-Loeb G (1997) Tachinid parasitoids aﬀect hostplant choice by caterpillars to increase caterpillar survival.
Ecology 78:603–611
Ochiai T, Matsuzawa T (1998) Planting trees in an outdoor compound of chimpanzees for an enriched environment. In: Hare
VL, Worley KE (eds) Proceedings of the third international
conference on environmental enrichment. The Shape ofEnrichment, San Diego, Calif., pp 355–364
Ochiai T, Matsuzawa T (1999) Environmental enrichment for
captive chimpanzees (Pan troglodytes): introduction of climbing
frames 15 m high. Primate Res 15:289–296
Schaik CP van (2003) Local traditions in orangutan and chimpanzees: social learning and social tolerance. In: Fragaszy DM,

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American Journal of Primatology 69:821–828 (2007)

BRIEF REPORTA New Case of Fish-Eating in Japanese Macaques:
Implications for Social Constraints on the Diffusionof Feeding Innovation
JEAN-BAPTISTE LECA1, NOËLLE GUNST2, KUNIO WATANABE3,
4
AND MICHAEL A. HUFFMAN
1
Equipe d’Ethologie des Primates, Institut Pluridisciplinaire Hubert Curier,Department Ecologie, Physiologie et Ethologie, Strasbourg, France
2
Institute of Ecology, University of Georgia, Athens, Georgia, USA
3
Field Research Center, Primate Research Institute, Kyoto University, Japan
4
Section of Ecology, Primate Research Institute, Kyoto University, Japan

This is the first detailed report of social factors affecting fish-eating inJapanese macaques under natural circumstances. We video-recorded acomplete event of fish eating, involving a new fish food species for themonkeys on Koshima island. Following the discovery of a large beachedsea bass by a peripheral male, we observed a total of 16 individuals
feeding on the fish in turns, and interacting around it. The rank order ofaccess to the fish was mainly explained by the spatial position of groupmembers, whereas dominance determined how long the fish wasmonopolized. Although limited, the tolerated presence of close-bystanders while feeding was affected by kinship and affiliation. Genealogic datasuggested that fish-eating behavior was well maintained in termsof maternal lineages. This report should contribute to a better understanding of how social features may constrain the long-term diffusionof feeding innovations in free-ranging primate groups. Am. J. Primatol.
69:821–828, 2007. c 2007 Wiley-Liss, Inc.
Key words: fish-eating; feeding tradition; behavioral diffusion; Macaca
fuscata
INTRODUCTION
On Koshima island, the first case of fish-eating by a Japanese macaque wasrecorded in 1979. By 1986, this new feeding habit had spread to 75% of the group,
seemingly from older to younger individuals [Watanabe, 1989]. On the basis of a
relatively small data set (six sample points over a 7-year period), mathematicalmodels suggested that fish-eating at Koshima island was a socially transmitted
behavioral tradition [Lefebvre, 1995]. It is critical to know the history of aContract grant sponsor: Lavoisier Grant, Ministère des Affaires Etrangères, France; Contract grantsponsor: National Science Foundation grant; Contract grant number: BCS-0352035.
Correspondence to: Jean-Baptiste Leca, 2360 West Broad Street, The Park on West Broad,Apt ] 321, Athens, GA 30606. E-mail: jbtleca@yahoo.com
Received 11 June 2006; revision accepted 14 September 2006
DOI 10.1002/ajp.20401
Published online 25 January 2007 in Wiley InterScience (www.interscience.wiley.com).

r 2007 Wiley-Liss, Inc.
86

822 / Leca et al.

behavioral innovation to assess how social learning processes may contribute toits diffusion within a group [Visalberghi & Fragaszy, 1990]. However, casesof behavioral innovation and diffusion have rarely been observed and specifically
documented in free-ranging primate populations [Huffman & Hirata, 2003]. In
several decades of regular observations on Koshima island, fish-eating by
Japanese macaques was only observed six times. The first two observations weremade by chance during routine work, and therefore were not described in detail[Watanabe, 1989]. The next four records of fish-eating did not occur undernatural conditions. Most macaques observed feeding on small fish (sardines) wereactually given this food by humans once a year [Watanabe, 1989]. Moreover, little
is known about the influence of sociodemographic variables (such as kinship,
dominance, and affiliative relationships) on the likelihood of learning andadopting innovative behaviors [Huffman & Hirata, 2003]. More quantitative
data, taking into account the social context of diffusion of feeding innovations, areneeded to obtain a deeper understanding of the cultural transmission processes[Lefebvre, 1995].
The goal of this report is threefold: (1) to provide a detailed descriptive
account (in terms of social status and relationships of the individuals involved) ofa seldom observed event of fish-eating at Koshima island, under natural
conditions; (2) to examine the social conditions, at least partially reconstructed,
under which feeding innovation and its subsequent propagation may occur inJapanese macaques; and (3) to assess the generalization, long-term diffusion,and maintenance of the fish-eating habit in Koshima monkeys by providing a
genealogy [after Watanabe, 1989] of lineages of fish eaters recorded on the island
to date.
METHODS
The observations took place at Koshima island, Japan. Figure 1 shows
genealogic information about the two groups of Japanese macaques living on theisland (main and Maki branch groups). Although the habitat of the island
provides them with various kinds of natural foods (including leaves, fruit, andsmall invertebrates), the monkeys are provisioned twice a week with 4 kg of wheat
grains by the staff technicians of the Koshima Field Station, Kyoto University. In
January and February 2004, two observers (JBL and NG) used video-recorded
focal-animal sampling and ad libitum recording of avoidance and aggressiveinteractions [Altmann, 1974]. On the day of the fish-eating event, the observation
procedure was altered to collect specific information about the identity andbehaviors of the individuals present around the fish. The first observer used focalplace sampling, with continuous video recording focused on the fish and the close
vicinity (within 3 m). The entire sequence of events was filmed from start (whenthe first monkey discovered the fish) to finish (when the last monkey discarded
the remains of the eaten fish). The second observer used a tape recorder to collect
all occurrences of changes in position and aggressive interactions involving all
individuals present within a radius of 1, 3, 5, and 10 m around the fish. Visibility
was excellent. The observers could stand on the beach within 3–10 m of thesampled monkeys.
We defined a foraging bout as the period of time during which an individual
exhibited an investigative or processing behavior directed to the fish (including
sniff, touch, probe into the fish, and remove scales with hand). We distinguishedthe durations of the activities of foraging and feeding (bite into and ingest) on thefish. A monkey sitting within 10 m around the fish for at least 0.5 min, and

Am. J. Primatol. DOI 10.1002/ajp

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Fish-Eating in Japanese Macaques / 823
Birth yr
1980
1981
1982
1983
1984
1985
1986
1987
1988
1989
1990
1991
1992
1993
1994
1995
1996
1997
1998
1999
2000
2001
2002
2003

Fig. 1. Distribution of the individuals observed feeding on the sea bass according to age, sex,
matrilineages, and group membership. Fish eaters in 2004 (framed) are labeled by their names. y,
Individuals observed to eat fish between 1980 and 1985; bold line, matrilineage of fish eaters before
1980; and dotted line: matrilineage of non-fish eaters before 1980 [after Watanabe, 1989]. Males:
regular font; females: bold font;. dead individual are engraved. Solitary individual; member ofthe Maki branch group; no asterisk: member of the main group.

intermittently watching the feeding animal was referred to as a bystander.
During the 2-month observation period, we recorded 704 avoidances andunidirectional aggressions. We ranked individuals in a dominance hierarchyand verified the linearity of the hierarchy (Matman, h0 5 0.23, Po0.001). We
categorized individuals into three classes according to dominance rank (high,middle, and low-ranking; N 5 18 for each dominance class) and two age classes(mature: over 5 year-old and immature: between 1 and 5 years).
RESULTSOn January 24, 2004 at 9:23 h, an adult male moving alone in the foremost
periphery of the main group, first arrived at Odomari beach, and discovered alarge dead fish (approximately 90 cm) recently beached on the sand. The fish wasan Asian temperate sea bass, Lateolabrax japonicus (Kanchi, personal communication). This species had never been recorded in the diet of Koshima monkeys
before. After inspecting the fish for a minute, the discoverer foraged and fed on it
for about 17 min, while being particularly vigilant toward possible newcomers. At
9:41 h the first-third of the main group, including the alpha male, arrived on thebeach. The discoverer left the beach, avoiding higher-ranking group members.
Most newly arrived individuals were already involved in an intense conflict anddid not notice the fish immediately. This allowed two females to forage and feedon the fish successively for the next 4 min, before being supplanted by the alphamale. For the next 3.5 hours, several individuals processed and/or ate the fish in

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88824 / Leca et al.

turns, surrounded by many bystanders. At 13:15 h, the last individual present on
the beach discarded the head of the fish and moved back to the forest. Except forsmall pieces of fins and scales scattered on the sand, every other part of the fish
was consumed by the monkeys. We recorded a total of 16 individuals processing
and eating the fish.
Each of the 16 individuals performed investigative foraging patterns (such as
sniff, touch, manipulate, and probe into) before starting to feed on the fish. Suchpatterns were significantly more frequent toward the fish than earthworms, anatural familiar food found in the habitat (sign test, n 5 16, 14 positive signs,
P 5 0.002).
SocioDemographic Features of the Individuals Involved in the Event
We report the group membership, age, sex, dominance class, and rank of the
fish eaters (Table I). We also report for each individual the rank order of first
access to the fish and the total durations of foraging and feeding activities. Amongthe 16 individuals observed processing and eating the fish, 15 were members ofthe main group and one was a solitary individual (the last eater in chronologicalorder). Fifteen individuals were mature and only one was an immature (with very
restricted access to the fish). Males spent significantly more time feeding on thefish than females (Mann–Whitney U-test: n1 5 9, n2 5 7, medians 5 11.6 and1.2 min, respectively; U 5 6.0, P 5 0.005).
We tested the effect of dominance on the capability to monopolize the fish. We
found a significant difference in the duration of foraging bouts among the high,middle, and low-ranking individuals present on the beach (Kruskal–Wallis H-test:nhigh 5 16, nmiddle 5 nlow 5 17, mean7SD 5 13.3717.3, 0.471.6, and 0.270.7 min,respectively, H 5 18.2, Po0.001). Multiple paired comparisons among meanranks showed that high-ranking individuals spent much more time foraging on
the fish than individuals belonging to the two other dominance classes (Po0.05).
We found a significant positive correlation between the duration of foraging bouts
and the dominance rank of the fish eaters (Spearman rank correlation coefficient
test: N 5 16, R 5 0.815, Po0.001). However, there was no significant correlation
between the hierarchical rank of the feeding animals and their rank order ofaccess to the fish (Spearman rank correlation coefficient test: N 5 16, R 5 0.238,
P 5 0.374).
Among the 64 monkeys observed on the beach at the time of the event, werecorded the presence of 42 bystanders (including 14 of the 16 fish eaters). Thismeans that 34% of the individuals present on the beach were not bystanders. Outof the 42 bystanders, 41 individuals were members of the main group, and one
individual was a solitary adult male. Among these 41 bystanders, there werefewer immature than mature individuals (14 and 27 monkeys, respectively), butwhen considering close bystanders (within 3 m), we found that immatures sat andwatched much longer than mature individuals (mean7SD 5 15.8716.2 and4.979.3 min, nimmat. 5 13, nmat. 5 18, Student’s t-test: t 5 2.190, df 5 29,
Po0.025). On average, there were two times fewer bystanders within 3 m than
within 5–10 m of the feeding animal (mean number of bystanders per
minute 5 2.273.0 and 4.474.3, respectively, Student’s t-test: t 5 1.709,
df 5 30, Po0.05), but contrasting differences appeared according to the identityof particular fish eaters (Table I). We never recorded the presence of a bystanderranking higher than the current fish eater.
Out of the 42 bystanders, only three immature individuals were observed
sitting in body contact with the feeding animal and touching the fish for short

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a

Main
Main
Main
Main
Main
Main
Main
Main
Main
Main
Main
Main
Main
Main
Main
Solitary

Iwana
Kinu
ChiikuHotate
Yuda
Usu
Hokke
Zuaka
Chigaya
Kame
Ponii
Momi
Kitsune
Zumi
PiimanYago
Total

For the first foraging bout only.

8
6
13
15
19
3
17
18
19
10
19
18
8
16
17
10

Group Age (yr)Individualname

Dominanceclass (rank)

MaleHigh ranking (12)Female Low ranking (51)Female High ranking (14)MaleHigh ranking (1)MaleHigh ranking (3)Female Low ranking (44)MaleHigh ranking (2)MaleHigh ranking (5)Female High ranking (11)MaleHigh ranking (8)MaleHigh ranking (4)Female High ranking (13)MaleMiddle ranking (29)
Female Low ranking (46)
Female Middle ranking (25)MaleHigh ranking (15)

Sex
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16

41.2
3.4
0.2
50.9
14.2
0.2
47.7
11.4
17.3
8.0
11.1
2.5
6.6
0.1
1.2
10.9
226.8

Total
foraging
Access ordera
29.9
2.3
0.2
50.4
13.9
0.2
34.8
10.5
16.5
8.0
11.6
2.0
6.5
1.0
1.2
10.6
199.4

0.470.5
0.070.0
0.07–
0.971.2
7.072.4
0.07–
1.771.1
6.071.3
9.471.6
1.070.00.870.6
5.070.0
0.070.0
1.07–
0.07–
0.070.0
2.273.0

Total
feeding Mean no. bystanders
duration
duration (min)(min)
within 3 m/min

0.370.6
0.070.0
1.07–
7.972.9
5.871.5
0.07–
6.675.0
5.773.8
6.670.5
0.070.0
2.970.5
0.070.0
0.070.0
0.07–
0.07–
0.070.0
4.474.3

Mean no. bystanders
within 5–10 m/min

TABLE I. Socio-Demographic Information about the Fish Eaters Ranked in Chronological Order of Access to the Fish,
Total Duration of Foraging and Feeding Activities, and Mean Number of Bystanders per minute According to the Distancefrom the Feeding Animal

Fish-Eating in Japanese Macaques / 825

Am. J. Primatol. DOI 10.1002/ajp

826 / Leca et al.

periods of time. The alpha female was contacted by her offspring for 3.8 min. The
third-ranked male was contacted by two young siblings (for 1.9 and 0.5 min,respectively) with whom he spent 71.1% of his social activity budget (127.7 min
interacting positively with the two siblings out of 179.6 min of total positive social
interactions). We never observed two or more individuals feeding together on thefish. We recorded one single event of food theft: a 16-year-old female grabbed a bitof fin from her 18-year-old sibling. We recorded a total of 69 aggressiveinteractions occurring within 10 m of the fish (17.9 aggressive interactions/hr).
As a comparison, we found a rate of aggression six times less (3.2 aggressiveinteractions/hr) during our daily observations in other feeding and non-feedingbaseline contexts. Out of the 69 aggressions, 44 involved bystanders only.
Maintenance of Fish-Eating Behavior by Lineage
The 16 fish eaters belonged to eight separate lineages. To trace themaintenance of fish-eating behavior in Koshima monkeys, we added the current
observations to Watanabe’s [1989] genealogy of fish-eating individuals (Fig. 1).
We found that 15 out of 16 monkeys confirmed to eat fish in 2004 belonged tomatrilineages of fish eaters recorded before 1986. Out of the six matrilineages of
non-fish eaters before 1980, five lineages still had no fish eaters in 2004.
DISCUSSION
To some extent, our observations allowed us to reconstruct some elements ofthe social contexts underlying the appearance, diffusion, and maintenance of the
fish-eating tradition in Japanese macaques living on Koshima island. We showedthat the monkeys treated the fish like a novel food rather than like a familiar food.
The investigative behaviors performed are reminiscent of food neophobia foundin macaques [Johnson, 2000]. The social status of the discoverer of the fish (ayoung adult male traveling in the periphery of the group) was consistent withearly observations of fish-eating at Koshima [Watanabe, 1989]. In some primate
species, peripheral individuals were more frequent innovators than central groupmembers [Kummer & Goodall, 1985]. Living on the outskirts of the group is likely
to make novel food sources more accessible to individuals whose social status
would not allow access if they were in a more central position [Di Bitetti &Janson, 2001]. This could account for the lack of correlation we found between
the rank order of access to the fish and dominance rank of the fish eaters. Whenfood location is unpredictable and group cohesion is relatively low [Mori, 1977],
food discovery may be better explained by the spatial position of group members
than by their social ranks.
After most group members arrived on the beach, we found that the capability
to monopolize and feed on the fish, as well as the presence and interactions
around the fish were mainly explained by social factors. First, group membershipappeared to be a major factor accounting for the presence of bystanders aroundthe fish. We found that 94% of the fish eaters and 98% of the bystanders weremembers of the main group. Living in a social group allows individuals to gain
valuable information from observing others’ exploitation of novel foods [Di Bitetti& Janson, 2001]. Second, the fact that only a relatively small proportion (25%) of
the individuals present could get access to, monopolize, and feed on the fish was
mainly explained in terms of dominance. By limiting access to the fish, dominanceis likely to limit individual opportunities to learn from this novel food. In
dominance-structured groups, social status may constrain feeding innovation andits subsequent propagation. Dominance style in Japanese macaques is stricter

Am. J. Primatol. DOI 10.1002/ajp

91

Fish-Eating in Japanese Macaques / 827

than in other macaque species [Thierry, 2000]. In macaques and capuchins, oncea novel food or a familiar clumped food source is encountered by several groupmembers, social rank is likely to significantly affect food competition and foraging
success [Belisle & Chapais, 2001; Di Bitetti & Janson, 2001].
Third, we found that feeding competition around a highly prized clumped
food source can significantly increase the rate of aggression compared with thebaseline situation. The high risk of aggression and possible injury related to foodcompetition may be the reason why there were more far-bystanders than closebystanders and a third of the individuals present on the beach did not evenapproach within 10 m of the fish. Compared with food sources involved in other
newly acquired feeding habits in Japanese macaques (wheat eating, potatowashing: e.g., Itani & Nishimura, 1973), the fish had a unique feature as a novel
food (one large food item). Higher competition around the fish may affect thesocial conditions under which the fish-eating habit is maintained within thegroup. Fourth, although limited, the tolerated presence of body contact whilefeeding seemed to be affected by kinship, and to some extent, affiliation. Close andpeaceful proximity to a feeding individual, namely co-feeding [King, 1994], hasbeen proposed as a major factor in the transmission of feeding innovations
because it is assumed to enhance opportunities for social learning [Coussi-Korbel& Fragaszy, 1995]. Young primates tend to feed at the same time and on the same
food items as their mothers, and such synchronous feeding may influence thedevelopment of food selection or feeding habits [e.g., Ueno, 2005]. Belisle andChapais [2001] found that rates of tolerated co-feeding increased significantlywith degree of kinship in Japanese macaques. Since Japanese macaques show ahigh degree of kin bias or favoritism in most behaviors and interactions,compared with other macaque species [Chapais et al., 1997], it is not surprisingthat many innovative foraging behaviors were shown to diffuse widely within kin
lineages.
From our anecdotal observation, we could not reliably estimate the rate ofdiffusion of the fish-eating behavior. The difference in the proportion of fisheaters recorded in 1986 [75%: Watanabe, 1989] and during this event (25%) may
depend on the conditions of fish-eating in the two studies (several little fish
artificially given to the monkeys vs. one single big fish discovered under natural
circumstances). However, we provided valuable information about the maintenance of the fish-eating habit in Koshima monkeys. The addition of a new fish
species to the diet of Koshima macaques can be regarded as a generalization ofthis feeding tradition. The continuation of the genealogy of fish eaters suggested
that this behavior was well preserved in terms of maternal lineages. Whenpracticed only occasionally and by very few group members, some traditional
behaviors may tend to disappear [Huffman & Hirata, 2003]. Although theprevalence and strictness of dominance in Japanese macaques may constrain the
spread of the fish-eating habit to all age, sex, and dominance classes, the rareoccurrence of beached fish may be sufficient to maintain the behavior in the study
group.

ACKNOWLEDGMENTS
We thank the staff of the Koshima Field Station, Messrs. Kanchi and
Suzumura. JBL’s field work was supported by a Lavoisier Grant, Ministère desAffaires Etrangères, France. NG was supported by a National Science Foundation
grant (BCS-0352035).

Am. J. Primatol. DOI 10.1002/ajp

92828 / Leca et al.

REFERENCES
Altmann J. 1974. Observational study of behaviour: Sampling methods. Behaviour 49:
227–265.
Belisle P, Chapais B. 2001. Tolerated co-feedingin relation to degree of kinship in Japanesemacaques. Behaviour 138:487–509.
Chapais B, Gauthier C, Prud’homme J, Vasey
P. 1997. Related threshold for nepotism
in Japanese macaques. Anim Behav 53:
1089–1101.
Coussi-Korbel S, Fragaszy DM. 1995. On therelation between social dynamics and social
learning. Anim Behav 50:1441–1453.
Di Bitetti MS, Janson CH. 2001. Social foraging
and the finders’ share in capuchin monkeys,
Cebus apella. Anim Behav 62:47–56.
Huffman MA, Hirata S. 2003. Biological andecological foundations of primate behavioral
tradition. In: Fragaszy D, Perry S, editors.
The biology of traditions: Models andevidence. Cambridge: Cambridge University
Press. p 267–296.
Itani J, Nishimura A. 1973. The study of infrahuman culture in Japan. In: Menzel E,
editor. Precultural primate behaviour. Karger: Basel. p 26–50.
Johnson E. 2000. Food-neophobia in semi-freeranging rhesus macaques: Effects of food
limitation and food source. Am J Primatol
50:25–35.

King BJ. 1994. The information continuum:
Evolution of social information transfer inmonkeys, apes, and hominids. Sante Fe,
NM: Sch Am Res Press.
Kummer H, Goodall J. 1985. Conditions ofinnovative behaviour in primates. Philos
Trans R Soc Lond B 308:203–214.
Lefebvre L. 1995. Culturally transmitted
feeding behaviour in primates: Evidence foraccelerating learning rates. Primates 36:
227–239.
Mori A. 1977. Intra-troop spacing mechanismof the wild Japanese monkeys of the
Koshima troop. Primates 18:331–357.
Thierry B. 2000. Covariation of conflict management patterns in macaque societies. In:
Aureli F, de Waal FBM, editors. Natural
conflict resolution. Berkeley: University ofCalifornia Press. p 106–128.
Ueno A. 2005. Development of co-feeding
behaviour in young wild Japanese macaques(Macaca fuscata). Inf Behav Dev 28:481–491.
Visalberghi E, Fragaszy DM. 1990. Foodwashing behaviour in tufted capuchin monkeys, Cebus apella, and crab eating macaques, Macaca fascicularis. Anim Behav 40:
829–836.
Watanabe K. 1989. Fish: A new addition to thediet of Koshima monkeys. Folia Primatol 52:
124–131.

Am. J. Primatol. DOI 10.1002/ajp

93

Japanese macaque cultures: Inter- and intra-troop
behavioural variability of stone handling patterns
across 10 troops

Jean-Baptiste Leca1,2) , Noëlle Gunst3) & Michael A. Huffman4)(1 Equipe d’Ethologie des Primates, Institut Pluridisciplinaire Hubert Curien, Département
Ecologie, Physiologie et Ethologie, UMR 7178 CNRS-ULP, Strasbourg, France; 3 Instituteof Ecology, University of Georgia, Athens, USA; 4 Section of Ecology, Primate ResearchInstitute, Kyoto University, Inuyama, Japan)(Accepted: 26 January 2007)

Summary
Stone handling (SH), a form of solitary object play, consists of an individual manipulatingstones by performing various behavioural patterns. Previous findings from the Arashiyama
population of Japanese macaques suggested that SH is socially transmitted across generations
as a behavioural tradition. To further test the hypothesis that SH is a traditional behaviour inthis species, we present the most systematic inter-troop comparison of this behaviour froman investigation of nine troops of Macaca fuscata fuscata and one troop of M. f. yakui living
at six sites in Japan. We analyzed a total 1280 video-recorded SH bouts and charted therelative frequency of occurrence of 45 SH behavioural patterns across age classes. Many SH
patterns showed geographically patchy distributions and were referred to as local variantsor SH traditions. In terms of behavioural complexity, we found three levels of SH culture,each level being defined by troop-dependent clusters of SH traditions. We found a positive
correlation between geographic proximity and cultural similarity in SH between troops. To
explain similarities in the SH repertoires between the free-ranging troops living at the same
site, we discussed the phenomenon of cultural zones. We interpreted intra-group variability
in the performance of SH patterns from the viewpoint of developmental factors. We found nomajor difference between the two subspecies in the occurrence and form of SH.
Keywords: stone handling, local variants, behavioural tradition, behavioural predispositions,
Macaca fuscata.

2) Corresponding author’s e-mail address: jbtleca@yahoo.com© Koninklijke Brill NV, Leiden, 2007

Behaviour 144, 251-281
Also available online - www.brill.nl/beh

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Leca, Gunst & Huffman

Introduction
Charting intra- and inter-group behavioural diversity in non-human primatesprovides valuable empirical information to test predictions and fit models
generated from theories about the role of cultural processes in human evolution (van Schaik et al., 1999; Whiten et al., 2001). Most evidence for behavioural variability between and within wild primate populations comes fromfour genera: Cebus (capuchins), Macaca (macaques), Pongo (orang-utans)and Pan (chimpanzees). Long-term collaborative field studies focusing on
various types of behaviour or variants of the same behaviour, including interspecific interactions, communicatory, courtship, display, grooming, object
play and social play behaviours, feeding habits, food processing techniques,
medicinal plant use and tool use, have documented troop-specific behavioural patterns and substantial inter-troop behavioural variability at different
field sites in Costa Rica (Curu, Lomas Barbudal, Palo Verde, Santa Rosa:
white-faced capuchins; Chapman & Fedigan, 1990; Panger et al., 2002;
Perry et al., 2003a,b; Rose et al., 2003; O’Malley & Fedigan, 2005), Japan(Arashiyama, Katsuyama, Koshima, Takasakiyama, Yakushima: Japanesemacaques; Itani, 1958; Kawai, 1965; Itani & Nishimura, 1973; Huffman,
1984, 1996; Huffman & Quiatt, 1986; Watanabe, 1989; Suzuki et al., 1990;
Kawai et al., 1992; Nakamichi et al., 1998; Huffman & Hirata, 2003), Indonesia (Gunung Palung, Kutai, Ketambe, Suaq Balimbing, Lower Kinabatangan, Muara Singgersing, Tanjung Putting: orang-utans; van Schaik &Knott, 2001; van Schaik, 2003; van Schaik et al., 2003; Fox et al., 2004)
and different African countries (Assirik, Senegal, Bossou, Diécké and Seringbara, Guinea, Budongo and Kibale, Uganda, Campo, Cameroon, Gombeand Mahale, Tanzania, Lopé, Gabon, and Taï and Yealé, Côte d’Ivoire: chimpanzees; Boesch et al., 1994; Huffman & Wrangham, 1994; Wrangham etal., 1994; Matsuzawa & Yamakoshi, 1996; Sugiyama, 1998; Whiten et al.,1999, 2001; Humle & Matsuzawa, 2001, 2002; McGrew et al., 2001, 2003;
Yamakoshi, 2001; Nakamura & Nishida, 2006).
Within the same species, a given behaviour can be customary in some
populations and rare or even absent in others although it is ecologicallypossible. When enduring across generations and largely dependent on social means for their diffusion and maintenance, such behavioural differences
are referred to as cultural or traditional (McGrew, 1998; Fragaszy & Perry,2003). Following Whiten (2005), we define a ‘tradition’ as a local behavioural variant, showing different frequencies of occurrence across the study

95

Inter- and intra-troop variability of stone handling

253

sites, i.e., being customary or habitual in at least one site, but absent elsewhere. We define a ‘culture’ as a package of multiple related traditions, and‘cultures’ as distinctive arrays of clustered traditions.
By defining culture more broadly (‘the way we do things’), McGrew(2003) pointed out the need for a systematic examination of the similarities and differences in the behavioural patterns between wild populations ofprimates. The first step to study cultural variation in a species is to do comparative analyses focusing on the motor patterns of spontaneous behaviours(McGrew, 1998). Like ethnography in human social sciences, the ethnographic approach to cultural primatology consists of documenting patternsof geographic variation in primate behaviour (Wrangham et al., 1994). In
chimpanzees and Japanese macaques, various sets of (sub)species-typicalbehaviours were found to occur in several geographically isolated populations, but with some minor alterations in the form of the actions performed.
When such local variants are demonstrated to be long-lasting and transmitted over generations via social means, a cultural phenomenon can be inferred(Huffman & Hirata, 2003).
The ethnographic approach to primate traditions emphasizes the product(which differences are observed in the form of behaviours) rather than themechanisms (which specific processes are involved in producing such differences). Since little is known about the factors affecting the maintenance ofsocially learned behaviours in the wild, a controversy arose about the validity of animal traditions (Galef, 1996). However, like the powerful comparative method used in ethology, the advantage of the ethnographic approachis to be deeply rooted in what the animals actually do or do not do in thewild. Patterns in the presence or absence of behavioural variants in particular populations have been largely considered as defining features of primate
traditions. Although still debatable, there is now a general consensus on theoccurrence of traditions in monkeys and apes (Whiten et al., 1999; Fragaszy& Perry, 2003; Huffman & Hirata, 2003; Perry & Manson, 2003; McGrew,
2004).
Although behavioural diversity is a possible starting point in demonstrating the occurrence of culture, it is neither a necessary nor sufficient condition(McGrew, 2003). The ‘method of elimination’ is a multi-step decision procedure that may be used to assess whether a geographically variable behaviour
is or is not a tradition (van Schaik, 2003; see also Boesch, 1996). First a geographic distribution of clear troop-dependent clusters of behavioural variants

96

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Leca, Gunst & Huffman

must be demonstrated. Second, simple alternative explanations should beruled out. Although there is evidence for inter-site behavioural differencesamong different subspecies of chimpanzees (Boesch et al., 1994; Whiten etal., 1999) and different macaque species (Huffman, 2005; C. Nahallage, pers.
comm.; A. Zeller, pers. comm.), it is acknowledged that the effects of genetic
and ecological factors should be minimal for such behavioural variability to
be regarded as cultural. Third, the behaviour should meet a set of criteria,such as being customary or habitual within one age class of one troop, beingsocially transmitted within age structures or along matrilineages and persistent over a number of years. As more elements congruent with the concept oftradition are provided, the likelihood of alternative interpretations decreases(van Schaik, 2003). Accordingly, socially-mediated behavioural diversity at
the group, population, or subspecies level could be cultural (McGrew, 2003).
Japanese macaques (Macaca fuscata) are renowned for their behaviouralinnovations. In this species, the diffusion of various types of newly acquired
behaviours has been investigated, such as the consumption of novel foods(caramel-eating: Itani, 1958; Itani & Nishimura, 1973; wheat-eating: Kawai,
1965; fish-eating: Watanabe, 1989; Leca et al., in press), food-processing
techniques (potato- and wheat-washing: Kawai, 1965; Itani & Nishimura,
1973; Kawai et al., 1992; grass root-washing: Nakamichi et al., 1998) andplay behaviour (stone handling: Huffman, 1984, 1996; Huffman & Hirata,
2003; swimming: Kawai, 1965). Most reported behavioural innovations inprimates occur in the context of foraging, probably because information
about food is critical to every individual (Reader & Laland, 2001).
However, the best-documented case of a non-subsistence traditional activity in monkeys is stone handling (SH), a form of solitary object play consisting of the manipulation of stones by performing various behavioural patterns,
such as gathering stones into a pile, clacking stones together, or repeatedly
pounding a stone on a substrate (Huffman, 1984). Previous findings fromtwo populations of Japanese macaques at Arashiyama and Takasakiyama,
Japan suggest that SH is a traditional behaviour for these groups (Huffman,
1984, 1996; Huffman & Quiatt, 1986; Huffman & Hirata, 2003). The appearance, initial and long-term diffusion, context of occurrence and behavioural
diversity of SH have been documented at several points in time for over two
decades at Arashiyama. This behaviour appears to be socially transmitted
across generations (Huffman, 1984, 1996; Huffman & Quiatt, 1986).

97Inter- and intra-troop variability of stone handling255

A survey conducted at Takasakiyama in 1989 has revealed striking similarities in the SH repertoire and the frequency of occurrence of SH behavioural patterns of the two troops. Out of the 17 behavioural patterns recorded
at Arashiyama, 16 were also observed at Takasakiyama, and at similar frequencies (Huffman, 1996; Huffman & Hirata, 2003). These first comparative
data showed no evidence for SH local variants (defined as SH patterns thatshow geographically patchy distribution) and were not consistent with intertroop variability in the form of SH. The SH patterns shared by both troops
included collecting, rubbing and percussive actions with stones. This suggests that such behaviours are Japanese macaque universals, i.e., they arepart and parcel of the common behavioural repertoire of the species (Huffman & Hirata, 2003). In both troops, age appeared to affect the diversity andtype of SH patterns displayed. As they grew older, individuals tended to perform less varied and more simple patterns, such as gather, scatter, or pick upstones (Huffman & Quiatt, 1986).
A recent study conducted on the captive Takahama troop (Primate Research Institute, Kyoto University), using similar observation methods, hasrevealed a remarkably greater diversity in SH behaviours, with 45 distinct
patterns recorded (Nahallage & Huffman, 2007). Age-related differences in
the form of SH were also found. SH patterns involving vigorous motor actions were mainly performed by young individuals whereas complex patterns
were almost exclusively observed in adults. Overall, immatures displayed agreater number of patterns than mature individuals (Nahallage & Huffman,2007). In addition to these three studied troops, SH activity has been reported
in at least nine other geographically isolated troops of Japanese macaques,but no quantitative data were recorded (Huffman & Hirata, 2003; Nahallage& Huffman, 2007). Until now, SH in Japanese macaques was only observedin the Macaca fuscata fuscata subspecies widely distributed in the Japanesearchipelago. Despite long-term studies including behavioural records, SH
has never been observed in M. f. yakui (G. Hanya, pers. comm.), the subspecies endemic to Yakushima, a small island at the southern limit of distribution of the species (cf. Fooden & Aimi, 2005). The lack of detailed documentation of SH from an ethnographic perspective and the above mentioned
differences in the repertoire and form of SH at the group and individual levels highlights the need for a more systematic investigation of inter- and intratroop variability in SH patterns.

98

256

Leca, Gunst & Huffman

We present what may be the most extensive and systematic survey focusedon the variability of a single type of behaviour between and within troops ofJapanese macaques to date. Through a detailed report of the occurrence ofvarious SH patterns across age classes in nine troops of M. f. fuscata andone troop of M. f. yakui living at six geographically isolated sites in Japan,
our main goal is to test the hypothesis that SH is a traditional behaviour inJapanese macaques. Our specific objectives are: 1) to establish the comprehensive repertoire of SH local variants in Japanese macaques; 2) to provide a
broader inter-group comparison of the form of SH and intra-group diffusion
patterns of SH variants according to age; 3) to test the association between
geographic proximity and cultural similarity; 4) to present the first survey ofSH patterns exhibited by M. f. yakui and compare them with those exhibitedby M. f. fuscata; 5) to explore the complexity and diversity in the form ofSH from the perspective of stone-tool use in non-human primates. We will
discuss our results from the perspective of behavioural predispositions (cf.
Huffman & Hirata, 2003) and socially transmitted behaviours.

Material and methods
Study conditions
A total of ten troops of Japanese macaques, four captive (PRI Arashiyama =Ara.A, Wakasa = Wak.A, Takahama = Takh. and Japan Monkey Center
Yakushima macaques = JMC) and six free-ranging troops (Koshima =Kosh., Arashiyama E = Ara.E, Shodoshima = Sho.A and Sho.B, Takasakiyama = Tak.B and Tak.C), were observed at six geographically isolated sites
in Japan (Figure 1). Nine troops belonged to the M. f. fuscata subspecies andone troop was M. f. yakui. In Table 1, we present the study conditions at eachsite. Captive troops were housed in large outdoor enclosures at the Kyoto
University Primate Research Institute and at the Japan Monkey Centre, andwere supplied with commercial primate pellets, vegetables or fruits. Freeranging troop members gathered regularly around feeding sites where they
were artificially provisioned with cereal grains by technicians of the Koshima
Field Station, Kyoto University or by the staff of monkey parks. Althoughprovisioning schedules were different, free-ranging troops living at the samesite (Sho.A/Sho.B and Tak.B/Tak.C) had overlapping home ranges and cameinto occasional contact.

99

Inter- and intra-troop variability of stone handling

257

Figure 1. Map of study sites in Japan; In parentheses: abbreviation of studied troops; Sharp
indicates the subspecies Macaca fuscata fuscata; Asterisk indicates the subspecies Macaca
fuscata yakui.

For each troop, basic demographic information was known (Table 2). The
ten study troops varied both in size and demography: two small-sized captive troops (Ara.A and Wak.A), two medium-sized captive troops (Takh. and
JMC), two medium-sized free-ranging troops (Kosh. and Ara.E) and fourlarge-sized free-ranging troops (Sho.A, Sho.B, Tak.B and Tak.C). The proportion of individuals belonging to the different age/sex classes also varied. Individual identification was possible for only some of the study troops(Ara.A, Wak.A, Takh., Kosh. and Ara.E), and for them the exact age in yearsof each individual and their matrilineages were known. For the other troops(JMC, Sho.A, Sho.B, Tak.B and Tak.C), every sampled subject was labelledaccording to its age and sex classes. Age classes were defined after Fedigan et al. (1983). The daily observation period was between 7:00 am and6:00 pm. Visibility was excellent. We sampled captive troop members fromobservation platforms overhanging the enclosures. Free-ranging troop members could be approached and sampled within 3-5 m.

100

Study site
Primate Research Institute,Inuyama, Aichi prefecturePrimate Research Institute,Inuyama, Aichi prefecturePrimate Research Institute,Inuyama, Aichi prefecture
Japan Monkey Centre,
Inuyama, Aichi prefecture
Koshima Islet, Miyazaki
prefecture
Iwatayama Monkey Park,
Arashiyama, Kyoto pref.
Wild Monkey Park,
Shodoshima island, Kagawa pref.
Wild Monkey Park,
Shodoshima island, Kagawa pref.
Takasakiyama Natural Zoo,
Takasakiyama, Oita pref.
Takasakiyama Natural Zoo,
Takasakiyama, Oita pref.

Troop name, subspecies
and ranging conditions

Arashiyama A(Ara.A# ), CP
Wakasa A(Wak.A# ), CP
Takahama(Takh.# ), CPJapan Monkey Centre(JMC*), CP
Koshima(Kosh.# ), FR
Arashiyama E(Ara.E# ), FR
Shodoshima A(Sho.A# ), FR
Shodoshima B(Sho.B# ), FR
Takasakiyama B(Tak.B# ), FR
Takasakiyama C(Tak.C# ), FR

101

431.3

JBL, MAH† , CN†
JBL, NG, CN
JBL, NG, CN
JBL, NG
JBL, NG

May-Aug 2004
Feb 2005
Feb 2005
Dec 2003-Jan 2004
Dec 2003-Jan 2004

73.8

22.8

51.5

77.6

339.7

JBL, NG

449.2
99.1

JBL

Sep-Dec 2003

224.6

JBL, NGNG

Aug-Nov 2003

179.9

T.O.T.

Aug-Dec 2003,
Mar-Apr 2004
Jan-Feb 2004

NG

Observers

Sep-Dec 2003

Study period

72

58

42

66

1010

252

275

1593

809

644

NS

Table 1. Inter-troop comparison of study conditions and total data sets. In parentheses: abbreviation of troop name; # :Macaca fuscata fuscata, *: Macaca fuscata yakui; CP: captive troop, FR: free-ranging troop; The first two authors werethe main observers († : occasionally assisted by M.A.H. and Charmalie A. D. Nahallage); T.O.T.: Total observation
time; NS: Number of scan sessions.

258
Leca, Gunst & Huffman

Ara.A
Wak.A
Takh.
JMC
Kosh.
Ara.E
Sho.A*
Sho.B*
Tak.B*
Tak.C*

Troop

1 (1)
0 (0)
3 (3)
3 (3)
2 (2)
7 (7)
20 (4)
10 (4)
30 (13)68 (17)



2 (2)
1 (1)
6 (6)
1 (1)
3 (1)
5 (5)
20 (11)10 (6)
35 (9)
69 (17)Yearling
(1)

1 (1)
2 (2)
4 (4)
9 (9)
11 (5)
10 (10)80 (6)
60 (11)60 (5)
96 (31)


2 (2)
2 (2)
2 (2)
12 (9)
10 (6)5 (5)80 (5)
60 (10)60 (8)
95 (26)Juvenile
(2-3)

0 (0)
4 (4)
1 (1)
8 (8)
7 (4)
15 (14)60 (10)50 (7)
50 (6)
80 (16)


0 (0)
3 (3)
4 (4)
14 (11)8 (6)4 (3)50 (5)
40 (6)
20 (6)
20 (12)



Subadult
(4-6)

0 (0)
3 (3)
7 (7)
15 (12)7 (4)20 (20)30 (2)
30 (3)
37 (3)
70 (17)


0 (0)
0 (0)
2 (2)
5 (5)
12 (9)5 (4)
10 (2)
20 (2)
10 (7)
10 (8)

Young adult(7-10)

Age class (years)

4 (4)
2 (2)
4 (4)
11 (7)4 (4)30 (26)40 (6)
30 (3)
60 (7)
86 (17)


0 (0)
0 (0)
0 (0)
9 (4)
7 (6)
2 (2)
10 (1)
10 (1)
16 (6)
20 (3)

Middle-aged adult(11-15)

5 (5)
2 (2)
10 (10)11 (5)8 (7)
31 (29)40 (3)
20 (1)
50 (4)
50 (8)



3 (3)
0 (0)
3 (3)
4 (2)
9 (7)
7 (7)
10 (0)
10 (0)
10 (0)
12 (0)



Old Adult(16-)

18 (18)19 (19)46 (46)102 (76)
88 (61)141 (132)450 (55)350 (54)438 (74)676 (172)

N totalTable 2. Distribution of individuals according to age and sex classes in each studied troop. N total: Total numberof individuals aged at least one year; Asterisk: In large-sized troops, figures were approximately assessed during
yearly surveys (Sho.A and Sho.B: after K. Watanabe, pers. comm.; Tak.B and Tak.C: after H. Kurita, pers. comm.); In
parentheses: number of sampled individuals.

Inter- and intra-troop variability of stone handling

102

259

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Leca, Gunst & Huffman

Data collection
We used the same observation procedure in all troops studied (except for
Tak.B and Tak.C troops, see below for details). Two observational sampling
methods were used: continuous focal-animal sampling interspersed with instantaneous group scan sampling (Altmann, 1974). Behavioural data collection was occasionally supplemented with ad libitum sampling.
Focal sampling
We video-recorded every focal session with Sony digital video cameras(DCR-TRV22 and DCR-TRV33). Whenever possible, the focal individual
was filmed from the front and about one-meter square in-frame. We focusedon all the behaviours and interactions of the focal individual. Since the fieldobservation conditions did not allow us to perform totally random focal sampling, we selected individual focal targets using a semi-random procedure.
The daily observation period was divided into one-hour blocks. We selected
the focal individual, independent of its activity, in an ordered list of temporarily under-sampled individuals or members of each age and sex class(when focal subjects were not individually identified).
We recorded the starting time of each focal session. As previously doneby Huffman (1996), the typical duration of a focal session was 15 minutes.
If the focal individual performed SH activity during the last two minutes ofthis period of time, the observation was extended for 5 minutes and ended
thereafter unless SH was still in progress.
Scan and ad libitum sampling
Before and after each focal session, the troop was scanned for evidenceof any SH activity. For each scan sampled stone handler, we recorded theidentity (or age and sex classes) and whenever possible the SH patterns
observed (Table 3). The observer recorded scans on data sheets, visually(for captive troops) or physically (for free-ranging troops) moving from one
side of the troop to the other, in a set direction, so that each individual was
sampled only once in a given scan session.
To supplement SH data sets, we devoted an average of 38.8 ± 31.8% of
total observation time to collect ad libitum data on individuals performing
SH patterns. Whenever possible, ad libitum sessions were video-recorded,103

Inter- and intra-troop variability of stone handling

261

Table 3. Forty five SH patterns performed by Japanese macaques and categorized according to general activity patterns (after Nahallage & Huffman,in press).
Category

Name (code)

Investigative activities (Inv.)
Bite (B)
Hold (H)
Lick (L)Move inside mouth (MIM)
Pick (P)Put in mouth (PIM)
Sniff (SN)Locomotion activities (Loc.)
Carry (CA)Carry in mouth (CIM)
Grasp walk (GW)
Move and push/pull (MP)Toss walk (TW)
Collection or gathering activities (Coll.)
Cuddle (CD)
Gather (GA)
Grasp with hands (GH)Pick up (PU)
Pick and drop (PUD)
Pick up small stones (PUS)

Definition
Bite a stone
Pick up a stone in one’s hand and hold on to it,
away from the body
Lick a stone
Make a stone move inside one’s mouth withtongue or hands
Pick up a stone
Put a stone in one’s mouth and keep it sometime
Sniff a stone
Carry a stone cuddled in hand from one place
to another
Carry a stone in mouth while locomoting
Walk with one or more stones in the palm of
one or both hands
Push/pull a stone with one or both hands while
walking forward/backward
Toss a stone ahead (repeatedly) and pick it up
while walking
Take hold of, grab or cradle a stone against thechest
Gather stones into a pile in front of oneself
Clutch a stone or a pile of stones gathered andplaced in front of oneself
Pick up a stone and place it into one’s hand
Pick up a stone and drop it repeatedly
Pick up small stones and hold them between
fingertips (like the picking up of wheat grains)or otherwise collected on a notepad. For Tak.B and Tak.C, we did not collect focal sessions, but only video-recorded ad libitum sessions during postfeeding periods, when SH is most likely to occur (Huffman, 1996). Whenthe sampled individual was filmed through the entire sequence of SH, fromstart (a few minutes after provisioning time, when it just left the feeding siteand began contacting stones) to finish (five minutes after it last discarded
stones), this ad libitum session was defined as complete. When a SH episode

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Leca, Gunst & Huffman

Table 3. (Continued).
Category

Name (code)

Definition

Percussive or rubbing sound producing activities (Perc.)
Clack (CL)Clack stones together (both hands moving in aclapping gesture)
Combine with object (COO)
Combine (rub or strike) a stone with an object different from a stone (food item, piece ofwood, metal, etc.)
Flint (FL)
Strike a stone against another held stationary
Flint in mouth (FLM)
Strike a stone against another held in mouth
Pound on surface (POS)
Pound a stone on a substrate
Rub in mouth (RIM)
Rub a stone against another held in mouth
Rub/roll on surface (ROS)
Rub or roll a stone on a substrate
Rub stones together (RT)
Rub stones together
Rub with mouth (RWM)
Rub a surface with a stone held in mouth
Scatter (SC)Scatter stones about, on a substrate, in front of
oneself
Shake in hands (SIH)
Take stones in one’s open palm hand and shakethe stones with the hand moving back and forth
Slap (SL)Slap, tap or pound a stone with one’s fingertips
or palm of hand
Swipe (SW)
Swipe stones together (both hands moving in a
sweeping gesture)
Tap in mouth (TIM)
Tap a stone held in mouth with fingertips or
palm of hand
Other complex manipulative activities (Comp.)
Flip (FP)Turn a stone over with both hands
Put in water (PIW)
Put a stone in water
Roll in hands (RIH)
Roll a stone in one’s hands
Rub/put on fur (ROF)
Rub or put a stone on one’s fur while selfgrooming
Rub with hands (RWH)
Hold a stone in one hand and rub it with theother (like potato-washing)Spin (SP)Spin a stone around on the ground using two
fingers of one hand or both hands (one moving
forward and the other backward)
Stone-groom (SGR)
Allo-groom with a stone
Throw (TH)Throw a stone without jumping or running
Throw and jump (TJ)
Throw a stone and jump (or vice versa)
Throw and run (TR)Throw a stone and run (or vice versa)
Throw and sway (TS)Throw a stone and sway (or vice versa)
Wash (W)
Put a stone in water or pick up a stone fromwater and rub it with hands
Wrap in leaf (WIL)
Wrap a stone in a leaf (or wrap a leaf around astone)

105

Inter- and intra-troop variability of stone handling263

was recorded on notepad or when the sampled individual was not filmed
through the entire sequence of SH, we referred to the ad libitum session as
incomplete.
Data analysis
Based on video-records, J.-B.L. transcribed each focal session onto a data
sheet and measured the duration of all activities (feeding, foraging, locomoting, resting, socializing, SH, non-stone object exploring, and other) andevery SH pattern in seconds. We defined the troop total observation time as
the total time in hours spent observing each troop, including focal time, scantime and time spent collecting ad libitum data, and summed the times of allobservers, when several were present. We verified inter-observer reliability
using the kappa coefficient of Cohen (1960). Based on individual identities,
activities and interactions, we found κ = 0.92. In Table 4, we present the total data sets per troop and age class. Individuals less than one year old were
not taken into account in the analyses.
We distinguished two types of SH records: SH bouts (collected from focal
sessions or complete ad libitum video-recorded sessions) and SH notes (collected from scan sessions or incomplete ad libitum sessions). We defined aSH bout as the display of SH activity with possible pauses of no longer than
120 seconds. If the individual resumed SH within 120 seconds after pausing,then the two SH episodes were considered as a single SH bout. If SH wasresumed more than 120 seconds after pausing, this would mark the start of a
new SH bout.
For the analyses of SH patterns, we grouped all observed SH patterns
into five categories according to general activity patterns (Table 3). Basedon the definitions by Whiten et al. (1999, 2001), we assessed the level ofoccurrence of each SH pattern in each troop by distinguishing among fivefrequencies of occurrence: customary, habitual, present, absent and unknown(Table 5). We drew on all SH bouts and SH notes available for analyses
regarding the frequency of occurrence of SH patterns and the percentage ofsampled individuals exhibiting each SH pattern in each troop. For analyses
about the mean percentage of SH patterns performed in each troop, we drewon all SH bouts. From the frequency value of each SH pattern recorded per
SH bout, we calculated the percentage of each pattern per bout and the mean
percentage for all SH bouts.

106

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Leca, Gunst & Huffman

Table 4. Data sets collected according to age classes in each studied troop.
Tot: All age classes pooled; FT: Focal time (total duration in hours of focal sessions); SH Bt (F, CAL): Number of SH bouts collected during focal
sessions (F) and during complete ad libitum sessions (CAL); SH Nt (IAL):
Number of SH notes collected during incomplete ad libitum sessions (IAL)(see methods for detail); n/a: Age class not available; –: Data not available.
Troop

Age class

Tot

Yng

Juv

SuAd

YgAd

MdAd

OlAd

Ara.A
FT
SH Bt (F, CAL)SH Nt (IAL)

23.3
12, 0
10

23.3
1, 0
15

n/a
n/a
n/a

n/a
n/a
n/a

31.5
0, 1
2

62.0
1, 0
1

140.1
14, 1
28

Wak.A
FT
SH Bt (F, CAL)SH Nt (IAL)

10.0
2, 4
18

39.3
16, 1445

59.8
35, 36
140

27.8
0, 4
3

19.8
4, 1
5

18.0
2, 3
13

174.7
59, 62
224

Takh.
FT
SH Bt (F, CAL)SH Nt (IAL)

70.2
108, 6
267

42.7
68, 5
254

39.9
38, 4
206

73.1
56, 6
190

31.1
17, 3
72

96.6
22, 4
210

353.6
309, 28
1199

JMC
FT
SH Bt (F, CAL)SH Nt (IAL)

4.3
2, 6
4

7.5
6, 38
33

12.3
10, 27
24

10.5
1, 24
27

13.8
3, 4
3

6.3
0, 0
0

54.7
22, 9991

Kosh.
FT
SH Bt (F, CAL)SH Nt (IAL)

13.3
5, 8
2

38.0
4, 6
5

30.3
0, 0
0

42.5
0, 0
0

38.0
0, 0
0

53.3
0, 0
0

215.4
9, 14
7

Ara.E
FT
SH Bt (F, CAL)SH Nt (IAL)

14.2
39, 8
57

14.9
57, 8
97

19.6
39, 3
75

21.1
56, 7
106

38.4
50, 2
106

52.4
76, 7
138

160.6
317, 35
579

Sho.A
FT
SH Bt (F, CAL)SH Nt (IAL)

5.0
13, 4
3

3.9
8, 3
4

3.8
6, 3
8

0.5
0, 0
4

3.1
3, 0
4

0.5
0, 0
4

16.8
30, 1027

Sho.B
FTSH Bt (F, CAL)SH Nt (IAL)

0.0
0, 1
10

0.5
3, 10
32

0.5
1, 8
16

0.0
0, 4
4

0.3
0, 2
4

0.0
0, 1
1

1.3
4, 26
67

107

265

Inter- and intra-troop variability of stone handling

Table 4. (Continued).
Troop

Age class

Tot

Yng

Juv

SuAd

YgAd

MdAd

OlAd

Tak.B
FT
SH Bt (F, CAL)SH Nt (IAL)

–
0, 9
17

–
0, 11
14

–
0, 17
14

–
0, 9
15

–
0, 11
13

–
0, 2
2

–
0, 59
75

Tak.C
FT
SH Bt (F, CAL)SH Nt (IAL)

–
0, 14
64

–
0, 67
163

–
0, 44
70

–
0, 32
51

–
0, 18
41

–
0, 7
2

–
0, 182391

Table 5. Frequency of occurrence of SH patterns ranked in descending orderin a given troop (after Whiten et al., 1999, 2001); Asterisk: in large-sized
troops (Sho.A, Sho.B, Tak.B and Tak.C), the number of sampled individuals
was substantially different from the number of group members (see Table 2).
Frequency of occurrence

Definition

Customary

Exhibited by at least 90% of the sampled* individuals in atleast one age class, or at least 70% of the sampled* individuals in at least two age classes
Not customary but observed at least three times in several individuals, consistent with some degree of social transmission
Not customary or habitual, but observed at least once
Not observed despite sufficient observation time (at least 90
hours of total observation time)
Not observed but absence uncertain because of insufficient
observation time (less than 90 hours of total observation time)

Habitual
Present
AbsentUnknown

To test the association between geographic proximity and cultural similarity, we used a matrix correlation (Matman program, Noldus). In a first
matrix, we assessed inter-troop geographic proximity by distinguishing between the troops living at the same site and having occasional encounters(Sho.A/Sho.B and Tak.B/Tak.C, with a ‘1’ proximity value) and all the othertroops (with a ‘0’ proximity value). In a second matrix, we entered the cultural similarity, defined as the number of SH patterns showing the same frequencies of occurrence across troops. We set the number of permutationsof matrices at 10 000 and used the Pearson’s correlation coefficient. To test
the effect of age on the complexity of SH patterns, we used a mixed-model

108

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Leca, Gunst & Huffman

ANOVA, with age classes as between factor and two degrees of complexity
as repeated measures (simple patterns: investigative, locomotion and collection activities and complex patterns: percussive/rubbing and other complex
manipulative activities). We used SPSS 12.0 for statistical analyses and set
significance level at α = 0.05.

Results
SH traditions (local variants) and levels of SH cultures
We found considerable differences in the occurrence of SH patterns among
the studied troops (Table 6). Out of the 45 patterns defined in Table 3, Takh.
exhibited a total of 44, whereas Ara.A and Kosh. displayed 17 and 16 SH
patterns, respectively. The other troops exhibited between 22 and 32 different patterns. It should be noted that most of the patterns found in Ara.A andKosh. were simple ones, corresponding to investigative and collection activities. These two troops also showed extremely low SH occurrences comparedto most other troops, with 0.2 and 0.1 SH bouts and notes per hour, respectively (Table 6). Accordingly, we will consider the interaction with stonesin the Ara.A and Kosh. troops as the baseline level of interest in stones byJapanese macaques.
Overall, Table 6 showed that the frequency of occurrence of SH patterns
was highly variable according to the pattern and troop in question. Even
though most simple SH patterns (corresponding to investigative, locomotion
and collection activities) could be observed in most study troops, their frequency of occurrence varied from present to customary. For example, the pattern consisting of licking a stone (L) was not observed in Sho.A and Sho.B,
merely present in Ara.A, JMC, Kosh., Ara.E, Tak.B and Tak.C, habitual in
Wak.A and customary in Takh. Although close in form, the pattern consisting of biting a stone (B) showed a different distribution: it was observed in all
troops, but only present in Ara.A, JMC, Sho.B and Tak.B, habitual in Ara.E,
Sho.A and Tak.C, and customary in Wak.A, Takh. and Kosh. Likewise, CA
was absent in Ara.A, present in Kosh., habitual in Takh., JMC, Sho.A, Sho.B,
Tak.B and Tak.C, and customary in Wak.A and Ara.E.
The frequent occurrence of more complex SH patterns, corresponding topercussive, rubbing and other complex manipulative activities was even more
restricted to particular troops, but again highly variable depending on the

109

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Inter- and intra-troop variability of stone handling

Table 6. Frequency of occurrence of the 45 SH patterns observed in Japanesemacaques according to studied troop; C: Customary, H: Habitual, P: Present,–: Absent, (–): Unknown; Tot. pattern occurrence: Total number of SH patterns scoring at least the Present status; SH occurrence per hr: Level of occurrence of SH obtained by dividing the total number of SH bouts and notes
scored by the total observation time.
SH pattern

Ara.A Wak.A Takh. JMC Kosh. Ara.E Sho.A Sho.B Tak.B Tak.C

Investigative activities
Bite
P
Hold
P
Lick
P
Move inside mouth–
PickC
Put in mouth
P
Sniff
C

C
H
H
H
P
H
C

C
P
C
H
P
H
C

P
P
P
P
P
P
H

C
P
P
–
P
–
P

H
H
P
P
P
P
H

H
H
(–)
(–)
P
H
P

P
P
(–)
(–)
(–)
P
P

P
H
P
P
(–)
P
H

H
H
P
P
P
P
H

Locomotion activities
Carry–
Carry in mouth–
Grasp walkP
Move and push/pull–
Toss walk
P

C
H
C
C
P

H
C
C
H
C

H
P
H
P
P

P
–
P
P
–

C
P
C
H
H

H
P
H
P
(–)

H
P
P
P
(–)

H
P
H
P
P

H
P
H
P
P

Collection (gathering) activities
CuddleC
C
GatherP
C
Grasp with hands
P
C
Pick upC
P
Pick and drop––
Pick up small stones
–
–

C
C
C
C
P
H

H
P
H
P
–
–

C
P
P
P
–
–

C
C
C
H
P
H

H
H
H
H
P
(–)

H
H
H
P
(–)
(–)

H
H
H
H
P
P

H
H
H
H
H
P

Percussive or rubbing sound producing activities
Clack
P
P
H
H
–
Combine with object –
P
C
P
–
Flint
–
H
C
P
–
Flint in mouth
–
P
P
–
–
Pound on surface
–
P
H
H
–
Rub in mouth
–
P
P
–
–
Rub/roll on surface
C
C
C
H
P
Rub stones together
–
H
C
P
–
Rub with mouth
–
P
P
–
–
ScatterP
H
CPP
Shake in hands
–
–
P
P
–
Slap
–
–
H
P
–
Swipe
–
P
P
–
–
Tap in mouth
–
–
P
–
–

–
H
P
–
P
–
H
C
–
C
P
–
P
–

P
(–)
P
(–)
P
(–)
H
P
(–)
H
(–)
(–)
(–)
(–)

P
P
P
(–)
(–)
(–)
H
P
(–)
P
P
(–)
(–)
(–)

P
(–)
P
(–)
(–)
(–)
H
H
(–)
H
P
(–)
P
(–)

P
P
H
P
H
P
H
H
(–)
H
P
(–)
H
(–)

110

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Leca, Gunst & Huffman

Table 6. (Continued).
SH pattern

Ara.A Wak.A Takh. JMC Kosh. Ara.E Sho.A Sho.B Tak.B Tak.C

Other complex manipulative activities
Flip
–
P
H
Put in water––P
Roll in hands
P
HC
Rub/put on fur–
HP
Rub with hands
P
H
C
Spin
–
–
P
Stone groom
–
–
–
Throw
–
P
P
Throw and jump––H
Throw and run––
PThrow and sway
–
–
P
Wash
–
–
P
Wrap in leaf
–
–
H

–
–
P
P
H
–
–
P
–
P
–
P
–

–
–
P
–
P
–
–
–
–
–
–
–
–

P
P
H
P
H
–
–
–
–
–
–
H
–

(–)
(–)
P
(–)
H
(–)
P
(–)
(–)
(–)
(–)
(–)
(–)

(–)
(–)
P
P
P
(–)
(–)
(–)
(–)
(–)
(–)
(–)
(–)

P
(–)
H
(–)
P
(–)
(–)
(–)
(–)
(–)
(–)
(–)
(–)

(–)
(–)
H
(–)
P
(–)
(–)
(–)
(–)
(–)
(–)
(–)
(–)

Tot. pattern occurrence
SH occurrence per hr

31
2.1

16
0.1

32
2.2

23
0.9

22
1.9

27
5.9

31
7.8

17
0.2

32
1.5

44
3.4

pattern. For example, COO was absent in Ara.A and Kosh., not observedin Sho.A and Tak.B, only present in Wak.A, JMC, Sho.B and Tak.C, but
habitual in Ara.E and customary in Takh. The pattern consisting of flinting
stones (FL) was absent in Ara.A and Kosh., present in JMC, Ara.E, Sho.A,
Sho.B and Tak.B, habitual in Wak.A and Tak.C, and customary in Takh.
Some complex SH patterns occurred in a few troops only, such as SW in
Wak.A, Takh. and Ara.E, W in Takh., JMC and Ara.E, RWM in Wak.A and
Takh., and SL in Takh. and JMC. Finally, a few complex SH patterns were
specific to one troop, such as TIM, SP and WIL in Takh., and SGR in Sho.A.
To further explore inter-troop cultural differences in terms of behaviouralcomplexity, we used a three-step procedure for the purpose of evaluating
whether some troops have a more complex set of SH patterns than others.
First, we pooled together complex SH patterns (i.e., percussive/rubbing andother complex manipulative activities). Second, we only considered the SH
patterns that were scored as having a cultural occurrence in a given troop(i.e., habitual and customary). Third, we distinguished among three categories of troops: 1) when a troop was scored as having none or only one
complex SH pattern, this troop was referred to as having a complexity level-1
SH culture, based on simple behavioural patterns (N CBP = number of complex behavioural patterns, Kosh.: N CBP = 0, Ara.A and Sho.B: N CBP = 1);

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Inter- and intra-troop variability of stone handling

2692) when a troop was scored as having from two to ten complex SH patterns,
this troop was referred to as having a complexity level-2 SH culture, basedon medium complexity behavioural patterns (Sho.A: N CBP = 3, JMC and
Tak.B: N CBP = 4, Wak.A, Ara.E and Tak.C: N CBP = 7); 3) when a troop
was scored as having more than ten complex SH patterns, this troop wasreferred to as having a complexity level-3 SH culture, based on high complexity behavioural patterns (Takh.: N CBP = 13).
Two out of the three troops showing a complexity level-1 SH culture(Ara.A and Kosh.) were considered ‘control groups’ with only a baseline
level interest in stones. Only Takh. showed a complexity level-3 SH culture.
This troop also exhibited the most numerous SH patterns (44 out of a totalof 45) and showed the highest frequencies of occurrence in SH patterns (28habitual or customary patterns) among all troops. Most study troops (sixout of ten) showed an intermediate level of complexity in their SH practice(level-2 SH culture).
Almost all SH patterns showed geographically patchy distributions, i.e.,
had different profiles of frequency of occurrence across the study sites, andwere referred to as local variants or SH traditions. In terms of behaviouralcomplexity, we found three levels of SH culture, each level being definedby troop-dependent clusters of SH traditions. Each troop presented a uniqueprofile in terms of mean percentages of SH patterns performed, which further
supported the geographic distribution of clear troop-dependent clusters of SH
variants. For example, GH represented 2.8% of the total patterns performed
in Takh., 4.8% in Ara.A, 7.1% in Wak.A, 7.2% in JMC, 15.0% in Sho.B,
15.6% in Sho.A, 16.5% in Kosh., 18.3% in Tak.C, 21.2% in Tak.B and 30.8%
in Ara.E.
We found a significantly positive correlation between geographic proximity and cultural similarity in SH between troops (r = 0.333, p = 0.008).
There were significantly greater similarities in SH patterns in the troops
living at the same site, compared to other troops. Neighbouring troops(Sho.A/Sho.B and Tak.B/Tak.C), had similar sets of SH patterns and their
total numbers of patterns observed were close (23 and 22 at Shodoshima, and27 and 31 at Takasakiyama). In the two free-ranging troops where SH waspreviously studied by using similar methods of data collection and analysis(Ara.E and Tak.C: Huffman, 1996; Huffman & Hirata, 2003), we found thatthe size of the SH repertoire almost doubled. We recorded a total 32 SH patterns in Ara.E (as opposed to 17 patterns in 1991) and 31 patterns in Tak.C

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Leca, Gunst & Huffman(as opposed to 16 patterns in 1989). The SH patterns that were not recorded
before were FP, PIW, ROF and W in Ara.E, PUD, FLM and RIM in Tak.C,
and B, H, L, MIM, P, PIM, SN, CIM, COO, POS, SIH and SW in Ara.E and
Tak.C.
Intra-group variability and age effect
The frequency of performance of the main SH patterns (representing at least
4% of all SH patterns performed) varied significantly according to the ageclass of the stone handler (goodness-of-fit tests, df = 5, all χ 2 > 25.0, p <0.001). After excluding the most common patterns (i.e., GA, GH and ROS),
we found in several troops a significant interaction effect between age andthe degree of complexity of SH patterns (Ara.A: F 1,12 = 18.8, p = 0.001;
Wak.A: F 2,97 = 5.1, p = 0.008; Takh.: F 2,315 = 3.1, p = 0.048; JMC:
F 2,103 = 7.9, p = 0.001; Ara.E: F 2,292 = 4.3, p = 0.015; Tak.C:
F 2,175 = 3.8, p = 0.024). Post-hoc comparisons showed that on average,
young individuals (yearlings and juveniles) performed more simple patterns
than complex patterns, whereas the opposite held true for older individuals(Figure 2). In Figure 3, we present several examples of age-related variability
in the mean percentage of simple versus complex SH patterns.
In several troops, the percentage of young individuals exhibiting simple
SH patterns was significantly higher than the percentage of older individuals (goodness-of-fit tests, df = 5, χ 2 = 237.5, 232.5, 431.4, 88.6, 250.8
and 197.7 in Ara.A, Wak.A, Takh., JMC, Kosh. and Ara.E, respectively,
p < 0.001). Within a given troop, certain complex SH patterns were only
performed by a small proportion of individuals belonging to only one ageclass. For example, in Takh., SP was only score in 8% of old adults, in JMC,
PIM was only displayed by 5% of subadults, and in Sho.B, CL was only
exhibited by 10% of the juveniles.
Similarities and differences at the subspecies level
This is the first study to document the occurrence and form of SH activity in
the M. f. yakui subspecies. The total number of patterns and SH occurrencein JMC (M. f. yakui) was almost the same as those found in Ara.E (31 and 32
patterns, 2.1 and 2.2 SH bouts and notes per hour, respectively (Table 6). The
SH repertoire of JMC was more comprehensive than that of M. f. fuscata113

Inter- and intra-troop variability of stone handling

271

Figure 2. Effect of age on the degree of complexity of SH pattern performed in four study
troops. Bars represent the mean frequency of SH patterns performed per bout ± standard
error. White bars: simple SH patterns (Inv., Loc. and Coll.); black bars: complex SH patterns(Perc. and Comp.).

troops Ara.A and Kosh., that showed only a baseline level of interest in
stones.
The SH repertoire of JMC did not notably differ from the SH repertoire ofM. f. fuscata troops. Like most M. f. fuscata troops, JMC exhibited almost all
the simple SH patterns (investigative, locomotion and collection activities)
and various more complex patterns, such as CL, COO, POS, ROS, RT and
RIH. The JMC troop even exhibited rare SH patterns, such as TH and W thatwere only observed in two M. f. fuscata troops (Wak.A, Takh. and Takh.,
Ara.E, respectively), as well as SL and TR that was observed in a single M.
f. fuscata troop (Takh.). However, we found no SH pattern that was uniqueto JMC.
The effect of age on the mean percentage of most SH patterns was also
found in JMC. Yearlings and juveniles performed more frequently certain
simple patterns (e.g., SN and CA), whereas young and middle-aged adults
performed more frequently certain complex patterns (e.g., POS) (Figure 3).
In JMC, like most M. f. fuscata troops, the proportions of individuals exhibiting simple patterns were higher in young than in older troop members

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Figure 3. Examples of age-related variability in the mean percentage of several SH patterns
performed (two simple patterns: SN and CA, and two more complex patterns: POS and RT).

(df = 5, χ 2 = 88.6, p < 0.001). Overall, our comparative study revealed
no major difference between M. f. fuscata and M. f. yakui in the occurrence,
form and intra-group variability of SH.
Discussion
We found that Japanese macaques have SH cultures in the sense that the
study troops showed distinctive levels of clustered SH traditions. Our detailed examination of the overall SH profiles showed major inter-troop differences in the occurrence and form of the behaviour. Contrary to the first comparative analysis based on data collected at Arashiyama and Takasakiyama,
we found substantial qualitative and quantitative evidence for local SH variants among most of the ten troops studied here. Each troop had a distinctive
set of 16-44 discrete SH patterns. Very few patterns were unique to certain
troops, most others were shared between two or more troops. Although the
SH profiles of each troop were distinctively different in nature and degree,
the clusters of SH variants found in each troop were not mutually exclusive.
However, our results revealed a significant inter-troop variability in the form

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of SH, consistent with the extensive and multiple inter-site behavioural differences recorded in chimpanzees, and interpreted as cultural variation (cf.
Whiten et al., 1999, 2001).
In explaining the overall inter-troop variability in the form of SH, andthe similarities in the SH repertoires between the free-ranging troops living
at the same site, we can reasonably consider the possibility of ecologicalfactors to be minimal. First, environmental conditions directly connected
to SH activity did not differ dramatically among the study sites. All thetroops were dependent to some extent upon artificial food provisioning byhumans. Although stone availability was variable according to the study site,stones were available at all sites. Comparative analyses showed that sitespecific stone availability was not significantly associated with inter-troop
differences in the occurrence of SH (Leca, unpub. data). This suggests thatthe performance of SH is more diverse and more complex than the direct
link to the number of stones locally available. Natural substrates (big rocks,
tree trunks, outcropping roots or water holes) and artificial surfaces (metallic
roofing, climbing structures, concrete walls or floors) to combine with stones(e.g., rub/roll on surface, pound on surface, wash) were available at all sites.
Second, SH is not considered to be a subsistence activity (Huffman, 1984,1996). Out of the 45 different SH patterns, none of them is directly adaptive. Despite the rare occurrence of complex patterns such as stone-groomor throw, the stones handled by Japanese macaques were never used as tools
to achieve an overt goal. Therefore, there is no local survival advantage inperforming a particular SH pattern rather than another. As long as the basic materials (stones and substrates) are available and since the capacity forsocial learning in Japanese macaques has been proven in controlled studies(e.g., Kumashiro et al., 2003), we suggest that a wide range of alterations in
the form of the same behaviour is likely to appear and diffuse. From a functional viewpoint, all SH variants should have similar expected frequenciesof occurrence at the group level. SH is a behaviour particularly well-suitedfor the ethnographic approach. Its apparent lack of direct adaptative consequences and the arbitrariness of its behavioural variants make it easier to ruleout ecological factors as potential causes of intergroup variation.
We found a positive correlation between geographic proximity and cultural similarity in SH between troops. The similarities in SH repertoires between free-ranging troops living at the same site may reflect the possibility ofinter-troop observation when monkeys come into occasional contact around

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the feeding sites where most SH activity occurs (Leca, pers. obs.). Anotherpossibility is that some SH may be transferred by males migrating from one
troop to the other. Inter-troop cultural transmission in wild chimpanzees has
been inferred from the geographical distribution of certain tool-using behaviours and social conventions (Boesch et al., 1994; McGrew et al., 1997,
2001), and suggested from field experiments (Biro et al., 2003). Thus wesuspect a phenomenon of ‘cultural zones’ (cf. Biro et al., 2003) to be at work
here, based on immigration or inter-troop observational learning of SH patterns, since any alternative explanation is hard to imagine.
We consider that genetic determinants may not account for the observed
inter-troop variability in the form of SH. First, we showed that SH patterns varied as much between sites associated with the same subspecies(M. f. fuscata at seven sites) as between subspecies themselves (M. f. fuscata versus M. f. yakui). Second, we can assume that most SH patterns are
Japanese macaque ‘universals’. All the basic motor actions involved in every
SH pattern are behavioural predispositions, i.e., they are already present in
the repertoire of Macaca fuscata species (Huffman & Hirata, 2003). Third,
it is acknowledged that genes determine the occurrence of general behavioural categories within a given species, such as the ability to handle stones
or use tools. For example, gene flow between the three chimpanzee subspecies is prevented by zoogeographical barriers across Africa. Far western
chimpanzees (Pan troglodytes verus) differ genetically from the others far
more than central and eastern subspecies (P. t. troglodytes and P. t. schweinfurthii) differ themselves (Morin et al., 1994). Interestingly, the former uses
percussive techniques to crack open nuts, while the latter are non-crackers(McGrew et al., 1997; but see Whiten et al., 1999 for a cultural rather thana genetic explanation). Fooden & Aimi (2005) provided information about
the geographic distribution of extant populations of Japanese macaques, including continuities and discontinuities, migration, and genetic variability.
Although there is evidence for geographic variation in mitochondrial DNA
of Japanese macaques (Hayasaka et al., 1991), we suggest that intraspecificgenetic differences are negligible in terms of possible implications for local
behavioural variants, such as the manual dexterity to clack rather than rub
stones together.
Our results showing high intra-group variability in most SH patterns are
consistent with those drawn from a longitudinal study of SH in the Takh.
troop (Nahallage & Huffman, 2007). Such variation can be interpreted from117

Inter- and intra-troop variability of stone handling275

the viewpoint of developmental factors and age-related behavioural differences. As suggested by Nahallage & Huffman (2007), higher proportions ofimmatures exhibiting preferentially simple patterns, involving investigative,
locomotion and collection activities, may reflect the development of perceptual and motor abilities in young monkeys. By contrast, the more frequent
performance of complex manipulative patterns by older individuals could
contribute to slow down the impairment of cognitive functions associatedwith advanced age (Nahallage & Huffman, 2007).
The ubiquity of certain SH patterns, such as cuddle, gather and grasp withhand, reemphasizes the general behavioural predispositions for Japanesemacaques to manipulate stones, regardless of age. Other SH patterns, suchas swipe, rub in mouth, or wrap in leaf, can be considered idiosyncratic oranecdotal. This finding supports the view that certain group members may‘specialize’ or at least be responsible for the occurrence of particular patterns at the group level (Huffman & Quiatt, 1986). The occurrence of groupmember ‘specialists’ in particular patterns emphasizes the role of individuality in group-level phenomena in primates. It has been suggested that theoccasional and restricted practice of a given behavioural pattern by very few
group members may not be sufficient to maintain these patterns in a troop
in the long-term (Huffman & Hirata, 2003; Leca et al., in press). When the
only practitioner of a particular behavioural pattern dies, this pattern is also
bound to disappear at the group level.
Our results allow to further discuss the maintenance of SH as a traditional
behaviour in two previously studied troops at Arashiyama and Takasakiyama(Huffman, 1996; Huffman & Hirata, 2003). The transformation phase of SH
innovation is defined as the late period in which long-enduring practice andacquired familiarity with the behaviour is gained through the integration of
SH with other daily activities (Huffman & Quiatt, 1986; Huffman & Hirata,
2003). Our data showed that within about 15 years of continued observation
at Arashiyama and Takasakiyama, the monkeys have largely extended anddiversified their SH repertoire. The appearance of patterns combining theuse of hands and mouth (e.g., carry in mouth, move inside mouth, bite andlick) suggests that SH has become more integrated with foraging and feeding activities. Newly appeared patterns such as combine with object, rub/put
on fur and wash reveals an increased diversity in the combination of stones
with other objects or substrates. Our results were not consistent with previous findings suggesting that with age, individuals tend to become more

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conservative in their SH patterns, limiting their performance to simple activity patterns (Huffman & Quiatt, 1986; Huffman, 1996). The more frequentand diversified practice of SH in all age classes associated with the transformation phase of SH could account for this discrepancy. Another explanation
could be that the young individuals growing up with SH 15 years ago are now
at an advanced age, and they carry on with more complex patterns than they
showed when they were young, compared to the earliest generation of stone
handlers. This would also be consistent with the transformation phase and agenerational ‘ratchet effect’ of increased complexity of SH behavioural patterns. This could lead in future to stone-tool use, as stone behaviour becomes
more deeply ingrained into the behavioural landscape of these monkeys at
the population level.
Although stone tool-using has been reported in Japanese macaques underexperimental conditions (Tokida et al., 1994), we found no direct evidence
for an adaptive transformation in SH practice. Even complex combinatorial
SH patterns did not meet the descriptive criteria of Beck’s (1980) definitionof tool use. The combination of stones with other objects, including fooditems, did not ‘efficiently alter the form, position, or condition’ (Beck, 1980,
p. 10) of these objects. Patterns such as rub/put on fur and stone-groom may
actually be cases of self- or allo-grooming while holding a stone (Weinberg& Candland, 1981). However, when practised on a daily basis and by mostmembers of a group, the non-instrumental manipulation of stones could beconsidered as a behavioural precursor to the possible use of stones as tools(Huffman & Quiatt, 1986; Huffman, 1996).
Although widely used by field primatologists as a way to identify traditions, the ethnographic approach has been recently questioned for having
two flaws (Fragaszy & Perry, 2003). The first flaw is conceptual. This approach does not necessarily consider an essential characteristic of traditions:
their dependence on social context for individual acquisition of the behaviour under study. Many authors suggest that demonstrating the social transmission and durability of a behaviour within a group is sufficient evidence initself of a behavioural tradition (Fragaszy & Perry, 2003; Perry et al., 2003b;
Visalberghi & Adessi, 2003). Developmental, experimental and long-term
studies could then compensate for this shortcoming. The second flaw is logical. When considered alone, the ethnographic approach can result in ‘false
negatives’ and more problematic ‘false positives’ (Fragaszy & Perry, 2003).

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277

When combining the ethnographic approach, evidence for social transmission and durability of SH, and the view of behavioural predispositions
in phylogenetically close taxa, several findings supported the hypothesis that
SH is a traditional behaviour: 1) we showed a geographic distribution of clear
troop-dependent clusters of SH variants suggestive of the notion of culturalzones; 2) we provided arguments to eliminate simple alternative explanations
for such behavioural variability, such as genetic or ecological differences; 3)
although SH is a primarily solitary activity, non-SH individuals have plentyof opportunities to observe performances of SH by other group members
and often show close interest in others’ stones (Leca, Huffman, pers. obs.);
4) after SH appeared at Arashiyama, developmental data showed that the
behaviour first spread laterally among young individuals and was then acquired vertically from mother to offspring through observational learning(Huffman, 1984, 1996); 5) SH is enduring in most troops, where it occurs ona regular basis; at Arashiyama and Takasakiyama, we found that this traditional behaviour has at least a 27-year history and provided evidence that it
has reached its transformation phase.
Along with a lack of evidence for an instrumental use of stones, thesearguments further support the notion of SH as being a non adaptive traditional behaviour (but see Nahallage & Huffman, 2007 for a possible ultimate
function of SH). We drew an overall picture of rich cultural diversity in a particular type of object play behaviour in Japanese macaques. Amongst the rare
non-adaptive proposed traditional behaviours (see also ‘leaf-pile pulling’ inchimpanzees: Nishida & Wallauer, 2003), SH is the most thoroughly documented. Additional evidence for inter-troop variability and long-term maintenance of stone-related behaviours in non-human primates may provide new
insights into the emergence of hominid material culture through stone-tool
technology.

Acknowledgements
J.-B.L.’s field work was supported by a Lavoisier Grant, Ministère des Affaires Etrangères,France. N.G. was supported by a National Science Foundation grant (BCS-0352035). This
study would not have been possible without the contribution of many people who helped inmany ways during the course of this research. We wish to thank the researchers, students,
staff and friends who provided permission to work, support, assistance and valuable specificinformation about the history, demography and environmental conditions of the troops at thedifferent study sites and general information from other field sites. We are grateful to the

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following people: G. Hanya, A. Kato, M. Matsubara, K. Nagata, H. Osawa, Y. Shimooka
and H. Takemoto (Primate Research Institute), M. Nakamura and Y. Takenoshita (Japan
Monkey Centre), F. Kanchi, A. Mori and T. Suzumura (Koshima Field Station), K. Watanabe(Koshima Field Station and Wild Monkey Park, Shodoshima), S. Asaba, S. Hanamura, T.
Kawashima, S. Kobatake and M. Shimada (Iwatayama Monkey Park, Arashiyama) and H.
Kurita (Takasakiyama Natural Zoo). We are indebted to the Enomoto family for generously
providing logistic assistance at Arashiyama. For occasional assistance in data collection,
we thank K.J. Petrzelkova. We are grateful to C.A.D. Nahallage for her assistance in datacollection, fruitful discussion about SH, and friendship. For providing us with comparative
data on object manipulation in long-tailed macaques, we thank A. Zeller. We thank D.M.
Fragaszy for insightful comments on a previous version of the draft.

References
Altmann, J. (1974). Observational study of behaviour: Sampling methods. — Behaviour 49:
227-267.
Beck, B.B. (1980). Animal tool behavior. — Garland STPM Press, New York, NY.
Biro, D., Inoue-Nakamura, N., Tonooka, R., Yamakoshi, G., Sousa, C. & Matsuzawa, T.
(2003). Cultural innovation and transmission of tool use in wild chimpanzees: Evidence
from field experiments. — Anim. Cogn. 6: 213-223.
Boesch, C. (1996). Three approaches for assessing chimpanzee culture. — In: Reaching intothought: The minds of the great apes (Russon, A.E., Bard, K.A. & Parker, S.T., eds).
Cambridge University Press, Cambridge, p. 404-429.
Boesch, C., Marchesi, P., Fruth, B. & Joulian, F. (1994). Is nut cracking in wild chimpanzees
cultural behavior? — J. Hum. Evol. 4: 325-338.
Chapman, C.A. & Fedigan, L.M. (1990). Dietary differences between neighboring Cebus
capucinus groups: local traditions, food availability or responses to food profitability?
— Folia Primatol. 54: 177-186.
Cohen, J. (1960). A coefficient of agreement for nominal scales. — Educ. Psychol. Meas. 20:
37-46.
Fedigan, L.M., Gouzoules, H. & Gouzoules, S. (1983). Population dynamics of Arashiyama
West Japanese macaques. — Int. J. Primatol. 4: 307-321.
Fragaszy, D.M. & Perry, S. (2003). Towards a biology of traditions. — In: The biology of traditions: Models and evidence (Fragaszy, D.M. & Perry, S., eds). Cambridge University
Press, Cambridge, p. 1-32.
Fooden, J. & Aimi, M. (2005). Systematic review of Japanese macaques, Macaca fuscata(Gray, 1870). — Fieldiana: Zool. 104: 1-200.
Fox, E.A., van Schaik, C.P., Sitompul, A. & Wright, D.N. (2004). Intra- and interpopulational differences in orang-utan (Pongo pygmaeus) activity and diet: implications forthe invention of tool use. — Am. J. Phys. Anthropol. 125: 162-174.
Galef, B.G., Jr. (1996). Tradition in animals: field observations and laboratory analyses. —In: Interpretation and explanation in the study of animal behavior. Vol I: Interpretation,
intentionality, and communication (Bekoff, M. & Jamieson, D., eds). Cambridge University Press, Cambridge, p. 74-95.

121Inter- and intra-troop variability of stone handling

279

Hayasaka, K., Ishida, T. & Horai, S. (1991). Heteroplasmy and polymorphism in the major noncoding region of mitochondrial DNA in Japanese monkeys: Association withtandemly repeated sequences. — Mol. Biol. Evol. 8: 399-415.
Huffman, M.A. (1984). Stone-play of Macaca fuscata in Arashiyama B troop: Transmissionof a non-adaptive behavior. — J. Hum. Evol. 13: 725-735.
Huffman, M.A. (1996). Acquisition of innovative cultural behaviors in non-human primates:
A case study of stone handling, a socially transmitted behavior in Japanese macaques.
— In: Social Learning in Animals: The Roots of Culture (Galef, B., Jr. & Heyes, C.,eds). Academic Press, Orlando, FL, p. 267-289.
Huffman, M.A. (2005). Stone handling behavior in Japanese macaques, a multiple-site comparative study. — Culture Conference 2005. Max Planck Institute for Evolutionary Anthropology, Leipzig, 15th-17th of September 2005.
Huffman, M.A. & Hirata, S. (2003). Biological and ecological foundations of primate behavioral tradition. — In: The biology of traditions: Models and evidence (Fragaszy, D.M.
& Perry, S., eds). Cambridge University Press, Cambridge, p. 267-296.
Huffman, M.A. & Quiatt, D. (1986). Stone handling by Japanese macaques (Macaca fuscata):
Implications for tool use of stone. — Primates 27: 427-437.
Huffman, M.A. & Wrangham, R.W. (1994). Diversity of medicinal plant use by chimpanzees
in the wild. — In: Chimpanzee Cultures (Wrangham, R.W., McGrew, W.C., de Waal,
F.B.M. & Heltne, P.G., eds). Harvard University Press, Cambridge, MA, p. 129-148.
Humle, T. & Matsuzawa, T. (2001). Behavioural diversity among the wild chimpanzee populations of Bossou and neighbouring areas, Guinea and Côte d’Ivoire, West Africa. —Folia Primatol. 72: 57-68.
Humle, T. & Matsuzawa, T. (2002). Ant-dipping among the chimpanzees of Bossou, Guinea,
and some comparisons with other sites. — Am. J. Primatol. 58: 133-148.
Itani, J. (1958). On the acquisition and propagation of a new food habit in the troop of
Japanese monkeys at Takasakiyama. — Primates 1: 84-98.
Itani, J. & Nishimura, A. (1973). The study of infra-human culture in Japan. — In: Precultural
primate behavior (Menzel, E., ed.). Karger, Basel, p. 26-50.
Kawai, M. (1965). Newly acquired pre-cultural behavior of a natural troop of Japanese monkeys on Koshima Island. — Primates 6: 1-30.
Kawai, M., Watanabe, K. & Mori, A. (1992). Pre-cultural behaviors observed in free-ranging
Japanese monkeys on Koshima islet over the past 25 years. — Primate Rep. 32: 143153.
Kumashiro, M., Ishibashi, H., Uchiyama, Y., Itakura, S., Murata, A. & Iriki, A. (2003). Natural imitation induced by joint attention in Japanese monkeys. — Int. J. Psychophysiol.
50: 81-99.
Leca, J.-B., Gunst, N., Watanabe, K. & Huffman, M.A. (in press). A new case of fish-eatingin Japanese macaques: Implications for social constraints on the diffusion of feeding
innovation. — Am. J. Primatol.
Matsuzawa, T. & Yamakoshi, G. (1996). Comparison of chimpanzee material culture between Bossou and Nimba, West Africa. — In: Reaching into thought: The mind of thegreat apes (Russon, A.E., Bard, K.A. & Parker, S., eds). Cambridge University Press,
Cambridge, p. 211-232.
McGrew, W.C. (1998). Culture in nonhuman primates? – A. Rev. Anthropol. 27: 301-328.
McGrew, W.C. (2003). Ten dispatches from the chimpanzee culture wars. — In: Animalsocial complexity, intelligence, culture, and individualized societies (de Waal, F.B.M.
& Tyack, P. L., eds). Harvard University Press, Cambridge, MA., p. 419-439.

122

280

Leca, Gunst & Huffman

McGrew, W.C., ed. (2004). The cultured chimpanzee: Reflections on cultural primatology. —Cambridge University Press, New York.
McGrew, W.C., Baldwin, P.J., Marchant, L.F., Pruetz, J.D., Scott, S.E. & Tutin, C.E.G.
(2003). Ethoarcheology and elementary technology of unhabituated wild chimpanzees
at Assirik, Senegal, West Africa. — Paleoanthropology 1: 1-20.
McGrew, W.C., Ham, R.M., White, L.J.T., Tutin, C.E.G. & Fernandez, M. (1997). Why don’t
chimpanzees in Gabon crack nuts? – Int. J. Primatol. 18: 353-374.
McGrew, W.C., Marchant, L.F., Scott, S.E. & Tutin, C.E.G. (2001). Intergroup differences ina social custom of wild chimpanzees: The grooming hand-clasp of the Mahale mountains. — Curr. Anthropol. 42: 148-153.
Morin, P.A., Moore, J.J., Chakraborty, R., Jin, L., Goodall, J. & Woodruff, D.S. (1994). Kin
selection, social structure, gene flow, and the evolution of chimpanzees. — Science 265:
1193-1201.
Nahallage, C.A.D. & Huffman, M.A. (2007). Age-specific functions of stone handling, asolitary-object play behavior, in Japanese macaques (Macaca fuscata). — Am. J. Primatol. 69: 267-281.
Nakamichi, M., Kato, E., Kojima, Y. & Itoigawa, N. (1998). Carrying and washing of grassroots by free-ranging Japanese macaques at Katsuyama. — Folia Primatol. 69: 35-40.
Nakamura, M. & Nishida, T. (2006). Subtle behavioral variation in wild chimpanzees, withspecial reference to Imanishi’s concept of kaluchua. — Primates 47: 35-42.
Nishida, T. & Wallauer, W. (2003). Leaf-pile pulling: an unsual play pattern in wild chimpanzees. — Am. J. Primatol. 60: 167-173.
O’Malley, R.C. & Fedigan, L.M. (2005). Variability in food-processing behavior amongwhite-faced capuchins (Cebus capucinus) in Santa Rosa Park, Costa Rica. — Am. J.
Phys. Anthropol. 128: 63-73.
Panger, M.A., Perry, S., Rose, L., Gros-Louis, J., Vogel, E., McKinnon, K.C. & Baker, M.
(2002). Cross-site differences in foraging behavior of white-faced capuchins (Cebus
capucinus). — Am. J. Phys. Anthropol. 119: 52-66.
Perry, S., Baker, M., Fedigan, L., Gros-Louis, J., Jack, K., McKinnon, K.C., Manson, J.H.,
Panger, M., Pyle, K. & Rose, L. (2003a). Social conventions in wild white-faced capuchin monkeys. — Curr. Anthropol. 44: 241-268.
Perry, S. & Manson, J.H. (2003). Traditions in monkeys. — Evol. Anthropol. 12: 71-81.
Perry, S., Panger, M., Rose, L.M., Baker, M., Gros-Louis, J., Jack, K., McKinnon, K.C.,
Manson, J., Fedigan, L. & Pyle, K. (2003b). Traditions in wild white-faced capuchins.
— In: The biology of traditions: Models and evidence (Fragaszy, D.M. & Perry, S., eds).
Cambridge University Press, Cambridge, p. 391-423.
Reader, S.M. & Laland, K.N. (2001). Primate innovation: Sex, age and social rank differences. — Int. J. Primatol. 22: 787-805.
Rose, L.M., Perry, S., Panger, M.A., Jack, K., Manson, J.H., Gros-Louis, J., MacKinnon,
K.C. & Vogel E. (2003). Interspecific interactions between Cebus capucinus and otherspecies: Data from three Costa Rican sites. — Int. J. Primatol. 24: 759-796.
van Schaik, C.P. (2003). Local traditions in orangutans and chimpanzees: social learning andsocial tolerance. — In: The biology of traditions: Models and evidence (Fragaszy, D.M.
& Perry, S., eds). Cambridge University Press, Cambridge, p. 297-328.
van Schaik, C.P., Ancrenaz, M., Borgen, G., Galdikas, B., Knott, C.D., Singleton, I., Suzuki,
A., Utami, S.S. & Merill, M.Y. (2003). Orangutan cultures and the evolution of material
culture. — Science 299: 102-105.

123

Inter- and intra-troop variability of stone handling281

van Schaik, C.P., Deaner, R.O. & Merrill, M.Y. (1999). The conditions for tool use in primates: implications for the evolution of material culture. — J. Hum. Evol. 36: 719-741.
van Schaik, C.P. & Knott, C.D. (2001). Geographic variation in tool use on Neesia fruits inorangutans. — Am. J. Phys. Anthrop. 114: 331-342.
Sugiyama, Y. (1998). Local variation of tool-using repertoire in wild chimpanzees. — In:
Comparative study of the behavior of the Genus Pan by compiling video ethogram(Nishida, T., ed.). Nissindo Printer, Kyoto, p. 82-91.
Suzuki, S., Hill, D.A., Maruhashi, T. & Tsukahara, T. (1990). Frog- and lizard-eating behaviour of wild Japanese macaques in Yakushima, Japan. — Primates 31: 421-426.
Tokida, E., Tanaka, I., Takefushi, H. & Hagiwara, T. (1994). Tool-using in Japanesemacaques: Use of stones to obtain fruit from a pipe. — Anim. Behav. 47: 1023-1030.
Visalberghi, E. & Adessi, E. (2003). Food for thought: social learning about food in feeding
capuchin monkeys. — In: The biology of traditions: Models and evidence (Fragaszy,
D.M. & Perry, S., eds). Cambridge University Press, Cambridge, p. 187-212.
Watanabe, K. (1989). Fish: A new addition to the diet of Koshima monkeys. — Folia Primatol. 52: 124-131.
Weinberg, S.M. & Candland, D.K. (1981). “Stone-grooming” in Macaca fuscata. — Am. J.
Primatol. 1: 465-468.
Whiten, A. (2005). The second inheritance system of chimpanzees and humans. — Nature
437: 52-55.
Whiten, A., Goodall, J., McGrew, W.C., Nishida, T., Reynolds, V., Sugiyama, Y., Tutin,
C.E.G., Wrangham, R.W. & Boesch, C. (1999). Cultures in chimpanzees. — Nature
399: 682-685.
Whiten, A., Goodall, J., McGrew, W.C., Nishida, T., Reynolds, V., Sugiyama, Y., Tutin,
C.E.G., Wrangham, R.W. & Boesch, C. (2001). Charting cultural variation in chimpanzees. — Behaviour 138: 1481-1516.
Wrangham, R.W., de Waal, F.B.M. & McGrew, W.C. (1994). The challenge of behavioral
diversity. — In: Chimpanzee Cultures (Wrangham, R.W., de Waal, F.B.M., McGrew,
W.C. & Heltne, P.C., eds). Harvard University Press, Cambridge, MA, p. 1-18.
Yamakoshi, G. (2001). Ecology of tool use in wild chimpanzees: Toward reconstructionof early hominid evolution. — In: Primate origins of human cognition and behavior(Matsuzawa, T., ed.). Springer, Tokyo, p. 537-556.

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Available online at www.sciencedirect.com

Journal of Human Evolution 53 (2007) 691e708

Age-related differences in the performance, diffusion, and maintenanceof stone handling, a behavioral tradition in Japanese macaquesJean-Baptiste Leca a,*, Noëlle Gunst b, Michael A. Huffman caEquipe d’Ethologie des Primates, Institut Pluridisciplinaire Hubert Curien, Département Ecologie, Physiologie et Ethologie,
UMR 7178 CNRS-ULP, 23 rue Becquerel, 67087 Strasbourg, FrancebInstitute of Ecology, University of Georgia, Athens, GA 30602-2202, USAc
Section of Ecology, Primate Research Institute, Kyoto University, 41-2 Kanrin, Inuyama, Aichi 484-8506, Japan
Received 4 December 2006; accepted 23 May 2007

Abstract
Identifying the sources of behavioral diversity in non-human primates is vital to understanding the evolution of human behavior. Stone handling (SH, hereafter) is a form of object play consisting of the manipulation of stones by performing various behavioral patterns. This behavior issocially transmitted from generation to generation in Japanese macaques (Macaca fuscata), as a behavioral tradition. SH behavior in particular
may reflect on the origin and evolution of stone-tool material culture. The objective of this study was to assess how group size, age structure, andage- and sex-related differences may account for the substantial intra- and inter-troop variations in SH reported in ten troops of Japanese macaques. Our results supported the hypothesis that patterns of variation in SH across troops reflected variability in group size and composition inage classes. We found that troop size was correlated with the proportion of troop members exhibiting SH simultaneously. The effect of troop sizeon the synchronized performance of SH may reveal the contagious nature of play. Our results suggest that the age structure of the group may
affect the diffusion of SH. As predicted by the surplus energy hypothesis, a major functional hypothesis about play, intra-group variation in SH
reflected more age- than sex-related differences. SH mainly occurred and was more frequent in younger than in older individuals, whereas no
significant sex differences were found. SH episodes were shorter, more vigorous, and SH patterns were more diverse and less complex in immature than in mature individuals. The present findings reveal that age-related factors and group size may constrain the performance, diffusion,and maintenance of SH within a troop. Contrary to most other socially transmitted stone-tool using behaviors in non-human primates and early
hominids, there is no optimal SH pattern. Provided some form of social learning, the non-adaptive nature of SH may allow particular SH pattern
preferences to emerge at the group level. Our findings urge the use of an inter-populational comparative approach based on multivariate analyses
when addressing the question of the evolution of behavioral traditions in primate and human populations.
Ó 2007 Elsevier Ltd. All rights reserved.
Keywords: Cultural play behaviors; Demographic constraints; Inter-troop variation; Macaca fuscata

Introduction
Identifying the sources of behavioral diversity in nonhuman primates is vital to better understand the evolution ofhuman behavior (Wrangham et al., 1994). Recently, many

* Corresponding author.
E-mail addresses: jbtleca@yahoo.com (J.-B. Leca), nogu@uga.edu (N. Gunst),
huffman@pri.kyoto-u.ac.jp (M.A. Huffman).
0047-2484/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jhevol.2007.05.009

125

researchers have sought explanations for behavioral differences within and between populations of various primate species (Wrangham et al., 1994; Perry et al., 2003; Fox et al.,
2004; Ganas and Robbins, 2004). Patterns of behavioral variation are typically attributed to genetic, environmental, or cultural factors (Goldberg and Wrangham, 1997; Whiten et al.,
1999; Yamakoshi, 2001). By contrast, the demographic context is seldom invoked to account for differences in behavior.
Overall, group size and composition have long been disregarded as possible major factors contributing to our692

J.-B. Leca et al. / Journal of Human Evolution 53 (2007) 691e708

understanding of the expression of behavior. The pioneeringresearch by Altmann and Altmann (1979) has brought us
closer to understanding how group size and age/sex structure
can both affect and be affected by behavior. We now understand that the demographic structure of primate social groups
can play an important role in various behavioral domains suchas dispersal patterns (Clutton-Brock, 1989), infanticide (Watts,
1989), mating strategies (Goldizen, 1988), hunting, territoriality, and male social relationships (Mitani and Watts, 1999;
Mitani, 2006).
The potential influence of demographic settings in the occurrence and diffusion of behavioral traditions, however, hasreceived relatively little attention. There is reason to suspectthat group size and age- and sex-related differences could bemajor constraints shaping behavioral traditions, given that traditional behaviors are long-enduring behavioral practices
shared among members of a population, which are largely dependent on social means for their appearance, propagation,and maintenance (Fragaszy and Perry, 2003). Like social parameters, the demographic structure, such as group size, or
distribution of age and sex classes, is likely to affect the possible range of behavioral options available for individuals toacquire. Group size and composition also influence the likelihood of individual innovations on others, therefore influencing
the probability of subsequent diffusion of a behavior (Huffman
and Hirata, 2003).
When considering the influence of demographic factors on
cultural transmission, mathematical models have yielded controversial results with respect to group size. Most mathematical models assume temporally accelerating rates of diffusion
within a population, with more and more potential demonstrators available to the remaining na€ıve individuals (CavalliSforza and Feldman, 1981). Under such circumstances, theexpected proportion of individuals performing the novel behavior will increase as group size increases (Lefebvre, 1995).
However, it seems that group size is a positive factor only below a certain threshold. Large-sized groups consist of many
uninformed bystanders who could also act in ways which
could slow down the diffusion (Lefebvre and Giraldeau,1994). While group size might be an important factor involvedin cultural transmission, it is not typically included in thesestudies of transmission, probably because a large variety of demographic settings is desirable for comparative analyses. It
should be noted that when considered alone, group size hadno significant effect on the diffusion rate of various novel behaviors in Japanese macaques (Huffman and Hirata, 2003).
Depending on the nature of the newly acquired behavior(e.g., a novel foraging technique which requires manual dexterity or physical strength, or a new form of play), the innovation may be restricted to a particular subset of the group (e.g.,
adult males or juveniles). With regards to the demographic
structure of the group, it is acknowledged that new habits
spread through ‘‘pivotal’’ individuals and follow certain set
transmission paths determined by the age and sex classes towhich the innovators belong (Cambefort, 1981; Huffman
and Quiatt, 1986; de Waal and Seres, 1997). Regarding adaptive food-related behaviors with a potential survival value, age

and sex differences in behavioral innovations and sociallylearned behaviors have been extensively described in many
primate species, including humans (see Choleris and Kavaliers, 1999; Reader and Laland, 2001, for reviews). In chimpanzees, gender affects the development and mastery ofvarious cultural tool-using behaviors. Young females acquirethe ‘‘termite-fishing’’ skill earlier than young males (Lonsdorf,2005). As adults, females devote more time to the termitefishing and nut-cracking activities, and are more proficientat these tasks than males (McGrew, 1979; Boesch and Boesch,1984). In Japanese macaques, novel food-processing techniques, such as ‘‘potato-washing’’ and ‘‘wheat-washing,’’ werefirst invented by a young female and then acquired by othergroup members except subadult and adult males (Kawai,1965).
In Homo sapiens, a sex-based difference in innovation andskill learning also exists. Males display more risk-taking behaviors than females do (Daly and Wilson, 1983), which
may result in more technological and behavioral innovation(Rogers, 1995). Age influences food production activities,
such as hunting or gathering, in traditional societies (Walker
et al., 2002). The influence of age and sex on the emergenceand propagation of behavioral traditions is likely to dateback at least to the last common ancestor of chimpanzees
and humans, and probably even before (Lonsdorf et al.,2004). Thus, by both facilitating and limiting the manifestation of adaptive behaviors, demographic factors, and particularly group size and age/sex composition, can be regarded as
major constraints to the emergence, transmission, and longterm diffusion of traditional behaviors.
When considering non-adaptive behaviors, such as object
play, age is also likely to be a key factor, whereas no consistenteffect of sex is expected. The surplus energy hypothesis, a major functional hypothesis about play, proposes that play enables the adaptive expenditure of excess metabolic energy(Barber, 1991). Since young mammals are often not limitedin energy, Barber (1991) argues that play should be more frequent, more vigorous, but shorter in young than in older individuals, regardless of sex. Most studies conducted on various
taxa, including rodents, carnivores, marsupials, and nonhuman primates, showed major age-related differences, withyoungsters playing considerably more often than older individuals, but no significant sex differences (see Glickman andSroges, 1966; Fagen, 1981, for a review). In chimpanzees,
the traditional play behavior called ‘‘leaf-pile pulling’’ ismainly performed by young individuals with no differences
between males and females (Nishida and Wallauer, 2003). In
humans, not only young children, but also boys play morewith objects than older individuals and girls (Pellegrini andGustafson, 2005).
Categorized as a form of solitary object play, stone handling (SH) consists of manipulating stones in combination
with various behavioral patterns (Huffman, 1984). For example, individuals may be observed putting a stone in their mouthand making it move inside their mouth with their tongue,
clacking or rubbing stones together, or repeatedly pounding
a stone on a substrate. Initially transmitted among young
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cohorts of playmates, then acquired from mother to offspringthrough observational learning, and socially passed from generation to generation in a long-term studied troop of Japanesemacaques (Macaca fuscata), SH is regarded as a behavioral
tradition (Huffman, 1984; Huffman and Quiatt, 1986; Huffman, 1996; Huffman and Hirata, 2003). By taking an ethnographic approach to chart inter- and intra-group diversity in
SH, Leca et al. (2007a) revealed substantial variability in thefrequency of occurrence and form of SH between ten troops.
Investigating the effect of age and sex on the patterns of variation of SH in non-human primates may offer new insights
into the origin of object play in hominids. Findings fromtwo free-ranging and one captive troop of Japanese macaquessuggest that age-related differences are involved in the performance of SH. Although individuals of all ages could handle
stones, analyses showed that the young stone handled far
more often and displayed more various behavioral patterns
than adults (Huffman, 1996; Huffman and Hirata, 2003;
Nahallage and Huffman, 2007). Like in most studies on object
play in animals, no consistent sex differences were foundamong immatures and adults (Huffman, 1996; Nahallage andHuffman, 2007).
A long-term study on SH in a captive troop has examined
the possible biological functions of this activity in Japanesemacaques with special reference to hypotheses proposed foradaptive value of object play in animals (Nahallage andHuffman, 2007). These authors have attributed age-relateddifferences in the performance of SH to possible age-specificbenefits of this activity. Nahallage and Huffman (2007)
showed that youngsters exhibited frequent and short SH bouts
including locomotion and vigorous behavioral patterns,
whereas adults engaged in fewer but longer SH episodes involving more stationary and complex body actions. These results were consistent with the motor-training hypothesis
developed to explain how play behaviors may contribute to
the neuro-motor development of critical behavioral patterns
in young individuals (see Byers and Walker, 1995). As a psychologically relaxing activity, SH in adults was hypothesized
to have long-term beneficial neurophysiological effects, suchas helping to maintain neural systems and prevent the deterioration of cognitive abilities in older monkeys (Nahallage andHuffman, 2007).
Regarding a possible effect of group size, an analysis conducted over a 10-year time period at Arashiyama, Japan
showed that the diffusion rate of SH (defined as the yearly total number of individuals for which SH was observed) was
considerably higher in a large-sized troop of Japanese macaques prior to a natural troop fission (with 236 troop members) than after the troop’s division into two smaller troops,
consisting of 139 and 97 members, respectively (Huffman
and Hirata, 2003). SH at Arashiyama was not acquired byadult individuals. Instead, only young monkeys continued topractice this activity into adulthood (Huffman, 1984; Huffman
and Quiatt, 1986). Huffman and Hirata (2003) demonstrated
that the increase in the number of new stone handlers resulted
from the addition of infants born as the initial spread of thisnovel behavior occurred horizontally through young troop
127

693

members, and diffused vertically from mother to offspring
thereafter (Huffman, 1984). These findings on two troops suggest that the performance and diffusion of SH may be affectedby group size and age, but not by sex. The question arises as towhether this tendency reflects a generalization of these effects
at the species level.
The goal of this paper is to assess how group size, age
structure, and age- and sex-related differences may accountfor the substantial intra- and inter-troop variations in SH reported in ten troops of Japanese macaques (cf. Leca et al.,2007a). First, due to the evidence from a previous study on effect of group size on SH diffusion rate (Huffman and Hirata,
2003), and based on our knowledge of the pathways of SH diffusion according to age classes (Huffman, 1984; Huffman and
Quiatt, 1986), we hypothesized that patterns of variation in SH
across troops reflected variability in group size and composition in age classes. We will test the two following predictions
derived from this hypothesis: Prediction #1: Considering thatthe sight of conspecifics engaged in SH may strengthen an
individual’s assessment that the current environmental conditions are sufficiently safe to start playing, and given the contagious nature of play activities, we predict that the larger thegroup, the more amplified the contagion effect, and the higher
the proportion of troop members exhibiting SH simultaneously; Prediction #2: Since the diffusion of SH depends
on age structure, we predict that a group with abnormal age
structure (i.e., missing age classes) will show a lower proportion of stone handlers and a lower frequency of SH thannormal groups with all age classes present.
Second, based on the surplus energy hypothesis (Barber,1991), the premise that SH is a form of object play (Huffman,
1984), and due to the evidence from previous studies of an effect of age on SH (Huffman, 1996; Huffman and Hirata, 2003;
Nahallage and Huffman, 2007), we hypothesized intra-groupvariation in SH reflected more age- than sex-related differences. Accordingly, we will test the six following predictions:
Prediction #3: SH occurrence will be higher in young than inolder troop members, whereas no significant sex differences inSH occurrence is expected; Prediction #4: SH frequency will
be higher in young than in older troop members, whereas no
significant sex differences in SH frequency is expected; Regarding SH form, SH episodes will be shorter (Prediction#5) and more vigorous (Prediction #6) in young than in older
troop members; SH patterns will be less diverse (Prediction#7) but more complex (Prediction #8) in mature than in immature individuals.
To address these questions, we conducted a systematiccomparative investigation of the occurrence, frequency, duration, and form of SH among ten troops of Japanese macaquescharacterized by high variability in size and age structure.
We will discuss the implications of our findings for the possible role of SH in neuro-motor and cognitive processes
across age classes (after Nahallage and Huffman, 2007).
We will draw conclusions that can be generalized to the performance and diffusion of SH at the species level, and provide insights into the origin of object play and stone-tool
use in hominids.

J.-B. Leca et al. / Journal of Human Evolution 53 (2007) 691e708

694

Materials and methods

conducted between 7:00 and 18:00. Visibility was excellent.
We sampled captive troop members from observation platforms overhanging the enclosures. Free-ranging troop members could be approached and sampled within 3e5 m.

General study conditions
The species under study was the Japanese macaque(Macaca fuscata). The first two authors, occasionally assisted
by M.A.H. and C.A.D. Nahallage, observed a total of ten
troops at six geographically isolated sites in Japan from August 2003 to February 2005. Four troops lived in large outdoor
enclosures in Inuyama, Aichi Prefecture (PRI Arashiyama ¼
Ara.A, Wakasa ¼ Wak.A, Takahama ¼ Takh., and Japan Monkey
Centre Yakushima macaques ¼ JMC), and six troops werefree-ranging (Koshima, Miyazaki Prefecture ¼ Kosh., Arashiyama, Kyoto Prefecture ¼ Ara.E, Shodoshima, Kagawa
Prefecture ¼ Sho.A and Sho.B, Takasakiyama, Oita Prefecture ¼
Tak.B and Tak.C).
Captive troops were mainly supplied with commercial primate pellets, vegetables, or fruits. Free-ranging troop members
gathered regularly around feeding sites where they were artificially provisioned with cereal grains by the staff techniciansof the Koshima Field Station, Kyoto University (Kosh.) or by
the staff members and managers of monkey parks (Ara.E,
Sho.A, Sho.B, Tak.B, and Tak.C). The free-ranging troops living at the same site (Sho.A and Sho.B at Shodoshima, and
Tak.B and Tak.C at Takasakiyama) had overlapping homeranges and came into occasional contact. Regarding the ethicaltreatment of the study subjects, we complied with the policies,
regulations, and guidelines implemented under protocols developed by the Kyoto University Primate Research Institute.
We used two types of age classifications to divide agegroups for observation, analysis, and description (Table 1).
Six age classes were used for observations (yearling, juvenile,subadult, young adult, middle-aged adult, and old adult: after
Fedigan et al., 1983), and three broader age group categories(young, growing, and grown-up) for the purpose of some analyses, according to the size of the data set. For each troop, demographic variables including troop size and the distributionof troop members according to age and sex classes are shownin Table 2. The ten studied troops varied both in size and composition: two small-sized captive troops (Ara.A and Wak.A),
two medium-sized captive troops (Takh. and JMC), two medium-sized free-ranging troops (Kosh. and Ara.E), and fourlarge-sized free-ranging troops (Sho.A, Sho.B, Tak.B, andTak.C). The proportion of individuals belonging to each of
the different age and sex classes also varied. For only
Ara.A, Wak.A, Takh., Kosh., and Ara.E were subjects individually identified. The exact age in years of each individual andtheir matrilineages were known. For JMC, Sho.A, Sho.B,
Tak.B, and Tak.C, every sampled subject was categorized according to its sex and estimated age class. Observations were

Data collection
We used the same observation procedure for all troops, except Tak.B and Tak.C (see below for details). The two main
observational methods used were continuous focal-animal
sampling and instantaneous group scan sampling (Altmann,
1974). Behavioral data collection was supplemented with ad
libitum sampling when necessary (Altmann, 1974).
Focal sampling
We video-recorded every focal session using Sony digital
video cameras (DCR-TRV22 and DCR-TRV33). Wheneverpossible, the focal individual was filmed from the front, withina one-meter square area. We focused on all the behaviors andinteractions of the focal individual. Since the field observation
conditions did not allow us to use a totally random focal sampling method, we selected the focal individual using a semirandom procedure. The daily observation period was divided
into one-hour blocks. To select the focal individual independently of its activity, the subject (or member of each age
and sex class, when focal subjects were not individually identified) with least cumulative data was given priority.
We recorded the starting time of each focal session. Following protocol used in previous surveys carried out at Takasakiyama and Arashiyama (see Huffman, 1996), the typicalduration of a focal session was 15 minutes. If the focal individual performed SH activity during the last 2 minutes of thisperiod of time, the observation was extended for 5 minutes
and continued until the SH bout ended.
Scan and ad libitum samplings
Before and after each focal session, the troop was scannedfor evidence of any SH activity. For each scan-sampled stone
handler, we recorded individual identity or age and sex class,and whenever possible, the SH patterns observed (Table 3).
The observer recorded scans on data sheets, visually scanning
across the enclosure for captive troops, or by walking fromone side of the free-ranging troop to the other, in a set direction, so that each individual was sampled only once in a given
scan session.
To supplement each troop’s SH data set, observers devoted
an average of 38.8  31.8% of total observation time to thecollection of ad libitum data on individuals performing SH.
Whenever possible, ad libitum sessions were video-recorded,or otherwise collected on a notepad. For Tak.B and Tak.C,

Table 1
Two types of age classifications used in the observations, analyses, and descriptions
Age in years

1 year2e3 years

4e6 years

7e10 years

11e15 years

16eyears

Classification 1
Classification 2

Young
Yearling

Juvenile

Growing
Subadult

Young adult

Grown-up
Middle-aged adult

Old adult

128

J.-B. Leca et al. / Journal of Human Evolution 53 (2007) 691e708695Table 2Distribution of individuals according to age and sex classes in each studied troop. F: Female; M: Male; Asterisk: In large-sized troops, figures were approximately
assessed during yearly surveys (Sho.A and Sho.B: after Watanabe, pers. comm.; Tak.B and Tak.C: after Kurita, pers. comm.)
Age and sex classes
Yearling

Juvenile

Subadult

Young adult

Middle-aged adult

Old adult

Total numberof individuals

Troop
Ara.A
Wak.A
Takh.
JMC
Kosh.
Ara.E
Sho.A*
Sho.B*
Tak.B*
Tak.C*

Female
1
0
3
3
2
7
20
10
30
68

M
2
1
6
1
3
5
20
10
35
69

Female
1
2
4
9
11
10
80
60
60
96

M
2
2
2
12
10
5
80
60
60
95

Female
0
4
1
8
7
15
60
50
50
80

M
0
3
4
14
8
4
50
40
20
20

Female
0
3
7
15
7
20
30
30
37
70

M
0
0
2
5
12
5
10
20
10
10

Female
4
2
4
11
4
30
40
30
60
86

M
0
0
0
9
7
2
10
10
16
20

Female
5
2
10
11
8
31
40
20
50
50

M
3
0
3
4
9
7
10
10
10
12

18
19
46
102
88
141
450
350
438
676

Total

144

152

333

328

275

163

219

74

271

74

227

68

2328

Table 3Thirty-six SH patterns performed by Japanese macaques and categorized according to general activity patterns (after Nahallage and Huffman, 2007)
Category

NameDefinition

Investigative activities

Bite
Hold
Lick
Put in mouthMove inside mouth
Sniff

Bite a stone
Pick up a stone in one’s hand and hold on to it, away from the body
Lick a stone
Put a stone in one’s mouth and keep it for some time
Make a stone move inside one’s mouth with tongue or hands
Sniff a stone

Locomotion activities

Carry
Carry in mouth
Grasp walkMove and push/pull
Toss walk

Carry a stone grasped in hand from one place to another
Carry a stone in mouth while locomoting
Walk with one or more stones in the palm of one or both hands
Push/pull a stone with one or both hands while walking forward/backward
Toss a stone ahead (repeatedly) and pick it up while walking

Collection (gathering) activities

CuddleGather
Grasp with hands
Pick up
Pick and drop
Pick up small stones

Take hold of, grab, or cradle a stone against the chest
Gather stones into a pile in front of oneself
Clutch a stone or a pile of stones gathered and placed in front of oneself
Pick up a stone and place it into one’s hand
Pick up a stone and drop it repeatedly
Pick up small stones and hold them between fingertips (like the picking up of wheat grains)

Complex manipulative activities*

Clack
Combine with object

Clack stones together (both hands moving in a clapping gesture)
Coordinated use of a stone with an object different from a stone (food, piece of wood, leaf,
metal, etc.)
Strike a stone against another held stationary
Strike or rub a stone against another held in mouth
Turn a stone over with both hands
Pound a stone on a substrate
Roll a stone in one’s hands
Rub or roll a stone on a substrate
Rub stones together
Hold a stone in one hand and rub it with the other (like potato-washing)
Rub a surface with a stone held in mouth
Scatter stones about, on a substrate, in front of oneself
Take stone(s) in one’s open palm hand and shake the stone(s) with the hand moving back and forthSlap, tap, or pound a stone with one’s fingertips or palm of handSpin a stone around on the ground using two fingers of one hand or both hands (one moving
forward and the other backward)
Self or allo-groom with a stone (put/rub a stone on fur)
Swipe stones together (both hands moving in a sweeping gesture)Throw a stone
Put a stone in water or pick up a stone from water and rub it with hands

Flint
Flint/rub/in mouth
Flip
Pound on surface
Roll in hands
Rub/roll on surface
Rub stones together
Rub with hands
Rub with mouth
Scatter
Shake in hands
Slap
Spin
Stone groom
Swipe
Throw
Wash

*
Combine a stone with other stones, other objects, or substrate and/or perform behavioral patterns involving percussive actions or a series of at least threedifferent actions, repeated or not.

129

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J.-B. Leca et al. / Journal of Human Evolution 53 (2007) 691e708

we did not collect focal sessions, but only video-recorded ad
libitum sessions during the periods after feeding, when SH ismost likely to occur (Huffman, 1996). In some cases, wewere able to record complete ad libitum sessions. The sampled individual was filmed through the entire sequence ofSH, from start (a few minutes after provisioning time, immediately after the macaque left the feeding site and picked up
or touched stones) to finish (five minutes after the last stone
was discarded).
Data analysis
Based on video-records, J.-B.L. transcribed each focal session onto a data sheet and measured the duration of all activities to the second (feeding, foraging, locomoting, resting,socializing, SH, non-stone object exploring, and other). EachSH pattern was also recorded. Data were then entered into
a computer for processing and statistical analysis.
We distinguished two types of SH records: SH bouts collected from focal sessions or complete ad libitum videorecorded sessions, and SH notes collected from scan sessions
or incomplete ad libitum sessions. A SH bout (Huffman, 1996)
is defined as the display of SH activity with possible pauses of
no longer than 120 seconds. If the individual resumed SH
within 120 seconds after pausing, then the two SH episodes
were considered as a single SH bout. If SH was resumed
more than 120 seconds after pausing, this would mark the startof a new SH bout. A SH bout could consist of several SH
phases interspersed with pauses of no longer than 120 seconds.
We defined a SH phase as the uninterrupted display of SH
activity within a SH bout.
We defined the total troop observation time as the total timespent observing each troop, including focal time, scan time,
and time spent collecting ad libitum data (Table 4). When multiple observers were present (i.e., during focal and ad libitum
sessions), two types of observation time were distinguished.
First, observation time during focal sessions was animalbased, and calculated by adding up the focal hours the animals
were observed. Second, observation time during ad libitum
sessions was observer-based, and calculated by adding up
the times each observer viewed the animals. The occurrenceof SH behavior and the presence of specific SH patterns
were determined by taking into account focal time, scantime, and ad libitum time. The frequencies of SH patterns,
as well as the duration and general form of SH bouts, were estimated from focal sessions and complete ad libitum sessions.
The frequencies of SH bouts were calculated from focal time
only.
To qualify as unequivocally present in a particular troop,
SH behavior must have been observed at a rate of at least
one record (SH bout or SH note) over 20 hours of total observation time (after Whiten et al., 1999, 2001). We defined SH
frequency as the number of SH bouts per focal hour. We referred to SH prevalence as the mean percentage of stone handlers among individuals sampled in scan sessions collectedduring the most frequent SH activity period. For troops inwhich provisioning had no significant effect on SH frequency(Ara.A, Wak.A, JMC, and Kosh.; cf. Leca et al., 2006), allscan sessions were taken into account. Since provisioning
had a significant effect on SH frequency and/or SH prevalencein other troops (cf. Leca et al., 2006), only scan sessions collected within 30 minutes after provisioning were taken into account for Ara.E, Sho.A, Sho.B, Tak.B, and Tak.C, and only
scan sessions collected during non-provisioning periods wereconsidered for Takh.
To assess SH occurrence at the individual level, we ascribedeach troop member to one of the three following SH categories: verified stone handler, verified non-stone handler, or
non-verified individual. In troops with individually identified
members (Ara.A, Wak.A, Takh., Kosh., and Ara.E), an individual was labeled a verified stone handler if it had been
observed to SH at least once during the troop’s total observation time. In a middle-sized troop with unidentified members(JMC), J.-B.L. determined the number, age, and sex of verified
stone handlers based on a comparison of physical features,age, and sex class of video-recorded stone handlers (67 different individuals identified out of 131 SH bouts and 91 SH
notes). In the large-sized troops with unidentified members(Sho.A, Sho.B, Tak.B, and Tak.C), we determined the number,age, and sex of verified stone handlers based on the maximum
number of stone handlers sampled during scan sessions. Welabeled an individual as a verified non-stone handler if it had
been sufficiently sampled (at least 2 hours of focal session
and 50 scan sessions) but was never observed SH. When an
individual was not observed SH but was insufficiently sampled,
it was labeled as non-verified.
We used several variables to assess the form of SH. We
evaluated SH persistence by calculating the mean duration of
SH bouts, and duration and number of SH phases per bout.
To evaluate SH vigorousness: 1) we measured the simultaneous performance of two SH patterns by the same individual,
defined as double SH patterns, 2) we calculated the number ofchanges in the sequence of SH patterns performed per SH
bout, defined as SH pattern turnover, and 3) we calculated
the number of different SH patterns performed per SH bout defined as SH pattern variety per bout. For example, in the following sequence of SH patterns: clack, bite, clack, and bite,the SH pattern turnover is three, and the SH pattern variety
per bout is two. To assess SH pattern diversity, we calculated
the total number of different SH patterns observed in each age
class, and derived from all available SH bouts and notes, defined as age-specific inclusive diversity of SH patterns. To
evaluate SH pattern complexity, we measured the frequencyof SH patterns grouped into three levels based on the four
categories of general activity patterns (Table 3): simple SH
patterns (belonging to the investigative and locomotion activities, such as lick, sniff, or carry a stone), intermediate SH
patterns (collection/gathering activity patterns, such as cuddle
or gather stones), and complex SH patterns (complex manipulative activities, such as combine with object, wash, clack, or
rub stones together).
In Table 4, we present the total data sets per age class andper troop. For analyses regarding SH frequency, we drew on
all focal sessions. The Sho.B, Tak.B, and Tak.C troops were130

J.-B. Leca et al. / Journal of Human Evolution 53 (2007) 691e708697

Table 4
Data sets collected according to age classes in each studied troop. Total: All age classes pooled; T.O.T.: total observation time; FT: Focal time (total duration inhours of focal sessions); SH Bt (F, CAL): Number of SH bouts collected during focal sessions (n.a.: not available), and during complete ad libitum sessions; SH Nt(IAL): Number of SH notes collected during incomplete ad libitum sessions
Age class
Troop
Ara.A
FT
SH Bt (F, CAL)SH Nt (IAL)Wak.AFTSH Bt (F, CAL)SH Nt (IAL)Takh.
FTSH Bt (F, CAL)SH Nt (IAL)JMCFTSH Bt (F, CAL)SH Nt (IAL)Kosh.
FTSH Bt (F, CAL)SH Nt (IAL)Ara.E
FTSH Bt (F, CAL)SH Nt (IAL)Sho.AFTSH Bt (F, CAL)SH Nt (IAL)Sho.B
FTSH Bt (F, CAL)SH Nt (IAL)Tak.B
FTSH Bt (F, CAL)SH Nt (IAL)Tak.CFTSH Bt (F, CAL)SH Nt (IAL)

Yearling

Juvenile

Subadult

Young adult

Middle-aged adult

Old Adult

Total

23.3
12, 0
10

23.3
1, 0
15

n.a.
n.a.
n.a.

n.a.
n.a.
n.a.

31.5
0, 1
2

62.0
1, 0
1

140.1
14, 1
28

10.0
2, 4
18

39.3
16, 1445

59.8
35, 36
140

27.8
0, 4
3

19.8
4, 1
5

18.0
2, 3
13

174.7
59, 62224

70.2
108, 6
267

42.7
68, 5
254

39.9
38, 4
206

73.1
56, 6
190

31.1
17, 3
72

96.6
22, 4
210

353.6
309, 28
1199

4.3
2, 6
4

7.5
6, 38
33

12.3
10, 27
24

10.5
1, 24
27

13.8
3, 4
3

6.3
0, 0
0

54.7
22, 99
91

13.3
5, 8
2

38.0
4, 6
5

30.3
0, 0
0

42.5
0, 0
0

38.0
0, 0
0

53.3
0, 0
0

215.4
9, 14
7

14.2
39, 8
57

14.9
57, 8
97

19.6
39, 3
75

21.1
56, 7
106

38.4
50, 2
106

52.4
76, 7
138

160.6
317, 35
579

5.0
13, 4
3

3.9
8, 3
4

3.8
6, 3
8

0.5
0, 0
4

3.1
3, 0
4

0.5
0, 0
4

16.8
30, 10
27

0.0
0, 1
10

0.5
3, 10
32

0.5
1, 8
16

0.0
0, 4
4

0.3
0, 2
4

0.0
0, 1
1

1.3
4, 26
67

n.a.
0, 9
17

n.a.
0, 11
14

n.a.
0, 17
14

n.a.
0, 9
15

n.a.
0, 11
13

n.a.
0, 2
2

n.a.
0, 59
75

n.a.
0, 14
64

n.a.
0, 67
163

n.a.
0, 44
70

n.a.
0, 32
51

n.a.
0, 18
41

n.a.
0, 7
2

n.a.
0, 182391

T.O.T.
179.9

224.6

449.2

99.1

339.7

431.3

77.6

51.5

22.8

73.8

excluded from these analyses because focal data were insufficient or not available. Among the other troops, focal sessions
lasting less than 15 minutes (i.e., when the focal subject waslost) were excluded from these analyses. We drew on all SH
bouts available for analyses on SH persistence and vigorousness. We drew on all SH bouts and SH notes available for analyses about SH pattern diversity per age class (defined as thenumber of different SH patterns observed in all individuals belonging to the same age class). For captive troops, we onlyused scans sessions in which at least 80% of troop members
were sampled. For free-ranging troops, we only consideredscans sessions taking into account at least 60% of troop members. Individuals aged less than one year old were not taken
into account in the analyses.
131

We verified inter-observer reliability between the two main
observers, J.-B.L. and N.G. using the kappa coefficient (Martin and Bateson, 1993). Based on individual identities, activities, and interactions, we found k ¼ 0.88, 0.92, and 0.96,
respectively. To measure the extent to which a single observer
obtains consistent results when transcribing the same videorecorded behaviors on different occasions, J.-B.L. transcribed
two times the same samples of SH video-records, involving
a total of 630 sample points. A good intra-coder reliability
kappa coefficient was also obtained: k ¼ 0.84 (cf. Martin
and Bateson, 1993). In most analyses, we reported meanvalues  the standard deviation (SD). When the assumptionsof normality, independence, and homogeneity of varianceswere verified, we used one-way ANOVAs to test the effectJ.-B. Leca et al. / Journal of Human Evolution 53 (2007) 691e708

698

rs ¼ 0.588, p ¼ 0.074), or inclusive diversity of SH patterns
at the group level (N ¼ 10, rs ¼ 0.061, p ¼ 0.867).
In Fig. 2aej, we present an inter-troop comparison of the
distribution of stone handlers and non-stone handlers according to age and sex class. We verified Prediction #2 that a groupwith abnormal age structure will show a lower proportion ofstone handlers and a lower frequency of SH than groups
with all age classes present. Ara.A was the only troop withan age gap in the distribution of group members: The growing
age class (subadult and young adult) was missing. Interestingly, among the troops in which SH was present in all age
classes (i.e., all the studied troops except Kosh.), Ara.A
showed the highest proportion of verified non-stone handlers
and the lowest SH frequency in the grown-up class (Fig. 2
and Table 5).
Although SH was found to be present in all troops studied,
we found marked differences in the presence of SH according
to age classes. For troops in which the focal data set was sufficient (at least 50 focal hours), except for Kosh. (i.e., Ara.A,
Wak.A, Takh., JMC, and Ara.E), most verified non-stone handlers were aged 11 or more (i.e., middle-aged or old adults;
eight individuals out of eight verified non-stone handlers in
Ara.A, one out of two in Wak.A, three out of three in Takh.,eight out of nine in JMC, and nine out of nine in Ara.E). Conversely, among immature individuals (yearlings, juveniles, andsubadults), 100% of verified individuals in these troops werestone handlers. In troops with few non-verified individuals,(i.e., to the exclusion of Sho.A, Sho.B, Tak.B, and Tak.C),
we found no significant sex difference among age classes in
the proportion of verified stone handlers (Ara.A: c22 ¼ 5.8,of age on the frequency and form of SH. When these assumptions were not verified, we used non-parametric tests (MannWhitney tests if two age classes were tested, and Kruskal-Wallis
tests if more than two age classes were tested). We used
Spearman rank-order correlation tests to evaluate the relationships between troop size and SH prevalence or SH frequency.
To test the sex differences in SH occurrence among age
classes, we used a chi-square test of independence from acontingency table (cf. Siegel and Castellan, 1988). Statisticalanalyses were performed using the SPSS 12.0 analytical program. Tests were two-tailed and significance levels were set
at a ¼ 0.05.

Results
Effect of troop size and composition on SH prevalenceand occurrence
We found a statistically significant positive correlation between troop size and SH prevalence (Spearman rank-order correlation test, N ¼ 10, rs ¼ 0.842, p ¼ 0.002). The correlation
was still significant after excluding the outlier dot Sho.A
that was outside the range of  2 SD around the regression
line (N ¼ 9, rs ¼ 0.800, p ¼ 0.010). We verified Prediction #1
stating that the larger the group, the higher the proportion of
troop members exhibiting SH simultaneously (Fig. 1a). By
contrast, troop size was not significantly correlated with SH
frequency (N ¼ 7, rs ¼ 0.679, p ¼ 0.094; Fig. 1b), SH persistence, defined as the mean duration of SH bouts (N ¼ 10,

(a)

35

Sho.A

SH prevalence

30
25
20
15
10

Tak.C
Wak.A
Ara.A
Ara.E

Sho.B

5
0
0
100
-5
Takh. Kosh.
3.5

200

300

Tak.B

400

500

600

700

800

Troop size

JMC
Ara.E

(b)

SH frequency

3
2.5

Sho.A

2
1.5
Takh.

1
0.5

Wak.A

JMC

0

100

0
Ara.A

50
Kosh.

150

200

250

300

350

400

450

500

Troop size

Fig. 1. SH prevalence (a), defined as the mean percentage of stone handlers among individuals sampled in scan sessions collected during the most frequent SH
activity period, and SH frequency (b), defined as the number of SH bouts per focal hour, according to troop size; Slopes for line of best fit ¼ 0.039 and 0.006,
respectively; Round shapes represent captive troops and triangular shapes represent free-ranging troops.

132

Age
OlAd
MdAd
YgAd
SuAd
Juv
Yrg

Age
OlAd
MdAd
YgAd
SuAd
Juv
Yrg

5 4 3 2 1
1 2 3
Nf = 11 Ntot = 18 Nm = 7

4 3 2 1
1 2 3
Nf = 13 Ntot = 19 Nm = 6(a) Ara.A(b) Wak.A

Age
OlAd
MdAd
YgAd
SuAd
Juv
Yrg

Age
OlAd
MdAd
YgAd
SuAd
Juv
Yrg
10 9 8 7 6 5 4 3 2 1
1 2 3 4 5 6
Nf = 29 Ntot = 46 Nm = 17(c) Takh.

15 14 13 12 11 10 9 8 7 6 5 4 3 2 1
1 2 3 4 5 6 7 8 9 1011121314
Nf = 57 Ntot = 102 Nm = 45(d) JMC
Age
OlAd
MdAd
YgAd
SuAd
Juv
Yrg

1110 9 8 7 6 5 4 3 2 1
1 2 3 4 5 6 7 8 9 10 11 12
Nf = 39
Ntot = 88 Nm = 49(e) Kosh

31 30 29 28 27 26 25 24 23 22 21 20 19 18 17 16 15 14 13 12 11 10 9 8 7 6 5 4 3 2 1
1 2 3 4 5 6 7
Nf = 113 Ntot = 141 Nm = 28(f) Ara.E
Age
OlAd
MdAd
YgAd
SuAd
Juv
Yrg

Age
OlAd
MdAd
YgAd
SuAd
Juv
Yrg

80 75 70 65 60 55 50 45 40 35 30 25 20 15 10 5
5 10 15 20 25 30 35 40 45 50 55 60 65 70 75 80
Nf = 270 Ntot = 450 Nm = 180

60 55 50 45 40 35 30 25 20 15 10 55 1015202530354045505560
Nf = 200 Ntot = 350 Nm = 150(g) Sho.A(h) Sho.B
Age
OlAd
MdAd
YgAd
SuAd
Juv
Yrg

60 55 50 45 40 35 30 25 20 15 10 5
5 10 15 20 25 30 35 40 45 50 55 60
Nf = 287 Ntot = 438 Nm = 151(i) Tak.B

Age
OlAd
MdAd
YgAd
SuAd
Juv
Yrg

J.-B. Leca et al. / Journal of Human Evolution 53 (2007) 691e708

Age
OlAd
MdAd
YgAd
SuAd
Juv
Yrg

95 90 85 80 75 70 65 60 55 50 45 40 35 30 25 20 15 10 5
5 10 15 20 25 30 35 40 45 50 55 60 65 70 75 80 85 90 95
Nf = 450 Ntot = 676 Nm = 226(j) Tak.C

Fig. 2. Inter-troop comparison of the distribution of stone handlers and non-stone handlers according to age and sex classes. Yearling, Juv: Juvenile, SuAd: Subadult, YgAd: Young adult, MdAd: Middle-aged adult,
OlAd: Old adult; Left part of the distributions represents the number of females (Nf), right part represents the number of males (Nm); Ntot: Total number of individuals; Black areas indicate verified stone handlers,
white areas indicate verified non-stone handlers, grey areas indicate non-verified individuals.

699

133

700
Table 5
SH frequency (mean  SD), defined as the number of SH bouts per focal hour, according to the two degrees of age classes (see Methods for detail). n/a: Age class not present; Yng: Young, Grg: Growing, Gup:
Grown-up, Yrg: Yearling, Juv: Juvenile, SuAd: Subadult, YgAd: Young Adult, MdAd: Middle-aged Adult, OlAd: Old Adult; Three types of tests were used (see Data analysis for detail): Mann-Whitney tests (MW,z value), Kruskal-Wallis tests (KW, chi-square value), and one-way ANOVAs (F values); Figures in brackets: Number of focally-sampled individuals
Troop

Age classes # 2
Yearling
Juvenile
Subadult
Young Adult
Middle-aged
Adult
Old Adult
TestpSig. diff.

Ara.A

Wak.A

Takh.

JMC

Kosh.

Ara.E

Sho.A

0.28  0.28 [6]n/a0.01  0.04 [12]MW ¼ 2.669
0.032
Yng > Gup*

0.36  0.34 [5]0.38  0.48 [10]0.15  0.19 [4]KW ¼ 0.808, df ¼ 2
0.668

1.67  0.56 [15]0.80  0.73 [14]0.32  0.40 [17]F2,45 ¼ 24.301<0.001
Yng > Grg*
Yng > Gup*
Grg > Gup*

0.68  1.73 [20]0.44  1.40 [32]0.15  0.76 [22]KW ¼ 6.235, df ¼ 2
0.034
Yng > Gup**
Yng > Grg*

0.18  0.24 [13]0.00  0.00 [25]0.00  0.00 [25]H ¼ 25.020, df ¼ 2<0.001
Yng > Grg*
Yng > Gup*

4.19  2.03 [24]3.28  2.46 [36]2.13  1.89 [67]F2,126 ¼ 9.070<0.001
Yng > Gup*
Grg > Gup*

3.36  2.96 [22]2.35  2.77 [10]1.23  1.87 [9]KW ¼ 5.985, df ¼ 2
0.040
Yng > Gup**

0.52  0.13 [3]0.04  0.07 [3]n/an/a0.00  0.00 [4]0.20  0.00 [1]0.40  0.38 [4]0.54  0.49 [7]0.00  0.00 [3]0.20  0.28 [2]1.67  0.64 [9]1.69  0.47 [6]0.93  0.40 [5]0.73  0.88 [9]0.63  0.57 [4]0.71  1.57 [4]0.67  1.84 [16]0.67  1.72 [17]0.19  0.86 [15]0.22  0.92 [13]0.40  0.35 [3]0.12  0.17 [10]0.00  0.00 [10]0.00  0.00 [15]0.00  0.00 [11]4.00  1.57 [12]4.40  2.45 [12]3.37  3.14 [15]3.21  1.92 [21]2.02  1.64 [30]3.17  3.34 [14]3.69  2.31 [8]2.61  2.80 [9]0.00  0.00 [1]1.59  2.00 [7]0.02  0.05 [8]KW ¼ 12.006, df ¼ 3
0.007
Yrg > MdAd*
Yrg > OlAd*

0.10  0.14 [2]KW ¼ 7.153, df ¼ 5
0.210

0.23  0.30 [13]F5,45 ¼ 9.853<0.001
Yrg > SuAd*
Yrg > YgAd*
Yrg > MdAd*
Yrg > OlAd*
Juv > SuAd*
Juv > YgAd*
Juv > MdAd*
Juv > OlAd*
SuAd > OlAd*

0.00  0.00 [9]KW ¼ 13.734, df ¼ 5
0.012
Yrg > OlAd*
Juv > OlAd*
SuAd > OlAd**
SuAd > YgAd*
MdAd > OlAd*

0.00  0.00 [14]H ¼ 27.739, df ¼ 5<0.001
Yrg > SuAd*
Yrg > YgAd*
Yrg > MdAd*
Yrg > OlAd*

2.22  2.08 [37]F5,126 ¼ 3.633
0.004
Yrg > MdAd*
Yrg > OlAd*
Juv > MdAd*
Juv > OlAd*
SuAd > MdAd*

0.00  0.00 [2]KW ¼ 9.041, df ¼ 5
0.039
Yrg > MdAd*
Yrg > OlAd*
Juv > MdAd*
Juv > OlAd*
Juv > OlAd*
SuAd > OlAd**p < 0.05**p < 0.025

134

J.-B. Leca et al. / Journal of Human Evolution 53 (2007) 691e708

Age classes # 1
Young
Growing
Grown-up
TestpSig. diff.

1352.80  2.70 (10)3.83  3.19 (12)
0.6900.539
1.60  2.19 (5)3.11  3.32 (5)0.5650.690
2.78  1.89 (4)0.00  0.00 (5)2.183
0.063

Sho.A
Ara.E

4.73  2.40 (36)3.80  2.95 (20)
0.671
0.491
3.41  3.32 (81)2.17  2.06 (9)0.6320.543
2.24  2.44 (167)
1.49  1.96 (24)
0.401
0.688
0.17  0.79 (118)0.18  0.84 (87)
0.311
0.836
0.00  0.00 (93)0.00  0.00 (198)
0.000
1.000
0.00  0.00 (146)0.00  0.00 (219)
0.000
1.000

Kosh.
JMC

0.74  1.93 (27)0.60  0.1.47 (20)
0.0350.972
0.71  1.83 (34)0.29  1.04 (56)
1.1840.236
0.08  0.57 (50)
0.27  1.01 (30)
1.0570.291
1.59  2.68 (186)1.67  2.50 (224)0.2310.867
0.45  1.52 (225)1.21  2.35 (166)2.0750.043
0.36  1.36 (364)0.15  0.76 (81).09020.432
0.70  1.89 (80)0.14  0.73 (117)1.7320.200
0.35  1.27 (257)0.52  1.59 (92)
0.5900.667
0.16  0.78 (151)
n/a
e
e

Takh.
Wak.A

0.19  0.87 (62)0.32  1.08 (124)0.705
0.481
n/a
n/a
e
e
0.01  0.24 (281)0.00  0.00 (93)
0.5770.564

SH persistence and vigorousness. In Table 7, we present aninter-troop comparison of the general form of SH according to
the following age classes: young, growing, and grown-up. In
each troop (except Kosh., because the data set was insufficient), we tested the effect of age on several variables related
to SH persistence and the vigorousness of SH performance. In
Ara.E, Sho.A, Tak.B, and Tak.C, grown-up individuals
displayed significantly longer SH bouts or total SH phases
than growing individuals. In Takh., JMC, Tak.B, and Tak.C,
growing or grown-up individuals performed significantly
longer SH bouts and total SH phases, and/or more numerous
SH phases than young individuals (Table 7). Overall, we verified Prediction #5 stating that SH episodes will be shorter inyoung than in older troop members.

Ara.A

Effect of age on SH form

Young Female
Young MaleMWp (two-tailed)Growing Female
Growing MaleMWp (two-tailed)
Grown-up Female
Grown-up MaleMWp (two-tailed)

In Table 5, we present SH frequency according to the twoage class classifications used, from the broader to the more detailed age group differences. Overall, younger individuals
showed higher SH frequencies than older individuals. In
Ara.A, Takh., JMC, Kosh., Ara.E, and Sho.A, SH frequency
was significantly higher in young than in grown-up individuals, and in Takh., JMC, and Kosh., SH frequency was significantly higher in young than in growing individuals. In Takh.
and Ara.E, growing individuals showed significantly higher
SH frequencies than grown-up individuals.
More detailed analyses showed that in all troops, except
Wak.A, SH was significantly more frequent in yearlings thanin old adults. In some troops, SH frequency was significantly
higher in yearlings than in middle-aged adults (Ara.A, Takh.,
Kosh., and Ara.E), young adults (Takh. and Kosh.), and subadults (Takh. and Kosh.). In some troops, SH frequency wassignificantly higher in juveniles than in old adults (Takh.,
JMC, Ara.E, and Sho.A), middle-aged adults (Takh., Ara.E,
and Sho.A), young adults (Takh.), and subadults (Takh.). In
Takh., JMC, and Ara.E, SH was significantly more frequentin subadults than in old or middle-aged adults.
In Table 6, we present SH frequency according to sex classes and within each of the following age classes: young, growing, and grown-up. Among all of the sex differences tested,
only one was statistically significant: In growing Takh. troop
members, SH was more frequent in males than in females.
We found no statistically significant sex difference in othertroop age classes. In sum, we found that SH frequency was
higher in young than in older troop members but did not significantly differ between males and females (Prediction #4).

Age/Sex classes

Effect of age and sex on SH frequency

Troop

p ¼ 0.055; Wak.A: c21 ¼ 0.0, p ¼ 1.000; Takh.: c24 ¼ 4.4,
p ¼ 0.358; JMC: c25 ¼ 1.6, p ¼ 0.899; Kosh.: c21 ¼ 0.8,
p ¼ 0.363; Ara.E: c25 ¼ 0.5, p ¼ 0.992). Therefore, we foundthat SH occurrence was higher in young than in older troop
members but did not significantly differ in males and females(Prediction #3).

Table 6
SH frequency (mean  SD), defined as the number of SH bouts per focal hour, according to sex classes and within each age class. MW: Mann-Whitney test z value; Figures in parentheses: Number of focal
sessions

J.-B. Leca et al. / Journal of Human Evolution 53 (2007) 691e708

701

J.-B. Leca et al. / Journal of Human Evolution 53 (2007) 691e708702

Table 7
Inter-troop comparison of SH persistence and SH vigorousness according to age classes. Yng: Young, Grg: Growing, Gup: Grown-up; Three types of tests wereused (see Data analysis for detail): Mann-Whitney tests (MW, z value), Kruskal-Wallis tests (KW, chi-square value), and one-way ANOVAs (F values); N: Numberof SH bouts; DurBt: Duration of SH bouts (sec), DurPh: Duration of all SH phases pooled per SH bout (sec); NbPh: Number of SH phases per SH bout; PatTnr: SH
pattern turnover; PatVar: SH pattern variety per bout; DurDbPat: Duration of double SH patterns per SH bout (sec); Figures represent mean  SD; Asterisks andsharps indicate significant post-hoc paired comparisons
Troop

Age

N

Duration
SH bouts

Duration
SH phases

NumberSH phases

SH pattern
turnoverSH patternvariety

Duration
double SH
patterns

Ara.A

Yng
Grg
Gup
MW
p
Yng
Grg
Gup
KW/F2,16
p
Yng
Grg
Gup
KW/F2,34
p
Yng
Grg
Gup
KW
p
Yng
Grg
Gup
KW
p
Yng
Grg
Gup
KW/F2,98
p
Yng
Grg
Gup
KW
p
Yng
Grg
Gup
KW
p
Yng
Grg
Gup
KW/F2,21
p
Yng
Grg
Gup
KW/F2,40p

13
0
2

14  14e
101  119
1.5330.171
71  10270  192
113  128
KW ¼ 3.496
0.174
73  113*
210  342*
132  163
KW ¼ 17.364< 0.00147  93*85  115*
67  51
10.8300.004
37  45eeee
227  249
187  257*
275  301*
KW ¼ 10.577
0.005
319  343
132  86592  330
5.292
0.071
44  22116  148
26  71.597
0.450
221  150#
194  146*
391  275*#
F ¼ 3.974
0.036
111  77#109  93*186  178*#
F ¼ 7.592
0.002

13  12e
69  73
1.701
0.114
49  7762  186
102  119KW ¼ 3.145
0.208
49  66*
161  260*87  96
KW ¼ 19.025< 0.00141  89*
72  100*
42  32
11.7570.003
33  41eeee163  213
115  163*
195  231*
KW ¼ 13.919
0.001
269  303
72  68*544  367*
7.247
0.027
41  2086  99
26  71.611
0.447
206  156
168  127*343  260*
F ¼ 3.515
0.040
99  68#98  86*172  170*#
F ¼ 9.133
0.001

1.2  0.4e
1.5  0.7
0.7740.571
1.6  1.1
1.3  0.6
1.4  0.7
F ¼ 0.223
0.803
1.8  2.0*
2.6  2.8*
2.1  2.1
KW ¼ 6.269
0.044
1.3  0.7
1.6  1.1
1.9  1.2
2.639
0.267
1.2  0.7eeee
4.3  4.4
4.8  6.4
4.4  4.1
F ¼ 0.049
0.952
4.0  4.0
5.0  3.5
7.0  4.2
2.492
0.288
1.5  1.3
3.1  4.4
1.0  0.0
1.875
0.392
2.5  1.5#
3.0  2.2*
5.7  2.8*#
F ¼ 4.868
0.020
2.0  1.4
2.2  1.8
2.3  2.0
F ¼ 0.715
0.496

0.9  1.9e
4.5  4.9
1.7690.114
4.9  7.9
4.9  9.5
9.7  11.7
F ¼ 0.258
0.776
5.7  9.0
5.0  8.2
11.9  16.2
KW ¼ 2.944
0.229
3.4  7.2
3.2  4.3
1.3  1.7
1.441
0.487
4.0  7.4eeee
27.4  34.0
15.8  22.4*
25.1  38.3*
KW ¼ 6.797
0.033
30.3  35.4
15.2  16.1
49.0  2.8
4.553
0.103
3.7  3.2
8.3  10.1
2.5  0.7
1.634
0.442
30.5  22.3
15.7  13.9*
40.9  38.8*
KW ¼ 7.706
0.021
18.8  14.2
16.6  14.5
28.4  22.4
KW ¼ 5.448
0.066

1.8  1.4e
2.0  0.0
1.1290.381
3.5  2.6
3.6  3.4
5.9  3.3
F ¼ 0.290
0.752
4.1  3.4
3.1  2.8
5.4  4.3
F ¼ 0.779
0.467
2.6  2.1
2.8  2.0
1.9  1.2
1.724
0.422
3.0  2.2eeee
6.4  4.0#
3.9  2.7*#
5.0  2.7*
KW ¼ 18.543< 0.001
6.9  3.3
5.0  2.9
7.0  0.0
1.501
0.472
3.0  2.0
4.6  2.9
3.0  1.4
1.762
0.414
7.9  2.1*
6.1  2.4*
7.7  3.2
F ¼ 3.725
0.043
6.0  2.3
5.9  2.2
6.2  2.1
F ¼ 1.100
0.343

01
e
00
0.3920.933
6  315  1222  56
KW ¼ 3.023
0.221
2  11
6  1910  31
KW ¼ 3.644
0.162
01
01
01
0.140
0.932
00
e
e
e
e
12  26#
4  13*#19  44*
KW ¼ 23.125< 0.001
11  24
4  10
11
0.675
0.713
12
18  45
00
0.841
0.657
43  71
12  24
63  101
F ¼ 0.612
0.553
9  1749
6  10KW ¼ 1.011
0.603

Wak.A

Takh.

JMC

Kosh.

Ara.E

Sho.A

Sho.B

Tak.B

Tak.C

36
75
10

187
104
46

52
62
7

23
0
0

112
105
135

28
9
3

14
13
3

20
26
13

81
76
25

However, Prediction #6 proposing that SH will be more vigorous in young than in older troop members was not verified.
In the Ara.A, Wak.A, Takh., JMC, Sho.A, Sho.B, and Tak.C,
we found no statistically significant difference in SH vigorousness according to age classes (Table 7). In Ara.E and Tak.B,
we found no consistent effect of age on SH vigorousness. In

Ara.E, SH pattern turnover, SH pattern variety per bout, andthe duration of double SH patterns per bout were significantly
higher in grown-up than in growing individuals, whereas SH
pattern variety per bout and the duration of double SH patterns
per bout were higher in young than in growing individuals. In
Tak.B, SH pattern turnover was higher in grown-up than in136

J.-B. Leca et al. / Journal of Human Evolution 53 (2007) 691e708

growing individuals, whereas SH pattern variety per bout was
higher in young than in growing individuals (Table 7).
Given the link between SH and feeding activities (see Huffman, 1984; Huffman and Quiatt, 1986; Huffman, 1996), thefact that SH persistence and vigorousness were considerably
higher in most free-ranging troops (Ara.E, Sho.A, Sho.B,
Tak.B, and Tak.C) than in captive troops may be due to the influence of repeated food provisioning with hard coated cereal
grains (in these free-ranging troops) on the duration of SH activity (Leca et al., 2006).
SH pattern diversity and complexity. To further investigate
the effect of age on the form of SH, we examined the total
number of different SH patterns observed in each of the six
age classes (yearling, juvenile, subadult, young adult, middle-aged adult, and old adult) of each troop (Fig. 3). In troops
in which all six age classes were represented (i.e., all troops
except Ara.A), we found that yearlings showed lower inclusive
diversity of SH patterns than juveniles (except in Takh., where
both age classes showed an equal number of SH patterns). In
each troop, the age classes exhibiting the highest SH pattern
diversity were the juvenile (Takh., JMC, Kosh., Ara.E,
Sho.B, and Tak.C), subadult (Wak.A and Takh.), or young
adult (Tak.B) classes. In all studied troops, old adults showed
the lowest SH pattern diversity, except in Wak.A and Ara.E,
in which the age classes showing the lowest SH pattern
diversity were underrepresented in terms of SH records
compared to other age classes (middle-aged adults: 10 out ofa total of 345 SH bouts and notes; subadults: 117 out ofa total of 931 SH bouts and notes, respectively; see Table 4).
In Takh., JMC, Sho.B, Tak.B, and Tak.C, SH pattern diversity
tended to decrease as a function of age (from young to oldadults). Therefore, we verified Prediction #7 stating that
SH patterns will be less diverse in mature than in immatureindividuals.
To examine potential age differences in the complexity ofSH patterns performed, we compared the frequency of SH patterns in each of the four pattern categories and according toage classes. For each troop, we drew on all available SH bouts
and calculated the sum of SH patterns performed in each category per SH bout. As presented in Table 8, we found703

a consistent tendency for grown-up individuals to perform
complex SH patterns more frequently than younger individuals in most troops (Ara.A, Wak.A, Takh., Ara.E, Sho.A,
Tak.B, and Tak.C). In Ara.A, grown-up individuals performed
significantly more complex SH patterns than young individuals. In Wak.A, Takh., and Tak.C, complex SH patterns
were significantly more frequent in grown-up than in growing
and young troop members. In JMC, growing individuals performed complex SH patterns significantly more often than
young individuals. In Ara.E, complex SH patterns were significantly more frequent in grown-up than in growing troop
members. In sum, we verified Prediction #8 stating that SH
patterns will be more complex in mature than in immatureindividuals.
By contrast, when considering simple SH patterns (belonging to the investigative and locomotion activities), we foundno major age difference, except in Ara.E, where investigativeand locomotion SH patterns were significantly more frequent
in young than in growing and grown-up individuals. Regarding
intermediate SH patterns (belonging to the collection activity),no clear, consistent difference appeared among the study
troops. In Takh. and Sho.B, collection patterns were significantly more frequent in growing than in young individuals,
whereas the converse was found in Tak.B. In Ara.E, grownup individuals performed significantly more collection patterns than growing individuals.
Discussion
We provided new evidence on the effect of group size, composition in age classes, and age-related differences on SH in
Japanese macaques. We verified the two predictions generated
by the first hypothesis that patterns of inter-troop variation in
SH reflect variability in group size and age structure. First, thelarger the group, the higher the proportion of troop members
exhibiting SH simultaneously (Prediction #1). The positive effect of troop size on the synchronized performance of SH suggests the contagious nature of play. Seeing group members
playing is a reliable cue for more individuals that the current
environmental conditions are safe enough to engage in playAge-specific inclusive diversity of SH patterns

Age classes #2
Yearling
Subadult
Middle-aged adult

35

Juvenile
Young adult
Old adult

30
25
20
15
10
5
0
Ara.A

Wak.A

Takh.

JMC

Kosh.

Captive troops

Ara.E

Sho.A

Sho.B

TakB

Tak.C

Free-ranging troops

Fig. 3. Inter-troop comparison of age-specific inclusive diversity of SH patterns, defined as the total number of different SH patterns observed in each age class.

137

J.-B. Leca et al. / Journal of Human Evolution 53 (2007) 691e708704

Table 8Inter-troop comparison of the frequency of the four SH pattern categories according to age classes. Yng: Young, Grg: Growing, Gup: Grown-up; Three types oftests were used (see Data analysis for detail): Mann-Whitney tests (MW, z value), Kruskal-Wallis tests (KW, chi-square value), and one-way ANOVAs (F values);
N: Number of SH bouts; Figures represent the number of SH patterns per bout (mean  SD); Asterisks and sharps indicate significant post-hoc paired comparisons
Troop

Age

N

Investigative
activities

Locomotion
activities

Collection
activities

Complex manipulative
activities

Ara.A

Yng
Grg
Gup
MW
p
Yng
Grg
Gup
F2,16
p
Yng
Grg
Gup
KW/F2,34
p
Yng
Grg
Gup
KW
p
Yng
Grg
Gup
KW
p
Yng
Grg
Gup
F2,98
p
Yng
Grg
Gup
KW
p
Yng
Grg
Gup
KW
p
Yng
Grg
Gup
KW/F2,21
p
Yng
Grg
Gup
KW/F2,40p

13
020.5  0.8e
0.0  0.0
0.8740.571
1.6  2.8
1.9  3.6
2.5  4.2
0.286
0.664
1.7  3.4
1.9  3.9
8.8  39.8
KW ¼ 5.019
0.081
0.6  1.1
0.4  0.8
0.1  0.4
2.502
0.286
0.1  2.5eeee
1.3  2.3*#
0.4  1.1*
0.5  1.3#
9.216
<0.001
3.5  5.9
0.3  0.5
2.7  4.6
5.099
0.078
0.3  0.7
0.2  0.4
0.0  0.0
0.498
0.780
1.2  1.5
1.1  2.0
4.2  8.4
KW ¼ 0.472
0.790
1.1  2.0
0.7  1.6
0.4  0.9
F ¼ 1.984
0.140

0.1  0.3e
0.0  0.0
0.3920.933
0.4  0.9
0.3  1.3
0.7  1.6
0.640
0.529
1.0  1.8
0.6  1.3
2.2  6.4
KW ¼ 4.587
0.101
1.0  2.2
0.4  0.9
0.0  0.0
4.929
0.085
0.5  0.8eeee
3.1  4.9*#
1.0  2.2*
1.0  2.1#
16.515<0.001
3.3  3.5
0.9  1.5
4.7  4.2
5.180
0.075
0.6  0.9
0.3  0.9
0.3  0.6
2.070
0.355
2.2  2.6
1.7  1.7
2.5  2.4
F ¼ 0.559
0.575
1.3  1.7
1.2  1.7
1.8  3.0
F ¼ 1.208
0.301

1.5  1.8e
0.0  0.0
2.0500.076
1.3  1.7
1.0  1.7
1.6  2.7
0.662
0.518
1.2  1.9*
2.2  3.4*
5.3  18.2
KW ¼ 8.199
0.017
1.0  1.6
0.9  1.3
0.7  1.1
0.933
0.627
2.3  2.9eeee
10.4  15.8
9.2  14.1*
14.0  17.2*
2.966
0.043
9.5  21.2
6.7  12.6
14.3  12.4
0.748
0.688
1.3  2.1*
3.6  5.7*
1.3  1.2
6.019
0.049
15.0  13.4*
5.8  5.6*
11.4  15.5
F ¼ 3.874
0.027
6.6  6.7
5.7  5.2
9.6  9.6
KW ¼ 2.161
0.339

0.0  0.0e
5.5  4.9
3.7320.019
2.8  4.3*
3.2  5.3#
8.2  10.1*#
3.953
0.022
3.4  5.5*
3.2  5.8#
8.3  25.4*#
F ¼ 4.388
0.013
1.8  3.6*
2.7  2.6*
1.4  0.5
10.6290.005
1.1  2.1eeee
7.5  16.6
4.7  8.6*
11.0  24.0*
3.656
0.027
8.6  13.9
2.9  3.1
12.3  10.7
2.881
0.237
1.1  1.3
2.5  3.6
1.0  1.0
1.004
0.605
10.6  11.3
6.9  8.0
18.9  17.4
KW ¼ 5.901
0.052
8.9  8.7*
8.7  11.1#
16.1  15.0*#
KW ¼ 7.093
0.029

Wak.A

Takh.

JMC

Kosh.

Ara.E

Sho.A

Sho.B

Tak.B

Tak.C

36
75
10

187
104
46

52
62
7

23
0
0

112
105
135

28
9
3

14
13
3

20
26
13

81
76
25

(Spinka et al., 2001). Although SH is primarily a solitary activity, the sight of nearby stone handlers and even the loudnoise generated by percussive patterns (Leca, pers. observ.)
may increase an individual’s probability to start handlingstones. This stimulation effect may be amplified by an increasing number of troop members and eventually result in a formof ‘‘hysterical contagion’’ (Kerckhoff, 2002). This may help to
explain the increase in number of SH individuals (synchronizedoccurrence) around feeding time in free-ranging provisioned
troops, as this is the only time when most troop members are
all together in the same location.
Regarding the effect of troop size on the synchronized performance of SH, we should bear in mind the more limited percentages of troop members sampled during scans collected infree-ranging troops compared with scans collected in captive
troops. Due to lower visibility in free-ranging than in captive
138

J.-B. Leca et al. / Journal of Human Evolution 53 (2007) 691e708

conditions, the consideration threshold for the percentage of
scan-sampled troop members was lower in the former thanin the latter (see Methods for details). Although this may affect, to some extent, the value of SH prevalence in free-ranging troops, we do not consider it a serious confounder of ourresults for two reasons: 1) as previously mentioned, scans sessions in free-ranging troops were conducted within 30 minutes
after food provisioning, when almost all troop members aregathered around the feeding site; this is why yearly censusesof most free-ranging populations are conducted during provisioning time (Shodoshima: Watanabe, pers. comm.; Takasakiyama: Kurita, pers. comm.); 2) most free-ranging troops
are considerably larger than most captive troops, and even
60% sampled troop members in the former represent 1.5 to
30 times more individuals than 80% sampled troop membersin the latter.
Second, we verified that a group with abnormal age structure showed lower proportion of stone handlers and lower
frequency of SH than normal groups (Prediction #2). Thevery low occurrence and frequency of SH in Ara.A, a troop
with no subadults and young adults, strongly support theview that a group’s age structure may affect the diffusion andmaintenance of SH behavior. When a behavioral practice is restricted to a particular class of group members, it is supposed tospread very slowly and its maintenance may be jeopardized(Huffman and Hirata, 2003; Leca et al., 2007b). Huffman(1984, 1996) noted that the acquisition of SH and its further
diffusion to the whole group require several years of practiceby different age classes. To become established in a troop,
SH needs to be passed from mother to infant (‘‘tradition
phase’’). As long as young and middle-aged mothers continue
to practice SH, this behavior will persist in young individuals(Huffman and Hirata, 2003). Moreover, as no individuals
over five years old were seen to acquire SH behavior, there
would be a critical period after which SH cannot be acquired(Huffman, 1984). We suggest that the age gap in the Ara.A
troop might have constrained the diffusion of SH from theyoung to the grown-up age class. The restricted practice ofSH by young individuals and only very occasional practiceby older troop members may not be sufficient to maintain the
behavior in this troop in the long-term.
Likewise, our data show that SH occurs in the Kosh. troop,
but is only observed very occasionally in young individuals,
compared to our other study troops. The question arises as
to whether this behavior has only recently appeared in thistroop, or if these findings also reflect an effect of the age ofstone handlers on the diffusion of the behavior. We suggestthat SH might have appeared at some time, but somehow
has never become well-established and widespread within
the Kosh. troop. One reason may be the poor nutritional conditions experienced by the monkeys on Koshima Island (Moriet al., 1997), which may lead adults to primarily focus on survival activities such as foraging instead of devoting time tosuch leisure activities as SH. If adults do not adopt this nondirectly adaptive behavior because of local ecological pressures, SH may eventually disappear from the Kosh. troop,and possibly reappear under more favorable environmental
139

705

conditions. In the Ara.A and Kosh. troops, the very low frequency of interaction with stones and the simple patterns
exhibited are more likely to reflect a baseline level of interestin stones by macaques (Leca et al., 2007a) than ecologicalconstraints such as shortage of stones (Leca, unpublisheddata). These are also relatively small troops, with lower chanceof contagion than larger-sized troops such as Ara.E or Tak.C,
where SH has persisted for the last 30 years. In white-faced
capuchins, the durability of traditional behaviors was foundto be readily disrupted by socio-demographic changes (Perryet al., 2003).
We verified five of the six predictions generated by the second hypothesis that intra-group variation in SH reflects moreage- than sex-related differences. We found that SH occurrence and frequency were higher in young than in older individuals, regardless of sex (Predictions #3 and 4). In all troops,
almost all individuals under the age of seven years were observed handling stones at least once, whereas most verified
non-stone handlers were aged 11 or more. As individuals
grow in age, they tend to handle stones less often than youngermonkeys. This is in agreement with earlier findings from the
Arashiyama and Takasakiyama troops (Huffman, 1996). Our
results were consistent with the surplus energy hypothesis(Barber, 1991), and extensive reports that young animals typically play more than older ones (Fagen, 1981). We found limited evidence for an effect of sex on the occurrence andfrequency of SH. Other studies have failed to find sex differences in socially learned behaviors (e.g., Pedersen et al.,
1990; Bugnyar and Huber, 1997).
Although we failed to verify Prediction #6 (age did notseem to affect SH vigorousness), the other predictions about
the effect of age on SH form were verified. We found thatyoung individuals engaged in shorter SH episodes than older
troop members (Prediction #5). The diversity of the comprehensive SH patterns displayed tended to increase between
one, two, or three years of age and then gradually decline asadults age (Prediction #7). We also showed that complex SH
patterns were more frequently performed by old rather than
younger individuals (Prediction #8). Overall, our results are
consistent with previous findings about the effect of age on
SH frequency and form in captive and free-ranging troops ofJapanese macaques (Huffman, 1984; Huffman and Quiatt,
1986; Huffman, 1996; Nahallage and Huffman, 2007), andfurther emphasize the view of SH as object play. SH is mainly
practiced by young individuals but is also continued into adulthood. In macaques, SH is probably the only example of routine object play among adults.
However, much care is required when discussing our resultsin subadults and young adults. We acknowledge that our second age classification may be regarded as problematic since it
fails to consider one of the most significant factors of life history and demography in the Japanese macaque (as well asother macaques and most Cercopithecines), namely sexual bimaturism. Although it may be quite reasonable to ascribe
a four- to ten-year-old male to the subadult or young adultage class, a five- or six-year-old female is already fully mature
and almost certainly not nulliparous. They are neither socially706

J.-B. Leca et al. / Journal of Human Evolution 53 (2007) 691e708

nor physiologically equivalent to a five- or six-year-old male.
We are aware that this age classification possibly affects our
results in an unknown direction (e.g., the patterns may be
more pronounced, less pronounced, or even qualitatively
different).
Developmental research conducted on other animal species
consistently show that play is most common in immatures(Fagen, 1981), but animals can continue to play well into adulthood (Pellis and Pellis, 1991; Pellis and Iwaniuk, 2000). Whenconsidering the ecological constraints imposed on young andolder animals, the energy-regulation approach generates predictions about the adaptive consequences of play in terms ofan anti-predator strategy, and resistance to pathogens or tocold exposure (Barber, 1991). New mechanistic hypotheses
suggest that animals would actively seek and create unexpected situations in play through self-handicapping (e.g., deliberately relaxing control over their movements) which
would enable them to develop flexible kinematic and emotional responses to stressful events (Spinka et al., 2001). As
in many types of play, our comparative results provide an
additional line of evidence that there are age-related differences in the underlying motivational processes, and potential
physiological and behavioral consequences of the practice ofSH. We suggest that all monkeys, regardless of age, may simply enjoy manipulating stones, and pleasurable feedback
potentially gained from the activity may be an immediate
reinforcement.
However, our comparative results from multiple troops also
provide wider support for the findings from the long-term
studied Takh troop. As Nahallage and Huffman (2007) pointed
out, there may be an age-related difference in the complex
emotional state that is referred to as ‘‘having fun’’ in humanfolk psychology (see also Spinka et al., 2001): namely
excitement in young individuals and feeling relaxed in older
individuals. As a form of object play, SH may promote thedevelopment of motor skills in young monkeys and contributeto slow down the impairment of cognitive functions in older
individuals (Nahallage and Huffman, 2007). Both of these possible proximate causes and ultimate functions may account for
the age-related differences found. First, more frequent andshorter SH episodes, with more diverse patterns observed injuveniles, may promote the development of motor skills
through physical excitement. Second, longer SH episodes
including more complex patterns may enable older monkeys
to maintain cognitive functions through a relaxation activity(Nahallage and Huffman, 2007).
The relative lack of diversity in the patterns of SH observedin yearlings and oldest individuals may simply reflect physicallimitations (such as lack of strength or manual coordination):body size, developmental constraints, and experience in theformer, whereas it may relate to a form of behavioral conservatism in the latter (Huffman and Quiatt, 1986; Nahallage andHuffman, 2007). However, the overall differences in the inclusive-pattern diversity across the studied troops (Fig. 3) are notreally surprising. Contrary to most other socially-transmitted
stone-tool using behaviors in primates, such as nut-cracking
techniques observed in wild capuchins (Fragaszy et al.,2004) and chimpanzees (e.g., Boesch and Boesch, 1984), or
the use of intentionally modified stones as tools by early hominids (Panger et al., 2002), there is no optimal SH pattern. Provided some form of social learning, the non-adaptive nature of
SH may allow particular SH pattern preferences to emerge at
the group level (Leca et al., 2007a).
These findings can be considered in the light of previous research in Japanese macaques on SH behavior and other formsof play. The consistent effect of age on the occurrence and frequency of SH is in agreement with surveys conducted several
years ago and at different points in time in two of the freeranging studied troops (Ara.E: Huffman, 1984; Huffman and
Quiatt, 1986; Huffman, 1996; Tak.C: Huffman, 1996), anda more recent long-term study on one of the captive studied
troops (Tak.h.: Nahallage and Huffman, 2007). Based oncross-sectional and longitudinal analyses on a several-yeartime scale, these studies also showed that most non-stone handlers were advanced age individuals, and young monkeys handled stones more often than older ones. When considering thepatterns of diffusion of SH among long-term observed identified troop members, it appeared that this behavior first spreadlaterally among young individuals, probably peer playmates.
Second, as young individuals become older, it could be acquired vertically from mother to offspring through observational learning (Huffman, 1984, 1996). Therefore, SH can be
regarded as one of the seldom studied, culturally-mediated object play behaviors in non-human primates. A few other instances have been recently reported, such as the ‘‘toy game’’in white-faced capuchins (Perry et al., 2003) and ‘‘leaf-pilepulling’’ in chimpanzees (Nishida and Wallauer, 2003). LikeSH, these traditional play behaviors mainly occur in young individuals, among which they initially spread, but are also present in adults. However, contrary to SH, which is a solitary
form of object play, the toy game and leaf-pile pulling canbe labeled as social object play since they consist of using
non-edible natural objects (such as sticks, pieces of bark, ordead leaves) in social playful interactions (Nishida and Wallauer, 2003; Perry et al., 2003).
Although age-related effects are expected over a wide rangeof behavioral domains, some behaviors, such as play and tooluse, should be more strongly influenced by age than others.
The significance of our results can be interpreted from the perspective of demographic constraints on culturally-transmitted
object play and stone-tool using behaviors in non-human primates and hominids. Age and sex affect material culture inmany primate species, including humans (Choleris and Kavaliers, 1999; Reader and Laland, 2001; Walker et al., 2002).
Cross-generational studies of traditional practices in monkeys(SH: Leca et al., 2007a; fish-eating: Leca et al., 2007b) andapes (handclasp grooming: Bonnie and de Waal, 2006) could
enable evaluation of whether non-human primates show the
cumulative cultural evolution found in humans, and also called
the ‘‘ratchet effect’’ (Boesch and Tomasello, 1998).
Our findings urge the use of an inter-populational comparative approach based on multivariate analyses when addressing the question of the evolution of behavioral traditions inprimate and human populations. In addition to demographic
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constraints (Lefebvre, 1995; this study), ecological factors(Boesch et al., 1994; McGrew et al., 1997) and social influences (van Schaik, 2003; Leca et al., 2007a) should be jointly
considered to identify the sources of behavioral diversity ingeneral, and variation in object play and stone-tool use inparticular. Like all stone-related behaviors in non-human primates, further investigation of the various factors constraining
the occurrence of SH may provide new insights into the emergence of hominid material culture through stone-tool technology (cf. Foley and Lahr, 2003).

Acknowledgements
J.-B.L.’s field work was supported by a Lavoisier Grant,
Ministère des Affaires Etrangères, France. N.G. was supported
by a National Science Foundation grant (BCS-0352035) during the preparation of this manuscript. This study would nothave been possible without the contribution of many people
who helped in many ways during the course of this research.
We wish to thank the researchers, students, staff, and friends
who provided permission to work, support, assistance, andvaluable specific information about the history, demography,
environmental conditions of the troops at the different study
sites, and general information from other field sites. We are
grateful to the following people: A. Kato, M. Matsubara, K.
Nagata, H. Osawa, and H. Takemoto (Primate Research Institute); M. Nakamura and Y. Takenoshita (Japan Monkey Centre); F. Kanchi, A. Mori, and T. Suzumura (Koshima Field
Station); K. Watanabe (Koshima Field Station and Wild Monkey Park, Shodoshima); S. Asaba, S. Hanamura, T. Kawashima, S. Kobatake, and M. Shimada (Iwatayama Monkey
Park, Arashiyama); and H. Kurita (Takasakiyama Natural
Zoo). We are deeply indebted to the Enomoto family for theirfriendship and for generously provided logistic assistance at
Arashiyama. For occasional assistance in data collection, we
thank K.J. Petrzelkova (Arashiyama). We are grateful to
C.A.D. Nahallage for her friendship, assistance in data collection (Arashiyama and Shodoshima), and fruitful discussion
about SH. We thank Sue Boinski, Melissa Gerald, William
C. McGrew, and two anonymous reviewers for insightful comments on a previous version of the manuscript.

References
Altmann, J., 1974. Observational study of behaviour: sampling methods.
Behaviour 49, 227e267.
Altmann, S., Altmann, J., 1979. Demographic constraints on behavior and social organization. In: Bernstein, I., Smith, E.O. (Eds.), Primate Ecology
and Human Origins. Garland STPM Press, New York, pp. 47e63.
Barber, N., 1991. Play and energy regulation in mammals. Q. Rev. Biol. 66,
129e147.
Boesch, C., Boesch, H., 1984. Possible causes of sex differences in the use ofnatural hammers by wild chimpanzees. J. Hum. Evol. 13, 415e440.
Boesch, C., Marchesi, P., Fruth, B., Joulian, F., 1994. Is nut cracking in wild
chimpanzees cultural behavior? J. Hum. Evol. 26, 325e338.
Boesch, C., Tomasello, M., 1998. Chimpanzee and human cultures. Curr.
Anthropol. 39, 591e614.

141

707

Bonnie, K.E., de Waal, F.B.M., 2006. Affiliation promotes the transmission ofa social custom: handclasp grooming among captive chimpanzees. Primate
47, 27e34.
Bugnyar, T., Huber, L., 1997. Push or pull: an experimental study on imitationin marmosets. Anim. Behav. 54, 817e831.
Byers, J.A., Walker, C., 1995. Refining the motor training hypothesis for theevolution of play. Am. Nat. 146, 25e40.
Cambefort, J.P., 1981. A comparative study of culturally transmitted patternsof feeding habits in the chacma baboon Papio ursinus and the vervet monkey Cercopithecus aethiops. Folia Primatol. 36, 243e263.
Cavalli-Sforza, L.L., Feldman, M.W., 1981. Cultural Transmission and Evolution: A Quantitative Approach. Princeton University Press, Princeton.
Choleris, E., Kavaliers, M., 1999. Social learning in animals: sex differences
and neurobiological analysis. Pharmacol. Biochem. Behav. 64, 767e776.
Clutton-Brock, T., 1989. Female transfer and inbreeding avoidance in social
mammals. Nature 337, 70e72.
Daly, M., Wilson, M., 1983. Sex, Evolution and Behavior. Wadsworth, Belmont, CA.
de Waal, F.B.M., Seres, M., 1997. Propagation of handclasp grooming among
captive chimpanzees. Am. J. Primatol. 43, 339e346.
Fagen, R., 1981. Animal Play Behavior. Oxford University Press, New York.
Fedigan, L.M., Gouzoules, H., Gouzoules, S., 1983. Population dynamics ofArashiyama West Japanese macaques. Int. J. Primatol. 4, 307e321.
Foley, R., Lahr, M.M., 2003. On stony ground: lithic technology, human evolution, and the emergence of culture. Evol. Anthropol. 12, 109e122.
Fox, E.A., van Schaik, C.P., Sitompul, A., Wright, D.N., 2004. Intra- and interpopulational differences in orangutan (Pongo pygmaeus) activity anddiet: implications for the invention of tool use. Am. J. Phys. Anthropol.
125, 162e174.
Fragaszy, D., Izar, P., Visalberghi, E., Ottoni, E.B., Gomes de Oliveira, M.,
2004. Wild capuchin monkeys (Cebus libidinosus) use anvils and stone
pounding tools. Am. J. Primatol. 64, 359e366.
Fragaszy, D.M., Perry, S., 2003. Towards a biology of traditions. In: Fragaszy, D.M., Perry, S. (Eds.), The Biology of Tradition: Models and Evidence.
Cambridge University Press, Cambridge, pp. 1e32.
Ganas, J., Robbins, M.M., 2004. Intrapopulation differences in ant eatingin the mountain gorillas of Bwindi Impenetrable National Park, Uganda.
Primates 45, 275e278.
Glickman, S.E., Sroges, R.W., 1966. Curiosity in zoo animals. Behaviour 27,
151e187.
Goldberg, T.L., Wrangham, R.W., 1997. Genetic correlates of social behaviour
in wild chimpanzees: evidence from mitochondrial DNA. Anim. Behav.
54, 559e570.
Goldizen, A.W., 1988. Tamarin and marmoset mating systems: unusual flexibility. Trends Ecol. Evol. 3, 36e40.
Huffman, M.A., 1984. Stone-play of Macaca fuscata in Arashiyama B troop:transmission of a non-adaptive behavior. J. Hum. Evol. 13, 725e735.
Huffman, M.A., 1996. Acquisition of innovative cultural behaviors in nonhuman primates: a case study of stone handling, a socially transmitted
behavior in Japanese macaques. In: Galef Jr., B., Heyes, C. (Eds.), Social
Learning in Animals: The Roots of Culture. Academic Press, Orlando, FL,
pp. 267e289.
Huffman, M.A., Hirata, S., 2003. Biological and ecological foundations of primate behavioral tradition. In: Fragaszy, D.M., Perry, S. (Eds.), The Biology
of Tradition: Models and Evidence. Cambridge University Press, Cambridge, pp. 267e296.
Huffman, M.A., Quiatt, D., 1986. Stone handling by Japanese macaques(Macaca fuscata): implications for tool use of stone. Primates 27, 427e437.
Kawai, M., 1965. Newly acquired pre-cultural behavior of a natural troop of
Japanese monkeys on Koshima Island. Primates 6, 1e30.
Kerckhoff, A.C., 2002. A theory of hysterical contagion. Hum. Nat. Coll.
Behav. 12, 81e93.
Leca, J.-B., Gunst, N., Huffman, M.A., 2007a. Japanese macaque cultures: inter- and intra-troop behavioural variability of stone handling patterns
across 10 troops. Behaviour 144, 251e281.
Leca, J.-B., Gunst, N., Watanabe, K., Huffman, M.A., 2007b. A new case offish-eating in Japanese macaques: implications for social constraints on
the diffusion of feeding innovation. Am. J. Primatol. 69, 821e828.

708

J.-B. Leca et al. / Journal of Human Evolution 53 (2007) 691e708

Leca, J.-B., Gunst, N., Nahallage, C.A., Huffman, M.A., 2006. Stone handlingin Japanese macaques (Macaca fuscata): a 10-troop comparative study
about a behavioral tradition. Am. J. Primatol. 68 (Suppl. 1), 110e111(Abstract).
Lefebvre, L., 1995. Culturally-transmitted feeding behaviour in primates: evidence for accelerating learning rates. Primates 36, 227e239.
Lefebvre, L., Giraldeau, L.-A., 1994. Cultural transmission in pigeons isaffected by the number of tutors and bystanders present. Anim. Behav.
47, 331e337.
Lonsdorf, E.V., 2005. Sex differences in the development of termite-fishingskills in the wild chimpanzees, Pan troglodytes schweinfurthii of Gombe
National Park, Tanzania. Anim. Behav. 70, 673e683.
Lonsdorf, E.V., Eberly, L.E., Pusey, A.E., 2004. Sex differences in learning in
chimpanzees. Nature 428, 715e716.
Martin, P., Bateson, P., 1993. Measuring Behaviour: An Introductory Guide.
Cambridge University Press, Cambridge.
McGrew, W.C., 1979. Evolutionary implications of sex differences in chimpanzee predation and tool use. In: Hamburg, D.A., McCown, E.R.
(Eds.), The Great Apes. B. Cummings, London, pp. 441e463.
McGrew, W.C., Ham, R.M., White, L.J.T., Tutin, C.E.G., Fernandez, M., 1997.
Why don’t chimpanzees in Gabon crack nuts? Int. J. Primatol. 18, 353e374.
Mitani, J.C., 2006. Demographic influences on the behavior of chimpanzees.
Primates 47, 6e13.
Mitani, J.C., Watts, D.P., 1999. Demographic influences on the hunting behavior of chimpanzees. Am. J. Phys. Anthropol. 109, 439e454.
Mori, A., Yamaguchi, N., Watanabe, K., Shimizu, K., 1997. Sexual maturationof female Japanese macaques under poor nutritional conditions and foodenhanced perineal swelling in the Koshima troop. Int. J. Primatol. 18,553e579.
Nahallage, C.A.D., Huffman, M.A., 2007. Age-specific functions of stone
handling, a solitary-object play behavior, in Japanese macaques (Macaca
fuscata). Am. J. Primatol. 69, 267e281.
Nishida, T., Wallauer, W., 2003. Leaf-pile pulling: an unsual play pattern inwild chimpanzees. Am. J. Primatol. 60, 167e173.
Panger, M.A., Brooks, A.S., Richmond, B.G., Wood, B., 2002. Older than the
Oldowan? Rethinking the emergence of hominin tool use. Evol. Anthropol.
11, 235e245.
Pedersen, F.A., Glickman, S.E., Franck, L.G., Beach, F.A., 1990. Sex differences in the play behavior of immature spotted hyenas, Crocuta crocuta.
Horm. Behav. 24, 403e420.

Pellegrini, A.D., Gustafson, K., 2005. Boys’ and girls’ uses of objects for exploration, play, and tools in early childhood. In: Pellegrini, A.D.,
Smith, P.K. (Eds.), The Nature of Play: Great Apes and Humans. The Guilford Press, New York, pp. 113e135.
Pellis, S.M., Iwaniuk, A.N., 2000. Adult-adult play in primates: comparative
analyses of its origin, distribution, and evolution. Ethology 106, 1083e1104.
Pellis, S.M., Pellis, V.C., 1991. Role reversal changes during the ontogenyof play fighting in male rats: attack versus defense. Aggress. Behav. 17,
179e189.
Perry, S., Baker, M., Fedigan, L., Gros-Louis, J., Jack, K., McKinnon, K.C.,
Manson, J.H., Panger, M., Pyle, K., Rose, L., 2003. Social conventions
in wild white-faced capuchin monkeys. Curr. Anthropol. 44, 241e268.
Reader, S.M., Laland, K.N., 2001. Primate innovation: sex, age and social rankdifferences. Int. J. Primatol. 22, 787e805.
Rogers, E.M., 1995. Diffusion of Innovations. Free Press, New York.
Siegel, S., Castellan, N.J., 1988. Nonparametric Statistics for the Behavioral
Sciences. McGraw-Hill, Singapore.
Spinka, M., Newberry, R.C., Bekoff, M., 2001. Mammalian play: training for
the unexpected. Q. Rev. Biol. 76, 141e168.
van Schaik, C.P., 2003. Local traditions in orangutans and chimpanzees: social
learning and social tolerance. In: Fragaszy, D.M., Perry, S. (Eds.), The Biology of Tradition: Models and Evidence. Cambridge University Press,
Cambridge, pp. 297e328.
Walker, R., Hill, K., Kaplan, H., McMillan, G., 2002. Age-dependency inhunting ability among the Ache of Eastern Paraguay. J. Hum. Evol. 42,639e657.
Watts, D.P., 1989. Infanticide in mountain gorillas: new cases and a reconsideration of the evidence. Ethology 81, 1e18.
Whiten, A., Goodall, J., McGrew, W.C., Nishida, T., Reynolds, V.,
Sugiyama, Y., Tutin, C.E.G., Wrangham, R.W., Boesch, C., 1999. Culturesin chimpanzees. Nature 339, 682e685.
Whiten, A., Goodall, J., McGrew, W.C., Nishida, T., Reynolds, V.,
Sugiyama, Y., Tutin, C.E.G., Wrangham, R.W., Boesch, C., 2001. Charting
cultural variation in chimpanzees. Behaviour 138, 1481e1516.
Wrangham, R.W., McGrew, W.C., de Waal, F.B.M., Heltne, P.G., 1994. Chimpanzee Cultures. Harvard University Press, Cambridge, MA.
Yamakoshi, G., 2001. Ecology of tool use in wild chimpanzees: toward
reconstruction of early hominid evolution. In: Matsuzawa, T. (Ed.),
Primate Origins of Human Cognition and Behavior. Springer, Tokyo,
pp. 537e556.

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RESEARCH ARTICLE
Age-Specific Functions of Stone Handling,a Solitary-Object Play Behavior, in Japanese Macaques(Macaca fuscata)
CHARMALIE A.D. NAHALLAGE AND MICHAEL A. HUFFMAN
Section of Ecology, Department of Ecology and Social Behavior, Primate ResearchInstitute, Kyoto University, Inuyama, Aichi, Japan

Stone handling (SH) in Japanese macaques, a form of solitary-object play,is newly acquired only by young individuals, and is the first example of adirectly nonadaptive behavior that is maintained as a behavioral tradition
within free-ranging provisioned social troops. We report here the firstsystematic investigation of this behavior in a stable captive social troop,
the Takahama troop, which is housed in an outdoor enclosure of thePrimate Research Institute (PRI), Kyoto University, Japan. This study
was conducted to evaluate relevant competing hypotheses regarding thefunction of object play (e.g., misdirected foraging behavior and motor
training) to explain the proximal causes and ultimate function(s) of SH.
The ‘‘misdirected foraging behavior’’ hypothesis can be ruled out becauseof the lack of a clear temporal relationship between feeding and theoccurrence of SH in any age class. Age-related differences in SH
performance and behavioral patterns were observed, suggesting possible
differences in the immediate cause and ultimate function between young
and adults. Young individuals engaged in frequent bouts of shortduration, involving locomotion and vigorous body actions throughout
the day, which is typical for play by young in general. This pattern of
behavior is consistent with the motor training hypothesis, which statesthat play occurs during the development of motor and perceptual skills
and is thus potentially critical for neural and cognitive development. This
practice is continued by those who acquire it at an early age, with adults
engaging in significantly fewer but longer bouts that involve morestationary, complex manipulative patterns, almost exclusively in thelate afternoon. We propose that for adults, at the proximate level SH
is psychologically relaxing, but ultimately functions to maintain andregenerate neural pathways, and potentially helps to slow down thedeterioration of cognitive function associated with advanced age in long-

Contract grant sponsor: Japanese Ministry of Education, Science and Culture.
Correspondence to: Michael A. Huffman, Section of Ecology, Department of Ecology and Social

Behavior, Primate Research Institute, Kyoto University, 41-2 Kanrin, Inuyama, Aichi 484-8506,
Japan. E-mail: Huffman@pri.kyoto-u.ac.jp
Received 12 October 2005; revised 12 March 2006; revision accepted 7 April 2006
DOI 10.1002/ajp.20348
Published online 4 December 2006 in Wiley InterScience (www.interscience.wiley.com).

r 2006 Wiley-Liss, Inc.
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268 / Nahallage and Huffman

lived provisioned and captive macaques. Am. J. Primatol. 69:267–281,
2007. c 2006 Wiley-Liss, Inc.
Key words: behavioral tradition; aging; adaptive function; object play;neural maintenance and regeneration
INTRODUCTION
Stone handling (SH) by provisioned Japanese macaques at Takagoyama was
first briefly reported in 1975 [Hiraiwa, 1975]. More intensive investigations began
independently at Arashiyama and Takasakiyama in 1979 after it was firstrecognized to occur there [Huffman, 1984, 1996; Huffman & Quiatt, 1986].
Currently, SH behavior can be seen in four captive troops and 11 provisioned
free-ranging troops in Japan (Fig. 1). This activity has yet to be observed in
nonprovisioned troops, and despite long-term research there are also provisioned
troops in which SH has not been recorded (e.g., at Yakushima, Katsuyama, andMinoo). At Arashiyama, the behavior was documented to initially arise as the

Jigokudani (12)Funakoshiyama (11)Gagyusan (10)Takagoyama (1)Miyajima (9)Inuyama (2)Takasakiyama (8)Arashiyama (3)Tsubaki (4)Shodoshima (5)Ohdo (6)
Koshima (7)Fig. 1. SH site map of Japan. (Sources: Huffman and Hirata [2003] (sites 1, 3, 8, 10, 11, and 12);
K. Watanabe, personal communication (sites 4, 5, 6, and 9); and C.A.D. Nahallage, personalobservation (sites 2, 5, and 7).

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innovation of a juvenile female that then spread to older immature kin relatives
and peer playmates. As these individuals aged, the behavior was then transmitted
to younger sibs or their own infants as a behavioral tradition [Huffman, 1984;
Huffman & Quiatt, 1986]. At both Arashiyama and Takasakiyama, SH mostfrequently occurs after daily scheduled provisioning times, while individuals still
have grain remaining in their cheek pouches [Huffman, 1984]. SH is definedas the repetitive manipulation of stones (e.g., gathering, picking up, andscattering them) and is considered as object play in Candland et al.’s [1978]
terminology. According to Fagen [1981], object play is a ‘‘divertive interaction
with an inanimate object y including exploratory manipulation’’ [cited in Hall,
1998, 45p].
While not every socially learned behavior has to be adaptive, the propensity
to learn and adopt new behaviors certainly is. In the immediate sense, SH appears
to be rewarding in itself, rather than the means to an end [Huffman, 1996]. Why
the behavior persists in troops over many generations, despite the lack of any
obvious function or direct adaptive value to those who practice it, has long been
an elusive question. Two hypotheses regarding the occurrence of other types ofobject play in animals are the ‘‘misdirected foraging behavior’’ hypothesis and the‘‘motor training’’ hypothesis. According to the misdirected foraging hypothesis,
play in captive or domesticated animals is motivationally directed to objects as
if they were food [e.g., Hall, 1998; Pellis, 1991; Pellis et al., 1988]. In the caseof captive otters, they become increasingly excited by the approaching feedingtime and devote less time to social play and more time to playing with objects as‘‘pseudo-feeding behavior’’ [Pellis, 1991]. Object play by adult animals was
described by Hall [1998] in a study of domestic cats as misdirected predatory
behavior. A variety of objects were given to the cats, and those that most closely
resembled mice were played with more than others.
The motor training hypothesis proposes a biological function for play, andstates that object play modifies the developing neuromuscular system [Bekoff &Byers, 1981; Byers & Walker, 1995; Fairbanks, 2000]. In vervets and rhesus
macaques, object play peaks at 3–6 months of age, coinciding with the time of
motor neuron differentiation, rapid synaptogenesis, and peak cerebral activity[Jacobs et al., 1995; Rakic et al., 1986; Zecevic et al., 1989]. According to
Fairbanks [2000], it is during this period of fine-motor development that theexperience of object manipulation may play a role in shaping the neuralconnections that control precise hand movements. Moreover, object playcontinues at high rates during the second and third years of juvenile life.
Another biological factor that determines the time course of object play is said tobe the reduction of unmyelinated pathways in the central nervous system[Gibson, 1991]. Unmyelinated neural regions have a high potential for change,
and a decline in the rate of object play was found to correlate with the age period(2–3 years) during which the number of unmyelinated pathways also begin to
decline. Fairbanks [2000] was the first to clearly propose the neural selection
model in these terms. The juvenile period is a time when heightened motivation
to explore objects and their surroundings enhances input to the developing
nervous system when the brain is still relatively plastic and is developing neural
structures that can be modified by experience.
However, when SH was observed and reported for the Takagoyama andArashiyama troops, it was exhibited only by infants and juveniles [Hiraiwa, 1975;
Huffman, 1984]. At Arashiyama, despite over 29 years of continuous research
prior to those observations, SH did not occur–at least not to the notice of many
watchful observers [Huffman, 1991]. Furthermore, in the more than 25 years

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since its assumed innovation at Arashiyama in 1979, SH behavior has neverbeen newly acquired by individuals over the age of 5 years, but the behavior
continues to be practiced by individuals who acquired it when they wereyoung into adulthood and old age [Huffman & Quiatt, 1986; Huffman & Hirata,
2003].
These long-term trends highlight the need for a closer systematic examination of SH behavior and beg for an explanation of the possible agerelated differences in the function of this behavior. Here we analyze data fromthe first systematic study of SH behavior in a captive troop of Japanese macaques
known to exhibit the behavior. First, a general behavioral description of SH
and the prevalence of occurrence in the Takahama troop is presented. Next,
the relationship between the occurrence of SH and feeding, and age-relateddifferences in performance (i.e., duration, frequency, and number of patterns
displayed) are analyzed and compared with those of the Arashiyama andTakasakiyama troops whenever possible. Based on these results, we reexamine
the causes and possible functions of this behavior in young with regard to
relevant existing hypotheses. Finally, we propose a new function for SH inadults, and assess the role of tradition in maintaining an innovated behavior of
potential biological and psychological importance to those individuals thatpractice it.
MATERIALS AND METHODSThe Takahama troop of monkeys was introduced into the Primate ResearchInstitute (PRI), Inuyama, from Takahama, Fukui Prefecture, in 1970. At the
beginning of the present study there were 55 monkeys, but seven (two adultmales, three adult females, one juvenile female, and one infant male) were
removed at different times due to injury or death. Unless otherwise stated, only
the 48 monkeys (18 males and 30 females) that remained to the end were usedin the analyses presented here (Fig. 2). They are broken down into the following
age-sex class distribution: infants (up to 12 months), yearlings (1 year), juveniles(2–4 years), young adults (5–15 years), and older adults (15–30 years). For
analyses of broader age group differences, individuals are grouped as young(0–4 years) or adult (5 years and older) [Huffman, 1996].
Presently the troop is kept in a 960 m2 outdoor enclosure with various metal
climbing structures and shelter boxes for enrichment and protection from theweather.
Data collection began in June 2003 and continued up to November 2004, andall members of the troop were equally observed in all seasons of the year. The
daily observation time was dependent on daylight length, which varied according
to season. The observation time was divided into 1-hr time blocks, and individuals
were sampled randomly in each time block. Equal numbers of focal samples werecollected for each individual, in all time periods of the day in every month, toavoid sampling bias of certain age-sex classes and possible seasonal differences.
Each individual was sampled 43 times, and a total of 878 focal observation hours
were obtained. From this 434 SH sessions (focal sessions in which SH occurred)and 578 bouts of SH were recorded. A bout of SH is defined as the continuationof this behavior with pauses of no longer than 120 sec. If SH resumed after a morethan 120-sec pause, it was counted as another bout.
Two sampling methods were used in the data collection: continuous focal
animal sampling with video, and instantaneous scan sampling [Altamann, 1974;
Martin & Bateson, 1993]. Each focal animal was video recorded for 15 min with a

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Takahama 2003

5

4

3
2
Femalesn = 34

1

30
29
28
27
26
25
24
23
22
21
20
19
18
17
16
15
14
13
12
11
10
9
8
7
6
5
4
3
2
1
0
Age

1

2

3
4
Males
n = 21

5

6

Fig. 2. Age-sex distribution of Takahama individuals. Black areas represent verified SH individuals.
Gray areas represent non-SH individuals.

digital video camera (Sony Digital Handycam). The focal session was extended if
SH was still in progress or started toward the end of the session. The session was
extended for 5 min, but was terminated thereafter if there was no further contact
with stones [Huffman, 1996]. In addition, before and after each focal session,
5-min scan samples were made to record the behavioral states of the troop as acontrol for average activity patterns of that time of the day for the troop.
The scans were recorded on data sheets, and the observers moved from one sideof the enclosure to the other so as not to sample each individual more than once.
The recorded behaviors included resting, feeding, foraging, walking, grooming,
playing, object handling, SH, aggression, and ‘‘other.’’ To determine the locationof an SH session within the enclosure, the area was divided into 32 equal blocks
labeled as a letter-number matrix. Each block was named accordingly (A1, A2,
A3, A4, y, H4).
The videotapes were analyzed on a TV monitor and the duration of each focal
sample, activity patterns exhibited, duration of SH bouts of each focal subject, andtheir location within the enclosure were recorded on the data sheets and thenentered into a Microsoft Excel spread sheet for statistical analysis.

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272 / Nahallage and Huffman

RESULTS
Prevalence of Stone Handlers and Behavioral Description
Of the 55 individuals present in the Takahama troop at the beginning of thisstudy, 90% were verified to stone-handle at some point during the study (Fig. 2).
All individuals 7 years or younger were observed to stone-handle. The oldest stone
handlers present in the troop throughout the entire study were five females aged
20, 20, 23, 25, and 30 years. The five individuals that were never observed tostone-handle were all adults (four females aged 8, 21, 25, and 26 years, and one
male aged 23). Only two of these individuals (the 23-year-old male and 26-year-old
female) were removed before SH could be confirmed. However, we are confident
that they were not stone handlers during the study because they had been
observed for 4 and 6 months, respectively, prior to their removal.
In the Takahama troop, 45 SH patterns were recognized (see Table I for
definitions of each behavior). This number far exceeds that reported by Huffman[1996] for Arashiyama (17 patterns) and Takasakiyama (16 patterns), eventhough similar methods of data collection and analysis were used. Of thesebehaviors, Pi, H, B, ROS, RIH, and SC were the most common, and these havealso been reported as common object manipulation patterns for primates ingeneral and macaque species in particular [Huffman, 1996; Torigoe, 1985]. Many
individuals displayed all of the above-mentioned behavioral patterns when they
manipulated food pellets, pieces of metal, and other novel objects they came acrossin the enclosure. On average, an individual was observed to perform 13.9 different
behavioral patterns (SD 5 5.2, n 5 45) over the course of the study. Males performed
an average of 15.2 patterns (SD 5 4.3, n 5 18), and females performed an average of
13.0 (SD 5 5.6, n 5 27); thus there was no statistically significant difference.
These 45 behaviors were classified into five categories according to their basic
motor patterns (Table I). Of all of these behaviors, 17.7% were investigative
activities. Locomotive and collecting/gathering activities accounted for 11.1%.
The greatest number of behaviors were sound-producing activities, accounting
for 33.3%. The majority of patterns exhibited produce sound, which can beinterpreted as a possible immediate stimulus for their practice. The secondlargest representative group of behaviors (26.7%) involved the manipulation ofstones together with other objects.
No single individual in the troop displayed all 45 behavioral patterns given
in Table I, and some were specific only to young individuals (e.g., MP, TH, PIW,
WIL, RIM, RWH, ROF, and SGR) or adults (e.g., GH, SW, FLM, TR, SP, and TS).
Infants at first exhibited only very basic behavioral patterns (CD, B, and H), but
their number and complexity increased with time (ROS, RIH, CA, and MP).
Juveniles engaged in behavioral patterns that involved more vigorous body
movements (CA, TW, MP, and CL), while adults engaged in more complex
manipulative behavioral patterns (e.g., PUS, F, FL, GA, and SC), as has also been
observed at Arashiyama and Takasakiyama [Huffman & Quiatt, 1986].
Diurnal Variation of SH in Relation to Feeding Activity
The Takahama troop was provisioned with monkey chow only once a day inthe late morning (1000–1100 hr). Only 5.6% (n 5 24/434) of all SH sessions
occurred between 1000–1100 hr. While SH was observed throughout the day,it occurred significantly more often in the afternoon between 1300 and 1900 hr
than in the morning between 0700 and 1200 hr (Wilcoxon signed-rank test,
Z 5 –5.36, n 5 48, P 5 0.001). Regardless of the provisioning time, the monkeys

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Stone Handling in Japanese Macaques / 273
TABLE I. Stone Handling Behaviors Classified by Activity Patterns
Investigative activities
Pi (Pick): Pick
H (Hold): Pick up a stone and hold it away from the body
B (Bite): Bite a stone
L (lick): Lick a stone
SN (Sniff): Sniff a stone
CD (Cuddle): Take hold of, grab or cradle a stone for a few secondsa,bPIM (Put In Mouth): Put a stone in one’s mouth and keep it sometime
MIM (Move inside Mouth): Make a stone move inside one’s mouth with tongue or hand
Locomotion activities
MP (Move and Push): Push/pull a stone with one or both hands while working forward/
backwarda,b
GW (Grasp Walk): Walk with one stone or more in the palm of one or both handsa,b
CA (Carry): Carry a stone cuddled in one’s hand from one place to anothera,bCIM (Carry in Mouth): Carry a stone in one’s mouth while locomoting
TW (Toss Walk): Toss a stone ahead (repeatedly) and pick it up while walkinga,bCollecting/gathering activities
GA (Gathering): Gather stones into a pile in front of oneself a,b
PU (Pick Up): Pick up a stone and placed it into one’s handa,b
PUS (Pick Up a Small stone): Pick up a small stone and hold it between finger tips (likewheat grains)a,b
PUD (Pick Up and Drop): Pick up a stone and drop it repeatedlya,bGH (Grasp with Hands): Clutch a pile of stone gathered and placed in front of one selfa,bSound producing activities
ROS (Rub on Surface): Rub or roll a stone on a surfacea,b
RIH (Roll in Hands): Roll a stone in one’s handa,b
RT (Rub Together): Rub stones togethera,bSC (Scatter): Scatter stones about, on a substrate, in front of oneselfa,b
CL (Clacking): Clack stones together (Both hands moving in a clapping gesture)a,b
RWH (Rub with Hands): Hold a stone in one hand and rub it with the othera,b
POS (Pound on a surface): Pound a stone on a substrate
SL (Slapping): Slap or pound a stone with ones fingertips or palm of ones hand
RWM (Rub With Mouth): Rub a surface with a stone held in mouth
RIM (Rub in Mouth): Rub a stone against another held in mouth
TIM (Tap in Mouth): Put a stone in ones mouth and tap it slightly with one’s finger tip or palm
FL (Flinting): Strike a stone against another held stationarya,bFP (Flip): Flip a stone
SW (Swiping): Swipe stones together in a sweeping gesture
FLM (Flint in Mouth): Strike a stone against another held in mouth
Combination of stone and other object activities
PIW (Put in Water): Put a stone in water
WIL (Wrap in Leaves): Wrap stones in leaves
ROF (Rub on Fur): Rub or put a stone on one’s fur
COO (Combine stones with other objects): Combine a stone with other objects that can befound in the enclosure e.g., pellets, pieces of strings, metals etc.
TH (Throw): Throw without jumping and running
SGR (Stone groom): Groom somebody with a stone
SIH (Shake in Hand): Take small stones into ones hand and shake it
W (Wash): Wash a stone in water
SP (Spin): Spin a stone with one hand or both hands
THS (Throw and Sway): Throw a stone and sway from front to back
JT (Jump and Throw): Jump and throw a stone forward or backward
TR (Run and throw): Run and throw a stone or vise versaaObserved in Arashiyama.
Observed in Takasakiyama.

b

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149274 / Nahallage and Huffman

Adults

Young

20
15
10
5

18:00-19:00

17:00-18:00

16:00-17:00

15:00-16:00

14:00-15:00

13:00-14:00

12:00-13:00

11:00-12:00

10:00-11:00

9:00-10:00

8:00-9:00

0
7:00-8:00

Percentage stone handling

25

Tim e
Fig. 3. Effect of age on the diurnal variation of SH.

TABLE II. Summary of Stone Handling Behavior in Different Age and Sex
Categories
Average Average number
Averageof patterns/
bouts/
Average time/ frequency/
hour (SD) individual (SD)individual (SD)bout (sec)Young
Adult (5–15 years)
Old adult (16–30 years)
Adult females
Young females
Adult males
Young males

15.92 (7.76)
8.81 (6.5)
9.57 (10.43)
6.87 (7.79)
18.25 (8.03)
14.33 (4.88)
13.58 (7.02)

82.29
136.16273.68188.02
73
180
94.19

1.48 (0.72)
0.81 (0.60)
0.89 (0.97)
0.64 (0.72)
1.69 (0.75)
1.33 (0.45)
1.26 (0.65)

16 (4.74)
12 (4.6)
10 (5.36)
10 (4.36)
17 (4.94)
15 (4.26)
15 (4.65)

n
24
14
7
15
12
6
12

were observed to have food in their mouths in only 24.0% of all recorded SH
sessions. The peak time for SH was between 1500 and 1600 hr. Young individuals
tended to stone-handle throughout the day, but with increasing age, adults
restricted their SH more to the latter part of the day (Fig. 3). In particular, 77.8%(28/36) of all SH sessions observed in old adults occurred after 1500 hr.
Effects of Age on the Occurrence of SH
Marked age and sex class differences in the frequency of SH, numberof patterns, and bouts performed were recognized (Table II). Young monkeys(0–4 years old) stone-handled significantly more often (Mann-Whitney, U 5 69.5,
n1 5 24, n2 5 21, P 5 0.001) and displayed a significantly greater number ofbehavioral patterns compared to adults (Mann-Whitney, 0–4 years, n1 5 24,
adults n2 5 21, U 5 126, P 5 0.004). This is supported by a statistically significant
negative correlation between age and the number of patterns displayed (Spearman rho 5 –0.376, P 5 0.011, n 5 45, Fig. 4a). Similar trends were recorded inboth the Arashiyama and Takasakiyama troops [Huffman, 1996].

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Stone Handling in Japanese Macaques / 275

Young individuals displayed twice as many bouts compared to adults (young
mean 5 15.9, SD 5 7.8, n 5 24, adults mean 5 9.0, SD 5 7.8, n 5 21). A statisticallysignificant difference was also recognized in the number of bouts performed byyoung and adults (Mann-Whitney, 0–4 years n1 5 24, adults n2 5 21, U 5 131,
P 5 0.006). This is supported by a significant negative correlation in the average
number of bouts performed by age (Spearman rho 5 –0.320, P 5 0.032, n 5 45;
Fig. 4b).
When compared by sex, juvenile females performed the highest number ofbouts per individual, and there was little difference between adult males andjuvenile males. However, adult females performed the lowest number of bouts aswell as the fewest number of patterns of all individuals (Table II).
Young individuals tended to exhibit many bouts of short duration, while
adults exhibited fewer bouts of longer duration (Fig. 5). There was a statistically
positive correlation between age and average time spent per bout (Spearmanrho 5 0.538, P 5 0.001, n 5 45, Fig. 4c). The time spent in a bout increased withage (Mann-Whitney, 0–4 years n1 5 24, adults n2 5 21, U 5 113, P 5 0.002).
Old adults stone-handled the longest per bout. Individuals tended to havetheir own specified small number of behavioral patterns, which they habituallyexhibited at the same location in the enclosure. There is a statistically significant
negative correlation between age and number of different places used within theenclosure to stone-handle (Spearman rho 5 –0.484, n 5 45, P 5 0.001; Fig. 4d).
Younger individuals tended to use more different places in the enclosure thanadults (Mann-Whitney, 0–4 years n1 5 24, adults n2 5 21, U 5 107, P 5 0.001).
There were no statistically significant differences between males and females
in the number of bouts displayed or the average time spent per bout (bouts
displayed: Mann-Whitney, males n1 5 18, females n2 5 27, U 5 198.5, P 5 0.302;
average time per bout: males n1 5 18, females n2 5 27, U 5 189.5, P 5 0.215).

DISCUSSION
The results presented in this study provide us with information necessary toevaluate the possible function(s) of SH in Japanese macaques from theperspective of hypotheses proposed for object play in other species, and toformulate a relevant new hypothesis that may explain age differences in theperformance of this behavior. Though many theories have been proposed
regarding the function of play behavior [Smith, 1978], no single one can beapplied across the board to all play behaviors in all species. Indeed, there aredifferences in play activities exhibited by the same species living under different
environmental conditions [e.g., Ramsey & McGrew, 2005]. SH is no exception, as
evidenced by the contrasts and similarities of the behavior between free-ranging
and captive provisioned troops, and age-class differences within the same troop
reported here.
The underlying function of play is expected to vary according to the content
of the behavior itself, potential motivational differences brought about bydifferences in social and natural environments, and species’ level characteristics.
For example, Hall [1998] described object play in predatory species asboisterousness and enjoyable. However, SH in Arashiyama Japanese macaques
occurs under low-arousal conditions [Huffman, 1984, 1996]. This was confirmed
for Takahama macaques also, in that the frequency of SH was significantly
greater on clear days than on cloudy or rainy days, as well as during warmer
seasons of the year, and the monkeys suppressed SH for days following periods of

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151276 / Nahallage and Huffman

Fig. 4. Distribution of (a) number of patterns displayed, (b) number of bouts, (c) average time spent
per bout, and (d) number of places used for SH by age of the stone handler.

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152

18

Ave. bouts/ animal

16
14
12
10

Ave. time (sec)/ bout

300
250
200
150

8
6

100

4
2
0

50

Average time (sec) /boutNumber of bouts/individual

Stone Handling in Japanese Macaques / 277

0Young(0-4yrs)

Adults(5-15yrs)

Adults(16-30yrs)

age-classFig. 5. Relationship between number of bouts displayed and average time spent per bout by age.

externally induced intense stress (e.g., capturing the entire troop for annual
checkups, or moving a group temporarily into a new enclosure) [Nahallage, 2005](Nahallage, personal observation).
SH, as described here, is not consistent with the misdirected foraging
behavior hypothesis (pseudo-feeding behavior) proposed by Pellis [1991]. Even inprovisioned free-ranging macaques (e.g., at Arashiyama and Takasakiyama[Huffman, 1984] and Shodoshima (Nahallage, unpublished data), SH occurs
predominantly after feeding, not before. Therefore, we conclude that thisbehavior is not elicited by the anticipation of food, as has been described for
captive otters and other zoo animals [Hediger, 1964; Pellis, 1991].
When we compare age-class differences in SH, the possible motivations for
performing the behavior appear to differ between young and adults. This is ofparticular interest to us, given that the behavior is acquired only by young
individuals. This leads us to speculate that unlike other play behaviors thatdisappear from the repertoire of most primates when they reach adulthood,presumably because they no longer serve a function, biological and cultural
selective forces may be acting on individuals that have acquired the SH behavior
to maintain the practice throughout life.
As regards SH in young macaques, it has been observed in many otherexamples of object play that young individuals are naturally curious and readily
explore new objects and environments [Hall, 1998]. The immediate motivation foryoung to stone-handle, like any other form of object play, is most likely that it is
intrinsically an enjoyable activity. Young individuals are naturally curious about
what others are doing, and often desire to play with an object that has been made‘‘popular’’ by others’ use of it [Huffman, 1984]. At the functional level, playing
with stones allows them to develop and practice the interactive use of motor andperceptual skills that support physical and neurophysiological development. In
macaques, a surge of synaptogenesis occurs roughly 2 months before birth andcontinues up to 3 years of age [Bourgeois et al., 1994; Rakic et al., 1986]. The
overall trend in the increasing complexity of SH behaviors (pattern and numberof behaviors) over time from infancy into the juvenile period is consistent withthis increase in neural-motor developmental activity. Young macaques displayed

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many behavioral patterns that required more vigorous body movements
compared to adult behaviors, and performed many short bouts of SH throughout
the day. These findings are consistent with Fairbanks’ [2000] model describing
the heightened frequency of object manipulation in correlation with synaptic
development in juvenile vervets and rhesus macaques [e.g., Rakic et al., 1986]. We
believe that this model is the best functional explanation for SH in young
Japanese macaques.
The immediate motivation of adults to stone-handle appears to differ fromthat of young. With age, adults exhibit fewer bouts of longer duration, and thesebouts involve relatively more complex behavioral patterns than those of theyoung. They concentrate on these more-demanding manipulative activities withseemingly intense concentration, often to the extent of ignoring or avoiding
attempts of their offspring and other social partners to interact with them.
They carry stones from various parts of the enclosure to their individually
preferred locations to stone-handle in an unhurried, seemingly ‘‘leisurely’’manner. Sometimes older individuals sit near their preferred location, waitingfor others to leave, before going there to stone-handle. At Takahama SH is
performed most often in the afternoon, and we suggest that adults may
temporarily divert their attention away from the social interactive network of
associations with others by concentrating on this solitary activity. In captive
conditions, less time is required for feeding and locomotion. This leaves more time
for social interactions, perhaps to the point that some animals experience a‘‘social overload’’ by the end of the day, and adult monkeys may seek to engage
in activities that divert their attention away from the routine of being in close
proximity to one another.
Since adults have already acquired the necessary motor skills during early
life, we propose that the ultimate function of SH differs between adults andyoung. However, an equally important neurophysiological benefit may be gainedby adults from the practice of SH. As macaques grow older, a decline in memoryand cognitive impairment, and associated pathology (e.g., senile plaque or synapse
loss) of the prefrontal cortex occurs (see Hof and Duan [2001] for review). In
humans, this process is similarly associated with cognitive decline, dementia, andAlzheimer’s disease [Hof & Duan, 2001]. Recently a number of clinical studies
have shown that elderly humans can significantly reduce the risk of acquiringsuch diseases by engaging in regular leisure activities involving concentrated
mental activity (e.g., reading, and playing board games, cards, and musicalinstruments) [e.g., Verghese et al., 2003]. The neurological mechanism for this is
not yet fully understood, but in simple terms, you either use it or you lose it. It has
been suggested that the mental exercise of such leisure activities may stimulate
new neural growth around damaged parts of the brain caused by aging [Coyle,2003]. In fact, voluntary physical exercise has also been associated with increases
in the production of brain-derived neurotrophic factor and other growth factorsthat stimulate neurogenesis and improved learning and mental performance inthe elderly [Cotman & Berchtold, 2002; Laurin et al., 2001]. Given the close
similarities in behavioral, physiological, and neurological aging processes between
human and nonhuman primates [Hof & Duan, 2001], these processes ofcompensation for cognitive degeneration in older adult humans may be
synonymous in macaques, making the potential benefits significant to all whostone-handle. A shift in the role of SH activity from neural-motor development in
the young to basic maintenance in adults and regeneration of neurophysiologicalpathways in aging adults may be the prominent functions behind the sustained
practice of this seemingly nonadaptive behavior in macaques.

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Stone Handling in Japanese Macaques / 279

SH may have significant positive implications for individuals that practice
it from birth, and provide yet-unmeasured benefits if continued into old age. The
benefits outlined here by the newly proposed ‘‘neural maintenance and regeneration’’ hypothesis could perhaps be partially tested by behavioral, demographic, andpostmortem neuroanatomical investigations of individuals in provisioned SH andcontrol study troops to look for possible differences in behavioral developmental
rate, cognitive performance, population-level differences in longevity, and anatomical/pathological differences in the brain. This remains to be done in future studies.
For both young and adults, SH is considered the consequence of provisioning
and a reflection of the spare time that is freed up from maintenance and survival
activities [Huffman, 1984]. This is supported by the fact that it occurs only incaptive and provisioned free-ranging troops, and not in wild troops. Differences in
the relative amount of free time among captive and free-ranging troops of stone
handlers are reflected by the data in various ways. In the captive Takahama troop,
time spent per SH bout was significantly longer in older individuals. The opposite
trend was observed in the free-ranging Arashiyama troop, where time spent perbout decreased with age and an increase in age/rank-related social activities. At
Arashiyama, monkeys come to the feeding area mainly at provisioning time (fourtimes a day), and it is after feeding that SH is most reliably seen. This is theirwindow of free time, during which they socialize and rest before moving back into
the forest [Huffman, 1984; Huffman & Quiatt, 1986]. Increased infant care within
the first 6 months and the maintenance of social bonds in both males and females
were two major reasons given for a decrease in SH time for adults at Arashiyama[Huffman, 1996]. However, Takahama monkeys are confined to a much smaller
space without natural vegetation and are fed only once a day. This frees up
significantly more time for socializing, resting, and infant care. In this light, the twodifferent functions hypothesized here to explain why young and adults perform SH
are interpreted to be due to a change in the combination of social and biologicalconditions associated with developmental and aging processes. To the best of ourknowledge, while tool use provides important immediate gains in nutrition to those
who practice it, only a few other behaviors of such potentially significant biologically
adaptive value (e.g., animal self-medication [Huffman, 2001]) have been reported tobe maintained within a primate group as a behavioral tradition.
ACKNOWLEDGMENTS
We thank Drs. Jean-Baptiste Leca and Massimo Bardi for their guidance inanalyzing the data, and two anonymous reviewers and Prof. Dorothy Fragaszy, formany helpful comments. We also thank the faculty and supporting veterinary staffof the Center for Human Evolution Modeling Research, PRI, for facilitating thisresearch and taking care of the captive monkey troops. Thanks are also due to thefaculty and students of the Department of Ecology and Social Behavior for theirvaluable advice and guidance, and the many graduate students and friends whohelped us in various ways during the study. C.A.D.N. received a scholarship from theJapanese Ministry of Education, Science and Culture for graduate studies in Japan.

REFERENCES
Altamann J. 1974. Observational study of
behavior: sampling method. Behavior
49:227–267.

Bekoff M, Byers JA. 1981. A critical reanalysis of the ontogeny and phylogeny of
mammalian social and locomotor play: an

Am. J. Primatol. DOI 10.1002/ajp10.1002/ajp.20348

155

280 / Nahallage and Huffman
ethological hornets nest. In: Immelmann K,
Barlow G, Main M, Petrinovich L, editors.
Behavioral development. Cambridge, UK:
Cambridge University Press. p 296–337.
Bourgeois J-P, Goldman-Rakic PS, Pakic P.
1994. Synaptogenesis in the prefrontal
cortex of rhesus monkeys. Cereb Cortex 4:
78–96.
Byers JA, Walker C. 1995. Refining the motor
training hypothesis for the evolution ofplay. Am Nat 146:25–40.
Candland DG, French DK, Johnson CN. 1978.
Object play: test of a categorize model by
the genesis of object play in Macaca fuscata.
In: Smith EO, editor. Social play inprimates. New York: Academic Press. p
259–296.
Cotman CW, Berchtold NC. 2002. Exercise: abehavioral intervention to enhance brain
health and plasticity. Trends Neurosci 25:
295–301.
Coyle JT. 2003. Use it or lose it–do effortful
mental activities protect against dementia?
New Engl J Med 348:2489–2490.
Fagen R. 1981. Animal play behavior. New
York: Oxford University Press. 684 p.
Fairbanks LA. 2000. The developmental timing of primate play: a neural selection
model. In: Parker ST, Langer J, McKinney
ML, editors. Biology, brains and behavior:
The evolution of human development.
Oxford: School of American Research Press.
p 131–158.
Gibson KR. 1991. Myelination and brain
development: a comparative perspective onquestions of neoteny, altrically and intelligence. In: Gibson KR, Peterson AC, editors.
Brain maturation and cognitive development: comparative and cross-cultural perspectives. New York: Aldine de Gruyter.
p 29–64.
Hall SL. 1998. Object play by adult animals.
In: Bekoff M, Byers JA, editors. Animal
play: evolutionary, comparative and ecological perspectives. Cambridge: Cambridge
University Press. p 45–60.
Hediger H. 1964. Wild animals in captivity.
New York: Dover Publications. 207 p.
Hiraiwa M. 1975. Pebble-collecting behavior
by juvenile Japanese monkeys [in Japanese]. Monkey 19:24–25.
Hof PR, Duan H. 2001. Age-related morphologic alteration in the brain of Old Worldand New World anthropoid monkeys. In:
Hof PR, Mobbs CV, editors. Functional
neurobiology of aging. San Diego: Academic
Press. p 435–445.
Huffman MA. 1984. Stone play of Macaca
fuscata in Arashiyama B troop: transmission of a non-adaptive behavior. J Hum Evol
13:725–735.
Huffman MA, Quiatt D. 1986. Stone handlingby Japanese macaques (Macaca fuscata):

implications for tool use of stones. Primates
27:413–423.
Huffman MA. 1991. History of the Arashiyama Japanese macaques in Kyoto, Japan. In:
Fedigan LM, Asquith P, editors. The macaques of Arashiyama: thirty-five years ofstudy in Japan and the West. New York:SUNY Press. p 21–53.
Huffman MA. 1996. Acquisition of innovative
cultural behaviors in nonhuman primates:
a case study of stone handling, a sociallytransmitted behavior in Japanese macaques. In: Galef Jr BG, Heyes C, editors.
Social learning in animals: roots ofculture. Orlando: Academic Press. p
267–289.
Huffman MA. 2001. Self-medicative behavior
in the African great apes: an evolutionary
perspective into the origins of human traditional medicine. Bioscience 51:651–661.
Huffman MA, Hirata S. 2003. Biological andecological foundations of primate behavioral
tradition. In: Fragaszy DM, Perry S, editors.
The biology of traditions: models andevidence. Cambridge: Cambridge University
Press. p 267–296.
Huffman MA, Hirata S. 2004. An experimental study of leaf swallowing in captive
chimpanzees–insights into the origin of aself-medicative behavior and the role ofsocial learning. Primates 45:113–118.
Jacobs B, Chugani HT, Allada V, Chen S.
Phelps ME, Pollack DB, Raleigh MJ. 1995.
Developmental changes in brain metabolism in sedated rhesus macaques and vervet
monkeys revealed by positron emission
tomography. Cereb Cortex 3:222–233.
Laurin D, Verreault MD, Lindsay J, MacPherson K, Rockwood K. 2001. Physical activity
and risk of cognitive impairment anddementia in elderly persons. Arch Neurol
58:498–504.
Martin P, Bateson P. 1993. Measuring behavior: an introductory guide. Cambridge:
Cambridge University Press. 222 p.
Nahallage C. 2005. Object play with stonesin the captive Takahama troop of Japanesemacaques (Macaca fuscata): the affectof environmental factors on its occurrence,
the acquisition process, development andtransmission. Master’s thesis, Primate
Research Institute, Kyoto University,
Aichi, Japan.
Pellis SM, O‘Brion DP, Pellis VC, Teitelbaum
P, Wolgin DL, Kennedy S. 1988. Escalationof feline predation along a gradient fromavoidance through ‘‘play’’ to killing. Behav
Neurol Sci 102:760–777.
Pellis SM. 1991. How motivationally distinct isplay? A preliminary case study. Anim Behav
42:851–853.
Rakic P, Bourgeois JP, Eckenhoff MF, Zecevic N,
Goldman-Rakic PS. 1986. Concurrent over-

Am. J. Primatol. DOI 10.1002/ajp10.1002/ajp.20348

156

Stone Handling in Japanese Macaques / 281
production of synapses in diverse regions of the
primate cerebral cortex. Science 232:232–235.
Ramsey JK, McGrew WC. 2005. Object play ingreat apes. Studies in nature and captivity.
In: Pellrgrini AD, Smith PK, editors. The
nature of play–great apes and humans.
New York: Guilford Press. p 89–112.
Smith EO. 1978. A historical view on the
study of play statement of the problem. In:

Smith EO, editor. Social play in primates.
New York: Academic Press. p 1–32.
Torigoe T. 1985. Comparison of object manipulation among 74 species of non-humanprimates. Primates 26:182–194.
Zecevic N, Bourgeois JP, Rakic P. 1989.
Changes in synaptic density in motor cortex
of rhesus monkey during fetal and postnatal
life. Dev Brain Res 50:11–32.

Am. J. Primatol. DOI 10.1002/ajp10.1002/ajp.20348

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Acquisition and development of stone handlingbehavior in infant Japanese macaques

Charmalie A.D. Nahallage & Michael A. Huffman1)(Section of Ecology, Department of Ecology and Social Behavior, Primate ResearchInstitute, Kyoto University, 41-2 Kanrin, Inuyama, Aichi 484-8506, Japan)(Accepted: 5 July 2007)

Summary
In this study we systematically investigate the mode of acquisition and the developmental
process of stone handling, a form of solitary object play, in a captive troop of Japanesemacaques (Macaca fuscata) housed in an outdoor enclosure at the Kyoto University Primate
Research Institute, Japan. This study was conducted to evaluate two alternative hypotheses
regarding the mode of acquisition of stone handling in infants: (1) environmental stimuli(availability of and exposure to stones) and (2) social stimuli (exposure to stone handlingindividuals). Early exposure to stones in the environment had no significant effect on wheninfants acquired the behavior. No significant correlations were recognized between the ageof stone handling acquisition and number of stones encountered per hour from birth to acquisition, or the time spent in a specific area of the enclosure as a function of the number ofavailable stones therein. However, being exposed to a stone handling model(s) was a social
stimulus that had an effect on the age of acquisition, with a significant negative correlation
between a mother’s stone handling frequency and the age of acquisition by her infant. Infantsof non-stone handling mothers acquired the behavior much later than others. Infant peers
who acquired stone handling earlier played no significant role as stone handling models. Of
the factors tested here, the timing of acquisition depended mainly on the level of proximity
to a demonstrator and the frequency at which those available demonstrators performed the
behavior.
Keywords: solitary object play, proximity, behavioral model, stimulus enhancement, transmission.

1) Corresponding author’s e-mail address: huffman@pri.kyoto-u.ac.jp© Koninklijke Brill NV, Leiden, 2007

Behaviour 144, 1193-1215
Also available online - www.brill.nl/beh

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Introduction
In group-living animals, one way of acquiring a new behavior by a naïve individual is to watch an experienced individual perform it. How quickly a naïve
individual can acquire the behavior depends on how frequently it can observe the experienced individual (model) perform that behavior. Therefore,
for the acquisition process, proximity (tolerance of the model), frequencyof the behavior performed, and the attention paid to the behavior are very
important factors which increase the possibility for socially biased learning (Coussi-Korbel & Fragazy, 1995; Whiten, 2000; van Schaik, 2003; van
Schaik et al., 2003; Perry & Manson, 2003; Londsdorf, 2006; Moscovice &Snowdon, 2006; Range & Huber, in press). For most behaviors, social affiliation plays an important role in the acquisition and pathway of transmission(Old World Monkeys: Kawai, 1965; Huffman & Hirata, 2003; New World
Monkeys: Perry et al., 2003a,b; Chimpanzees: de Waal, 2001; Matsuzawa
et al., 2001; Biro et al., 2003; Bonnie & de Waal, 2006; Dolphins: Mann &Sargeant, 2003). Affiliation can be measured as the amount of time two individuals spend in proximity to one another or engage in positive interactions(Mason, 1966; Bonnie & de Waal, 2006). Thus, individuals who have strong
affiliative ties, and spend more time in proximity, are more likely to show
similar behaviors.
If socially biased learning is to be evoked as the primary mode of acquisition for a given behavior, acquisition of that behavior by naïve individuals should be faster in those individuals with greater opportunity to observe
and learn from experienced models (van Schaik et al., 2003; Perry & Manson, 2003). However confounding this are environmental, social, and developmental constraints that can affect the efficiency and speed by which aparticular behavior is individually acquired and diffused through the group(Huffman & Hirata, 2003). When considering the acquisition of new behaviors by infants, it is assumed that the mother is the key source of informationin the first few months of life due to a total dependence on her for all basic
survival needs, and many of these behaviors are food related, e.g., food preferences or feeding techniques for food items difficult to eat (Hall, 1963; Itani& Nishimura, 1973; Watts, 1985; Goodall, 1986; Whitehead, 1986; Aisner& Terkel, 1992; Fragaszy & Visalberghi, 1996; Laland et al., 1996; Schuchmann, 1999).
There are some behaviors displayed by primates that do not have any
direct adaptive value for the performer but are still transmitted to succes-

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sive generations (Goodall, 1986; de Waal & Seres, 1997; van Schaik etal., 2003; Matsusaka et al., 2006). One such behavior acquired by infant
Japanese macaques is stone-handling, which is a form of solitary object play(see Huffman, 1984, 1996; Nahallage & Huffman, 2007). In the free-ranging
Arashiyama troop outside of Kyoto Japan, stone-handling behavior was first
documented in 1979 as an innovation of a juvenile female. The behavior subsequently spread horizontally to peer playmates and older immature kin relatives over several years in what was termed the ‘transmission phase’ (Huffman, 1984). As female stone handlers matured, their infants began to exhibit
the behavior within the first six months of life. It was proposed that mothers
were the primary route of transmission to young during the subsequent ‘tradition phase’ (Huffman, 1984, 1996; Huffman & Quiatt, 1986). This makes
sense, as individuals highly tolerant of each other are most likely to observe
the activity of each other in more detail, affording a greater potential forlearning (e.g., Huffman & Quiatt, 1986; Aisner & Terkel, 1992; van Schaik,
2003; Huffman & Hirata, 2003). Social life in group-living animals is complex, and this makes it essential to view the dynamics of social learning fromthe perspective of the social group’s interactive network. Thus, understanding the process of acquiring stone-handling behaviors is expected to increase
our knowledge on the role that demonstrators play in the learning and transmission processes of social living animals (e.g., Lefebvre, 1995).
Details of the mode of acquisition and the developmental process of stone
handling have not yet been systematically clarified. This is in large part due
to the difficulty of conducting systematic longitudinal observations on individuals in free-ranging troops. In captivity, there are also logistical and ethical limitations to the study of social living primate groups such as invasive
manipulations to mother-infant pairs at critical periods of infant development. Working within these limitations, this study is the first to systematically investigate the acquisition and development of a behavioral tradition ina social living troop of monkeys maintained under semi-natural conditions.
We adopt the Coussi-Korbel & Fragazy (1995) framework of social learningin terms of behavioral coordination between individuals, and in terms of thekind of information that may be acquired by an observer from a demonstrator without considering the underlying psychological mechanism. A captive
stone-handling troop was chosen to facilitate detailed observations and environmental quantification. We examine the relative influence of an infant’s

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exposure to stones in the environment, and the exposure to active stone handling models or demonstrators, on the acquisition and development of stonehandling behavior. We test two alternative hypotheses for the acquisition ofstone handling behavior: (1) environmental stimuli hypothesis predicts thatthe total time spent in areas with high stone availability and, therefore, being exposed to more stones, increases the likelihood that an infant acquires
stone-handling behavior and (2) social stimuli hypothesis predicts that theage at which infants acquire stone-handling behavior is influenced by thefrequency the behavior is exhibited by their mothers.

Materials and methods
This study was conducted on the Takahama troop of Japanese macaques kept
in a 960 m2 outdoor enclosure at the Primate Research Institute, Kyoto University, Inuyama City, Japan. This is part of an on-going systematic study
on the social, ecological and functional aspects of stone handling (Nahallage& Huffman, 2007). The data presented were collected over two study periods: June 2003 to November 2004 (18 months) and May 2005 to December
2005 (6 months). The age-sex class distribution of the troop during the study
periods is given in Table 1.
All data were collected using the continuous focal animal sampling
method (Altmann, 1974). Basic protocol for recording stone handling behavior in this study was adopted from Huffman (1996). In a previous study,
45 different stone handling behaviors were recorded and described (Nahallage & Huffman, 2007; see Table 2). Each focal session was recorded inits entirety by video (Sony Digital Handycam) for a minimum of fifteen
minutes. The focal session was extended for 5 min if stone-handling wasstill in progress or began near the end of the session, and it was terminatedif no further contact with stones was made. Stone-handling behavior was recorded as bouts, and a bout was defined as the continuation of the behavior
with pauses of no longer than 120 s. If stone handling resumed after a 120-s
pause, it was considered a separate bout (Huffman, 1996).
A total of 14 infants were born into the troop from 12 mothers during
the study and observations for all were recorded. They accounted for eightmother-infant pairs in 2003 (172 h observation) and six mother-infant pairs
in 2005 (72 h). With the exception of one particular mother, all mothers and

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Table 1. Age/sex class distribution of individuals in Takahama troop.
Class category(Age)
Adult males(over 10 years)
Adult females(over 7 years)
Adolescent males(5-9 years of age)
Adolescent females(5-6 years of age)
Juvenile males(1-4 years of age)
Juvenile females(1-4 years of age)
Infant males(0-1 years of age)
Infant females(0-1 years of age)
Total

Number of individuals in 2003
(No. sampled)

Number of individuals in 2005
(No. sampled)*

1 (1)

1

18 (18)15 (6)

5 (5)

6

—

2

9 (9)

11

7 (7)

11

3 (3)

3 (3)

5 (5)

3 (3)

48 (48)52 (12)* Only the new born infants and their mothers were sampled.

Table 2. Stone handling behavioral repertoire of the Takahama troop (modified from Nahallage, 2005; Nahallage & Huffman, 2007).
Bite: Bite a stone
Carry in Mouth: Carry a stone in one’s mouth while locomoting
Carry: Carry a stone cuddled in one’s hand from one place to another
Clacking: Clack stones together (Both hands moving in a clapping gesture)
Combine stones with other objects: Combine a stone with other objects that can be found in
the enclosure eg. pellets, pieces of strings, metals etc.
Cuddle: Take hold of, grab or cradle a stone for a few seconds
Flint in Mouth: Strike a stone against another held in mouth
Flinting: Strike a stone against another held stationary
Flip: Flip a stone
Gathering: Gather stones into a pile in front of oneself
Grasp Walk: Walk with one stone or more in the palm of one or both hands
Grasp with Hands: Clutch a pile of stone gathered and placed in front of one self
Hold: Pick up a stone and hold it away from the bodyJump and Throw: Jump and throw a stone forward or backward
Lick: Lick a stone
Move and Push: Push/pull a stone with one or both hands while working forward/backward

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Table 2. (Continued.)
Move inside Mouth: Make a stone move inside one’s mouth with tongue or hand
Pick Up a Small stone: Pick up a small stone and hold it between finger tips (like wheat
grains)Pick Up and Drop: Pick up a stone and drop it repeatedly
Pick Up: Pick up a stone and placed it into one’s hand
Pick: Pick
Pound on a surface: Pound a stone on a substrate
Put in Mouth: Put a stone in one’s mouth and keep it sometime
Put in Water: Put a stone in water
Roll in Hands: Roll a stone in one’s hand
Rub in Mouth: Rub a stone against another held in mouth
Rub on Fur: Rub or put a stone on one’s fur
Rub on Surface: Rub or roll a stone on a surface
Rub Together: Rub stones together
Rub with Hands: Hold a stone in one hand and rub it with the other
Rub With Mouth: Rub a surface with a stone held in mouth
Run and throw: Run and throw a stone or vise versa
Scatter: Scatter stones about, on a substrate, in front of oneself
Shake in Hand: Take small stones into ones hand and shake it
Slapping: Slap or pound a stone with ones fingertips or palm of ones hand
Sniff: Sniff a stone
Spin: Spin a stone with one hand or both hands
Stone groom: Groom somebody with a stone
Swiping: Swipe stones together in a sweeping gesture
Tap in Mouth: Put a stone in ones mouth and tap it slightly with one’s finger tip or palm
Throw and Sway: Throw a stone and sway from front to backThrow: Throw without jumping and running
Toss Walk: Toss a stone ahead (repeatedly) and pick it up while walking
Wash: Wash a stone in water
Wrap in Leaves: Wrap stones in leaves

infants were observed to handle stones in both years. In 2005, observations
were conducted in the peak period of stone handling activity for the whole
troop, i.e., between 15:00 and 17:00 h (Nahallage & Huffman, 2007). In both2003 and 2005 infants stayed very close to their mothers during their first
three months of life and were, therefore, recorded together in full monitor
view at all times. Mother and infant behaviors collected from the same video
record were later transcribed into two separate data sheets, and considered
independent of each other since different data were transcribed and analyzed
for mother and infant. Infants began to move further away from their mothers
after 3 months and, therefore, separate focal sessions were recorded for each163

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at these times. Mother stone-handling frequency per hour was calculated
from the transcribed focal records. An infant’s proximity to other individuals,
stone-handling behaviors displayed and time spent in each location of theenclosure were transcribed. Proximity was defined as being within one meterto another individual, and the identity of that individual was recorded.
For the analysis of the development of stone handling behavior in infants
and a comparison with other age groups, only data from the first study period were used, and included all members of the troop. A total of 516 h offocal observations (43 focal observation sessions per individual) distributed
equally across time of day (7:00 to 19:00) and season were used in the analysis.
The entire monkey enclosure floor area was divided into 32 blocks that
ranged in size of 18.9 m2 and 24 m2 , depending on the enclosure’s boundaries, to determine the location of infant stone-handling bouts within the enclosure, and the relative effect of the number of stones on the first observedstone-handling behavior by individual infants. Each plot was assigned a letter and number code, e.g., A1, A2, A3, A4, etc. The enclosure had threeterrace or flat areas at different elevations that were separated by two cement slopes, but stones could only be found on the flat areas. Stones were
not distributed equally across all plots in the enclosure because individuals
have preferred stone handling sites that they repeatedly return to (Nahallage
and Huffman, 2007). In addition, inter-plot differences exist because gravitational force may contribute to the clustering of stones in certain areas. The
average number of stones per plot was 604 ± 784 (range 0 to 3228). We
estimated the distribution of stones in the enclosure by counting the number of stones in each block at the end of each study period, and only stones
within the size range observed during stone handling, i.e., 8×10×7 mm and92 × 62 × 41 mm, were counted. For data analysis we used the mean numberof stones per each respective plot over the two years since there was no statistically significant difference between years in the distribution and numberof stones in each block (Wilcoxon signed-ranks test: T = 1.07, N = 32,
p = 0.284).
Non-parametric two-tailed tests were used and significance was at p <0.05. SPSS (version 10) was used for analyses.

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Results
Infant’s proximity to the mother and other individuals
The mother was the primary determinant of an infant’s early exposure to
the physical and social environment. For the first three months, the average
percent of time the infant spent in proximity to its mother (75 ± 12.72%,
N = 14 infants) was greater than that spent with any other troop member(Figure 1, Table 3). Mothers kept their young infants from wandering off
alone by picking them up or by holding onto a leg or arm. Thus, infants
had very little contact with older juveniles or with other adults in the groupduring early life.
After 3 months, the average percent of time an infant spent within 1 m
proximity to its mother decreased (58 ± 15.50%, N = 14) while proximity
to peers increased (22 ± 13.23%, N = 14). Around this time, infants also
started to interact with other members (older juveniles and adults) of thegroup (5 ± 3.76%). A low level of contact between infants and their siblings(2 ± 3.87%) across the first six months occurred because 6 out of 14 infants
had no siblings. Siblings were between two to three years old and spent moretime with their peers than with their mothers and newborn infants.

Figure 1. Infant’s average time spent in proximity (1 m) to others in the first 6 monthsof life.

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Table 3. Percentage of time spent by infants with mother, peers and others
between 0-3 months and 4-6 months of life by a mother’s frequency of stone
handling (SH).
Age

N

Mother’s frequencyof SHTime spent
with mother

Time spent
with peersTime spent
with others

0-3 months

2
10High (4)Moderate-Low(0.05-1.09)
Non-SH (0)

0.74
0.73

0.18
0.10

0
0.01

0.86

0.02

0

0.78

0.13

0.05

0.54
0.59

0.25
0.20

0.10
0.01

2
4-6 months

2
102High (4)Moderate-Low(0.05-1.09)
Non-SH (0)Environmental effects on infant’s acquisition of stone handling
We analyzed environmental factors that might contribute to the acquisitionof stone handling. Exposure to stones in the environment did not have a significant effect on stone handling behavior (Figure 2). There was no significant correlation between the amount of time spent in plots and the approximate number of stones in plots (Spearman rank correlation: rS = 0.016,
p = 0.741, N = 445, Figure 2a), or the approximate number of stones encountered per hour from the time the first stone handling observation bout by
an infant was recorded and the age (weeks) at which an infant was first observed stone handling (Spearman rank correlation: rS = 1.137, p = 0.641,
N = 14, Figure 2b). These data suggest that spending time in places withmany, or few stones does not influence the timing of an infant’s acquisitionof stone-handling behavior.
Effect of mother’s stone handling frequency on infant’s age at first stone
handling
All but one of the 14 infants started stone handling within the first 6 months
after birth. Their age at first stone handling ranged from as early as 6 weeks
to as late as 31 weeks (15.78 ± 7.0, N = 14). We calculated the percentileof stone handling frequencies by mothers, and individuals falling above 75
were classified as frequent stone handlers (2 mothers), while females falling
below this level were classified as less-frequent stone handlers (10 mothers).
One female did not stone handle and was classified as non-handler. Infants of

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Figure 2. Relative influence of encountering stones versus exposure to active stone handling model on the acquisition of stone handling; (a) mother’s frequency of stone handlingbouts/h (Spearman rank correlation: rS = −0.630, N = 14, p = 0.016); (b) number of stones
encountered/h (pearman rank correlation: rS = 1.137, N = 14, p = 0.641); (c) time spentper plot, before stone handling for the first time (Spearman rank correlation: rS = 0.016,
N = 445, p = 0.741).

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frequent stone handling mothers generally exhibit the behavior earlier than
infants of less-frequent stone handling mothers. There was a statistically significant negative correlation between the mothers’ frequency of stone handling bouts per hour and the age at which infants first started stone handling(Spearman rank correlation: rS = 0.630, N = 14, p = 0.016, Figure 2c).
Furthermore, the average stone handling time per bout for frequent stone
handling mothers was 133 ± 57.25 s (range 42-267 s, N = 7 bouts), andfor less-frequent stone handling mothers it was 73 ± 72.95 s (range 5-194 s,
N = 16 bouts). Also, the infants of frequent stone handling mothers werewatching their mothers’ stone handling in 83% (931 s) of the mother’s total
time handling stones, and in 75% of these stone-handling bouts they tried totake the stones away. Infants of less frequent stone handling mothers watched
their mother stone handle in only 42% (1183 s) of their time handling stones,
and tried to take stones away in 33% of these bouts. One effect of the difference in a mothers’ stone handling frequency is that some infants have longer
exposure to stone-handling, more opportunities handling stones, and morepractice stone-handling than other infants.
Only three adult females out of the total 48 individuals in Takahama troop
did not stone handle. Two of these three adult females were 25 and 21 years
old, and gave birth for the last time in 1999 and 2002, respectively. The third,
an 8 year old female is the only reproductively active non-stone handlingfemale in the troop, and she gave birth for the first time in 2003 and thenagain in 2005.
The two infants of the only non-stone handling mother were the last toacquire the behavior among their peers. In the first study period, this nonstone handling mother was highly protective of her infant, which spent 88%
and 70% of its time within 1 m of her in the first 0-3 month and 3-6 month
periods, respectively. Consequently, the infant spent relatively little time withpeers. It first displayed stone handling 31 weeks after birth, and after it had
begun to spend more time with peers (13%). When this female gave birthagain in the second study period, she appeared less protective and the infant
spent less time in proximity after the first 3 months (3-6 months: 47%), andmore than twice as much time in proximity with peers (28%) than its older
sibling. This infant first displayed stone handling 23 weeks after birth, whichis 8 weeks earlier than its older sibling. This finding highlights the fact thatin this semi-natural troop, mothers were the primary stone-handling models
for infants, and suggests that peers play a secondary role as models in the

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acquisition of stone handling behavior when a mother does not display the
behavior. This is consistent with the hypothesized effect of early proximity
to a stone-handling model on the acquisition of this behavior. Acquisitionof stone handling was substantially delayed if the mother was a non-stone
handler.
The infants that acquired stone handling behavior between 10 and 22
weeks spent 73% of their time in proximity with their mothers during thefirst 3 months, but later gradually spent more time with peers and others.
Two possible sources for the acquisition of stone handling exist for these
individuals: (1) the mother is the primary influence but with a lower frequency of stone handling displayed per hour; since her impact is less thanhigh frequency stone handling mothers, it may take more time for infants
to reach a critical level of exposure before acquisition, or (2) increased timespent in proximity with peers already stone handling may increase the acquisition of the behavior. However, proximity with older juveniles or otherstone-handling adults was extremely low and they were not considered likely
to have had any significant role in the transmission of stone handling to infants in this early period of their lives.
To evaluate the potential influence that infants which have already acquired stone-handling may have on acquisition of infants that have not yet
done so, we assessed the average frequency of stone handling per hour ofstone handling infants while in proximity to the non-stone handling infants.
There was no significant correlation between the average frequency of stone
handling infant peers per hour and the age at which the non-stone handlinginfant peers in proximity acquired the behavior (Spearman rank correlation:rS = 0.362, N = 10, p = 0.304, Figure 3a). The average frequency ofstone handling per hour and the amount of time spent in proximity to stone
handling infant peers was also not correlated (Spearman rank correlation:rS = 0.512, N = 10, p = 0.130, Figure 3b). These data suggest that exposure to stone handling peers had little effect on the timing of these infants’
first acquisition of stone handling behavior, and that delay in acquisition wasa consequence of their mother’s low stone handling frequency.
The two infants of the non-stone handling mother spent more time with
her than other individuals, and only displayed the behavior after 21 and 31
weeks of age, respectively, when they began to spend more time with peers.
For them the primary models are definitely troop members other than theirmother. In these cases, it was shown that the individuals found to be in closest
proximity to the infants were their peers (Table 3).

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Figure 3. Influence of stone handling infant peers for the acquisition of SH by late stone
handling infants; (a) peers average frequency of stone handling and infant’s first age of stone
handling (Spearman rank correlation: rS = 0.362, N = 10, p = 0.304); (b) total time spent
with SH peers (Spearman rank correlation: rS = 0.512, N = 10, p = 0.130).

Development of stone handling behavior
We found a gradual increase in the number and complexity of stone handling
patterns displayed by infants, which reveals a developmental phase of thisbehavior. During the first six months of life the average number of patterns
displayed by individuals was 3.75 ± 1.90, and these simple patterns involving minimal manipulation included Pickup, Cuddling, Biting and Holding(Table 4).
After six months, individuals started to engage in more manipulative actions with stones, and the average number of patterns displayed by an individual between ages seven and twelve months increased to 8.85 ± 2.26.
Patterns included combining more than one stone in the same action such as

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Table 4. Development of those stone handling patterns displayed in infants
over the first 18 months of life compared with juveniles.
Patterns displayed

Up to 6 months

7-12 months

13-18 months

24-48 months

Pick
Cuddle
Hold
Bite
Lick
Carry
Rub on Surface
Wrap in Leaves
Scatter
Rub in Hand
Put in Mouth
Carry in Mouth
Sniff
Rub Together
Move and Push
Grasp Walk
Clack
Rub on Fur
Combine with Object
Rub with Hand
Slap
Toss Walk
Flint
GatherTap in Mouth
Wash
Shake in Hand
Pick up and Drop
Pick up Small Stones
Throw stones
Flip
Pound
Move in Mouth
Rub in Mouth
Rub with Mouth
Jump and Throw
Stone Groom

x
x
x
x
x
x
x
x
x
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—

x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—

x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
—
—
—
—
—
—
—
—
—
—

x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
–
x
x
x
–
x
x
x
x
x
x
x
x
x

Total

9

18

27

35

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Acquisition of stone handling behavior

1207

Figure 4. Comparison of average number of stone handling patterns performed by individuals during their early period of development with other age classes.

clacking or rubbing stones together, or rubbing stones on other substrates.
Also, individuals started to carry stones with their hands and/or feet, andpushed them with both hands while walking (Table 4).
The average number of patterns displayed by an individual over 12 months
was 11.71 ± 4.30, and the most common pattern was to combine stones withother objects. At this age individuals were more familiar with their environment and attempted to combine stones with other objects. For example,
they tried wrapping leaves around stones or other metallic and plastic objects
found within the enclosure. In addition, patterns such as flinting of stones together, shaking stones in the palm of the hand like dice, or washing stones inwater were recorded (Table 4).
The number of behavioral patterns displayed by individuals gradually increased up to four years of age. Older juveniles displayed the highest numberof patterns among all age classes, but the number of patterns displayed decreased into adulthood (Figure 4).

Discussion
Our study found no support for the effect of environmental stimuli, i.e.,
exposure to stones in the environment, for the acquisition of the behavior
in infants. Instead, our data strongly supported the social stimuli hypothesisthat predicts infants acquire stone handling behavior by means of exposure
to stone handling models, i.e., the behavior is transmitted socially.

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Transmission of information about a behavior from one individual to another can be addressed in two ways. One way is to identify the underlying
learning mechanism involved in the information transfer such as imitation,emulation, stimulus and/or local enhancement (Whiten, 2000). Although thismethod is widely applied it requires controlled experimental settings, which
are difficult to achieve in field studies (Perry & Manson, 2003) or in situations where separation of individuals from others in their social group is
not preferred. The second complementary and equally important approach is
to explore not how, but from whom a behavior is learned, and traditionally
this has been addressed with observational methods (Kawai, 1965; Huffman,
1984; Hirata et al., 2001; Perry et al., 2003a,b; Lonsdorf et al., 2004).
There are no records of when stone handling started in the Takahama troop
studied, but at the time the research presented here was being conducted theoldest stone handling individual was 30 years old. Long-term observations at
Arashiyama suggest that individuals do not acquire the behavior after the ageof 5 (Huffman, 1996), and if conditions were similar in our Takahama troop,
it is likely that stone handling started nearly 25-30 years ago. Presently, andsimilar to the Arashiyama population, all the newborn infants and individuals
in Takahama below the age of 7 stone-handle, and the behavior is passed
down from older to younger individuals in each successive generation. Thus,
our data suggest that stone handling has reached the ‘tradition phase’ in the
Takahama group (see Huffman, 1984, 1996).
The proximity to an available model and the frequency of the behavior displayed by that model plays an important role in the process of acquiring stone
handling behavior by infants. Infants are capable of ‘copying’ the behaviorsof close associates even though they do not obtain any reward for performing
them (Biro et al., 2003). The model for infants is frequently the mother since
it is constantly exposed to the behaviors that she displays during the critical
period of its early development. This motivation for wanting to act like themother is explained as “education by master-apprenticeship”. For example,
chimpanzee infants are driven to copy not by motivation for food but simply
to copy their mother’s actions due to the strong affectionate bond of young
with their mother and because of the mother’s consistent tolerance toward
her infant (Matsuzawa et al., 2001). This phenomenon is also described as
Bonding and Identification-based Observational Learning (BIOL), where an
infant’s learning is “born out to be like others” (de Waal, 2001, p. 231). Whenthe mother displays the behavior frequently and for a longer time the infant173

Acquisition of stone handling behavior1209

has more opportunity to observe her than an infant whose mother does not
display the behavior as often and for a shorter time, or not at all. This isin agreement with van Schaik et al. (2003) in saying that the speed of acquisition of a behavior depends on the rate it was performed. The infant’s
desire to take part in the mother’s action, by trying to take the stones fromher, may result in stimulus enhancement learning. As a result, those infants
were observed to stone handle considerably earlier. Stimulus enhancement(Spence, 1937; Thorpe, 1956) occurs when a naive animal is attracted to theobject, or type of object that a conspecific has been manipulating. When themother infant bond is strong and proximity is high, it leads to the infants’ repeated observation and sometimes taking part in its mother’s activity (Hirata& Celli, 2003). This gives the opportunity for stimulus enhancement and social facilitation. Similarly, Coussi-Korbel & Fragazsy (1995) stated that oneof the first requirements for the occurrence of social learning is a stimulusthat draws the naïve individual’s attention and provide it with the information. This information could be provided from one animal to another throughthree forms of stimulation namely affective, physical and active stimuli. In
the case of stone handling, though all three forms likely contribute, the mostobvious form of stimulation may be affective stimuli produced by the percussive sounds of stone handling that draws an infant’s attention to the mother’s
action. Coussi-Korbel & Fragazsy (1995) go on to say that if individuals canspend a long time in proximity they are more likely to acquire specific behavioral patterns from each other. That is the more frequent a certain behavior isdisplayed the more chance the naïve individual has to acquire it (van Schaik
et al., 2003). Hence from our study we can say that it is not only proximity toa model but also the frequency that stone-handling behavior is displayed by
the model that is important for acquisition. In the case of our study, mothers
were the primary source of an infant’s early information about stone handling. This form of information transmission is known as vertical/traditionaltransmission, in which information is transmitted from parent to offspring(Cavalli-Sforza & Feldman, 1981). Coussi-Korbel & Fragazsy (1995) named
this type of learning as ‘directed social learning’ (i.e., “social learning that
occurs differentially as a function of the identity of the active individual”,
p. 1444). According to them, the moderately hierarchical social system andstrong matrilineal relationships prevailing in Japanese macaque society could
assist directed social learning among group members.

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In natural conditions an infant generally first acquires information about abehavior from its mother, but in situations where the mother does not display
the behavior, an infant must acquire the information from another individualwith whom it spends adequate time in proximity. In our study the otherindividual(s) were mainly peers. For example, the two infants born to themother that did not display stone handling were the last among their peers toacquire the behavior, and did so only after they started interacting with otherindividuals that did stone handle. The difference in timing of acquisition ofthese two siblings, born in consecutive years, was also dependent on therelative amount of time each spent with stone handling peers versus theirmother. The second infant spent more time with peers than the first infant
and, as predicted, acquired the behavior considerably earlier. Similarly, at
Arashiyama, the behavior first diffused among the young troop members,i.e., from a juvenile female to her peers and kin of relatively the same age(Huffman, 1984). In this case, because none of the mothers exhibited the
behavior, it could only spread horizontally from the innovator to other young
playmates.
The social learning process of stone handling in infants cannot be explained in terms of true imitation (reproducing the exact behavior of themodel) since when stone-handling was first acquired infants did not display
the same behavioral patterns as their mothers, and developmental constrainsare considered to prohibit this possibility. Our data show that there is a gradual increase in the number and complexity of patterns displayed, and thisvaries according to age (Table 4). In general, immature primates need relatively long maturation periods to master tasks that require complex sensorymotor actions (Boinsky & Fragaszy, 1989; Visalbergi & Fragaszy, 1990;
Drapier & Thiery, 2003). Among primates, the index of dexterity and theuse of relatively independent finger movement (RIFM) is thought to reflect
the degree to which motoneurons innervating the muscles acting on handand fingers receive direct, monosynaptic projections from the cerebral cortex (Phillips, 1971; Kuypers, 1981; Bortoff & Strick, 1993). It is known thatthe earliest sign of RIFM occurred at 2-3 months, with mature patterns at 7-8
months (Lawrence & Hopkins, 1976; Olivier et al., 1997). Galea & DarianSmith (1995) recently reported that performance on a reach and grasp test
by a group of young macaques approach adult levels by 6 months. These
results agree with our observations of the development of stone handling behavioral patterns. Although the infants in our study acquired the basic stone175

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handling behaviors at around 2-3 months, they only started to display moredemanding manipulative patterns from around 6 months. Even though thecortico-motoneuronal projections, responsible for RIFM, develop rapidly inthe first neonatal months, they do not mature fully until the second year oflife (Armand et al., 1996). This explains the observed increase in the numberof stone handling patterns up to 3-4 years of age. The increase in the numberof behaviors displayed with increasing age and the level of dexterity required
to perform them are evidence in support of a gradual refinement of neuromotor skills over the first 18 months of an infant’s life. Juveniles displayed
the greatest number of behavioral patterns. By this age they are highly active
and explorative by nature as well as physiologically capable of generating
many different stone handling behavioral patterns. Combined, these factors
could contribute to this increase in behavioral patterns displayed. Fragaszy &Adams-Curtis (1991), discuss this in terms of generativity aspects of object
manipulation in tufted capuchin monkeys.
In general, as stone handling is not a means to an immediate functionalend, there are no specific affordences guiding which behavioral patterns
should be displayed over others. However, the fact that there is significant
inter-site variation in the stone handling behavioral patterns displayed by
Japanese macaques (Leca et al., 2007) suggests that innovation of new stone
handling behavior patterns can occur. Given motoneuronal developmental
constraints in the young and a trend toward increasing behavioral conservatism in adults, we predict that in the case of stone handling, the route oftransmission (vertical or horizontal) of such new behavioral patterns is likely
to be determined by the level of behavioral dexterity required to display the
behavior and the social interactive network of the innovator. Investigation
into the propagation of such new behaviors is needed to test this prediction
in more detail.
Active teaching of stone handling to infants was not observed, unlike nut
cracking in Tai chimpanzees (Boesch, 1991) or prey-handling skills in wild
meerkats (Thornton & McAuliffe, 2006). However on rare occasions at both
Takahama and Arashiyama when an infant approaches its mother while she
is stone handling, she throws a stone towards it or allows the infant to takestones from her. The infants pick up these stones and start to stone handle.
While anecdotal, such generalized actions of the mother are expected toincrease an infant’s opportunity and motivation to interact more with stones.

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In conclusion, we can state that for stone handling, social learning in theform of stimulus enhancement plays a role in the acquisition of the behavior by infants. At this stage however, we do not rule out the possibility oftrue imitation of new behaviors or individual learning for the acquisition of
behavioral variants between individuals of sufficient motorneuronal development to perform them. More detailed observations and analysis of this aspect
is now underway. The timing of acquisition depends mainly on two factors,
proximity to a demonstrator and the frequency at which the primary demonstrator performs the behavior. Mothers were found to be the primary models
for infants, with the exception of those infants whose mother did not display
stone handling behavior. Another factor that may contribute to acquisitionis the degree of a mother’s willingness to let the infant interact with others.
Individual differences in the exposure to stones and their distribution in theenvironment did not influence the acquisition of stone handling.
Generalizing from our study, we conclude that acquisition of many socially learned behaviors can occur along multiple pathways from a varietyof potential demonstrators. This may vary according to the phase of transmission of the behavior within the population, i.e., transmission, tradition,transformation (Huffman & Quiatt, 1986), the nature of the behavior, theindividual’s stage of social and physical development and, availability of appropriate and reliable models. The fabric of social life in-group living animals is indeed complex. The rules of social learning too are complex, making
it essential to view the dynamics of social learning from the perspective of
the social group’s interactive network.
Acknowledgements
CADN’s graduate studies, of which this study is a part, were supported by the Japanese
Ministry of Education, Science and Culture. We are grateful to the HOPE Project, a Coreto-core program sponsored by JSPS (Japan Society for the Promotion of Science), for travel
funds to present this and related work at the 2006 IPS Congress in Entebbe, Uganda and theSocial Learning Conference in St. Andrews, Scotland where we benefited from many fruitfulcomments and criticisms by colleagues. This research was conducted in accordance with
PRI’s Rules and Guidelines for Animal Health and Welfare. We sincerely thank Drs. J.-B.
Leca, M. Bardi and A.D. Hernandez for their comments on data analysis. We thank Andrew
MacIntosh for reading and commenting on the manuscript. We also thank the faculty andsupporting veterinary staff of the Center for Human Evolution Modeling Research, PRI for
facilitating this research and for taking care of the captive monkey troops. Thanks are also
due to the faculty and students of the Department of Ecology and Social Behavior for theirvaluable advice and guidance. Many thanks are due to the many graduate students and friends
who helped us in various ways during the study.

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References
Aisner, R. & Terkel, J. (1992). Cultural transmission of pine cone opening behavior in theblack rat, Rattus rattus. — Anim. Behav. 44: 327-336.
Altmann, J. (1974). Observational study of behavior: sampling methods. — Behaviour 49:
227-267.
Armand, J., Olivier, E., Edgley, S.A. & Lemon, R.N. (1996). The postnatal development ofcorticospinal projections from motor cortex to the cervical enlargement in the macaquemonkey. — J. Neurosci. 17: 251-266.
Biro, D., Inoue-Nakamura, N., Yamakoshi, G., Sousa, C. & Matsuzawa, T. (2003). Cultural
innovation and transmission of tool use in wild chimpanzees: Evidence from field experiments. — Anim. Cogn. 6: 213-223.
Boesch, C. (1991). Teaching among wild chimpanzees. — Int. J. Primatol. 41: 530-532.
Boinsky, S. & Fragaszy, D.M. (1989). The ontogeny of foraging in squirrel monkeys, Saimiri
oerstedi. — Anim. Behav. 37: 415-428.
Bonnie, K.E. & de Waal, F.B.M. (2006). Affiliation promotes the transmission of a social
custom: handclasp grooming among captive chimpanzees. — Primates 47: 27-34.
Bortoff, G.A. & Strick, P.L. (1993). Corticospinal terminations in two New World primates:
further evidence that corticoneuronal connections provide part of the neural substrate
for manual dexterity. — J. Neurosci. 13: 5105-5118.
Cavalli-Sforza, L.L. & Feldman, M.W. (1981). Cultural transmission and evolution: A quantitative approach. — Princeton University Press, Princeton, NJ.
Coussi-Korbel, S. & Fragaszy, D.M. (1995). On the relationship between social dynamics
and social learning. — Anim. Behav. 50: 1441-1453.
De Waal, F.B.M. (2001). The ape and the sushi master. — Basic Books, New York, NY.
De Waal, F.B.M. & Seres, M. (1997). Propagation of handclasp grooming among captive
chimpanzees. — Am. J. Primatol. 43: 339-346.
Drapier, M. & Thierry, B. (2002). Social transmission of feeding techniques in Tonkean
macaques? — Int. J. Primatol. 23: 105-122.
Fragaszy, D.M. & Adams-Curtis, L.E. (1991). Generative aspects of manipulation in tufted
capuchin monkeys (Cebus apella). — J. Comp. Psychol. 105: 387-397.
Fragaszy, D.M. & Visalberghi, E. (1996). Social learning in Monkeys: Primate “Primacy”
reconsidered. — In: Social learning in animals: the roots of culture (Galef, B.G. &Heyes Jr., C.M., eds). Academic Press, San Diego, CA, p. 65-81.
Galea, M.P. & Darian-Smith, I. (1995). Postnatal maturation of the direct corticospinal projections in the macaque monkey. — Cereb. Cortex 5: 518-540.
Goodall, J. (1986). The chimpanzees of Gombe: patterns of behavior. — Harvard University
Press, Cambridge, MA.
Hall, K.R.L. (1963). Observational learning in monkeys and apes. — Br. J. Psychol. 54: 201226.
Hirata, S. & Celli, M.L. (2003). Role of mothers in the acquisition of tool-use behaviors bycaptive infant chimpanzees. — Anim. Cogn. 6: 235-244.
Hirata, S., Watanabe, K. & Kawai, M. (2001). Sweet-potato washig revisited. — In: Primate
origins of human cognition and behavior (Matsuzawa, T., ed.). Springer, Tokyo, p. 487528.
Huffman, M.A. (1984). Stone play of Macaca fuscata in Arashiyama B troop: Transmissionof a non-adaptive behavior. — J. Human Evol. 13: 725-735.

178

1214

Nahallage & Huffman

Huffman, M.A. (1996). Acquisition of innovative cultural behaviors in nonhuman primates: A case study of stone handling, a socially transmitted behavior in Japanesemacaques. — In: Social learning in animals: Roots of culture (Galef, B.G. & Heyes
Jr., C.M., eds). Academic Press, San Diego, CA, p. 267-289.
Huffman, M.A. & Quiatt, D. (1986). Stone handling by Japanese macaques (Macaca fuscata):
Implications for tool use of stones. — Primates 27: 413-423.
Huffman, M.A. & Hirata, S. (2003). Biological and ecological foundations of primate behavioral tradition. — In: The biology of traditions: Models and evidence (Fragaszy, D.M.
& Perry, S., eds). Cambridge University Press, Cambridge, p. 267-296.
Itani, J. & Nishimura, A. (1973). The study of infrahuman culture in Japan. — In: Precultural
primate behavior (Menzel Jr., E.W., ed.). Karger, Basel, p. 26-60.
Kawai, M. (1965). Newly acquired pre-cultural behavior of a natural troop of Japanese monkeys in Koshima island. — Primates 6: 1-30.
Kuypers, H.G.J.M. (1981). Anatomy of the descending pathways. — In: Handbook of physiology. The nervous system II (Brookhart, J.M. & Mountcastle, V.B., eds). American
Physiological Society, Bethesda, MD, p. 597-666.
Laland, K.N., Richerson, P.J. & Boyd, R. (1996). Developing a theory of animal social
learning. — In: Social learning in animals: Roots of culture (Galef, B.G. & Heyes Jr.,
C.M., eds). Academic Press, San Diego, CA, p. 129-154.
Lawrence, D.G. & Hopkins, D.A. (1976). The development of motor control in rhesus monkeys: evidence concerning the role of corticomotoneuronal connections. — Brain 99:
235-254.
Leca, J.-B., Gunst, N. & Huffman, M.A. (2007). Japanese macaque cultures: inter- and intratroop behavioral variability of stone handling patterns across 10 troops. — Behaviour
144: 251-281.
Lefebvre, L. (1995). Culturally-transmitted feeding behavior in primates: Evidence for accelerating learning rates. — Primates 36: 227-239.
Lonsdorf, E.V. (2006). What is the role of mothers in the acquisition of termite fishing
behaviors in wild chimpanzees (Pan troglodytes schweinfurthii)? — Anim. Cogn. 9:36-46.
Lonsdorf, E.V., Pusey, A.E. & Eberly, L. (2004). Sex differences in learning in chimpanzees. — Nature 428: 715-716.
Mann, J. & Sargeant, B. (2003). Like mother, like calf: the ontogeny of foraging traditions ofwild Indian Ocean bottlenose dolphins (Tursiops sp.). — In: The biology of traditions:
Models and evidence (Fragaszy, D.M. & Perry, S., eds). Cambridge University Press,
Cambridge, p. 236-266.
Mason, W.A. (1966). Social organization of the South American monkey. Callicebus
moloch. — Tulane Stud. Zool. 13: 23-28.
Matsusaka, T., Nishie, H., Shimada, M., Kutsukake, N., Zamma, K., Nakamura, M. &Nishida, T. (2006). Tool use for drinking water by immature chimpanzees of Mahale:
prevalence of an unessential behavior. — Primates 47: 113-122.
Matsuzawa, T., Biro, D., Humle, T., Inoue-Nakamura, N., Tonooka, R. & Yamakoshi, G. (2001). Emergence of culture in wild chimpanzees: Education by masterapprenticeship. — In: Primate origins of human cognition and behavior (Matsuzawa, T.,ed.). Springer, Tokyo, p. 557-574.
Moscovice, L.R. & Snowdon, C.T. (2006). The role of social context and individual experience in novel task acquisition in cottontop tamarins, Saguinus oedipus. — Anim. Behav.
71: 933-943.

179

Acquisition of stone handling behavior

1215

Nahallage, C.A.D. & Huffman, M.A. (2007). Age specific functions of stone handling, a solitary object play behavior in Japanese macaques (Macaca fuscata). — Am. J. Primatol.
69: 267-281.
Olivier, E., Edgley, S.A., Armand, J. & Lemon, R.N. (1997). An Electrophysiological studyof the postnatal development of the corticospinal system in the macaque Monkey. —J. Neurosci. 17: 267-276.
Perry, S. & Manson, J.H. (2003). Traditions in monkeys. — Evol. Anthropol. 12: 71-81.
Perry, S., Baker, M., Fedigen, L., Gros-Louis, J., Jack, K., McKinnon, K.C., Manson, J.,
Panger, M., Pyle, K. & Rose, L.M. (2003a). Social conventions in wild white-faced
capuchin monkeys. — Curr. Anthropol. 44: 241-268.
Perry, S., Panger, M., Rose, L.M., Baker, M., Gros-Louis, J., Jack, K., McKinnon, K.C.,
Manson, J., Fedigen, L. & Pyle, K. (2003b). Traditons in wild white-faced capuchins. —In: The biology of traditions: Models and evidence (Fragaszy, D.M. & Perry, S., eds).
Cambridge University Press, Cambridge, p. 391-423.
Phillips, C.G. (1971). Evolution of the corticospinal tract in primates with special reference tothe hand. — In: Proceedings of the 3rd International Congress in Primatology. Karger,
Zurich, p. 22-23.
Range, F. & Huber, L. (in press). Attention of common marmosets — Implications for social
learning experiments. — Anim. Behav.
Schuchmann, K.L. (1999). Family Trochilidae (Hummingbirds). — In: Handbook to the birdsof the world (del Hoyo, J., Elliott, A. & Sargatal, J., eds). Lynx Edicions, Barcelona,p. 468-680.
Spence, K.W. (1937). Experimental studies of learning and higher mental processes in infrahuman primates. — Psychol. Bull. 34: 806-852.
Thornton, A. & McAuliffe, K. (2006). Teaching in wild meerkats. — Science 313: 227-229.
Thorpe, W.H. (1956). Learning and instinct in animals. — Methuen, London.
van Schaik, C.P. (2003). Local traditions in orangutans and chimpanzees: social learning andsocial tolerance. — In: The biology of traditions: Models and evidence (Fragaszy, D.M.
& Perry, S., eds). Cambridge University Press, Cambridge, p. 297-327.
van Schaik, C.P., Fox, E.A. & Fechtman, L.T. (2003). Individual variation in the rate ofuse of tree-hole tools among wild orang-utans: Implications for hominin evolution. —J. Human Evol. 44: 11-23.
Visalberghi, E. & Fragaszy, D.M. (1990). Do monkeys ape? — In: Language and intelligencein monkeys and apes (Parker, S.T. & Gibson, K.T., eds). Cambridge University Press,
New York, NY, p. 247-273.
Watts, D.P. (1985). Observations on the ontogeny of feeding behavior in mountain Gorillas(Gorilla gorilla beringei). — Am. J. Primatol. 8: 1-10.
Whitehead, J.M. (1986). Development of feeding selectivity in mantled howling monkeys,
Alouatta palliata. — In: Primate ontogeny, cognition and social behavior (Else, J.G. &Lee, P.C., eds). Cambridge University Press, Cambridge, p. 105-117.
Whiten, A. (2000). Primate culture and social learning. — Cogn. Sci. 24: 477-508.

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CURRENT DIRECTIONS IN PSYCHOLOGICAL S CIENCE

Cultured Monkeys
Social Learning Cast in Stones
Michael A. Huffman, Charmalie A.D. Nahallage, and Jean-Baptiste Leca
Section of Social Systems Evolution, Primate Research Institute, Kyoto University

ABSTRACT—Sixty years ago, the notion that animals could
have culture was unthinkable to most behavioral scientists.
Today, evidence for innovation, transmission, acquisition,
long-term maintenance, and intergroup variation of behavior exists throughout the animal kingdom. What can
the longitudinal and comparative study of monkeys handling stones tell us about how culture evolved in humans?
Now in its 30th year, the systematic study of stone-handlingbehavior in multiple troops of Japanese macaques has
shown that socially mediated learning is essential to explain the spread, persistence, and transformation of individual behavioral innovations among group members.
The integrative research paradigm presented here canbe applied to the study of various candidate behavioral
traditions in other species.
KEYWORDS—solitary object play; socially biased learning;development; behavioral tradition; cultural zones

The concept of culture (also referred to as behavioral tradition)in animals was first proposed in 1952 by the founder of primatology in Japan, Kinji Imanishi, who predicted that culture
should be present in all socially living animals. The first evidence for culture in primates came shortly thereafter from fieldresearch on Japanese macaques. The innovation by the juvenile
female ‘‘Imo,’’ for washing sandy sweet potatoes in seawater, andthe behavior’s subsequent transmission widely within the group(Kawai, 1965), is now a frequently cited example for social
learning and culture in animals.
Evidence now exists for socially mediated learning and culture
in many species including the great apes, New World monkeys,
rats, cetaceans, birds, and fish (see Fragaszy & Perry, 2003). Allof these studies have looked at determinants of cultural behavior,including innovation, transmission, acquisition, developmental
constraints thereof, long-term maintenance, and intergroup
Address correspondence to Michael A. Huffman, Section of Social
Systems Evolution, Primate Research Institute, Kyoto University, 412 Kanrin, Inuyama, Aichi 484-8506, Japan; e-mail: huffman@pri.kyoto-u.ac.jp.

410

variation. However, none have considered the role of all of thesefactors within an integrated framework of social learning.
There are two basic approaches to the study of social learning.
The first focuses on underlying mechanisms—that is, how the
information is transferred between two individuals. In a controlled experimental setting, a naive subject, faced with aproblem-solving task, is given the opportunity to observe anexperienced subject and learn from its behavioral strategies(Custance, Whiten, & Fredman, 1999). The second approach
focuses on the pathway of behavioral diffusion under natural
conditions in a stable social group—that is, from whom theinformation is transferred (Biro, Inoue-Nakamura, Yamakoshi,
Sousa, & Matsuzawa, 2003). Interindividual tolerance allowing
spatial proximity, frequency of the behavior performed, andthe attention paid to the behavior are essential factors to predict
the speed of diffusion of a novel behavior and pathway oftransmission (Coussi-Korbel & Fragaszy, 1995; Huffman &Hirata, 2003; van Schaik, Fox, & Fechtman, 2003). However, notonly social, but also environmental, demographic, and developmental constraints can affect the efficiency and speed of acquisitionand diffusion of a particular behavior (Huffman & Hirata, 2003).
Only the study of stone handling (SH) in Japanese macaques has
embraced all of these determinants into the understanding of asingle cultural behavior. Our long-term study supports the idea ofSH culture and provides insights into the nature of social learning,
its role in the spread of behavioral innovations, and the importanceof culture in the process of behavioral evolution.
SH is a seemingly nonadaptive, solitary object-play activity(Huffman, 1984, 1996; but see Nahallage & Huffman, 2007a).
SH consists of manipulation of stones in various ways, including
rubbing or clacking them together; pounding them onto otherhard surfaces; picking up and rolling them together in the hands;
and cuddling, carrying, pushing, or throwing them (Fig. 1; Box1). Currently, 45 different behavioral patterns are documented inJapanese macaques (Leca, Gunst, & Huffman, 2007a).
SH occurs in four captive troops and six provisioned freeranging troops across Japan. This behavior has been followed
for 30 years across multiple generations in the Arashiyama
troop, Kyoto, Japan, beginning from its innovation in 1979 by ajuvenile female named ‘‘Glance 6476’’ (Huffman, 1984;

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Michael A. Huffman, Charmalie A.D. Nahallage, and Jean-Baptiste Leca

Fig. 1. Four stone-handling behaviors: (a) carry, (b) clacking, (c) rub on surface, and (d) rub
together.

BOX 1
Representative Stone-Handling Behaviors
MP (Move and Push): Push/pull a stone forward/backward with one orboth hands while walking
GW (Grasp Walk): Walk with one stone or more in the palm of one orboth hands
CA (Carry): Carry a stone cuddled in one’s hand from one place toanother
GA (Gathering): Gather stones into a pile in front of oneself
ROS (Rub on Surface): Rub or roll a stone on a surface
RT (Rub Together): Rub stones together
RWH (Rub With Hands): Hold a stone in one hand and rub it with theother
SC (Scatter): Scatter stones about, on a substrate, in front of oneself
CL (Clacking): Clack stones together (both hands moving in a clapping
gesture)FL (Flinting): Strike a stone against another held stationary
POS (Pound on a Surface): Pound a stone on a substrate

Volume 17—Number 6

Huffman, 1996). Unlike potato washing, SH was first transmitted
horizontally among playmates. Transmission began to occur
vertically from elder to younger individuals around 1984. Since
then, SH has been acquired by every infant in the group, but it
was never acquired by individuals over 5 years of age in the years
right after the behavioral innovation.
ACCESS TO DEMONSTRATORS BY NAIVE
INDIVIDUALS AND THE ACQUISITION OF BEHAVIORSThis long-term study at Arashiyama allows us to understand thepathways of diffusion of SH. Mothers were presumed to be theprimary source of an infant’s early exposure to SH (Huffman,
1984, 1996). Through controlled captive conditions, we wereable to systematically evaluate the effect of pivotal individuals
as demonstrators on the initial acquisition and developmentof SH behavior by focusing on interindividual interactions,

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particularly mother–infant pairs. We (Nahallage & Huffman,2007b) studied a group of 48 Japanese macaques at the Primate
Research Institute, Kyoto University, for 24 months spanning
two breeding seasons over a 3-year period, during which 14
infants were born. In these 14 mother–infant pairs, all but one
infant started SH within the first 6 months after birth. There wasgreat variability among them in the age SH was first displayed(6–31 weeks). During their first 3 months of life, infants spent
75% of the time within 1 meter of their mother, significantly moretime than they spent with other individuals. This high level ofproximity to the mother had a significant impact on the age at
which SH was acquired. Infants of mothers with higher SH frequencies exhibited the behavior earlier than did infants of lessfrequent SH mothers. Two infants born in consecutive years to
the same non-SH mother were the last to acquire the behavior.
These results suggest that the acquisition of SH behavior in
infants was strongly influenced by the amount of time spent inproximity to a stone handler and the frequency of the behavior
displayed by that model. Infants of frequent SH mothers spent
twice as much time (83%) watching their mothers when she
engaged in that behavior than did infants whose mother showed
low SH frequency (42%). The former tried to take stones awayfrom their mothers in 75% of the SH bouts whereas the latter
tried to do so in only 33% of these bouts, resulting in a differencein the amount of time an infant took part in its mother’s activity.
Differences in mothers’ SH frequency could affect their infants’
exposure to SH, opportunities of handling stones, and practiceof SH.

To better understand how the SH culture in Japanese macaques
may appear, spread, and be maintained within a group overgenerations, we (Leca, Gunst, & Huffman, 2007a) investigated
the roles of social and demographic factors in explaining intergroup similarities and differences in SH. We conducted a systematic comparison of SH in 10 troops of Japanese macaques,
including two troops studied over a long period of time at
Arashiyama and Takasakiyama. The analysis of 1,950 hours ofobservation revealed substantial variability in the frequency andform of SH between the troops. Most of the 45 SH patterns wedocumented were customary in some troops and rare or evenabsent in others even though they were ecologically possible(Leca, Gunst, & Huffman, 2008).
When we only considered the 33 SH patterns that were notobserved in all 10 troops studied, we found cultural similarity to
be significantly related to geographic proximity. Neighboring
troops living at the same site, with overlapping home ranges andcoming into occasional contact around the provisioning site—where SH activity most often occurs—tended to share similar SH
patterns. The numbers of patterns showing the same occurrencein the two troops at Shodoshima and in the two troops at

Takasakiyama were 26 and 25, out of 33, respectively. We propose the phenomenon of cultural zones, based on intertroop
observation and possibly males transferring SH patterns when
migrating from one troop to another. When such intertroop social
influences do not exist (e.g., troops separated by substantial
geographic distance in natural situations or by artificial barriers
like concrete walls in captive conditions), the troops showed
more differences in their SH repertoires: Their mean number ofbehaviors showing the same frequency of occurrence was only
12.1  7.3.
To test the hypothesis that SH will be more prevalent in morecohesive groups, we calculated, for the 10 study troops, a grouplevel index of social tolerance, defined as the mean percentage ofgroup members within 1 meter of each other, and recorded every
15 minutes by the observer visually or physically moving fromone side of the troop to the other, in a set direction. Group-levelsocial tolerance was not significantly correlated with the frequency and rate of diffusion of SH (Leca, unpublished data). In
other words, the troops showing higher levels of positive social
interactions (e.g., grooming and playing) were not necessarily
the troops with more frequent episodes of SH and higher percentages of stone handlers. Instead, group size and group spatialcohesion after food provisioning was positively correlated withthe prevalence of SH. Larger troops characterized by closer
physical proximity among individuals feeding on provisioned
food also showed higher percentages of troop members exhibiting SH simultaneously, which may reveal the contagious natureof play (Leca, Gunst, & Huffman, 2007b).
Another demographic factor, age structure of the group, mayalso affect the diffusion and maintenance of SH. Troops withabnormal age structure (e.g., missing age classes) showed alower proportion of stone handlers and a lower frequency of SH
than did more normally age-structured groups (Leca, Gunst, &Huffman, 2007b). These findings are consistent with long-term
observations at Arashiyama suggesting that (a) after initial innovation by youngsters, SH behavior first spreads among young
individuals, probably peer playmates; (b) there is a critical period after which SH cannot be acquired by an individual (> 5years); and (c) when a behavioral practice is restricted to aparticular class of group members, its propagation should beslow and its maintenance may be jeopardized (Huffman, 1996).
At Arashiyama and Takasakiyama, the SH culture has at least
a 30-year history. By using similar methods of data collection inthese troops, 13 and 15 years apart, respectively, we found thatthe size of the SH repertoire almost doubled in both troops. The
SH patterns not recorded before involved complex manipulative
actions, such as combining stones with other objects andgrooming with a stone (Leca, Gunst, & Huffman, 2007a). Theselongitudinal data suggest a ‘‘ratchet effect,’’ defined as an increase in the diversity and complexity of SH patterns comparedto earlier generations of stone handlers. As the duration of agroup’s experience with SH increases, so does the variety of patterns displayed, possibly as a product of an increase in the183

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FACTORS RESPONSIBLE FOR INTERGROUPVARIATION

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Michael A. Huffman, Charmalie A.D. Nahallage, and Jean-Baptiste Leca

number of ‘‘individual contributions’’ to the group’s behavioral
repertoire, which gradually diffuse through the group (e.g., shakein-hands and stone-throwing patterns in the Takahama group).
Our comparative approach revealed that intergroup variability
in SH may be best explained by demographic factors, opportunities
for observational learning, and behavioral coordination at thegroup level.

We concluded that at the time of acquisition, infants acquire arudimentary form of SH but are constrained from matchingspecific behaviors due to their level of neuromotor development.
Our findings support juvenile-primate developmental theories(Pereira & Fairbanks, 1993). Later on, however, this kind ofmatching does appear to occur, and is noticeable particularly inrare behaviors displayed by the mother, which are now being
seen to diffuse among offspring and others.

CONSTRAINTS OF NEUROMOTOR DEVELOPMENT ON
THE EXPRESSION OF SH BEHAVIORS

Few longitudinal studies have been conducted on the ontogenyof specific cultural behaviors; most research has tended to deduce development from cross-sectional observations (Lonsdorf,2005). Furthermore, neuromotor development has rarely been
considered as a constraint in the expression of matched behavioral patterns between experienced and naı̈ve individuals.
Our study shows that, though mothers have a strong influence on
infants’ initial acquisition of SH behavior, infants do not performthe same behavioral patterns as adults, mainly because ofdevelopmental constraints in the kinds of behaviors they can
perform (Nahallage & Huffman, 2007b). There is a gradualincrease in the number and complexity of SH patterns displayed
by infants, which reveals a neuromotor developmental phase ofthis behavior. The infants we studied acquired the basic SH
behaviors at around 2 to 3 months. Common to other behavioral
traits observed during the early stages of infant development in
macaques, stone-manipulation patterns are simple actions—mainly, picking them up or cuddling, licking, or biting them.
Such actions are typically short in duration. Infants do not perform any complex manipulative action with stones during thistime. The average number of patterns performed by an individual up to 6 months of age was 3.75  1.90. Around 6 months,
individuals started to perform clacking or rubbing two stones
together or on a substrate. On average, they displayed 8.85 
2.26 patterns from 6 to 12 months of age. The earliest sign ofrelative independent finger movement occurs at 2 to 3 months,
with mature patterns occurring at 7 to 8 months (Bortoff & Strick,1993). Galea and Darian-Smith (1995) reported that performance on a reach-and-grasp test by a group of young macaques
approached adult levels by 6 months. This agrees with our study
showing infants starting with only the very basic SH behaviors
between 2 and 3 months and performing activities that requires
firm grasp of the stones around 6 months. Though the motoneuronal projections responsible for finger movement develop
rapidly in the first months after birth, they do not mature until thesecond year of life. This explains the increase in the number ofSH patterns up to 3 to 4 years of age. Older juveniles displayed
the highest number of patterns among all age classes (18.14 
5.38), whereas the number of patterns displayed decreased into
adulthood, which may reveal the appearance of individual
preferences or behavioral routines over the years (Nahallage &Huffman, 2007b).

Volume 17—Number 6

FUTURE DIRECTIONSSH is one of the longest-studied cultural behaviors in animals to
date. Research on this behavior in both captive and free-ranging
groups of monkeys has opened up new ways of addressing thecomplexities of learning in socially living animals through a
deeper understanding of the dynamics of behavioral transmission. In order to understand the mechanisms associated withsocially biased learning, future studies need to integrate thismethodology with controlled experimentation on captive groups.
This will allow us to more clearly address behavioral innovationand the underlying mechanism of diffusion within social groups.
Object manipulation provides a pool of behavioral variants
that, if fortuitously reinforced, can become tool-use patterns.
Long-term observations and documentation of the transformation of behavioral patterns are important to fully appreciate thepotential transformation of noninstrumental use of objects into
their instrumental use as tools. Longitudinal studies of SH already suggest that this could happen. The recent emergence of aunique behavior, stone throwing, may serve to augment the effectof intimidation displays. Research on such transformations may
shed light on the evolution of stone-tool use in early hominids.

Recommended Reading
Fragaszy, D.M., & Perry, S. (Eds.). (2003). (See References). A collection of papers reviewing the current state of knowledge on animal
traditions.
Huffman, M.A. (1984). (See References). The first detailed publishedaccount of SH in Japanese macaques.
Moscovice, L.R., & Snowdon, C.T. (2006). The role of social context andindividual experience in novel task acquisition in cottontop
tamarins, Saguinus oedipus. Animal Behaviour, 71, 933–943.
Recent research article detailing the role of social attention in theacquisition of behaviors, of interest to those contemplating sociallearning studies.
Pereira, M.E., & Fairbanks, L.A. (1993). Juvenile primates: life history,
development, and behavior. Oxford, UK: Oxford University Press.
Reviews major papers on primate development in terms of behavior and ecology by focusing on the juvenile period in primatesfrom an evolutionary and life-history perspective.

Acknowledgments—This paper is dedicated to Professors
Junichiro Itani and Duane Quiatt, who provided invaluable
encouragement and insight at the early stages of this research.

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Cultured Monkeys

Both MAH and CADN received support from the HOPE Project,a core-to-core program sponsored by the Japan Society for the
Promotion of Science (JSPS), to present some of this work at
international conferences. J.-B.L. was supported by a Lavoisier
Grant, Ministère des Affaires Etrangères, France, and a JSPS
postdoctoral fellowship (No. 07421). CADN’s graduate studies,of which this study is a part, were supported by the Japanese
Ministry of Education, Science and Culture. We thank Noëlle
Gunst for assisting in data collection.

Biro, D., Inoue-Nakamura, N., Yamakoshi, G., Sousa, C., & Matsuzawa,T. (2003). Cultural innovation and transmission of tool use in wild
chimpanzees: Evidence from field experiments. Animal Cognition,
6, 213–223.
Bortoff, G.A., & Strick, P.L. (1993). Corticospinal terminations in two
New World primates: Further evidence that corticoneuronal connections provide part of the neural substrate for manual dexterity.
Journal of Neuroscience, 13, 5105–5118.
Coussi-Korbel, S., & Fragaszy, D.M. (1995). On the relationshipbetween social dynamics and social learning. Animal Behaviour,
50, 1441–1453.
Custance, D., Whiten, A., & Fredman, T. (1999). Social learning of an
artificial fruit task in capuchin monkeys (Cebus apella). Journal ofComparative Psychology, 113, 13–23.
Fragaszy, D.M., & Perry, S. (Eds.). (2003). The biology of traditions: Models
and evidence. Cambridge, UK: Cambridge University Press.
Galea, M.P., & Darian-Smith, I. (1995). Postnatal maturation of thedirect corticospinal projections in the macaque monkey. Cerebral
Cortex, 5, 518–540.
Huffman, M.A. (1984). Stone play of Macaca fuscata in Arashiyama B
troop: Transmission of a non-adaptive behavior. Journal of Human
Evolution, 13, 725–735.

Huffman, M.A. (1996). Acquisition of innovative cultural behaviors in
nonhuman primates: A case study of SH, a socially transmitted
behavior in Japanese macaques. In B.G. Galef Jr. & C. Heyes(Eds.), Social learning in animals: Roots of culture (pp. 267–289).
San Diego, CA: Academic Press.
Huffman, M.A., & Hirata, S. (2003). Biological and ecological foundations of primate behavioral tradition. In D.M. Fragaszy & S.
Perry (Eds.), The biology of traditions: Models and evidence (pp.
267–296). Cambridge, UK: Cambridge University Press.
Kawai, M. (1965). Newly acquired pre-cultural behavior of a natural
troop of Japanese monkeys on Koshima Island. Primates, 6, 1–30.
Leca, J.-B., Gunst, N., & Huffman, M.A. (2007a). Japanese macaquecultures: Inter- and intra-troop behavioural variability of SH patterns across 10 troops. Behaviour, 144, 251–281.
Leca, J.-B., Gunst, N., & Huffman, M.A. (2007b). Age-related differences in the performance, diffusion, and maintenance of SH, abehavioral tradition in Japanese macaques. Journal of Human
Evolution, 53, 691–708.
Leca, J.-B., Gunst, N., & Huffman, M.A. (2008). Of stones and monkeys:
Testing ecological constraints on SH, a behavioral tradition in
Japanese macaques. American Journal of Physical Anthropology,
135, 233–244.
Lonsdorf, E.V. (2005). Sex differences in the development of termitefishing skills in the wild chimpanzees, Pan troglodytes schweinfurthii of Gombe National Park, Tanzania. Animal Behaviour, 70,
673–683.
Nahallage, C.A.D., & Huffman, M.A. (2007a). Acquisition and development of SH behavior in infant Japanese macaques. Behaviour,
144, 1193–1215.
Nahallage, C.A.D., & Huffman, M.A. (2007b). Age-specific functions ofSH, a solitary object play behavior in Japanese macaques (Macaca
fuscata). American Journal of Primatology, 69, 267–281.
van Schaik, C.P., Fox, E.A., & Fechtman, L.T. (2003). Individual variation in the rate of use of tree-hole tools among wild orang-utans:
Implications for hominin evolution. Journal of Human Evolution,
44, 11–23.

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REFERENCES

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 135:233–244 (2008)

Of Stones and Monkeys: Testing Ecological Constraints
on Stone Handling, a Behavioral Traditionin Japanese MacaquesJean-Baptiste Leca,1* Noëlle Gunst,2 and Michael A. Huffman3
1

Equipe d’Ethologie des Primates, Institut Pluridisciplinaire Hubert Curien, Département Ecologie,
Physiologie et Ethologie, UMR 7178 CNRS-ULP, 67087 Strasbourg, France
2
Institute of Ecology, University of Georgia, Athens, GA
3
Section of Ecology, Primate Research Institute, Kyoto University, Inuyama, Japan
KEY WORDS

stone availability; terrestriality; culture; Macaca fuscata

ABSTRACTJapanese macaques are known tomanipulate stones by displaying various seemingly functionless behavioral patterns, including carrying a stone,
rubbing two stones together, or gathering several stones
into a pile. This form of solitary object play called stone
handling (SH) is a behavioral tradition in Japanese macaques, showing striking intertroop differences in frequency and form. Here, we evaluated two ecologically
based hypotheses invoked to account for these differences. We hypothesized that the occurrence and form of SH
would be affected by stone availability and the degree ofterrestriality. We used standardized sampling methods
to assess differences in SH and terrestriality amongfour captive and six free-ranging troops of Japanesemacaques, and determine site-specific stone availability.
Although we demonstrated that SH is almost exclusively

a terrestrial activity, our comparative analyses showedthat the number of stones readily available and the relative amount of time spent on the ground by the macaques were not associated with the intertroop differencesin the occurrence of SH. Failure to accept the terrestriality and stone availability hypotheses suggests that theperformance of SH and the motivation to engage in thisactivity are both more diverse and more complex thanthe direct links to time spent on the ground or the number of stones locally available. Other environmental
influences and sociodemographic factors should be jointly
considered to identify the sources of variation in SH, asa beginning to better understand the constraints on theappearance and subsequent diffusion of stone-use traditions in nonhuman primates. Am J Phys Anthropol
135:233–244, 2008. V 2007 Wiley-Liss, Inc.

During the past decade, primatologists have found evidence of interpopulational behavioral differences in several nonhuman primate species (e.g., McGrew et al.,
1997; Whiten et al., 2001; Panger et al., 2002; van
Schaik et al., 2003; Leca et al., 2007a). When obvious
genetic and ecological causations can be ruled out, such
behavioral variation is largely considered cultural (oftenlabeled ‘‘traditional’’ in ethology). In recent years,
attempts have been made to study such variability in behavioral traditions between populations, using similar
methodologies, and in conjunction with rigorous documentation of the ecological context of occurrence of the
behavior in question (Perry, 2003). The comparative
method mainly involves accumulating information about
several groups and then correlating specific environmental conditions with the populations’ attributes, to draw
conclusions concerning the ecological factors responsible
for promoting the evolution of the phenomenon understudy (Fragaszy and Perry, 2003).
Early studies have documented some features of thephysical environment that favor the evolution of tool use
in primates (see Beck, 1980, for a review). The critical
ecological conditions are ‘‘embedded food’’ and ‘‘environmental opportunity’’ (Beck, 1980, p. 190 and 193; seealso Parker and Gibson, 1977; Hamilton et al., 1978).
According to the former, a diet including foods protectedby hard husks or encased inside woody substrates
requires extractive foraging techniques, among which
tool use may have been promoted as an adaptive behavioral innovation (Beck, 1980), According to the latter, fora tool-related behavior to evolve, the environment must
make it not only advantageous, but also possible. If theanimals have more time to manipulate objects readily
available in their habitat, they have more opportunities
to discover a novel tool pattern (Hamilton et al., 1978;
Beck, 1980).
Recently, these plausible explanations of how ecological factors may constrain the emergence of stone-tool use
traditions in nonhuman primates have been integrated
into three major hypotheses. First, the ‘‘necessity hypothesis’’ (after Fox et al., 2004) proposes that primaryresource scarcity may force group members to exploit
novel food sources that require the invention of new
food-processing techniques, including the use of stones
as tools to extract food from a substrate. For example,
seasonal variation in main food abundance may explain

C 2007 WILEY-LISS, INC.
V

186

C

Grant sponsor: National Science Foundation; Grant number:
BCS-0352035; Grant sponsor: Ministère des Affaires Etrangères(Lavoisier Grant), France.
*Correspondence to: Jean-Baptiste Leca, 2360 West Broad Street,
The Park on West Broad, Apt # 321, Athens, GA 30606, USA.
E-mail: jbtleca@yahoo.com
Received 18 January 2007; accepted 28 August 2007
DOI 10.1002/ajpa.20726
Published online 25 October 2007 in Wiley InterScience(www.interscience.wiley.com).

234

J.-B. LECA ET AL.

the appearance of nut-cracking for oil-palm kernels as
backup embedded foods in Bossou chimpanzees (Yamakoshi, 1998).
Second, the ‘‘stone availability hypothesis’’ (derived
from the ‘‘environmental opportunity conditions’’: Beck,1980, and the ‘‘opportunity hypothesis’’: Fox et al., 2004)
proposes that favorable local conditions, such as theabundance of loose stones suitable to manipulation,enhance chances for stone-tool invention via repeated exposure to stones, and acquired familiarity with stonerelated behaviors through the integration of stones withvarious daily activities. For instance, the common occurrence of Coula nut-cracking in Taı̈ chimpanzees may correspond to the concomitant presence of stones, transportable by hand, as appropriate natural hammers, surface
roots as adequate anvils, and Coula nuts, a staple foodresource at this site (Boesch and Boesch, 1984).
Third, the ‘‘terrestriality hypothesis’’ proposes thatengaging in various activities on the ground, rather thanin the trees, increases an individual’s chance of coming
across stones, also present on the ground. This may provide significant opportunities for stone-tool use, such as
the seed-cracking behavior observed in the brown capuchins of the Caatinga dry forest (Visalberghi et al.,2005). However, Beck (1980) highlighted the difficulty of
associating terrestriality and tool use in primates. In
some cases, time spent on the group may not be sufficient to account for the emergence of stone-tool behavior(Lee and Moura, 2005).
In primates, most cases of material culture and the
majority of reported behavioral innovations involving
stones occur under the context of foraging, probably
because information about food is critical to every individual (see Reader and Laland, 2001 for a review).
Instead of being labeled ‘‘cultural,’’ some group-specificforaging variants could be more parsimoniously explained on ecological grounds, because of subtle sitespecific differences in food, object and substrate availability (Laland and Hoppitt, 2003; Galef, 2004; Lalandand Janik, 2006). In contrast, behaviors unrelated tosubsistence, such as communicative signals, are likely to
be more flexible in form and less affected by ecologicaldifferences than food-related behavioral traditions, andin that sense, they would make better candidates for
culture (Perry et al., 2003; Moura, 2007).
The best-documented case of a nonsubsistence traditional activity in monkeys is stone handling (SH hereafter) in Japanese macaques, a form of solitary object
play consisting of the manipulation of stones by performing various behavioral patterns (Huffman, 1984, 1996;
Huffman and Quiatt, 1986; Huffman and Hirata, 2003;
Leca et al., 2006, 2007a; Nahallage and Huffman, 2007a).
For example, individuals in different troops may beobserved repeatedly pounding a stone on a substrate,
clacking two stones together, or gathering several stones
into a pile in front of them. SH mainly occurs and ismore frequent in young than in older individuals. SH
episodes are shorter, more vigorous, and SH patterns are
more diverse and less complex in immature than inmature individuals (Nahallage and Huffman, 2007a;
Leca et al., in press). These age-related differences in
the performance of SH could be attributed to possible
age-specific benefits of this activity. As a form of object
play strenuously performed by young monkeys, SH may
promote the development of motor skills in immaturesystems (Nahallage and Huffman, 2007a). As a psychologically relaxing activity in older monkeys, SH could

contribute to slow the impairment of cognitive functions
in aging individuals (Nahallage and Huffman, 2007a).
In free-ranging provisioned troops, most SH activity
occurs immediately after provisioning time, while monkeys chew cereal grains stored inside their cheekpouches (Huffman, 1984; Huffman and Quiatt, 1986; Lecaet al., submitted1). In contrast, SH in captive troops canbe observed throughout the day, regardless of feeding activity (Nahallage and Huffman, 2007a; Leca et al., submitted). Previous findings from two troops of free ranging and one captive troop of Japanese macaques showedthat SH is socially transmitted from generation to generation as a behavioral tradition (Huffman, 1984, 1996;
Huffman and Quiatt, 1986; Huffman and Hirata, 2003;
Nahallage and Huffman, 2007b). A recent interpopulational comparison of this behavior from a systematicinvestigation of four captive and six free-ranging troopsof Japanese macaques reported major differences in thefrequency of occurrence and the form of SH, and discussed the phenomenon of cultural zones (Leca et al.,2007a).
The ecological factors that contribute to these differences require investigation. While the ‘‘necessity hypothesis’’ is relevant to explain tool-use traditions, which are
behavioral adaptations potentially critical to individual
survival (e.g., Whiten et al., 2001; van Schaik et al.,2003), it can be a priori ruled out to explain variation in
SH behavior, which is regarded as the noninstrumental
manipulation of stones with no direct survival value(Huffman, 1984, 1996; Leca et al., 2007a). Although SH
does not meet the descriptive criteria of Beck’s (1980)
definition of tool use, the daily practice of stone-related
combinatorial patterns by most members of a group
could be considered as a behavioral precursor to the possible use of stones as tools (Huffman and Quiatt, 1986;
Huffman, 1996; Leca et al., 2007a). Because stone-tool
behaviors in nonhuman primates may reflect on the origin and evolution of lithic technology in hominids (Foley
and Lahr, 2003), it is critical to identify the environmental sources of SH variation in Japanese macaques. However, the most obvious ecological differences which could
affect SH, such as site-specific availability in stone number and size, and the degree of terrestriality of individuals have not been studied.
The present study is the first to use an intertroop comparative approach to explore ecological constraints on
SH activity in Japanese macaques. On the basis ofextensive research showing that SH may be affected by
nonecological factors such as troop size, age-related differences, and social proximity (Leca et al., 2007a, inpress; Nahallage and Huffman, 2007b), it is reasonable
to assert that SH is not purely a function of stone availability and access to stones. However, variability in theseenvironmental conditions may contribute to account forthe major intertroop differences in SH (cf. Leca et al.,2007a). The goal of this study is to evaluate the influence of stone-related ecological factors on the occurrence
and form of SH.
On the basis of 1) the fact that SH involves particular
objects present in the local environment (i.e., stones), 2)
the assumption that SH is primarily a terrestrial activity, and 3) the finding that Japanese macaques (Macaca
fuscata) are considered semiterrestrial, behaviorally in1
Leca J-B, Gunst N, Huffman MA. Influence of food provisioning
on the transformation phase of the stone handling tradition in Japanese macaques. Submitted for publication.

American Journal of Physical Anthropology—DOI 10.1002/ajpa
187

ECOLOGICAL CONSTRAINTS ON STONE HANDLING
termediate between arboreal long-tailed macaques (M.
fascicularis) and terrestrial pig-tailed macaques (M.
nemestrina) (Chatani, 2003), we tested the two following
hypotheses: 1) the ‘‘stone availability hypothesis,’’ statingthat the number and size of stones readily available in
the local environment provides various SH opportunities,
affecting the occurrence and form of the SH behavior,and 2) the ‘‘terrestriality hypothesis,’’ proposing that thedegree of terrestriality of individuals contributes to
explain differences in the occurrence and form of SH.
The two hypotheses are not mutually exclusive, since
they both relate to the relative opportunity to encounterstones. Failure to accept these hypotheses would imply
that the performance of SH and the motivation to
engage in this activity are better explained by sociodemographic factors and ecological factors that are notstone-related than the number of stones locally available
and the time spent on the ground.
Our specific objective was to test a series of predictions
derived from these hypotheses. On the basis of the‘‘stone availability hypothesis,’’ we tested the following
predictions. First, the availability in stone number
should be positively correlated with the occurrence of SH
namely SH frequency, prevalence, and diffusion rate
(Prediction #1a), the persistence and diversity of SH
namely SH duration, number of phases, pattern turnover, and number of different patterns (Prediction #1b),
the number of stones used during SH bouts (Prediction#1c), and the frequency of SH patterns typically involving a great number of stones, such as gathering or scattering (Prediction #1d). Second, the availability of stones
belonging to different size categories should be associated with the frequency of use applied to the stones ineach size category during SH bouts (Prediction #2). On
the basis of the ‘‘terrestriality hypothesis,’’ we tested thefollowing predictions. First, among all major activities,
SH should be most often performed on the ground (Prediction #3). Second, the occurrence, persistence, and diversity of SH should be positively correlated with thetime spent on the ground at the group level (Prediction#4a) and at the individual level (Prediction #4b).
To address these questions, we compared 10 troops ofJapanese macaques by using a standardized observation
procedure to assess quantitative differences and similarities across troops in the frequency, prevalence, and diffusion rate of SH, as well as the duration, sequence, anddiversity of SH patterns. We used ecological sampling
methods to determine the site-specific availability instone number and size, and the degree of terrestriality
at the activity, group, and individual levels.

METHODS
General study conditions
The species under study was the Japanese macaque(Macaca fuscata). The first two authors, occasionallyassisted by M.A.H. and C.A.D. Nahallage observed a
total of 10 troops at six geographically isolated sites inJapan from August 2003 to February 2005 (Fig. 1). Four
troops lived in large outdoor enclosures in Inuyama,
Aichi Prefecture (Kyoto University Primate ResearchInstitute: Arashiyama 5 Ara.A, Wakasa 5 Wak.A, Takahama 5 Takh., and Japan Monkey Centre Yakushima
macaques 5 JMC), and six troops were free-ranging(Koshima, Miyazaki Prefecture 5 Kosh., Arashiyama,
Kyoto Prefecture 5 Ara.E, Shodoshima, Kagawa Prefecture 5 Sho.A and Sho.B, Takasakiyama, Oita Prefecture

235

Fig. 1. Map of study sites in Japan, with abbreviations ofstudied troops mentioned in parentheses.

5 Tak.B and Tak.C). This research was conducted in accordance with PRI’s Rules and Guidelines for Animal
Health and Welfare.
In Table 1, we present the general study conditions,
including the troop ranging conditions, surfaces of enclosures or feeding sites, troop size, study periods, andnumber of observers. Captive animals were mainly supplied with commercial primate pellets, vegetables orfruits, scattered throughout large areas inside enclosures. Free-ranging troop members gathered regularlyaround feeding sites where they were artificially provisioned with cereal grains by technicians of the Koshima
Field Station, Kyoto University or by the staff of monkey
parks (Kosh., Ara.E, Sho.A, Sho.B, Tak.B, and Tak.C
troops). Free-ranging animals were mainly supplied withcereal grains scattered throughout the feeding site.
Various stones occur at all study sites. A variety ofvertical settings were present in the outdoor enclosures
including climbing structures (e.g., metal or woodenrods, chains, ropes, spinning wheels, etc.), platforms,
roofs, and elevated shelter boxes. Free-ranging troops
could also use many vertical structures surrounding thefeeding sites, either artificial structures such as roofs
and wall ledges, or natural ones such as bushes andtrees. There was no dramatic change in the environmental conditions of each troop over the past decade, including site-specific stone availability (e.g., stones artificiallybrought or removed by humans) and vertical settings.
The detailed distribution of all troop members according to age and sex classes is described elsewhere (Lecaet al., 2007a, in press). Individual identifications werepossible for only some of the study troops (Ara.A, Wak.A,
Takh., Kosh., and Ara.E), and for them the exact age inyears of each individual and their respective matrili-

American Journal of Physical Anthropology—DOI 10.1002/ajpa
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236

1,000
400
1,200
1,200
1,000
1,000
Koshima (Kosh.), FR
Arashiyama E (Ara.E), FR
Shodoshima A (Sho.A), FR
Shodoshima B (Sho.B), FR
Takasakiyama B (Tak.B), FR
Takasakiyama C (Tak.C), FR

neages were known. For the other troops (JMC, Sho.A,
Sho.B, Tak.B, and Tak.C), every sampled subject was labeled according to its age and sex class. Observations
were conducted between 7:00 a.m. and 6:00 p.m. Visibility was excellent. We sampled captive troop members
from observation platforms overhanging the enclosures.
Free-ranging troop members could be approached andsampled within 3–5 m.

In parentheses: abbreviation of troop name; CP: captive troop; FR: free-ranging troop; TS: troop size (number of troop members aged at least one year); TOT: total observation
time in hours; FT: focal time (total duration in hours of focal sessions); NS: number of scan sessions; SH Bt (F): number of SH bouts collected during focal (F) sessions (n.a.: notavailable); SH Bt (CAL): number of SH bouts collected during complete ad libitum (CAL) sessions; SH Nt (IAL): number of SH notes collected during incomplete ad libitum (IAL)
sessions.
a
Occasionally assisted by M.A.H. and Mrs. Charmalie Nahallage. The first two authors were the main observers.

7
579
27
67
75
391
14
35
10
26
59
182
215.4
160.6
16.8
1.3
0.0
0.0
88
141
450
350
438
676
JBL, NG
JBL, MAH,a CNa
JBL, NG, CN
JBL, NG, CN
JBL, NG
JBL, NG

339.7
431.3
77.6
51.5
22.8
73.8

252
1,010
66
42
58
72

9
317
30
4
n.a.
n.a.

28
224
1,252
91
1
62
28
99
140
174.5
353.6
54.4
18
19
46
102
850
500
960
4,000
Arashiyama A (Ara.A), CP
Wakasa A (Wak.A), CP
Takahama (Takh.), CPJapan Monkey Centre (JMC), CP

Sep–Dec 2003
Aug–Nov 2003
Sep–Dec 2003
Aug–Dec 2003,
Mar–Apr 2004
Jan–Feb 2004
May–Aug 2004
Feb 2005
Feb 2005
Dec 2003 – Jan 2004
Dec 2003 – Jan 2004

NG
NG
JBL
JBL, NG

179.9
224.6
449.2
99.1

644
809
1,593
275

14
59
309
22

SH Bt
(IAL)
FT
TOT
TS
Observers
Study period
Surface of
enclosure (CP)or feedingsite (FR) in m2
Troop nameand ranging
conditions

TABLE 1. Inter-troop comparison of study conditions and total data sets

NS

SH Bt
(F)

SH Bt
(CAL)

J.-B. LECA ET AL.

Data collection
We used the same observation procedure for all troops,
except Tak.B and Tak.C (see below for details). The twomain observational methods used were continuous focalanimal sampling and instantaneous group scan sampling(Altmann, 1974). Behavioral data collection was supplemented with ad libitum sampling when necessary (Altmann, 1974). We also collected data about a particularenvironmental feature which we proposed could have an
influence on the occurrence and form of SH namely stone
availability.
Focal sampling. We video-recorded every focal session
with Sony digital video cameras (DCR-TRV22 and DCRTRV33). Whenever possible, the focal individual was
filmed head on and about one-meter square in-frame. We
focused on all the behaviors and interactions of the focal
individual. Since the field observation conditions did notallow us to use a totally random focal sampling method,
we selected the focal individual using a semirandom procedure. The daily observation period was divided into
1-h blocks. We selected the focal individual, independentlyof its activity, in an ordered list of temporarily undersampled individuals or members of each age and sex class,when focal subjects were not individually identified.
We recorded the starting time of each focal session.
Following protocol used in previous surveys carried out
at Takasakiyama and Arashiyama (see Huffman, 1996),
the typical duration of a focal session was 15 min. If the
focal individual performed SH activity during the last
2 min of this period of time, the observation was extended for 5 min and ended thereafter unless SH wasstill in progress.
Scan and ad libitum samplings. Before and after
each focal session, the troop was scanned to assess terrestriality at the group level and for evidence of any SH
activity. All individuals located above 1-m height werelabeled ‘‘off the ground,’’ whereas others were labeled‘‘on the ground.’’ For each scan sampled stone handler,
we recorded individual identity or age and sex classes,
and whenever possible the SH patterns observed (seeLeca et al., 2007a for a comprehensive list of SH patterns). The observer recorded scans on data sheets, visually scanning across the enclosure for captive troops, orby walking from one side of the free-ranging troop to theother, in a set direction, so that each individual was
sampled only once in a given scan session.
To supplement each troop’s data set, observers devoted
an average of 38.8% 6 31.8% of total observation time tothe collection of ad libitum data on individuals performing SH. Whenever possible, ad libitum sessions werevideo-recorded or otherwise, collected on notepad. For
Tak.B and Tak.C troops, we did not collect focal sessions,but only video-recorded ad libitum sessions during theperiods after feeding, when SH is most likely to occur(Huffman, 1996). In some cases, we were able to record
complete ad libitum sessions. The sampled individual

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ECOLOGICAL CONSTRAINTS ON STONE HANDLING
was filmed through the entire sequence of SH, from start(a few minutes after provisioning time, immediately after
it left the feeding site and picked up or touched stones) tofinish (5 min after the last stone was discarded). When aSH episode was recorded on notepad or when thesampled individual was not filmed through the entire
sequence of SH, we referred to the ad libitum session as
incomplete.
Site-specific availability in stone number and size.
We assessed availability of stones (estimate abundance)
at each site by using the quadrat method (Krebs, 1999).
A total of ten 1-m2 quadrats were alternately drawn oneach side of a 10-m transect. In each quadrat, wecounted the number of stones bigger than 2 mm 3 2 mm
3 2 mm. Likewise, we drew three 10-m transects at andaround the feeding site of each study site. We estimatedthe site-specific availability in stone number by calculating the average number of stones per meter square,
based on a total of thirty 1-m2 quadrats surveyed. In
these quadrats, we also randomly sampled the type ofstones present (e.g., quartzite, granite, schist, sandstone,
pumice, pebble and concrete block).
We estimated the site-specific availability in stone size
from standardized video quadrats, defined as still images
extracted from video-recorded focal sessions or, when notavailable, video records of SH bouts. In each video quadrat,
the only filmed individual (always a juvenile) was locatedat the center of the image in a sitting posture, zoomed on
about one-meter square in-frame, with no object or background blocking the view of the ground. We used particular parts of the sampled subject’s hand (finger width, palmsurface, and hand total length) as standards to estimate
the size of stones present around it. We ascribed the stones
to four size categories: S1 (2–10 mm), S2 (11–50 mm), S3(50–100 mm), and S4 (more than 100 mm).
To test the reliability of the estimation of stone size
from video records, we used a sample of stones collected in
the field (N 5 86, 19 S1 stones, 38 S2 stones, 24 S3 stones,
and 5 S4 stones, respectively) and compared the estimatedsizes with the actual sizes of the stones obtained by using
a caliper. We found good correspondences between sizes
estimated from video records and actual sizes: 100% for
S1 and S4 stones, 95% for S2 stones, and 92% for S3stones. In each video quadrat, we checked for the presenceof at least one S2, S3, and S4 stones, and at least a dozen
of S1 stones. We added up the frequency of presence ofstones for each size category out of 100 randomly chosen
video quadrats per study site (QdS1, QdS2, QdS3, and QdS4,
respectively). We ascribed the same values of site-specificavailability in stone number and size to the free-ranging
troops living at the same site.

Data analysis
On the basis of video-records, J.-B.L. transcribed eachfocal session onto a data sheet and measured the duration to the second of all activities (feeding, foraging, locomoting, resting, socializing, SH, nonstone object exploring, and other), as well as each SH pattern, and the timespent on and off the ground. Data were then enteredinto a computer for processing.
We distinguished two types of SH records: SH bouts
collected from focal sessions or complete ad libitumvideo-recorded sessions, and SH notes collected fromscan sessions or incomplete ad libitum sessions. We
defined a SH bout (Huffman, 1996) as the display of SH
activity with possible pauses of no longer than 120 s. If

TABLE 2. Definition of different variables representing
SH occurrence and form
Variable
SH occurrence
Frequencya
Prevalence
Diffusion rate

SH form
Persistenceb
Repetitivityb
Pattern turnoverb
Pattern diversity
per boutb
Pattern inclusive
diversityc
Pattern frequency

Definition
Average number of SH bouts per focal
hour
Mean percentage of stone handlers
among individuals sampled in scansessions
Total percentage of stone handlers per
troop (either exactly calculated from
SH bouts and notes in troops withindividually identified members, or
estimated by dividing the maximum
number of stone handlers by theaverage number of unidentified troop
members sampled during postprovisioning scans: cf., Huffman, 1996;
Leca et al., in press)
Mean duration of SH bouts in seconds
Average number of SH phases per SH
bout
Average number of changes in thesequence of SH patterns performed per
SH bout
Average number of different SH patterns
performed per SH boutTotal number of different SH patterns
observed in each troop or individual
For each SH pattern, average number ofoccurrence in 10 min of SH phasesaWere derived from all focal sessions and all troop members
were considered.
b
Were derived from all SH bouts available and only verified
stone handlers were considered.
c
Were derived from all SH bouts and SH notes available.

the individual resumed SH within 120 s after pausing,then the two SH episodes were defined as two SH phases
within a single SH bout. If SH was resumed more than
120 s after pausing, this would mark the start of a new
SH bout. To assess the occurrence of SH at the grouplevel, we used three variables namely SH frequency,
prevalence, and diffusion rate. To describe the form of
SH at the group level, we used six variables namely SH
persistence, repetitivity, pattern turnover, pattern diversity per bout, pattern inclusive diversity, and pattern frequency (Table 2).
Number and size of stones handled. To test possible
troop-specific preferences in the number of stones usedduring SH bouts, we calculated for each troop the frequency of SH bouts in which one or two stones werehandled (Nb1/2), from 3 to 5 (Nb3/5), 6 to 10 (Nb6/10), andmore than 10 stones were handled (Nb110). These four
categories are mutually exclusive. Regarding the size ofstones, we also calculated the number of SH bouts during which one S1, S2, S3, or S4 stone was handled atleast once (NbS1, NbS2, NbS3, or NbS4, respectively andnot mutually exclusive).
Data sets and statistical analysis. In Table 1, we
present the total data sets for each studied troop. We
defined the total troop observation time as the total timespent observing each troop, including focal time, scantime, and time spent collecting ad libitum data. The cumulative time of multiple observers, when present, wascalculated for total troop observation time. For the anal-

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J.-B. LECA ET AL.

TABLE 3. Results of Spearman rank-order correlation tests (one-tailed) at the group level between site-specific availability
in stone number (average number of stones/m2) or troop-specific terrestriality (mean percentage of time spent on the ground drawn
from focal sessions and mean percentage of troop members on the ground drawn from scan sessions) and different variables
representing SH general occurrence and form in each corresponding troop
Troop-specific terrestriality
Site-specific availability instone number
Variables
SH occurrence
Frequency
Prevalence
Diffusion rate
SH form
Persistence
Repetitivity
Pattern turnoverPattern diversity per bout
Pattern inclusive diversity

Mean percentage of time on
the ground

Mean percentage of troop
members on the ground

N

rs

P

N

rs

P

N

rs

P

7
10
10

0.429
0.421
0.000

0.169
0.113
0.500

7
7
7

0.321
0.285
20.321

0.241
0.213
0.241

7
10
10

0.321
0.285
20.297

0.241
0.213
0.202

10
10
10
10
10

0.396
0.551
0.476
0.506
0.291

0.128
0.056
0.082
0.068
0.207

7
7
7
7
7

0.429
0.321
0.500
0.500
20.396

0.169
0.241
0.127
0.127
0.190

10
10
10
10
10

0.358
0.467
0.553
0.532
0.079

0.155
0.087
0.050
0.064
0.414

yses about the mean percentage of time spent on the
ground at the group level, we drew on all focal sessions.
To assess terrestriality at the individual level, only individuals with more than 120 min of focal data were considered. The Sho.B, Tak.B, and Tak.C troops were
excluded from these analyses because focal data wereinsufficient or not available. Among the other troops,
focal sessions lasting less than 15 min (i.e., when the
focal subject was lost) were excluded from these analyses. We drew on all SH bouts available for analyses on
the number and size of the stones handled. For analyses
about the mean percentage of troop members on the
ground, we drew on scan sessions. For captive troops, weonly used scan sessions in which at least 80% of troop
members were sampled. For free-ranging troops, we only
considered scans sessions taking into account at least
60% of troop members. Individuals aged less than 1 year
were not taken into account in the analyses.
We verified interobserver reliability using the kappa
coefficient of Cohen (1960). On the basis of individual
identities, activities, and interactions, we found k 5 0.92
between the first two authors. We tested possible correlations between site-specific stone availability or terrestriality at the group and individual levels, and the different variables representing the occurrence and form ofSH, by using a series of Spearman rank-order correlation tests (one-tailed, on the basis of directional hypotheses). To evaluate the relationship between site-specificavailability in stone sizes and the corresponding troop
preference in stone sizes, we used Kendall rank-ordercorrelation tests (two-tailed). To assess troop preferencesin the number of stones used during SH bouts, we used
v2 goodness-of-fit tests. To test the association between
troop-specific preference in the number of stones handled
and site-specific stone availability, we used a v2 test of
independence from a contingency table. For post hoc examination of v2 tests, we calculated the adjusted standardized residuals, and considered statistically significant
those values of z-scores that were |1.96|. Statisticalanalyses were performed using the SPSS 12.0 analyticalprogram. Significance levels were set at a 5 0.05.

RESULTS
Stone availability hypothesis
Stones were available at all sites, but stone availability was highly variable according to the study site (aver-

age number of stones/m2: Kosh. 5 3; Takh. 5 81; JMC 5
92; Sho.A/Sho.B 5 192; Ara.A 5 236; Wak.A 5 410;
Tak.B/Tak.C 5 620; and Ara.E 5 855).
Prediction #1a: Number of stones and SH occurrence. We found no statistically significant correlation
between site-specific stone availability and the different
variables representing the occurrence of SH in each corresponding troop namely SH frequency, prevalence, diffusion rate (Table 3).
Prediction #1b: Number of stones and SH persistence and diversity. We found no statistically significant
correlation between site-specific stone availability andthe different variables representing the general form of
SH in each corresponding troop namely SH persistence,
repetitivity, pattern turnover, and pattern diversity perbout, and pattern inclusive diversity (Table 3). However,it should be noted that in a few instances, the P values
were very close to 0.05 (e.g., repetitivity: P 5 0.056 andpattern diversity per bout: P 5 0.068).
Prediction #1c: Availability in stone number andnumber of stones handled. We found that each of theseven troops with sufficient data (more than 30 SH
bouts) presented a strongly significant preference in thenumber of stones used during SH bouts (v2 goodness-offit tests, df 5 3, Wak.A: Nb1/2 5 89, Nb3/5 5 24, Nb6/10 55, Nb110 5 3, v2 5 161.02, P \ 0.001; Takh.: Nb1/2 5221, Nb3/5 5 58, Nb6/10 5 35, Nb110 5 23, v2 5 303.46,
P \ 0.001; JMC: Nb1/2 5 101, Nb3/5 5 11, Nb6/10 5 5,Nb110 5 4, v2 5 221.58, P \ 0.001; Ara.E: Nb1/2 5 53,
Nb3/5 5 32, Nb6/10 5 59, Nb110 5 208, v2 5 222.75, P \0.001; Sho.A: Nb1/2 5 7, Nb3/5 5 5, Nb6/10 5 2, Nb110 5
26, v2 5 35.40, P \ 0.001; Tak.B: Nb1/2 5 3, Nb3/5 5 1,
Nb6/10 5 9, Nb110 5 46, v2 5 90.63, P \ 0.001, Tak.C:
Nb1/2 5 13, Nb3/5 5 13, Nb6/10 5 18, Nb110 5 138, v2 5251.10, P \ 0.001). Post hoc examination of residuals
showed that members of the captive troops (Wak.A,
Takh., and JMC) were more likely to use fewer (one ortwo) stones over more than two stones, whereas members of the free-ranging troops (Ara.E, Sho.A, Tak.B, andTak.C) were more likely to use a great number of stones(more than 10).
To test whether such troop preferences in the numberof stones handled may also be related to stone availability, we conducted a v2 test of independence based on acontingency table representing the frequency of SH

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ECOLOGICAL CONSTRAINTS ON STONE HANDLING

bouts involved one or two stones and fewer involved
more than 10 stones, whereas when stone availability
was high, significantly more SH bouts involved morethan 10 stones and fewer involved one or two stones.
In total, these four cells accounted for 96.4% of thev2 value.

bouts involving different number of stones in two conditions of stone availability namely low (less than 250
stones/m2, three captive and three free-ranging troops)
and high (at least 250 stones/m2, one captive and three
free-ranging troops) (Table 4). We found a significant
association between stone availability and the number ofstones used during SH bouts (N 5 1,280 SH bouts, Pearson v2 5 330.44, df 5 3, P \ 0.001). Post hoc examination of adjusted standardized residuals showed thatwhen stone availability was low, significantly more SH

Prediction #1d: Number of stones and frequency of
SH patterns involving numerous stones. This correlation between the number of stones readily available forthe monkeys and the number of stones actually used bythem during SH bouts led us to test a possible association between stone availability and the frequency ofoccurrence of particular SH patterns. Among the mostrepresentative SH patterns (recorded at least once infive of the 10 study troops), we tested the correlations
between the pattern frequencies in each troop and thesite-specific stone availability (Table 5). The SH patterns
whose frequency presented a significant positive correlation with stone availability were patterns involving agreat number of stones, either collected and manipulated
simultaneously as a pile (GA, GH, PU, SC) or integrated
one by one as part of a locomotion sequence (GW), or bysets of two stones successively handled then discarded(RT). All other SH patterns generally involved one or
few stones and were not positively correlated with thesite-specific stone availability.

TABLE 4. Contingency table representing the frequency of SH
bouts involving different number of stones (one or two, three tofive, six to ten, and more than ten stones, respectively) in two
conditions of availability in stone number, namely low (less than
250 stones/m2) and high (at least 250 stones/m2)
Number of SH bouts involving
different number of stones

Availability instone number
Low (\250 stones/m2)
High ([250 stones/m2)

Nb1/2

Nb3/5

Nb6/10Nb110

370(8.9)*
158(28.0)*

85
(1.9)
70
(21.8)

50(21.6)
91(1.4)

61(29.9)*
395(8.8)*

Adjusted standardized residuals are mentioned in parentheses
and asterisks represent statistically significant values.

TABLE 5. Relationships between pattern frequencies of the 25 most representative SH patternsa
and site-specific availability in stone numberb
Category name (code)
Investigative activities
Bite (B)
Hold (H)
Lick (L)Move inside mouth (MIM)
Pick (P)Put in mouth (PIM)
Sniff (SN)Locomotion activities
Carry (CA)Carry in mouth (CIM)
Grasp walk (GW)
Move and push/pull (MP)Toss walk (TW)
Collection or gathering activities
Cuddle (CD)
Gather (GA)
Grasp with hands (GH)Definition

rs

P

Bite a stone
Pick up a stone in one’s hand and hold on to it, away from the body
Lick a stone
Make a stone move inside one’s mouth with tongue or hands
Pick up a stone
Put a stone in one’s mouth and keep it sometime
Sniff a stone

20.6770.085
20.2040.039
0.069
20.12520.2320.016*
0.407
0.286
0.457
0.425
0.365
0.260

Carry a stone cuddled in hand from one place to another
Carry a stone in mouth while locomoting
Walk with one or more stones in the palm of one or both hands
Push/pull a stone with one or both hands while walking forward/
backward
Toss a stone ahead (repeatedly) and pick it up while walking

20.39020.2410.628
20.5190.132
0.251
0.026*
0.062

0.099

0.393

20.189
0.585
0.665

0.300
0.038*
0.018*

0.707

0.011*

20.08620.052

0.407
0.443

0.122
0.044
20.409
0.673
0.616

0.368
0.452
0.121
0.017*
0.029*

20.04320.364

0.453
0.151

Take hold of, grab or cradle a stone against the chest
Gather stones into a pile in front of oneself
Clutch a stone or a pile of stones gathered and placed in front of
oneself
Pick up (PU)
Pick up a stone and place it into one’s hand
Percussive or rubbing sound producing activities
Clack (CL)Clack stones together (both hands moving in a clapping gesture)
Combine with object (COO)
Combine (rub or strike) a stone with an object different from a stone(piece of wood, metal, etc.)
Flint (FL)
Strike a stone against another held stationary
Pound on surface (POS)
Pound a stone on a substrate
Rub/roll on surface (ROS)
Rub or roll a stone on a substrate
Rub stones together (RT)
Rub stones together
Scatter (SC)Scatter stones about, on a substrate, in front of oneself
Other complex manipulative activities
Roll in hands (RIH)
Roll a stone in one’s hands
Rub with hands (RWH)
Hold a stone in one hand and rub it with the other (like potatowashing)* P \ 0.05.
aDefined and categorized according to general activity patterns: after Leca et al., 2007a; Nahallage and Huffman, 2007.
b
Spearman rank-order correlation tests, one-tailed, N 5 10.

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J.-B. LECA ET AL.

TABLE 6. Quantification of the size of stones handled andavailable for each troop
Stone size
S1

S2

S3

S4

Troop

Nb

Qd

Nb

Qd

Nb

Qd

Nb

Qd

Ara.A
Wak.A
Takh.
JMC
Kosh.
Ara.E
Sho.A
Sho.B
Tak.B
Tak.C
Total

1
5
67
8
0
83
25
5
31
79
304

42
64
67
71
21
73
67
67
79
79
630

10
110
218
71
11
341
34
27
45
152
1019

51
50
44
57
15
42
58
58
59
59
493

7
29
114
47
9
112
6
17
24
73
438

22
73
30
36
5
22
40
40
34
34
336

0
7
15
20
4
7
2
0
9
16
80

13
65
11
22
4
14
15
15
12
12
183

Nb: number of SH bouts during which a stone of a particularsize was handled at least once; Qd: percentage of quadrats containing at least a dozen of S1 stones, at least one S2, S3, and S4
stones (see Methods for details).

Prediction #2: Availability in stone size and size ofstones handled. Table 6 shows that stones belonging to
the four size categories were present at all sites andhandled by most troops. Although these frequencies varied substantially across troops, we found no significant
correlation between the site-specific availability in stone
size and the corresponding troop preference in stone
sizes, represented by the number of SH bouts during
which S1, S2, S3, or S4 stones were handled at least
once (Kendall rank-order correlation tests, N 5 4, Ara.A:
T 5 0.667, P 5 0.174; Wak.A: T 5 0.000, P 5 1.000;
Takh.: T 5 0.333, P 5 0.497; JMC: T 5 0.000, P 5
1.000; Kosh.: T 5 0.000, P 51.000; Ara.E: T 5 0.333, P 5
0.497; Sho.A: T 5 0.667, P 5 0.174; Sho.B: T 5 0.333,
P 5 0.497; Tak.B: T 5 0.667, P 5 0.174; Tak.C: T 5
0.667, P 5 0.174).
Several types of stones such as quartzite, granite, andschist rocks were sampled at the different natural sites(Arashiyama, Shodoshima, and Takasakiyama), with the
exception of Koshima island where only sandstones andpumices were sampled. In addition to quartzite andschist rocks, a variety of pebbles and pieces of concrete
blocks, artificially brought by humans, were sampled in
the enclosures of the captive troops (PRI and JMC).
Although the size and type of stones varied, we foundthat loose stones suitable for SH were available at all
the study sites.

Terrestriality hypothesis
Prediction #3: SH as the activity most performed on
the ground. On the basis of the focal sessions collected
in seven troops, we calculated the percentage of timespent on and off the ground by the monkeys while
involved in eight major types of activity (Fig. 2). Overall,
we found that SH was the activity showing the greatest
difference in terms of terrestriality, with 89.7% of thetime devoted to SH being spent on the ground. Thisvalue came to 100.0% in four troops (Ara.A, JMC, Kosh.,and Sho.A), 94.2% in Ara.E, and 83.6% in Takh. In the
Wak.A troop, the relatively low terrestriality in SH(55.7%) could be attributed to the unique presence of alarge central platform in a relatively small enclosure(see Table 1). Unlike narrow bars and branches or sloping roofs encountered at other sites, this flat surface
may be regarded as a ‘‘ground above the ground,’’ where

the monkeys spent a comparatively great percentage oftime resting and socializing (Fig. 2), and where they
could readily find discarded stones to handle, even performing locomotion SH patterns typically observed on
the ground, such as GW, MP, and TW (Gunst, personalobservation).
The other activity close to SH in terms of terrestriality
was object exploring, with an overall 88.2% of time spenton the ground. When considering the six other major
activities together (feeding, foraging, locomoting, resting,socializing, and other), the overall percentage of timespent on the ground was 67.8%. The discrepancy between SH and most other activities found in the terrestriality profile led us to further explore a possible link
between Japanese macaque terrestriality and SH activity.
Prediction #4a: SH and time spent on the groundat the group level. Terrestriality was highly variableaccording to the study troop, either defined as the mean
percentage of time spent on the ground for all troop
members sampled during focal sessions (Wak.A 5 38.3%,
Ara.A 5 44.8%, Takh. 5 72.7%, JMC 5 73.3%, Ara.E 5
76.7%, Kosh. 5 77.9%, and Sho.A 5 92.4%) or as themean percentage of troop members on the ground duringscan sessions (Wak.A 5 35.0%, Ara.A 5 43.2%, Sho.A 5
69.5%, JMC 5 69.9%, Sho.B 5 70.9%, Takh. 5 75.6%,
Kosh. 5 78.4%, Ara.E 5 78.8%, Tak.C 5 85.4%, and
Tak.B 5 88.0%). However, in both cases, we found nostatistically significant correlation between troop-specificterrestriality and the different variables representing
the occurrence and general form of SH in each corresponding troop (Table 3). It should be noted that in a
few instances, the P values related to the mean percentage of troop members on the ground were equal or very
close to 0.05 (e.g., pattern turnover: P 5 0.050 and pattern diversity per bout: P 5 0.064). The general tendency for captive troops to spend less time on the groundthan free-ranging troops may be due to the abundance of
climbing structures in the enclosures, such as bars, platforms, and shelter boxes.
Prediction #4b: SH and time spent on the ground at
the individual level. In Wak.A, Takh., and Ara.E(where troop members were individually identified andSH relatively frequent), we found no significant positive
correlation between the mean percentage of time spenton the ground by the different troop members and their
SH frequency (Spearman rank-order correlation tests,
Wak.A: N 5 19, rs 5 0.401, P 5 0.050; Takh.: N 5 45,
rs 5 20.308, P 5 0.020; Ara.E: N 5 17, rs 5 0.064, P 5
0.404; all three troops: N 5 81, rs 5 0.182, P 5 0.051),
pattern diversity per bout (Wak.A: N 5 17, rs 5 20.542,
P 5 0.013; Takh.: N 5 39, rs 5 20.047, P 5 0.389;
Ara.E: N 5 17, rs 5 0.182, P 5 0.243; all three troops:
N 5 73, rs 5 0.057, P 5 0.316), and pattern inclusive diversity (Wak.A: N 5 17, rs 5 20.332, P 5 0.097; Takh.:
N 5 39, rs 5 20.237, P 5 0.073; Ara.E: N 5 17, rs 5
0.187, P 5 0.237; all three troops: N 5 73, rs 5 20.100,
P 5 0.199). Interestingly, significant negative correlations were found with SH frequency in Takh. and SH
pattern diversity per bout in Wak.A.

DISCUSSION
In this study, we used an intertroop comparative
approach to explore ecological constraints on SH activity
in Japanese macaques, and tested a series of predictions
generated from two hypotheses related to stone avail-

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ECOLOGICAL CONSTRAINTS ON STONE HANDLING

241

Fig. 2. Terrestriality profiles according to activity for seven separate troops and for the seven troops pooled together. The Y-axis
represents complementary and mutually exclusive percentages of time namely the percentage of time spent on the ground (black
areas) and the percentage on time spent off the ground (hatched areas). Expl.: Object exploring; Feed.: feeding; Forag.: foraging;
Loc.: locomoting; Rest.: resting; Soc.: socializing; SH: stone handling.

ability and terrestriality. The hypotheses, predictions,and results of the tests are summarized in Table 7. First,
we found that the number of stones readily available
was not associated with the major intergroup differencesin the occurrence of SH (namely SH frequency, prevalence, and rate of diffusion), and the general form of SH(namely duration of SH bouts and diversity of SH patterns). Moreover, the size of stones handled was not
associated with the size of stones available. Because
three of its major constituent predictions were rejected,
we failed to accept the ‘‘stone availability hypothesis.’’Only two minor constituent predictions regarding therelationship between stone availability and some specificaspects of SH form were verified. When more stones
were available in the local environment, the monkeys
used more stones during SH activity and performed
more SH patterns typically involving a great number ofstones, such as those characteristic of a collection orgathering activity. Although the latter findings suggestthat the number of stones available may influence thenumber of stones handled and the way to manipulatethem, this was clearly insufficient to accept the ‘‘stone

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J.-B. LECA ET AL.
TABLE 7. Hypotheses, predictions, and statistical tests results related to the ecological constraints on SH
Hypothesis

Prediction‘‘Stone availability hypothesis’’:The number and size ofstones readily available in
the local environment
provides various SH
opportunities, affecting theoccurrence and form of the
SH behavior#1. Availability in stone number is positively correlated with:a. The occurrence of SH (frequency, prevalence, and diffusion rate)b. The persistence and diversity of SH (duration, number of phases, pattern
turnover, and number of different patterns)
c. The number of stones used during SH bouts
d. The frequency of SH patterns typically involving a great number ofstones (e.g., gathering, scattering)#2. The size of stones used during SH bouts is associated with the size of stones
available#3. Among all major activities, SH is the most performed on the ground#4. The occurrence, persistence, and diversity of SH are positively correlatedwith the time spent on the ground:a. At the group levelb. At the individual level‘‘Terrestriality hypothesis’’:The degree of terrestriality of
individuals contributes to
explain differences in theoccurrence and form of SH

availability hypothesis.’’ Second, we provided the firstquantitative evidence that SH is almost exclusively aterrestrial activity. However, we showed that the relative
amount of time spent on the ground by the macaques
was not associated with this vertical bias at the groupand individual levels. Therefore, we failed to accept the‘‘terrestriality hypothesis.’’We do not intend to infer causal relationships frommeasures of association between variables, mainly basedon correlation and crosstabulation analyses. However,the present study undoubtedly shows that the relative
stone availability and the degree of terrestriality areprobably not key factors for SH innovation, subsequentdiffusion, and daily occurrence in Japanese macaques.
This does not imply that any dramatic local change in
the availability of stones or vertical structures would notaffect the chance of SH to occur in a particular troop. We
believe that there are favorable environmental circumstances under which the innovation and initial diffusionof SH could be facilitated. Provisioned free-ranging
troops faced atypical environmental conditions, such as
the concomitant presence of novel foods (hard-coated cereal grains) and a great number of stones, sometimes
artificially brought by humans as hard-packed groundfor the open space of feeding areas. Wild monkeys spend
more time foraging for natural foods in the forest, whereclimbing substrates are widespread and a substantial
proportion of stones is covered by the vegetation. The
former have more opportunities to encounter stones thanthe latter.
Failure to accept the stone availability and terrestriality hypotheses suggests that the performance of SH andthe motivation to engage in this activity are both morediverse and more complex than the direct links to timespent on the ground or the number of stones readily
available in the local environment. First, SH has notbeen reported at other sites where stones occur and several provisioned troops (e.g., Katsuyama: N. Nakamichi,
pers. comm.) and all nonprovisioned troops of Japanesemacaques (e.g., Kinkazan: Y. Shimooka, pers. comm.;
Yakushima: G. Hanya, pers. comm.) have long beenstudied.
Second, once a particular stone or set of stones are
involved in a SH episode, they seem to become valuableobjects for the handler who pick them up and carrythem to different places rather than leave them behind,and appear to trigger great interest from others who try
to snatch them away from the handler as if they were
the only stones available (Huffman and Quiatt, 1986).
When subordinate individuals are supplanted from

Not verified
Not verified
Verified
VerifiedNot verified
VerifiedNot verified
Not verified

stones, they often wait nearby until the dominant leaves
the stones behind, and they return to handle the verysame stones again (Huffman, personal observation).
Occasionally, human observers or tourists were threatened or even charged by a monkey while trying to takethe stones it had just discarded after handling them
(Leca, personal observation). These reports suggest theexistence of a rudimentary form of ‘‘possession’’ in monkeys, already reported in chimpanzees at Bossou,
Guinea, where some individuals seem to have their favorite stone tool (Matsuzawa, 1999).
Other environmental factors, such as the frequency offood provisioning, the size of the feeding site, and seasonality may influence to some extent the daily occurrence of SH, and therefore the overall opportunity forthe behavior to diffuse within a troop through observational learning (Huffman and Hirata, 2003; Leca et al.,submitted). Food provisioning has been performed for
decades by Japanese primatologists and monkey park
managers throughout Japan to help compensate for theunpredictable appearances of Japanese macaque groups
and to accelerate the process of habituation. Nevertheless, food provisioning undoubtedly affects the animals’
activity budget (Huffman, 1991; Huffman and Hirata,
2003; Leca et al., submitted). Attracting monkeys to theopen space of feeding areas, where many stones occur,
increases considerably their opportunities to encounter
these objects. Feeding monkeys gives them ‘‘free’’ timesince they can devote less time to foraging. Therefore,food provisioning is likely to enhance the chances for SH
to emerge. At the other extreme, after food provisioning
was stopped in the Japanese macaque troop living at
Takagoyama, SH gradually disappeared (Fujita, pers.
comm. cited in Huffman, 1984). By affecting the timespent to manipulate objects, food availability and especially food provisioning are environmental determinantsof tool use appearance and transmission in groups of animals (Beck, 1980).
A recent longitudinal study on a captive troop of Japanese macaques showed a seasonal variation in the occurrence of SH, with a decrease in SH frequency recorded
in winter (Nahallage and Huffman, submitted2). The visibility and availability of stones were rarely reduced during winter as snowfall was limited to a few days, but insome years and at some locations, snow may affect SH

2Nahallage CAD, Huffman MA. Proximate factors associated withthe occurrence of stone handling behavior in a captive troop of Japanese macaques. Submitted for publication.

American Journal of Physical Anthropology—DOI 10.1002/ajpa
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Test result

ECOLOGICAL CONSTRAINTS ON STONE HANDLING
to some extent. Instead, temperature was the key factor
correlated with the decrease in SH activity in winterand its increase in summer. It could also be argued thatfood scarcity associated with winter may affect the monkeys’ activity budget, forcing them to spend more time
foraging in the forest, which in turn may impact on theoccurrence of SH. Although the troops living at Shodoshima and Takasakiyama were solely studied during
winter months (see Table 1), seasonal conditions are not
likely to affect our findings for several reasons. No snowfall occurred during our observations of these troops(Leca, personal observation). Because of frequent foodprovisioning at these sites, the monkeys spent most ofeach day around the feeding sites, where stones arereadily available (Leca et al., submitted). Finally, despite
the cold weather, Sho.A, Sho.B, Tak.B, and Tak.C had
the highest SH frequencies among the studied troops(Leca et al., in press).
When considered alone, terrestriality or stone availability often prove to be insufficient to account for all
interpopulational differences in primate stone-tool use.
Beck (1980) emphasized the absence of simple correlation between terrestriality and tool use behavior in primates. A closer examination of the ecological conditionsof seed-cracking in the brown capuchins of the Caatinga
dry forest revealed that terrestriality may not be sufficient to explain this stone-tool innovation. Moura andLee (2004) suggested tool use is key to survive in impoverished habitats. Lee and Moura (2005) provided more
support to the link between periods of food scarcity
and the emergence of tool use behavior as an efficient
foraging strategy that contributes to meet energy
requirement.
Intersite variation in the instrumental use of stones inchimpanzees is obviously culturally based and beyond
ecological determinism (Boesch et al., 1994; McGrew etal., 1997; Whiten et al., 1999). If chimpanzees at Lopé,Gabon do not use stones to crack open nuts, despite theavailability and suitability of both stones and nuts, it isprobably because they lack the appropriate technicalknowledge to exploit this resource (McGrew et al., 1997).
To further explore the effect of the physical characteristics of stones and the sensory consequences of stone
manipulation on the form of SH, additional analyses areunderway to test a possible preference in the size, shape,
weight, and chemical properties of stones selected by themonkeys to display SH patterns associated with particular sensory effects (e.g., auditory, olfactive, or gustative
effects). Additional analyses should enable us to determine if our result on the substantial troop-specific variation in the size of stones handled may be related to thetype of SH patterns preferentially performed by a particular troop (see Leca et al., 2007a, for intertroop variationin SH patterns).
Our findings urge the use of a multivariate approach
when addressing the question of the evolution of behavioral traditions in nonhuman primates. In addition to ecological constraints, social factors (e.g., van Schaik,
2003; Leca et al., 2007b), and demographic influences(Lefebvre, 1995; Leca et al., in press) should be jointly
considered to identify the sources of behavioral diversity
in general, and variation in stone-tool use in particular.
Like all stone-related behaviors in nonhuman primates,
further investigation of the various factors constraining
the occurrence of SH may provide new insights into theemergence of hominid material culture through stonetool technology (cf. Foley and Lahr, 2003).

243

ACKNOWLEDGMENTS
This study would not have been possible without thecontribution of many people who helped in many ways
during the course of this research. We wish to thank theresearchers, students, staff, and friends who provided
permission to work, support, assistance, and valuable information about the history, demography, and environmental conditions of the troops at the different study
sites and useful information from other field sites. We
are grateful to the following people: G. Hanya, A. Kato,
H. Ohsawa, Y. Shimooka, and H. Takemoto (Primate
Research Institute), M. Nakamura and Y. Takenoshita(Japan Monkey Centre), F. Kanchi, A. Mori, and T. Suzumura (Koshima Field Station), K. Watanabe (Koshima
Field Station and Wild Monkey Park, Shodoshima), S.
Asaba, S. Hanamura, T. Kawashima, S. Kobatake, and
M. Shimada (Iwatayama Monkey Park, Arashiyama),and H. Kurita (Takasakiyama Natural Zoo). We are
deeply indebted to the Enomoto family for generously
providing logistic assistance at Arashiyama. For occasional assistance in data collection, we thank K.J. Petrzelkova (Arashiyama). We are grateful to C.A.D. Nahallage for assistance in data collection (Arashiyama andShodoshima), and fruitful discussion about SH. We also
thank M. Gerald and three anonymous reviewers for
insightful comments on a previous version of the manuscript.

LITERATURE CITED
Altmann J. 1974. Observational study of behaviour: sampling
methods. Behaviour 49:227–267.
Beck BB. 1980. Animal tool behavior. New York: Garland STPM
Press.
Boesch C, Boesch H. 1984. Possible causes of sex differences in
the use of natural hammers by wild chimpanzees. J Hum
Evol 13:415–440.
Boesch C, Marchesi P, Fruth B, Joulian F. 1994. Is nut cracking
in wild chimpanzees cultural behavior? J Hum Evol 26:325–
338.
Chatani K. 2003. Positional behavior of free-ranging Japanesemacaques (Macaca fuscata). Primates 44:13–23.
Cohen J. 1960. A coefficient of agreement for nominal scales.
Educ Psychol Meas 20:37–46.
Foley R, Lahr MM. 2003. On stony ground: lithic technology,
human evolution, and the emergence of culture. Evol Anthropol 12:109–122.
Fox EA, van Schaik CP, Sitompul A, Wright DN. 2004. Intraand interpopulational differences in orangutan (Pongo pygmaeus) activity and diet: implications for the invention of tooluse. Am J Phys Anthropol 125:162–174.
Fragaszy DM, Perry S. 2003. Towards a biology of traditions.
In: Fragaszy DM, Perry S, editors. The biology of tradition:models and evidence. Cambridge: Cambridge University
Press. p 1–32.
Galef BG Jr. 2004. Approaches to the study of traditional behaviors of free-living animals. Learn Behav 32:53–61.
Hamilton WJ III, Buskirk RE, Buskirk WH. 1978. Environmental determinants of object manipulation by chacma baboons(Papio ursinus) in two Southern African environments. J Hum
Evol 7:205–216.
Huffman MA. 1984. Stone-play of Macaca fuscata in Arashiyama B troop: transmission of a non-adaptive behavior.
J Hum Evol 13:725–735.
Huffman MA. 1991. History of Arashiyama Japanese Macaquesin Kyoto, Japan. In: Fedigan LM, Asquith PJ, editors. The
monkeys of Arashiyama: thirty-five years of research in Japanand the West. Albany: SUNY Press. p 21–53.
Huffman MA. 1996. Acquisition of innovative cultural behaviors
in non-human primates: a case study of stone handling, aAmerican Journal of Physical Anthropology—DOI 10.1002/ajpa
196

244

J.-B. LECA ET AL.

socially transmitted behavior in Japanese macaques. In: Galef
B Jr, Heyes C, editors. Social learning in animals: the roots ofculture. Orlando: Academic Press. p 267–289.
Huffman MA, Hirata S. 2003. Biological and ecological foundations of primate behavioral tradition. In: Fragaszy DM, PerryS, editors. The biology of tradition: Models and evidence.
Cambridge: Cambridge University Press. p 267–296.
Huffman MA, Quiatt D. 1986. Stone handling by Japanese macaques (Macaca fuscata): implications for tool use of stone. Primates 27:427–437.
Krebs CJ. 1999. Ecological methodology, 2nd ed. Menlo Park:
Benjamin/Cummings.
Laland KN, Hoppitt W. 2003. Do animals have culture? Evol
Anthropol 12:150–159.
Laland KN, Janik VM. 2006. The animal cultures debate.
Trends Ecol Evol 21:542–547.
Leca J-B, Gunst N, Nahallage CAD, Huffman MA. 2006. Stone
handling in Japanese macaques (Macaca fuscata): a 10-troop
comparative study about a behavioral tradition. Am J Primatol 68 (Suppl 1):110–111.
Leca J-B, Gunst N, Huffman MA. 2007a. Japanese macaque cultures: inter- and intra-troop behavioural variability of stone
handling patterns across 10 troops. Behaviour 144:251–281.
Leca J-B, Gunst N, Watanabe K, Huffman MA. 2007b. A newcase of fish-eating in Japanese macaques: implications forsocial constraints on the diffusion of feeding innovation. Am J
Primatol 69:821–828.
Leca J-B, Gunst N, Huffman MA. Age-related differences in theperformance, diffusion, and maintenance of stone handling, abehavioral tradition in Japanese macaques. J Hum Evol, inpress, available online: doi:10.1016/j.jhevol.2007.05.009.
Lee PC, Moura ACA. 2005. Terrestriality and tool use—
response. Science 308:951–952.
Lefebvre L. 1995. Culturally-transmitted feeding behaviour inprimates: evidence for accelerating learning rates. Primates
36:227–239.
Matsuzawa T. 1999. Communication and tool use in chimpanzees: cultural and social context. In: Hauser M, Konishi M,
editors. The design of animal communication. Cambridge:
MIT Press. p 645–671.
McGrew WC, Ham RM, White LJT, Tutin CEG, Fernandez M.
1997. Why don’t chimpanzees in Gabon crack nuts? Int J Primatol 18:353–374.
Moura ACA. 2007. Stone banging by wild capuchin monkeys: anunusual auditory display. Folia Primatol 78:36–45.

Moura ACA, Lee PC. 2004. Capuchin stone tool use in Caatinga
dry forest. Science 306:1909.
Nahallage CAD, Huffman MA. 2007a. Age-specific functions ofstone handling, a solitary-object play behavior, in Japanesemacaques (Macaca fuscata). Am J Primatol 69:1–15.
Nahallage CAD, Huffman MA. 2007b. Acquisition and development of stone handling behavior in infant Japanese macaques. Behaviour 144:1193–1215.
Panger MA, Perry S, Rose L, Gros-Louis J, Vogel E, McKinnon
KC, Baker M. 2002. Cross-site differences in foraging behavior of white-faced capuchins (Cebus capucinus). Am J Phys
Anthropol 119:52–66.
Parker ST, Gibson KR. 1977. Object manipulation, tool use andsensorimotor intelligence as feeding adaptations in Cebus
monkeys and great apes. J Hum Evol 6:623–641.
Perry S. 2003. Conclusions and research agendas. In: Fragaszy
DM, Perry S, editors. The biology of tradition: models and evidence. Cambridge: Cambridge University Press. p 426–440.
Perry S, Baker M, Fedigan L, Gros-Louis J, Jack K, McKinnon
KC, Manson JH, Panger M, Pyle K, Rose L. 2003. Social conventions in wild white-faced capuchin monkeys. Curr Anthropol 44:241–268.
Reader SM, Laland KN. 2001. Primate innovation: sex, age andsocial rank differences. Int J Primatol 22:787–805.
van Schaik CP. 2003. Local traditions in orangutans and chimpanzees: social learning and social tolerance. In: Fragaszy
DM, Perry S, editors. The biology of tradition: models and evidence. Cambridge: Cambridge University Press. p 297–328.
van Schaik CP, Ancrenaz M, Borgen G, Galdikas B, Knott CD,
Singleton I, Suzuki A, Utami SS, Merill M. 2003. Orangutan
cultures and the evolution of material culture. Science 299:
102–105.
Visalberghi E, Fragaszy DM, Izar P, Ottoni EB. 2005. Terrestriality and tool use. Science 308:951–952.
Whiten A, Goodall J, McGrew WC, Nishida T, Reynolds V,
Sugiyama Y, Tutin CEG, Wrangham RW, Boesch C. 1999. Cultures in chimpanzees. Nature 339:682–685.
Whiten A, Goodall J, McGrew WC, Nishida T, Reynolds V,
Sugiyama Y, Tutin CEG, Wrangham RW, Boesch C. 2001.
Charting cultural variation in chimpanzees. Behaviour 138:
1481–1516.
Yamakoshi G. 1998. Dietary responses to fruit scarcity of wild
chimpanzees at Bossou, Guinea: possible implications for ecological importance of tool use. Am J Phys Anthropol 106:283–
295.

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American Journal of Primatology 70:803–813 (2008)

RESEARCH ARTICLE
Food Provisioning and Stone Handling Tradition in Japanese Macaques:
A Comparative Study of Ten Troops
JEAN-BAPTISTE LECA1, NOËLLE GUNST2, AND MICHAEL A. HUFFMAN1

1
Section of Social System Evolution, Primate Research Institute, Kyoto University, Inuyama, Aichi, Japan
2

Odum School of Ecology, University of Georgia, Athens, Georgia

By addressing the influence of food provisioning on stone handling (SH), a behavioral tradition in
Japanese macaques, this study contributes to the ongoing debate in cultural primatology by asking
whether human intervention influences the emergence or propagation of behavioral traditions. SH is aform of object play consisting of the manipulation of stones by performing various behavioral patterns.
We tested the hypothesis that the frequency of food provisioning affects the daily performance, form,and context of occurrence of SH by influencing a troop’s feeding-related activity budget. We used astandardized observation procedure to investigate SH in ten troops of Japanese macaques. In troops
provisioned several times a day, SH was more frequent, longer, and more prevalent during provisioning
than nonprovisioning periods. These effects of provisioning were not significant in troops provisioned
less frequently. SH was more frequently integrated with food-related activities in troops supplied withfood several times a day than in the other troops. Food provisioning may be a key factor in theinnovation and transformation phases of the SH tradition in Japanese macaques. Am. J. Primatol.
c 2008 Wiley-Liss, Inc.
70:803–813, 2008.
Key words: food provisioning; stone handling; behavioral tradition; transformation phase;
Macaca fuscata
Watanabe, 1989]. Most reported behavioral innovations in Japanese macaques occur in the artificial
context of food provisioning [but see Nakamichi etal., 1998]. Provisioning has been used for decades by
primatologists and monkey park managers throughout Japan to enhance visibility and habituation of
the monkeys and to reduce crop-raiding. However,provisioning undoubtedly affects not only the animals’ feeding habits but also their entire activity
budget [Huffman, 1991; Huffman & Hirata, 2003].
SH is a form of object play consisting of themanipulation of stones by performing various behavioral patterns, socially transmitted across generations, as a behavioral tradition in Japanese macaques

INTRODUCTION
Culture is typically defined as a group-specificbehavioral practice, persistent in several individuals
over a number of years, and dependent on social
means for its diffusion and maintenance [Perry &Manson, 2003]. Field studies on geographic variationin the occurrence of numerous behavioral patterns,
supported by longitudinal and experimental investigations of whether and how these behaviors aresocially learned, have provided extensive evidence forbehavioral traditions in several primate species [e.g.,
Huffman & Hirata, 2003, 2004; Leca et al., 2007a;
Nahallage & Huffman, 2007a; Perry et al., 2003;
Whiten et al., 1999]. By addressing the influence offood provisioning on stone handling (SH), a strong
candidate for a long-studied behavioral tradition in
Japanese macaques (Macaca fuscata) [cf. Huffman,
1984, 1996; Huffman & Hirata, 2003; Huffman &Quiatt, 1986; Leca et al., 2007a], this study contributes to the ongoing debate in cultural primatology
concerning how human intervention influences theinnovation or propagation of behavioral traditions
Japanese macaques are known for their behavioral traditions. In this species the diffusion ofseveral newly acquired behaviors has been investigated, such as the consumption of novel foods andnovel food-processing techniques [Itani & Nishimura, 1973; Kawai et al., 1992; Leca et al., 2007b;r 2008 Wiley-Liss, Inc.

Contract grant sponsor: Lavoisier postdoctoral Grant, Ministèredes Affaires Etrangères, France; Contract grant sponsor: JSPS
postdoctoral fellowship; Contract grant number: P07421; Contract grant sponsor: NSF; Contract grant number: BCS-0352035;
Contract grant sponsor: Grant-In-Aid for scientific research (No.
1907421) sponsored by Ministry of Education, Science, Sports
and Culture, Japan.
Correspondence to: Jean-Baptiste Leca, Section of Ecology,

Primate Research Institute, Kyoto University, 41-2 Kanrin,
Inuyama, Aichi 484-8506, Japan. E-mail: jbtleca@yahoo.com
Received 13 August 2007; revised 10 January 2008; revision
accepted 26 March 2008
DOI 10.1002/ajp.20551
Published online 12 May 2008 in Wiley InterScience (www.
intersciencewiley.com).

198

804 / Leca et al.

the temporal relationship between SH and feeding
activities [Huffman, 1984, 1991; Huffman & Quiatt,
1986; Nahallage & Huffman, 2007b], the goal of thisstudy was to determine whether this pattern held true
when several troops were systematically compared. We
hypothesized that the frequency of provisioning affects
the daily performance, form, and context of occurrenceof SH in a given troop, through its influence on thefeeding-related activity budget.
We tested the following three predictions: Prediction ]1: In troops provisioned several times a day,SH should be more frequent, longer (at the individual level), and more prevalent (at the group level)
during provisioning than during nonprovisioning
periods; Prediction ]2: These effects of provisioning
should not hold for troops provisioned less frequently; Prediction ]3: Owing to the long-term
effects of provisioning on the SH tradition, theintegration of SH with food-related activities (i.e.,their simultaneous or interspersed performance)
should be especially prevalent in troops provisioned
several times a day.
To address these issues, we used a standardized
observation procedure to record detailed data on
the differences and similarities in the SH activity
among ten troops of Japanese macaques, characterized by high variability in the frequency of foodprovisioning. The aim is to better understand theinfluence of food provisioning on the maintenanceand transformation phase of the SH tradition in
Japanese macaques.

[Huffman, 1984, 1996; Huffman & Quiatt, 1986;
Nahallage & Huffman, 2007a]. In recent reports, we
focused on how socio-demographic factors (troop
size, age structure, and observational learning) andecological factors (stone availability and terrestriality) influenced intertroop variation in SH [Leca et al.,2007a,c, 2008]. Preliminary intertroop comparison
suggests contrasting relationships between SH andprovisioning [Huffman & Hirata, 2003]. To date, SH
has never been reported in free-ranging, nonprovisioned troops of Japanese macaques. However, SH
has not been recorded in all provisioned troops either[Huffman & Hirata, 2003]. At Takagoyama, the SH
tradition gradually disappeared after food provisioning was stopped and the monkeys began to feedsolely on natural vegetation [Fujita, personal communication, cited in Huffman, 1984].
Provisioning frequency varies across free-ranging and captive troops of Japanese macaques. To
lure them out of the forest and make them more
visible to visitors, some free-ranging troops in parks
are provisioned especially frequently [Huffman,1991]. Interestingly, there are contrasting findings
regarding the temporal link between SH and feeding
activities. In Arashiyama E and Takasakiyama freeranging troops, where the emergence of the SH
tradition was first documented about 25 years ago,
SH is mainly observed immediately after feeding on
provisioned food, which occurs several times a day[Huffman, 1984, 1996]. By contrast, the captive
Takahama troop at the Primate Research Instituteof Kyoto University shows SH throughout the day,regardless of feeding time, which occurs only once a
day [Nahallage & Huffman, 2007b]. These reportssuggest that the frequency of provisioning may
somehow influence the frequency of SH. However,no systematic comparison of the relationships between SH and food provisioning across several troopsof Japanese macaques has yet been conducted.
A troop’s history in relation to feeding may be
crucial for the transformation phase of the SH
tradition, defined as the late period during which
the behavior is consolidated through integration
with other daily activities [Huffman & Hirata,
2003]. Increased familiarity with the properties ofstones in a feeding context may expand the monkeys’
SH repertoire and lead to greater stone-related
behavioral diversity [Huffman & Quiatt, 1986]. This
does not mean that a particular type of foodprovisioning is a necessary and sufficient condition
for SH to appear and spread within a group.
However, the occurrence of SH and its integration
with other activities may vary across troops inrelation to provisioning frequency.
Based on (1) earlier research on the causal links
between food-related activities and object play [Mistlberger, 1994; Terlouw et al., 1993], and (2) preliminary comparisons of a few troops of Japanese macaquessuggesting that provisioning frequency may influence

Am. J. Primatol.

METHODS
General Study Conditions
The species under study was the Japanesemacaque (M. fuscata). We observed ten troops at
six geographically isolated sites in Japan from
August 2003 to February 2005 (Table I). Four troops
lived in outdoor enclosures in Inuyama, Aichi
Prefecture (Kyoto University Primate ResearchInstitute: Arashiyama 5 Ara.A, Takahama 5 Takh.,
Wakasa 5 Wak.A, and Japan Monkey Centre Yakushima macaques 5 JMC), and six troops were freeranging (Arashiyama, Kyoto Prefecture 5 Ara.E,
Koshima, Miyazaki Prefecture 5 Kosh., Shodoshima,
Kagawa Prefecture 5 Sho.A and Sho.B, Takasakiyama, Oita Prefecture 5 Tak.B and Tak.C).
The age and sex composition of all troops is
described in detail elsewhere [Leca et al., 2007a,c].
Individual identities, exact age, and matrilineal
membership were known for only some troops(Ara.A, Ara.E, Kosh., Takh., and Wak.A). For theother troops, every sampled subject was labeledaccording to its age class and sex. Observations wereconducted between 7:00 and 18:00 hr. We observed
captive troops from platforms located above theenclosure walls. Free-ranging troop members could
be approached and observed within 3–5 m. This
199

200

102
88

676
141

J.-B. L.
J.-B. L., N. G.
J.-B. L., N. G.
J.-B. L., N. G.
J.-B. L., N. G.
J.-B. L., M. A. H.a, C. N.a
J.-B. L., N. G., C. N.
J.-B. L., N. G., C. N.

September–December 2003

August–December 2003,
March–April 2004
January–February 2004

December 2003–January 2004

December 2003–January 2004

May-August 2004

February 2005

February 2005

350

450

438

46

18

N. G.

September–December 2003

19

TS

N. G.

Observers

August–November 2003

Study period

51.5

77.6

431.3

73.8

22.8

339.7

99.1

449.2

179.9

224.6

TOT

1.0

11.3

94.8

0.0

0.0

18.1

15.5

39.8

15.5

18.5

PFFT

0.3

5.5

65.8

0.0

0.0

197.3

39.0

313.8

124.5

156.0

OFT

12

40

302

36

29

84

52

131

74

84

PFNS

12

26

708

36

29

168

223

1462

570

725

ONS

4

30

317

n.a.

n.a.

9

22

309

14

59

SH
Bt (F)

26

10

35

182

59

14

99

28

1

62

SH
Bt (CAL)

67

27

579

391

75

7

91

1252

28

224

SH
Nt (IAL)

In brackets: abbreviation of troop name. TS, troop size; TOT, total observation time in hours; PFFT, provisioning–feeding focal time (total duration in hours of focal sessions collected within 20 min after
provisioning); OFT, other focal time (total duration in hours of focal sessions collected during other periods); PFNS, provisioning–feeding number of scan sessions (collected within 20 min after
provisioning); ONS, other number of scan sessions (collected during other periods); SH Bt (F), number of SH bouts collected during focal sessions (n.a., not available); SH Bt (CAL), number of SH bouts
collected during complete ad libitum sessions; SH Nt (IAL), number of SH notes collected during incomplete ad libitum sessions.
a
The first two authors were the main observers (occasionally assisted by M. A. H. and Charmalie A. D. Nahallage).

Wakasa A(Wak.A)
Arashiyama A(Ara.A)
Takahama(Takh.)
Japan Monkey Centre(JMC)
Koshima(Kosh.)
Takasakiyama B(Tak.B)
Takasakiyama C(Tak.C)
Arashiyama E(Ara.E)
Shodoshima A(Sho.A)
Shodoshima B(Sho.B)

Troop name

TABLE I. Troops Studied, Study Periods, Number of Observers, and Total Data Sets

Stone Handling and Food Provisioning / 805

Am. J. Primatol.

806 / Leca et al.

TABLE II. Ranging and Food Provisioning Conditions, Grouped According to the Level of Provisioning
Frequency, and Ordered According to the Frequency of Regular Provisioning

Troop

Surface of
enclosure
ExtraRegular
Level of food(CP) orRanging feeding site provisioning provisioning provisioning
frequency
frequency
frequency
conditions (FR) in m2

Food
supplied

Kosh.

FR

1,000aLevel-1

2/week1/monthb

Wh, Spb

Ara.A
Takh.
Wak.A

CP
CP
CP

850c
960c
500c

Level-2
Level-2
Level-2

1/day
1/day
1/day

3/weekb
3/weekb
3/weekb

JMC

CP

4,000dLevel-2

2/day

All daye

Sho.A

FR

1,200fLevel-3

3–4/day

Sho.B

FR

1,200fLevel-3

3–4/day

Ara.E

FR

400f

Level-3

4/day

1/dayb,all daye
1/dayb,all dayeAll daye

Pl, Spb
Pl, Spb
Pl, Whb,
Spb
Sp, Ap,Wh, PleRi, Spb, Pne

Tak.B
Tak.C

FR
FR

1,000f
1,000fLevel-3
Level-3

6/day
12/day1/dayb
1/daybRi, Spb, Pne
Wh, Be(Sp,
Pn, Ap)e
Wh, Spb
Wh, Spb

Totalamountof food(kg)

Averageamount offood perindividual(kg)

4, 10b

Averageduration(hr) of foodavailability

0.070,
0.175b5, 2b0.278, 0.111b
10, 5b0.217, 0.109b
5, 2b, 1b 0.263, 0.105b,
0.053b30, 10, 1, 0.432, unke
unke
6, 15b,0.020, 0.051b,
e
unk
unke
5, 15b,0.030, 0.090b,
unke
unke
1.8, 0.8, 0.022, unke
unke

1.670.3

3.8, 50b2.8, 75b0.270.0
0.270.0

0.012, 0.165b
0.007, 0.202b

5.270.8
5.471.5
6.671.0
2.170.80.370.1
0.170.0
0.270.0

CP, captive; FR, free-ranging; no superscript alphabet: regular food; Pl, commercial primate pellets; Sp, sweet potatoes; Wh, wheat grains; Ap, apples; Be,soybeans; Pn, peanuts; Ri, rice grains; unk, unknown amount of extra food supplied by visitors (highly variable depending on the presence and number ofvisitors); JMC, Japan Monkey Centre. The average amount of food per individual was estimated by dividing the total amount of food by the average numberof feeding individuals sampled during prov.15 min scans.
aSandy beach.
bExtra food supplied by staff.
cConcrete and gravel surfaces.
dGrass areas and stony ground.
eExtra food supplied by visitors.
fClay-stony ground.

been no dramatic changes in the provisioning
conditions of any troop for at least a decade.
The ten troops were categorized into three levels
according to the frequency of regular provisioning(Table II): level-1 with the lowest frequency (twice aweek), level-2 with food supplied once or twice a day,and level-3 with food distributed several times a day(3–12 times a day: 1.5–42 times more often than in theother troops). We also recorded the total amount offood supplied to each troop, and estimated the averageamount of food per individual. To calculate theaverage duration of food availability at the feeding
site, we used scan samples (see below) to measure thetime elapsed between provisioning time and no foodleft. Overall, members of level-3 troops received asmall amount of food (from 7 g per individual in Tak.C
to 30 g in Sho.B) for a relatively short time (6 min in
Sho.B to 18 min in Sho.A). Members of level-1 andlevel-2 troops received a larger amount of food (from70 g in Kosh. to 432 g in JMC) for a longer time
(96 min in Kosh. to 396 min in Wak.A).

research was conducted in accordance with Primate
Research Institute’s Guidelines for Animal Healthand Welfare.
Comparative Ranging and Provisioning
Conditions
Table II presents information on the troops’
ranging and provisioning conditions. Captive troops
were supplied regularly with commercial primate
pellets, and occasionally with vegetables or fruits,
scattered throughout feeding sites, i.e., specific areas
inside the enclosures, either concrete and gravel
surfaces or grass areas and stony ground. On ascheduled basis, free-ranging troop members gathered around feeding sites, i.e., specific areas within
their home ranges where they were provisioned withcereal grains by technicians or park staff. Cereal
grains were scattered throughout the feeding site,
either clay-stony ground or sandy beach. At theJapan Monkey Centre, Arashiyama, and Shodoshima, visitors were allowed to give a small amount of
extra food to the monkeys. Although their provisioning schedules were different, the free-ranging troops
living at the same site (Sho.A/Sho.B and Tak.B/
Tak.C) had overlapping home ranges. There have

Am. J. Primatol.

Data Collection
The two main observational methods used were
continuous focal-animal sampling and instantaneous201

Stone Handling and Food Provisioning / 807

SH records: SH bouts collected from focal orcomplete ad libitum video-recorded sessions, andSH notes collected from scan sessions or incomplete
ad libitum sessions. We defined an SH bout as thedisplay of SH activity containing pauses of no longer
than 120 sec [see Huffman, 1996]. If the individual
paused then resumed SH within this time, this wasconsidered as two SH episodes within a single SH
bout. A resumption of SH more than 120 sec after
pausing marked the start of a new SH bout.
We defined SH frequency as the average numberof SH bouts per focal hour, SH duration as the mean
duration of SH bouts, and SH prevalence as themean percentage of stone handlers among individuals sampled in scan sessions. We defined SH mixed
activity as the mean duration (per hour of SH bout)of performance of other activities (food-related
activities, socializing, and other) ‘‘integrated’’ withSH, i.e., either performed simultaneously with SH or
during pauses between SH phases. To qualify for aprovisioning–feeding focal session, the subject had tofeed for at least 30 sec on provisioned food.

group scan sampling, supplemented with ad libitum
sampling [Altmann, 1974].

Focal sampling
We recorded every focal session with Sonydigital video cameras (Sony, Tokyo, Japan). Whenever possible, the focal individual was filmed face-on
and about 1-m2 in-frame. We selected focal individuals semi-randomly [for details, see Leca et al.,2007a]. To use a nonindividually identified subject as
its own control, efforts were made to sample thesame individual just before and just after theprovisioning time. The typical duration of a focal
session was 15 min. If the focal individual performed
SH during the final 2 min, the observation was
extended for 5 min, or longer if SH was still inprogress [see Huffman, 1996].
Scan and ad libitum samplings
Before and after each focal session, the troop
was scanned and the activity of all sampled individuals was noted (feeding, foraging, SH, other). For
each scan-sampled stone handler, we recorded
individual identity or age and sex class, and whenever possible the SH patterns performed [for acomprehensive list, see Leca et al., 2007a]. In order
to investigate whether changes in group activity
were related to food provisioning, we conducted
additional group scans within 10 min before provisioning time and every 5 min up to 35 min after
provisioning (namely pre-prov., and from prov.1
5 min to prov.135 min, respectively). Other scansessions were labeled nonprovisioning scans.
To supplement the data set, observers devoted
an average7standard deviation (SD) of 38.8731.8%
of total observation time to collect ad libitum data on
individuals performing SH. Whenever possible, ad
libitum sessions were video-recorded; otherwise
records were written onto a notepad. We did notconduct focal sessions for Tak.B and Tak.C troops
owing to the short observation period (7 days) andthe very large troop sizes (cf. Table I), which madefocal follows difficult. Instead, for these troops wevideo-recorded ad libitum sessions after feeding,when SH is most likely to occur [see Huffman,1996]. In some cases we recorded complete ad
libitum sessions: The subject was filmed from thestart (shortly after provisioning, immediately after itleft the feeding site and touched stones) to the end ofSH (5 min after the last stone was discarded). For SH
episodes recorded on notepad or when the filmed
sequence of SH was incomplete, the ad libitum
session was classified as incomplete.

Data Sets and Statistical Analysis
Table I summarizes the data sets for each troop
in relation to provisioning. Total troop observation
time included focal observation time, scan time, andtime spent collecting ad libitum data. To analyze SH
frequency, we used all focal sessions excluding Sho.B,
Tak.B, and Tak.C troops owing to insufficient focal
data, along with any focal sessions lasting less than
15 min. We used all available SH bouts to analyze SH
duration and SH mixed activity, and all available SHbouts and SH notes for analyses regarding frequencyof food-directed SH patterns. For captive troops, weonly used scan sessions in which at least 80% of troop
members were sampled. For the more widelydispersed free-ranging troops, we only consideredscan sessions that sampled at least 60% of troop
members. In the troops where individual identities
were not known, any subjects that could be reliably
recognized by morphological features on video (e.g.,scars, broken finger) were used for analyses requiring independent subjects. Individuals less than 1
year old were not included in analyses. We assessedinterobserver reliability between J.-B. L. and N. G.
for individual identities, activities, and interactions(k 5 0.88, 0.92, and 0.96, respectively), and intracoder reliability for J.-B. L. when transcribing thesame samples of SH video-records twice, involving a
total of 630 sample points (k 5 0.84) [Martin &Bateson, 1993].
As age may affect SH frequency, we distinguished immature (up to 6 years old) from matureindividuals (at least 7 years old) [cf. Leca et al.,2007c]. For most analyses, we report mean values(X)7SD. When the assumptions of normality, independence, and homogeneity of variances were

Data Processing
Using video-records, J.-B. L. measured theduration (in sec) of all the above-mentioned activities
and each SH pattern. We distinguished two types of202

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808 / Leca et al.

differ significantly (P40.05). In level-3 troops, SH
frequency was considerably higher during provisioning–feeding focals than other focals, and the overall
SH frequency was at least two times higher than inlower-level troops (mean number of SH bouts per
focal hour, Ara.E: X1 5 XProv.–feeding 5 3.172.1,
X2 5 XOther 5 0.770.5, X3 5 XOverall 5 1.971.5; Sho.A:
X1 5 2.972.9, X2 5 0.070.0, X3 5 1.471.4). In lowerlevel troops, there were no significant differencesin SH frequency between the two periods (minimum
values for all troops combined: X1 5 0.170.3,
X2 5 0.170.2, X3 5 0.170.2; maximum: X1 5
0.571.2, X2 5 1.070.8, X3 5 0.770.7).

satisfied, we used parametric tests. General linear
models (GLM) with repeated measures were used toassess the effect of the frequency of provisioning on
SH frequency during provisioning–feeding periods
and other periods. The models used the SH
frequency as the dependent variable, the type of
periods as the within-subject factor, the levels ofprovisioning frequency, the troops, and the age as
the fixed factors, and the Scheffe tests for the post
hoc multiple paired comparisons.
When parametric assumptions were violated, weused nonparametric tests to compare SH duration
between feeding and nonfeeding individuals (Wilcoxon signed-ranks tests), and the frequency of fooddirected SH patterns between level-3 troops andlower-level troops (Mann–Whitney U test). To assess
the effect of the timing of provisioning–feeding on
SH prevalence, we used w2 goodness-of-fit tests. To
test the association between the level of provisioning
frequency and SH mixed activity, we used w2 tests of
independence. For post hoc examination of w2 tests,
we calculated the adjusted standardized residuals,
and considered z-scoresZ|1.96| as significant. All
tests were two-tailed. Statistical analyses were
performed using SPSS 12.0 (SPSS Inc., Chicago).
The significance level was set at a 5 0.05.

SH duration
To test the effect of feeding activity on SH
duration, we compared the duration of SH bouts infeeding and nonfeeding individuals. In all level-3
troops, SH duration while feeding was significantly
longer than when not feeding (Wilcoxon signedranks tests, Ara.E: X1 5 XFeeding 5 2297295, X2 5
XNonfeeding 5 40748, z 5 3.48, N 5 25, Po0.001;
Sho.A:
X1 5 3197210,
X2 5 1375,
z 5 2.93,
N 5 11, P 5 0.003; Sho.B: X1 5 63774, X2 5 19710,
z 5 2.80, N 5 10, P 5 0.005; Tak.B: X1 5 2067159,
X2 5 56758, z 5 3.18, N 5 13, P 5 0.001; Tak.C:
X1 5 158799, X2 5 20710, z 5 4.78, N 5 30,
Po0.001). In lower-level troops, we found no
significant differences (minimum values for all
troops combined: X1 5 1175, X2 5 17715; maximum: X1 5 1037106, X2 5 1227195, P40.05).

RESULTS
Effect of Provisioning Frequency on SH
Occurrence (Predictions ]1 and ]2)

SH frequency
When analyzing whether provisioning frequency
affected SH occurrence at the individual level, the main
effect of provisioning frequency was significant,whereas the main effect of age and the interaction
between these factors were not significant (GLM
repeated measures, N 5 224, provisioning frequency:
F2,218 5 72.87, Po0.001; age: F1,218 5 0.12, P 5 0.724;
provisioning frequency  age: F2,218 5 1.05, P 5 0.352).
Post hoc comparisons between provisioning frequencies
showed that level-3 troops differed significantly fromlower-level troops (Po0.001) but level-1 and level-2
troops did not differ from each other (P 5 0.448).
When troops instead of the levels of provisioning
frequency was used as a fixed factor, the main effectof troop was significant, whereas the main effect ofage and the interaction between troop and age were
not significant (GLM repeated measures, N 5 224,
troop: F6,210 5 22.16, Po0.001; age: F1,210 5 0.79,
P 5 0.376; troop  age: F6,210 5 1.51, P 5 0.176). Post
hoc comparisons showed that the two level-3 troops,
Ara.E and Sho.A, did not differ significantly fromeach other (P 5 0.746) but each of them differed fromall the lower-level troops (Ara.E vs. all the lowerlevel troops: Po0.001; Sho.A vs. Kosh.: P 5 0.010;
Sho.A vs. Ara.A: P 5 0.029; Sho.A vs. Takh.:
P 5 0.030; Sho.A vs. Wak.A: P 5 0.027; Sho.A vs.
JMC: P 5 0.016). All level-1 and level-2 troops did not

Am. J. Primatol.

SH prevalence
To assess the effect of provisioning frequency on
SH activity at the group level, from scan samples wecompared the mean percentage of stone handlers ineach troop in relation to provisioning frequency leveland different periods (provisioning or not) (Fig. 1).
Only in level-3 troops was SH prevalence affected by
the timing of feeding on provisioned foods (w2goodness-of-fit tests, N 5 7 periods, namely nonprov.,
pre-prov., and from prov.15 min to prov.125 min;Ara.E: w26 5 26.34, Po0.001; Sho.A: w26 5 111.24,
Po0.001; Sho.B: w26 5 32.02, Po0.001; Tak.B:
w26 5 63.18, Po0.001; Tak.C: w26 5 117.16, Po0.001).
In all level-3 troops, provisioning resulted in
more troop members SH simultaneously for about
30 min. After rapidly (9.879.0 min) reaching a peak
(24.6715.7% of stone handlers), SH activity at thegroup level gradually decreased to a low baseline(0.470.3% of stone handlers) within 30 min. By
contrast, the troops provisioned less frequently
showed consistently low levels of SH regardlessof period (w2 goodness-of-fit tests, Kosh.: w26 5 0.00,
P40.05;
Ara.A:
w26 5 0.00,
P40.05;
Takh.:
2
w6 5 1.60, P40.05; Wak.A: w26 5 1.80, P40.05; JMC:
w26 5 0.60, P40.05).
203

Stone Handling and Food Provisioning / 809

SH prevalence (mean percentage of stone
handlers among scan sampled individuals)

50
45
40
35
30
25
20
15
10
5

prov.+35minprov.+30min

Provisioning period

prov.+25minprov.+20minprov.+15minprov.+10minprov.+5min

pre-prov.

non prov.

0

Sho.A
Sho.B
Tak.C
Tak.B
Ara.E
Troops
JMC
Wak.A
Takh.
Ara.A
Level-1
Kosh.
Level-2
Level-3

Fig. 1. Effect of provisioning on SH prevalence: intertroop comparison of the mean percentage of stone handlers among scan-sampledindividuals according to the provisioning period and the level of food provisioning frequency. Nonprov., nonprovisioning scans; pre-prov.,
scan sessions recorded within 10 min before provisioning time; from prov.15 min to prov.135 min, scan sessions recorded every 5 minwithin 35 min after provisioning time; SH, stone handling.

N 5 131 mixed-activity bouts, w24 5 102.91, Po0.001).
Post hoc examination of residuals showed that the
integration of food-related activities with SH wassignificantly higher in the level-3 troops than inlower-level troops (Fig. 2a).
We conducted the same analysis to determine
which of the three types of activity were interspersedwith SH; that is, performed during pauses between
SH phases, in relation to provisioning frequency. We
found a significant association between the twovariables (Pearson w2 test: N 5 1,848 mixed-activity
bouts, w24 5 958.17, Po0.001). Post hoc examinationof residuals showed that the integration of foodrelated activities with SH was significantly higher inthe level-3 troops than in lower-level troops, whereas
other activities (resting, locomoting, vigilance, selfgrooming, and object play) were more often integrated with SH in lower-level troops than in level-3
troops (Fig. 2b).
Finally, we quantified the frequency of thefollowing food-directed SH patterns: (1) rub or clacka stone with a food item, such as a pellet or piece ofsweet potato, and (2) gather, cuddle, or grasp a pile ofstones mixed with supplied or natural food items,
such as peanut pods or acorns. These frequencies
were weighted by the total observation time for eachtroop and, given their rarity, plotted on a 1,000-hr
scale (adjusted frequency: AF). The direct integra-

Integration of SH with Food-Related Activities(Prediction ]3)
To assess the integration of SH with feeding
activity, we measured the frequency of SH whilechewing food. In all level-3 troops, stone handlers
simultaneously chewed food or at least had food intheir cheek pouches in more than 60% of SH bouts(Ara.E: 82.7%, N 5 352; Sho.A: 72.5%, N 5 40; Sho.B:
63.3%, N 5 30; Tak.B: 78.0%, N 5 46; Tak.C: 83.5%,
N 5 182). In lower-level troops, these rates werearound 50% or below (Kosh.: 52.2%, N 5 23; Ara.A:
40.0%, N 5 15; Takh.: 42.1%, N 5 337; Wak.A: 21.5%,
N 5 121; JMC: 41.3%, N 5 121).
To test whether other activities co-occurringwith SH varied with provisioning frequency, we
conducted a w2 test of independence based on acontingency table representing the duration of thisform of SH mixed activity in troops belonging to thethree levels and three types of simultaneous activities, namely food-related activity (food intake andforaging), socializing (allo-grooming, nursing, aggression, and social play), and other (resting, selfgrooming, and object play). During most socializing
or other activities, the monkey held, cuddled, or
carried the stone(s) [for definitions, cf. Leca et al.,2007a]. There was a significant association between
the type of activity ‘‘integrated’’ with SH and thelevel of provisioning frequency (Pearson w2 test:

204

Am. J. Primatol.

810 / Leca et al.

a

2.5

Mean duration (min) of other activities
performed simultaneously to SH

Food-related
Socializing
2
Other

1.5

1

0.5

0

b

20

Mean duration (min) of other activities
performed during pauses between SH phase

Kosh.
Ara.A
Takh.
Wak.A
JMC
Sho.A
Sho.B
Ara.E
Tak.B
Tak.C
(Level-1) (Level-2) (Level-2) (Level-2) (Level-2) (Level-3) (Level-3) (Level-3) (Level-3) (Level-3)
Troop (and level of food provisioning frequency)

18

Food-related

16

Socializing

14

Other

12
10
8
6
4
2
0
Kosh.
Ara.A
Takh.
Wak.A
JMC
Sho.A
Sho.B
Ara.E
Tak.B
Tak.C
(Level-1) (Level-2) (Level-2) (Level-2) (Level-2) (Level-3) (Level-3) (Level-3) (Level-3) (Level-3)
Troop (and level of food provisioning frequency)

Fig. 2. SH mixed activity in terms of mean duration of other activities (food-related activities, socializing, and other) performed (inminutes per hour of SH bout) simultaneously to SH (a) or during pauses between SH phases (b). SH, stone handling.

(Prediction ]2). Furthermore, integration of SH withfood-related activities occurred more frequently introops provisioned several times a day, reflecting
long-term effects of provisioning on the transformation phase of the SH tradition (Prediction ]3).
The three predictions were upheld, supporting the
hypothesis that provisioning frequency affects thedaily performance, form, and context of occurrenceof SH by influencing the feeding activity budget.
The troops provisioned several times a day
received relatively small amounts of small-sized fooditems (e.g., cereal grains, see Table II), which wereavailable at the feeding sites for short periods oftime. Although not directly analyzed, the particular
combination of food availability and size associatedwith frequent provisioning might give rise tounusual food-related responses. At the feeding site,
most individuals rapidly fill their cheek pouches
while also eating on the spot. After leaving thefeeding site, they can eat in a more leisurely fashion,tion of food items with SH activity was markedly
more frequent in level-3 troops (Ara.E: N 5 52,
AF 5 121; Sho.A: N 5 4, AF 5 51; Sho.B: N 5 2,
AF 5 39; Tak.B: N 5 4, AF 5 175; Tak.C: N 5 6,
AF 5 81) than in lower-level troops (Kosh.:N 5 AF 5 0; Ara.A: N 5 AF 5 0; Takh.: N 5 2,
AF 5 4; Wak.A: N 5 AF 5 0; JMC: N 5 1, AF 5 10)(Mann–Whitney U test: Nlevel-1 and -2 5 Nlevel-3 5 5,z 5 2.64, P 5 0.008).
DISCUSSION
This is the first systematic investigation of theinfluence of food provisioning on the SH tradition in
Japanese macaques. In troops provisioned several
times a day, SH was significantly more frequent(regardless of age), longer, and more prevalentduring provisioning than during nonprovisioning
periods (Prediction ]1). None of these effects weresignificant in troops provisioned less frequently

Am. J. Primatol.

205

Stone Handling and Food Provisioning / 811

living on Koshima island was quite similar to those ofwild troops, with individuals foraging in a 33 haforest for natural foods [see Leca et al., 2007b; Mori,
1977]. Interestingly, Kosh. is the troop provisioned
least of all and the troop showing the least amountof SH both at the individual and the group level[see Leca et al., 2007c]. The original motivations
underlying SH may be different from what they aretoday. Most monkeys observed handling stones in
2003–2005 were born into troops with well-established SH traditions. Furthermore, individuals grew
up into a troop with either a strong or a weakconnection between SH and provisioning. The conformity-enforcing hypothesis, which proposes that
culturally nonconforming individuals may be discriminated against [cf. Lachlan et al., 2004], predicts
that immature individuals should integrate the same
type of connection between SH and feeding activities
as most older group members.
The general behavioral predispositions of a
species make behavioral innovation relatively predictable [Huffman & Hirata, 2003]. Considering thenatural propensity for Japanese macaques to manipulate stones [cf. Leca et al., 2007a], and provided
equivalent stone availability [cf. Leca et al., 2008],
SH traditions are theoretically equally likely toemerge in all provisioned troops, although relative
rate of exposure to stones does not influence thelatency of infants to acquire SH [Nahallage &Huffman, 2007a]. This may account for the occurrence of SH in all the troops studied here, despite
differences in its characteristics. Thus, we argue that
occurrence of SH in a given troop is not directly
influenced by provisioning parameters, but thecontext of occurrence, frequency, duration, prevalence, and form of SH are.
Anthropogenic influences can create major intertroop differences in activity budgets. Provisioning infree-ranging troops results in the daily concentrationof most troop members around feeding grounds, i.e.,
open areas with stones. Some troop members returnto the forest between provisioning periods, but mostof them rest and socialize around the feeding site.
This opportunity and free time may be at the origin ofSH first occurring in the feeding context in frequently
provisioned free-ranging troops. If the SH tradition
appears in a free-ranging troop where food provisioning influences the activity budget, its long-termtransformation phase is likely to include the integration of SH with food-related activities and the gradualemergence of food-directed SH patterns. This is thecase for all level-3 troops, where various SH patterns
combining provisioned food items were observed.
However, at Arashiyama and Takasakiyama, we also
observed stones gathered into piles in the forest,
distant from the feeding area. This suggests that infree-ranging provisioned troops SH may occasionallybe integrated with activities other than feeding on
provisioned foods, such as feeding on natural foods.

with few opportunities for further food-processing
behaviors.
Studies suggest that the organization of foodrelated behaviors may be partly ‘‘preprogramed’’, sothat feeding-like behavior persists for some timeafter provisioning [Lawrence & Terlouw, 1993].
If feeding motivation is high and food-related
activities are interrupted, foraging-like behaviors
might be directed at alternative objects [Haskell
et al., 1996]. During all provisioning episodes in thelevel-3 troops studied here, cereal grains are quickly
depleted at the feeding site, as is the opportunity tomanipulate these small food items. Handling stones
may be an extension of foraging-like behaviors, acontinuation of manipulatory actions while chewing
food. With provisioning repeated several times a dayover long periods of time (as in level-3 troops), cooccurrence of food-related and SH activities isfacilitated. This interpretation is consistent with
reports of controlled feeding and persistent postfeeding foraging behaviors or object manipulation insows [Haskell et al., 1996; Terlouw et al., 1993]. This
proximate explanation builds on the argument that
SH may replace other activities that are normallyassociated with foraging [Huffman & Hirata, 2003].
In troops provisioned less frequently but withlarger food items in large amounts, some of which
may still be available hours later (see Table II),
postfeeding foraging-like behaviors are not interrupted; therefore, the monkeys can continue tomanipulate food items while chewing. This isprobably why there was no temporal connection
between feeding and SH in level-1 and level-2 troops.
Therefore, food provisioning constraints, including
frequency, duration of food availability, and the sizeof food items, may strongly influence a troop’s foodrelated activities and feeding style, which in turn
could affect several aspects of SH. However, ourresults on the less frequently provisioned troops
must be viewed with caution owing to a possible floor
effect, as these troops showed few episodes of SH.
Nevertheless, a recent longitudinal study on one ofthese troops found that SH activity occurred
throughout the day, regardless of provisioning time
[Nahallage & Huffman, 2007b].
These proximate explanations are in agreementwith the gradual disappearance of SH at Takagoyama after provisioning was stopped [Fujita, personalcommunication, cited in Huffman, 1984], and withthe lack of observations of SH in wild, nonprovisioned troops of Japanese macaques at other sites[e.g., Kinkazan: Shimooka, personal communication;
Yakushima: Hanya, personal communication]. In
nonprovisioned troops, foraging interspersed withtraveling between food patches accounts for a large
proportion of the daily activity budget [Hanya, 2004];
therefore, there may simply be less time available fornonsubsistence activities such as SH [see Huffman &Hirata, 2003]. The activity budget of the study troop
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feeding activities, to further explore the proximate
causes of this behavior and its longer-term transformation. As with stone-related behaviors in nonhuman primates, a better understanding of theinfluence of environmental factors in the transformation of this behavioral tradition in Japanesemacaques may provide new insights into the emergence of hominid material culture through stone-tool
technology.

Indeed, even before provisioning was started at
Arashiyama in the late 1940s, monkeys were seen tohandle hard, inedible fruits much as they handle
stones today [Huffman, 1984].
The transformation phase of the SH tradition,
revealed by the increase in contexts in which SH
occurs, is all the more likely and flexible as SH
appears to be a nonadaptive behavior with no
obvious immediate survival value [Huffman, 1984,
1996; but see Nahallage & Huffman, 2007b], as
opposed to stone-tool-use traditions for which an
efficient behavioral pattern should be maintained
unchanged [e.g., Boesch, 1991]. However, an eventual ‘‘ratchet effect’’ of increased complexity of SH isconceivable, possibly ultimately resulting in future
use of stones as tools [Huffman & Quiatt, 1986; Lecaet al., 2007a].
Although SH in Ara.E and Tak.C is now strongly
linked to provisioning, the SH tradition emerged
over three decades after the onset of food provisioning in these two troops. The reasons for the late
appearance of SH are not fully understood. Possibly,
sporadic SH appeared earlier without spreading
within the troop, and without being noticed byhuman observers [Huffman, 1984]. However, thefirst individuals observed to perform SH at Arashiyama were all under 4 ears of age, emphasizing
the playful nature of this behavior [Huffman, 1984].
Developmental correlates and age differences in the
motivation to engage in SH should be addressed infuture studies [Nahallage & Huffman, 2007b].
Changes in the local environmental conditions (e.g.,
provisioning style, stone availability) may also play arole [Huffman & Hirata, 2003]. Between the time
when SH was first noticed, in December 1979, up to1984 when observations were resumed by Huffman[1984, 1996], the behavior had spread within thetroop. This rapid diffusion of SH may have occurredowing to construction projects when a large numberof stones were left at the edge of the feeding area.
In conclusion, we demonstrated that food provisioning conditions, especially frequency of provisioning, affect the daily performance of SH. This study
using data from several troops supports earlier
observations suggesting that provisioning is a key
factor in the innovation, diffusion, and long-term
maintenance of the SH tradition in troops living in
natural habitats [cf. Huffman, 1984]. The persistence of SH in food-related contexts may eventuallyturn into the instrumental use of stones by Japanesemacaques [Huffman & Quiatt, 1986]. Evidence forrelationships between SH and provisioning does notargue against a cultural interpretation of SH, as thislong-enduring behavior is socially transmitted [Huffman, 1984, 1996; Nahallage & Huffman, 2007a],
which some authors suggest is sufficient evidence ofa behavioral tradition [e.g., Perry & Manson, 2003].
Our findings call for experimental approaches totest the strength of the connection between SH and

Am. J. Primatol.

ACKNOWLEDGMENTS
Field work was supported by a Lavoisier postdoctoral Grant, Ministère des Affaires Etrangères,
France to J.-B. Leca. The authors’ work during partof the preparation of this manuscript was funded by
a Grant-In-Aid for scientific research (No. 1907421 to
M.A. Huffman) sponsored by Ministry of Education,
Science, Sports and Culture, Japan, by a JSPS
postdoctoral fellowship of J.-B. Leca (No. 07421),
and by a NSF grant to N. Gunst (BCS-0352035). We
thank S. Asaba, F. Kanchi, T. Kawashima, S.
Kobatake, H. Kurita, M. Nakamura, T. Suzumura,Y. Takenoshita, K. Watanabe, the Enomoto family,
and C. A. D. Nahallage. We thank J. Anderson,
M. Gerald and two reviewers for helpful comments
on a previous version of the manuscript.
REFERENCES
Altmann J. 1974. Observational study of behavior: sampling
methods. Behaviour 49:227–267.
Boesch C. 1991. Symbolic communication in wild chimpanzees? Hum Evol 6:81–90.
Hanya G. 2004. Seasonal variations in the activity budget ofJapanese macaques in the coniferous forest of Yakushima:
effects of food and temperature. Am J Primatol 63:165–177.
Haskell MJ, Terlouw EMC, Lawrence AB, Erhard HW. 1996.
The relationship between food consumption and persistenceof post-feeding foraging behaviour in sows. Appl Anim
Behav Sci 48:249–262.
Huffman MA. 1984. Stone-play of Macaca fuscata in Arashiyama B troop: transmission of a non-adaptive behavior. J Hum
Evol 13:725–735.
Huffman MA. 1991. History of Arashiyama Japanese macaques in Kyoto, Japan. In: Fedigan LM, Asquith PJ, editors.
The monkeys of Arashiyama: thirty-five years of research inJapan and the West. Albany, NY: SUNY Press. p21–53.
Huffman MA. 1996. Acquisition of innovative cultural behaviors in non-human primates: a case study of stone
handling, a socially transmitted behavior in Japanesemacaques. In: Galef Jr G, Heyes C, editors. Social learningin animals: the roots of culture. Orlando, FL: Academic
Press. p 267–289.
Huffman MA, Hirata S. 2003. Biological and ecologicalfoundations of primate behavioral tradition. In: Fragaszy
DM, Perry S, editors. The biology of tradition: models
and evidence. Cambridge: Cambridge University Press.
p267–296.
Huffman MA, Hirata S. 2004. An experimental study of leaf
swallowing in captive chimpanzees: insights into the originof a self-medicative behavior and the role of social learning.
Primates 45:113–118.
Huffman MA, Quiatt D. 1986. Stone handling by Japanesemacaques (Macaca fuscata): implications for tool use ofstone. Primates 27:427–437.

207

Stone Handling and Food Provisioning / 813

Itani J, Nishimura A. 1973. The study of infra-human culture
in Japan. In: Menzel E, editor. Precultural primate
behavior. Basel: Karger. p26–50.
Kawai M, Watanabe K, Mori A. 1992. Pre-cultural behaviors
observed in free-ranging Japanese monkeys on Koshima
islet over the past 25 years. Primate Rep 32:143–153.
Lachlan RF, Janik VM, Slater PJB. 2004. The evolution ofconformity-enforcing behaviour in cultural communication
systems. Anim Behav 68:561–570.
Lawrence AB, Terlouw EMC. 1993. A review of behavioral
factors involved in the development and continued performance of stereotypic behaviours in pigs. J Anim Sci
71:2815–2825.
Leca JB, Gunst N, Huffman MA. 2007a. Japanese macaquecultures: inter- and intra-troop behavioural variability ofstone handling patterns across 10 troops. Behaviour
144:251–281.
Leca JB, Gunst N, Watanabe K, Huffman MA. 2007b. A newcase of fish-eating in Japanese macaques: implications forsocial constraints on the diffusion of feeding innovation. Am
J Primatol 69:821–828.
Leca JB, Gunst N, Huffman MA. 2007c. Age-related differences in the performance, diffusion, and maintenance ofstone handling, a behavioral tradition in Japanese macaques. J Hum Evol 53:691–708.
Leca JB, Gunst N, Huffman MA. 2008. Of stones andmonkeys: testing ecological constraints on stone handling,a behavioral tradition in Japanese macaques. Am J Phys
135:233–244.
Martin P, Bateson P. 1993. Measuring behaviour: an introductory guide. Cambridge: Cambridge University Press.

Mistlberger RE. 1994. Circadian food-anticipatory activity:
formal models and physiological mechanisms. Neurosci
Biobehav Rev 18:171–195.
Mori A. 1977. Intra-troop spacing mechanism of the wild
Japanese monkeys of the Koshima troop. Primates
18:331–357.
Nahallage CAD, Huffman MA. 2007a. Acquisition and development of stone handling behaviour in infant Japanesemacaques. Behaviour 144:1193–1215.
Nahallage CAD, Huffman MA. 2007b. Age-specific functions ofstone handling, a solitary-object play behavior, in Japanesemacaques (Macaca fuscata). Am J Primatol 69:267–281.
Nakamichi M, Kato E, Kojima Y, Itoigawa N. 1998. Carrying
and washing of grass roots by free-ranging Japanesemacaques at Katsuyama. Folia Primatol 69:35–40.
Perry S, Manson JH. 2003. Traditions in monkeys. Evol
Anthropol 12:71–81.
Perry S, Panger M, Rose LM, Baker M, Gros-Louis J, Jack K,
McKinnon KC, Manson J, Fedigan L, Pyle K. 2003.
Traditions in wild white-faced capuchins. In: Fragaszy
DM, Perry S, editors. The biology of tradition: models andevidence. Cambridge: Cambridge University Press. p
391–423.
Terlouw EM, Wiersma A, Lawrence AB, MacLeod HA. 1993.
Ingestion of food facilitates the performance of stereotypies
in sows. Anim Behav 46:939–950.
Watanabe K. 1989. Fish: a new addition to the diet of Koshimamonkeys. Folia Primatol 52:124–131.
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.

208

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Journal of Human Evolution 55 (2008) 989–998

Contents lists available at ScienceDirect

Journal of Human Evolution
journal homepage: www.elsevier.com/locate/jhevol

Stone-throwing by Japanese macaques: form and functional aspectsof a group-speciﬁc behavioral tradition
Jean-Baptiste Leca a, *, Charmalie A.D. Nahallage a, Noëlle Gunst b, Michael A. Huffman aab

Section of Social Systems Evolution, Primate Research Institute, Kyoto University, 41-2 Kanrin, Inuyama, Aichi 484-8506, Japan
Odum School of Ecology, University of Georgia, Athens, GA 30602-2202, USAa r t i c l e i n f o

a b s t r a c t

Article history:
Received 31 October 2007
Accepted 4 June 2008

Throwing is a major behavioral component of hominid evolution. Comparison of this behavior acrossa broad range of non-human primate species is needed to elucidate the phylogenetic constraints on
throwing behavior. In this study of stone-throwing in Japanese macaques, we present a systematic multigroup comparison of the frequency and prevalence of this behavior as well as detailed descriptions andquantitative data on the form, context, and possible social transmission of stone-throwing. Stone-throws
were mainly underarm, performed from a tripedal posture, and often accompanied by repeated verticalleaps. We found marked individual hand preferences for throwing, but no consistent group-level
handedness. Our results support the hypotheses relating body posture, throwing style, and handedness
in throwing by primates. Based on the analysis of the contexts that may elicit the behavior, we postulatethat unaimed stone-throwing in Japanese macaques may serve to augment the effect of agonistic displays, and accordingly, can be regarded as spontaneous tool-use. Our ﬁndings are consistent with thecomparative data using modern non-human primate species to model the structural processes andfunctional aspects of throwing evolution in early hominids. This study supports the view that tool-use
evolves from initially non-functional behaviors, such as stone handling, which is a form of object play.
Stone-throwing by Japanese macaques meets several criteria of a behavioral tradition, including groupspeciﬁcity. This ﬁrst report of a stone-tool-use tradition in Japanese macaques is of direct relevance to thequestion of the evolution of stone technology in hominids.
Ó 2008 Elsevier Ltd. All rights reserved.

Keywords:
Body posture
Handedness
Stone handling
Agonistic display
Tool-use
Social transmission
Macaca fuscata

Introduction
Throwing is considered a major behavioral component of human evolution. There is little doubt that the emergence of throwing
behavior had important socio-ecological and neuro-cognitive effects during all stages of hominid evolution (Darlington, 1975).
First, the ability to project objects with force, velocity, and accuracy
probably provided our prehistoric primate ancestors with numerous advantages, such as greater hunting and offensive success,better defense against predators and rivals, and the possibility tocooperate through food-sharing by transferring food items thrownwithin and between social groups (Dennell, 1997; Westergaard
et al., 1998; Watson, 2001). Second, throwing is predominantly
a one-handed sequential-movement operation exposed to selection pressures in the natural environment of early hominids.
Throwing constraints may have contributed to the pre-adaptationof their growing brain and changing body to a variety of traits,* Corresponding author.
E-mail addresses: jbtleca@yahoo.com (J.-B. Leca), nahallag@pri.kyoto-u.ac.jp(C.A.D. Nahallage), nogu@uga.edu (N. Gunst), huffman@pri.kyoto-u.ac.jp (M.A.
Huffman).
0047-2484/$ – see front matter Ó 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jhevol.2008.06.004

209

including handedness, bipedalism, and complex language processing (Calvin, 1983; Fifer, 1987; Hopkins et al., 1993; Churchill andSchmitt, 2002; Schmitt et al., 2003).
Due to their physical properties and ubiquity, stones are likely tohave been the ﬁrst effective and ready-to-use missile-weapons forour primate ancestors (Fifer, 1987; Isaac, 1987). Unfortunately,archeological evidence for the evolution of stone-throwing behavior in hominids is rare: fossil forelimb bones are rare and unlike
most other stone-tools, thrown stones were presumably scatteredaway from body parts (Darlington, 1975; but see Leakey, 1948).
Although the cognitive processes which underlay the throwing
behavior in humans are more complex than those which underlay
the throwing behavior in monkeys and apes, models of early
hominid throwing behavior can be tested by a comparative approach using modern non-human primate species (Calvin, 1983;
Westergaard and Suomi, 1995; Cleveland et al., 2003).
From the structural viewpoint, several hypotheses have been
proposed to relate skeletal modiﬁcations, body posture, throwing
style, and handedness in throwing (Calvin, 1983; Fifer, 1987; Knüsel, 1992; Hopkins et al., 2005). As opposed to monkeys that exhibit
underarm throwing from a tripedal posture, the ability for chimpanzees, bonobos, and humans to perform overarm throws by

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J.-B. Leca et al. / Journal of Human Evolution 55 (2008) 989–998

maintaining a bipedal stance may be due to similar structures of hipand shoulder joints (Beck, 1980; Calvin, 1983; Savage-Rumbaugh
et al., 2001). This distinction in throwing style and posture plays
a crucial role in the explanation of the prevalence of right-handedness observed in human populations (Annett, 2002), whereas
chimpanzees and capuchin monkeys did not show clear handpreference for throwing at the group level (Westergaard et al.,
2000; McGrew and Marchant, 2001; but see Hopkins et al., 2005).
Regarding functional aspects, Calvin (1993) hypothesized that
predatory or defensive-aimed stone-throwing by early hominids(deﬁned as the goal-directed projection of stones toward an identiﬁable target: Westergaard and Suomi, 1994) emerged from
unaimed or non-directional throwing of objects, similar to thatwhich has been observed in non-human primates as part of agonistic displays (Beck, 1980).
Therefore, research examining the form, context, and learning ofstone-throwing in various non-human primate species, including
throwing posture, handedness, direction, and distance, descriptionof the thrown stones, and assessment of the situations that may
elicit the performance and social transmission of throwing, canprovide vital insight into the biological basis and evolution ofstone-throwing in humans (Fifer, 1987; Westergaard et al., 2000;
Hopkins et al., 2005). A variety of monkeys and apes living in natural and captive conditions, particularly capuchins (Cebus spp.),baboons (Papio spp.), macaques (Macaca spp.), and chimpanzees(Pan spp.), were reported to perform aimed and unaimed stonethrowing, either spontaneously or in problem-solving tasks (e.g.,
Goodall, 1964; Hamilton et al., 1975; Tokida et al., 1994; Westergaard et al., 2000).
However, with respect to spontaneous stone-throwing in nonhuman primates, we lack detailed descriptions and quantitative
data on the form, context, and learning of the behavior, systematically collected and based on long-term observations of multiplesocial groups of various species across the primate order. There areat least four reasons for this lack of information: 1) most reports on
this behavior are based on interviews of primate keepers in zoos oranecdotal accounts relayed from anonymous travelers encountering wild primates (Hall, 1963; Kortlandt and Kooij, 1963; Beck,1980); 2) the performance of stone-throwing in non-human primates is uncommon (Torigoe, 1985); 3) throwing behavior is generally exhibited by one individual or at the most a few groupmembers, depending on their age/sex class or social status, mostly
dominant adult males, although this is more inferred from incomplete evidence than signiﬁcant correlations (e.g., Schaller, 1963;
Goodall, 1964; Struhsaker, 1975; Nishida et al., 1999); and 4) stonethrowing has been reported most frequently in primate species that
use tools in other contexts, namely capuchins and chimpanzees(Beck, 1980; Torigoe, 1985).
The genus Macaca is the most widely distributed of non-humanprimates. Its 20 extant species feature a broad diversity of social
relationships, and present a variety of morphological and behavioral adaptations to different environments that make this taxon ofparticular interest for research on evolutionary biology and ecology(Fa and Lindburg, 1996; Thierry et al., 2004). However, macaques
are not frequent tool-users and are not considered frequent stonethrowers (Beck, 1980; Torigoe, 1985). More data are needed toprovide a broader inter-species comparison and to elucidate thephylogenetic constraints on throwing behavior. Any further information on stone-throwing (or lack thereof) in macaques is ofinterest to the debate surrounding the evolution of this behavior inhumans.
Stone-throwing in Japanese macaques has recently been listed as
one of the numerous behavioral patterns of the stone handling (SH)repertoire of this species (Leca et al., 2007a,b; Nahallage andHuffman, 2007a). Deﬁned as seemingly-playful stone-directed manipulative actions, SH is considered a traditional behavior, sociallytransmitted between same-age partners, such as peer playmates andacross generations from mother to offspring (Huffman, 1984, 1996;
Huffman and Quiatt, 1986; Nahallage and Huffman, 2007b). We
found major inter-group differences in the frequency of occurrence
and the prevalence of SH patterns, with local variants being customary in some troops, and rare or even absent in others, performed
by a majority of individuals in some troops, and only idiosyncraticallyin others (Leca et al., 2007a,b).
Although showing inter-group differences is not sufﬁcient evidence for culture, the ‘‘group-contrast’’ method has often been used
as a ﬁrst step to identify candidates for cultural behaviors, particularly in primate stone-tool cultures (e.g., Whiten et al., 1999).
However, data on the rate and form of stone-throwing behavior indifferent troops within the same monkey species have not beenreported in the literature so far (but see Leca et al., 2007a forgeneral data). From a functional viewpoint, the current SH patterns
observed in Japanese macaques are regarded as a non-instrumental
manipulation of stones with no obvious survival value (Huffman,
1984, but see Nahallage and Huffman, 2007a for a possible ultimate
function of SH). However, Huffman (1996) suggested that if SH
persists sufﬁciently in a given troop, direct material beneﬁts may be
acquired in the future, provided some modiﬁcations of the behavioral patterns or the direct integration of SH with foraging activities(e.g., stone-tool-use) or social interactions (e.g., agonistic display)(Huffman and Quiatt, 1986; Huffman and Hirata, 2003; Leca et al.,2008a). Since stone-throwing is considered tool-use according to
Beck’s (1980) deﬁnition, this particular SH pattern is a strong candidate for such transformations. From this perspective, Japanesemacaques could be used as a non-human primate model for processes that contributed to the evolution of stone-throwing in early
hominids.
In an effort to encourage the compilation of relevant data onstone-throwing in non-human primate species and stimulate
general interest in the evolution of hominid throwing behavior, thispaper will address the following questions: When Japanese macaques throw stones, do they perform an overarm action? Do theystand bipedally? Do they show hand preference? Do they throwfrom an elevated position? How far do they throw? Do they selectparticular stones? Do they aim or do they throw at random as partof a display sequence? Does stone-throwing occur in all troops or isit a group-speciﬁc behavioral practice? Is there evidence for socialtransmission of this behavior among group members? Can stonethrowing in Japanese macaques be referred to as a behavioral
tradition?
In this study of stone-throwing in Japanese macaques, we aim
to: 1) present a systematic multi-group comparison of the frequency and prevalence of this behavior; 2) provide further descriptive and quantitative data on the form of stone-throwing,
including motor patterns, postures, handedness, throwing location,
direction, and distance, as well as the number and size of stones
thrown; 3) document the contexts of occurrence of stone-throwing
events and propose functional explanations for this behavior; and
4) investigate the channels and modes of intra-group diffusion ofstone-throwing with regards to age, sex, and dominance classes.
Materials and methods
Subjects and study conditions
We observed a total of 10 troops of Japanese macaques (Macaca
fuscata) at six geographically isolated sites in Japan (Table 1). Captive
troops were supplied with commercial primate pellets, vegetables,or fruits. Free-ranging troop members gathered regularly around
feeding sites where they were artiﬁcially provisioned with cereal
grains by the staff technicians of the Koshima Field Station, Kyoto
University (Kosh.) or by the staff members and managers of monkey
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J.-B. Leca et al. / Journal of Human Evolution 55 (2008) 989–998
Table 1
Ranging condition and location of the 10 study troops
Troop full name(abbreviated name)Study site
Ranging
conditiona

Arashiyama A (Ara.A)

CP

Wakasa A (Wak.A)

CP

Takahama (Takh.)

CPJapan Monkey Centre (JMC) CP
Koshima (Kosh.)
Arashiyama E (Ara.E)

FR
FR

Shodoshima A (Sho.A)

FR

Shodoshima B (Sho.B)

FR

Takasakiyama B (Tak.B)

FR

Takasakiyama C (Tak.C)

FR

aPrimate Research Institute, Inuyama,
Aichi prefecturePrimate Research Institute, Inuyama,
Aichi prefecturePrimate Research Institute, Inuyama,
Aichi prefecture
Japan Monkey Centre Inuyama,
Aichi prefecture
Koshima Islet, Miyazaki prefecture
Iwatayama Monkey Park,
Arashiyama, Kyoto prefecture
Wild Monkey Park, ShodoshimaIsland, Kagawa prefecture
Wild Monkey Park, Shodoshima Island,
Kagawa prefecture
Takasakiyama Natural Zoo, Takasakiyama,
Oita prefecture
Takasakiyama Natural Zoo, Takasakiyama,
Oita prefecture

CP: captive (large outdoor enclosure); FR: free-ranging.

parks (Ara.E, Sho.A, Sho.B, Tak.B, and Tak.C). The free-ranging troops
living at the same site (Sho.A and Sho.B at Shodoshima, and Tak.B
and Tak.C at Takasakiyama) had overlapping home ranges and cameinto occasional contact. Although stone availability was highlyvariable according to the study site, we found no signiﬁcant correlation between site-speciﬁc stone availability and SH frequency(Leca et al., 2008b).
The daily observation period was between 7:00 am and 6:00
pm, divided into one-hour blocks, and observations were roughly
equalized across the blocks. Visibility was excellent since captive
troop members could be sampled from observation platforms
overhanging the enclosures, with no major obstacles blocking theview, and free-ranging troop members could be approached andsampled within 3–5 m. This research was conducted in accordancewith PRI’s Rules and Guidelines for Animal Health and Welfare.
Data collection procedure
As Hopkins et al. (2005) pointed out, since throwing in animals
is a rare and somewhat unpredictable behavior, the methods ofdata collection can be very ﬂexible. Like most other surveys on
throwing behavior in non-human primates (e.g., Goodall, 1964;
Hamilton et al., 1975; Visalberghi, 1993; Nakamichi, 1998; Hopkins
et al., 2005; Wittiger and Sunderland-Groves, 2007), this study ofstone-throwing in Japanese macaques was based on opportunistic
observations. In conjunction with focal and group scan sampling(cf. Leca et al., 2007a for further detail on these observational
methods), the throwing events were also collected by all occurrence sampling (data set #1 collected by JBL and NG on the 10
troops from August 2003 through February 2005) and ad libitum
sampling (data set #2 collected by CADN on the Takh. troop fromMay 2003 through December 2006; cf. Altmann, 1974). All occurrence sampling (also referred to as ‘conspicuous behavior recording’ by Martin and Bateson, 1993) was made possible because
throwing behavior meets the three criteria set by Altmann (1974):
1) observation conditions are excellent, 2) throwing events arehighly ‘attention-attracting,’ and 3) throwing events never occur
too frequently to record.
A throw was considered to occur any time an individual picked
up a stone from the ground, released it with an active swinging
movement of the forelimb, and propelled it through the air ina ballistic motion. The movement of the forelimb differentiates thisbehavior from dropping, pushing, or kicking down a stone from an
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991

off-ground position. Subjects were never encouraged to throw for
the purpose of this study, but instead observations were made on
spontaneous stone-throwing behaviors.
For each throwing event reported here, the three observers
recorded the date, the identity of the thrower, and the throwing
variant (throw, throw and jump, throw and sway, or throw and run:cf. Leca et al., 2007a). Regarding data set #1, JBL and NG also systematically recorded whether the individual threw the stone: 1)
from a position located on or off the ground; 2) from a tripedal,
bipedal, or sitting posture; 3) overhand or underarm; 4) with its leftor right hand; 5) forward, backward, upward, or sideways; and 6) ata distance of less than 1 m, 1–3 m, 3–5 m, or greater than 5 m. They
also recorded the number of stones thrown and an estimation of
their sizes (highest dimension of a stone) according to four size
categories: S1 (2–10 mm), S2 (11–50 mm), S3 (50–100 mm), and S4(more than 100 mm; cf. Leca et al., 2008b). To evaluate the contexts
or situations that may elicit the throwing behavior, JBL and NG
recorded the activity of the thrower 15 seconds before throwing aswell as the occurrence and location of major intra-group and external disturbances (e.g., aggressive interactions, and loud noise,respectively).
In a good proportion of cases (71 out of 83 throwing events, i.e.,
85% of the cases), all these data were dictated as verbal comments
on video-recorded focal samples, even when the thrower was not
the focal subject (cf. Martin and Bateson, 1993). In the remainingcases (12 out 83 throwing events, i.e., 15% of the cases), these data
were collected by pen and paper (cf. Leca et al., 2007a for a detailed
description of the observation procedure used in the study of SH
behaviors). In Table 2, we present information on data set #1 collected in each troop. Regarding data set #2, CADN did not systematically collect the above mentioned data on how the individual
threw the stone. Depending on the type of analyses, these data
were pooled with data set #1 or not (see below).
Data analysis
We deﬁned the total troop observation time as the total time inhours spent observing each troop, including focal time, scan time,
and time spent collecting all occurrence samples and ad libitum
data. When multiple observers were present (i.e., during focal andad libitum sessions), two types of observation time were distinguished and summed. First, observation time during focal sessions
was subject-based and calculated by adding up the focal hours the
subjects were observed. Second, observation time during ad libitum sessions was observer-based and calculated by adding up thetimes each observer viewed the subjects. We veriﬁed interobserver reliability using the kappa coefﬁcient of Cohen (1960).
Based on individual identities, activities, and interactions, we foundk ¼ 0.92.
For only some of the study troops (Ara.A, Wak.A, Takh., Kosh.,and Ara.E) were all members identiﬁable. In the troops whereindividual identities of all members were not known during theobservation (JMC, Sho.A, Sho.B, Tak.B, and Tak.C), only subjects that
could be reliably recognized, based on obvious morphological criteria retrieved from video records (e.g., scars, broken ﬁnger), wereused in the analyses requiring individually sampled subjects (Lecaet al., 2008a). For the purpose of analyses, we distinguished three
age classes, namely ‘‘young’’ (1–3 years), ‘‘growing’’ (4–10 years),and ‘‘grown-up’’ (11 years and greater; Leca et al., 2007b). In eachtroop, there were individuals belonging to all age and sex classes,with the exception of Ara.A, where the age class labeled as‘‘growing’’ was missing (Leca et al., 2007b).
Individuals over one year of age were ranked in a dominancehierarchy according to the direction of agonistic interactions. We
carried out hierarchical rank order analysis with the aid of Matman,
Noldus, a software program that calculates Landau’s linearity index

992

J.-B. Leca et al. / Journal of Human Evolution 55 (2008) 989–998

Table 2
Data set #1 collected in the 10 studied troopsa
Troop

Study period

Ara.A
Wak.A
Takh.
JMC
Kosh.
Ara.E
Sho.A
Sho.B
Tak.B
Tak.C

Sep–Dec 2003
Aug–Nov 2003
Sep–Dec 2003b
Aug 2003–Apr 2004
Jan–Feb 2004
May–Aug 2004
Feb 2005
Feb 2005
Dec 2003–Jan 2004
Dec 2003–Jan 2004

TOTAL

Troop size

No. subjects
sampled ingroup scansc

No. subjects
indivitually
sampledd

18
19
46
102
88
141
450
350
438
676

18  018  145  195  647  1377  22227  48
156  22299  31394  51

18
19
46
76
61
132
55
54
74
172

2,328

1,376  195

707

Total troop
observation
time (hr)No. SH
records

Percentage ofindividuals observed
throwing

Observed
frequency ofthrowing

Expected
frequency ofthrowing

179.9
224.6
449.2
99.1
339.7
431.3
77.6
51.5
22.8
73.8

43
345
1,536
212
30
1,031
167
97
134
573

0
5
24
2
0
0
0
0
0
0

0
2
83
2
0
0
0
0
0
0

1.9
2.4
11.9
5.6
9.4
19.6
10.4
4.7
4.0
17.1

1,949.5

4,168

n/a

87

87.0

a

Frequency is deﬁned as the total number of occurrences. Expected values are derived from a total of 87 throw events recorded in the 10 troops and weighted by the mean
number of scan sampled subjects and the total troop observation time. n/a ¼ not applicable.
b
Data set #1 only.
c
Mean values  SD.
d
In focal, all occurrence, and ad libitum samples.

(h’), which is corrected for ties and unknown relationships (de Vries
et al., 1993). We veriﬁed the linearity of the dominance hierarchy
for 46 individuals belonging to the Takh. troop (h’ ¼ 0.52, directional consistency index ¼ 0.97, p < 0.001; cf. de Vries, 1995). We
distinguished three classes of individuals according to their dominance rank: high-ranking, middle-ranking, and low-ranking individuals (n ¼ 15, 16, and 15, respectively). Based on 354 hours ofsubject-focal samples collected in the Takh. troop, we calculated
the afﬁliation scores within each of the 1,035 possible dyads byadding up the duration of body contact and the time spent within
one meter proximity. According to the afﬁliation score, we distinguished three types of dyads (n ¼ 345 dyads for each type): weakly
afﬁliated dyads (afﬁliation score: mean  SD ¼ 0.3  0.4 min),moderately afﬁliated dyads (3.3  1.5 min), and strongly afﬁliateddyads (26.0  41.9 min).
Stone handling activity was deﬁned as the manipulation ofstones by performing at least one of the 36 behavioral patterns
listed in Table 3 (Leca et al., 2007b). We deﬁned ﬁve classes ofprevalence of SH patterns, namely widespread (when the pattern
was observed in more than 50% of individually-sampled troop
members), common (between 20 and 50%), scarce (between 5 and20%), idiosyncratic (between 0 and 5%), and absent (0%). A SH episode collected by focal or ad libitum sampling was referred to asa SH record. Individuals that were observed to throw a stone at least
once were categorized as throwers, and those that were neverobserved to throw a stone were categorized as non-throwers. The
activities of the thrower 15 seconds before throwing were ascribed
to ﬁve categories (after Kortlandt and Kooij, 1963): 1) inactive(resting and grooming), 2) locomotion, 3) stone handling, 4) social
or locomotor play, and 5) disturbance-related vigilance.
To characterize hand preference in throwing, we did not use thehandedness index (HI) because of its total insensitivity to sample
size (cf. McGrew and Marchant, 1997; but see Hopkins et al., 1993,
considering that a single observation of throwing per subject is
sufﬁcient to evaluate individual hand preferences). Instead, weused binomial tests (two-tailed) at the individual and populationlevels with a minimum of six data-pointsdthat is, at least six
throws per subject to allow subjects to be tested for lateralization,
and at least six lateralized subjects to allow populations to be tested
for lateralization (cf. McGrew and Marchant, 1997). After suchtesting, subjects reaching statistical signiﬁcance were categorized
as left- or right-handed, depending on the direction of the difference, and those failing to reach statistical signiﬁcance were categorized as ambilateral. Subjects with less than six throws wereclassiﬁed as unknown.

We used data set #1 to: conduct inter-troop comparisons;provide quantitative data on throwing postures, directions, anddistances; estimate the size of stones thrown; and assess the context of throwing events. We used data sets #1 and 2 to: report theidentity of throwers; provide quantitative data on throwing variants, the number of stones thrown, and handedness; and assess
throwing dissemination in the Takh. troop. With the exception ofa few iterative throws, most throws were not consecutive events,
but instead were separated by long periods of time on the order ofhours or even days. On temporal grounds, we believe that the occurrence of a throwing event was not likely to bias the chances ofthe occurrence of another equivalent throwing event. Thus,
throwing events could be considered independent data-points,
allowing statistical tests based on pooled data to be conducted.
To evaluate the inﬂuence of different contexts on the number ofthrows observed, we conducted a Friedman test followed by multiple paired comparisons based on mean ranks (cf. Siegel andCastellan, 1988). To test the effect of sex and dominance or age on
throwing rate, we used Mann-Whitney and Kruskal-Wallis tests,
respectively. To test the difference between the observed andexpected distributions of throwing frequencies in the study troops,
we used a chi-square goodness-of-ﬁt test. We used chi-square tests
of independence from contingency tables to test the associations
between: 1) throwing distance and throwing direction, posture, orvariant; 2) the size of the stones thrown and the size of the stones
used in other SH patterns; 3) throwing direction and the location of
the disturbance source; and 4) age, sex, and dominance classes andthe distribution of throwers and non-throwers. For post-hoc
examination of chi-square tests, we calculated the adjusted standardized residuals and considered statistically signiﬁcant those zscores that were  j1.96j. The Yates’ correction for continuity wasincorporated into chi-square tests. Statistical analyses were performed using the SPSS 12.0 analytical program. Signiﬁcance levels
were set at a ¼ 0.05.
Results
Stone-throwing as a troop-speciﬁc behavior
When considering data set #1, we found striking inter-troop
differences in the frequency of stone-throwing. Throwing eventswere recorded 83 times in the Takh. troop, whereas the behavior
was recorded only twice in the Wak.A troop and twice in the JMC
troop. Stone-throwing was never recorded in the other troops.
After weighting the data by the number of sampled subjects and212

J.-B. Leca et al. / Journal of Human Evolution 55 (2008) 989–998
Table 3
Inter-troop differences in the prevalence of the 36 major SH patterns categorizedaccording to general activity pattersn (after Leca et al., 2007b)
Category name

Troop
Ara.A Wak.A Takh. JMC Kosh. Ara.E Sho.A Sho.B Tak.B Tak.C

Investigative activities
Bite
S
Hold/pickC
LickS
Put in mouth
S
Move inside mouth A
SniffS
Locomotion activities
Carry
A
Carry in mouth
A
Grasp walkS
Move andA
push/pull
Toss walk
S

W
W
W
W
C
W

W
C
W
W
C
W

S
S
I
I
I
S

S
S
I
A
A
S

S
C
S
S
I
C

S
C
A
S
A
I

I
S
A
S
A
I

S
S
S
S
I
C

S
S
S
I
I
C

S
C
C
S

C
C
W
C

S
I
S
S

S
A
I
I

C
I
W
S

C
I
C
I

S
I
S
S

C
I
C
I

C
I
C
S

S

W

S

A

S

A

A

I

I

W
W
W
W
C
S

S
I
S
I
A
A

S
I
S
I
A
A

W
W
W
W
I
S

C
C
C
S
I
A

C
C
C
S
A
A

C
C
W
C
S
I

C
C
C
C
S
S

C
C

S
I

A
A

A
S

I
A

I
I

S
A

I
I

C
S

S
A

A
A

S
A

I
A

S
A

S
A

C
I

C
C
W
W
C

A
S
S
C
I

A
A
I
I
A

I
I
C
C
W

A
I
C
C
S

A
A
S
C
C

I
A
C
C
C

A
S
C
C
C

W
I
W
I
S
I
S

S
A
S
I
I
A
I

S
A
I
A
A
A
A

C
A
W
I
A
A
I

S
A
C
A
A
A
I

I
A
C
I
A
A
I

S
A
C
I
A
A
A

S
A
C
I
A
A
A

I
C

A
I

A
A

I
A

A
A

A
A

I
A

S
A

S

I

A

S

A

A

A

A

Collection (gathering) activities
CuddleC
W
GatherS
C
Grasp with hands S
W
Pick upCC
Pick and dropA
A
Pike up smallAAstonesComplex manipulative activities
Clack
S
S
Combine withAC
objectFlint
A
C
Flint/rub/tap
AS
in mouthFlip
AS
Pound on surface A
S
Roll in hands
SC
Rub/roll on surface C
W
Rub stonesAC
together
Rub with hands
SC
Rub with mouth
A
S
ScatterS
C
Shake in hands
A
A
Slap
A
A
Spin
A
A
Stone groom,AC
put on fur
Swipe
A
S
Throw
A
I
(all variants)
Wash/put in water A
A

W ¼ Widespread (pattern observed in more than 50% of individually-sampled troop
members); C ¼ Common (20<– 50%); S ¼ Scarce (5<– 20%); I ¼ Idiosyncratic(0<– 5%); A ¼ Absent (0%).

the total observation time in each troop to obtain expected
throwing frequencies, we found a statistically signiﬁcant difference
between the observed and expected distributions of throwing
frequencies in the 10 study troops (chi-square goodness-of-ﬁt test,
df ¼ 9, c2 ¼ 493.7, p < 0.001; cf. Table 2). In the Takh. troop, theobserved frequency of throwing was considerably greater than the
expected frequency, whereas the reverse was found in the othertroops, and particularly in large and/or long-observed troops (Ara.E,
Sho.A, and Tak.C).
Interestingly, the Takh. troop also presented the largest numberof SH records. It could be argued that the observed frequency ofthrowing may simply reﬂect the number of SH records collected ina given troop. Although we could not statistically test this correlation (due to the large number of zero values in the former dataset), we found no sign for such a tendency. For example, there wasno stone-throwing event in the 1,031 SH records of the Ara.E troop
and in the 573 SH records of the Tak.C troop.
213

993

We also found major inter-troop differences in the prevalence ofstone-throwing in comparison with the other 35 SH patterns
reported in Japanese macaques (Table 3). ‘‘Throw’’ is the only SH
pattern that is common in one troop (i.e., observed in about a fourthof sampled individuals [Takh.: 11 throwers out of 46 individuals, or
24% of troop members in data set #1, and 14 throwers out of 46
individuals, or 30% of troop members in data sets #1 and 2]),whereas it was idiosyncratic in two other troops (JMC: two
throwers out of 102 individuals, or 2% of troop members, and
Wak.A: one thrower out of 19 individuals, or 5% of troop members),
and absent in most other troops (0% in Ara.A, Kosh., Ara.E, Sho.A,
Sho.B, Tak.B, and Tak.C).
By contrast, most other SH patterns were either widespread and/or common in two or more troops (e.g., ‘‘sniff’’: bring a stone near to
one’s nose and sniff it; ‘‘grasp walk’’: walk with one or more stonesin the palm of one or both hands; ‘‘cuddle’’: grab or cradle a stone
against the chest; and ‘‘roll in hands’’: roll a stone in one’s hands), or
scarce and/or idiosyncratic in some troops but absent in the others(e.g., ‘‘pick up small stones’’: pick up small stones and hold thembetween ﬁngertips; ‘‘ﬂint in mouth’’: strike a stone against another
held in mouth; ‘‘shake in hands’’: take stone(s) in one’s open palm
hand and shake the stone(s) with the hand moving back and forth;and ‘‘wash’’: put a stone in water or pick up a stone from water andrub it with hands). Finally, a few other SH patterns were widespreador common in one troop, and scarce or idiosyncratic in several
others (e.g., move and push, clack, pound on surface, and stone
groom). These ﬁrst analyses show that stone-throwing as a common
behavioral practice is speciﬁc to the Tahk. troop.
Form of the stone-throwing behavior
Throwing styles and postures. With the exception of two throws, allthrowing events recorded in the Takh. troop from data set #1
consisted of a stone being picked up from the ground and released
with an underarmed shoveling movement of one forelimb. Of 83
throws, only two overhand throwing actions (2.4%) were observed.
There was no obvious preparation phase before throwing, deﬁned
as the movement of the forelimb up and away from the next
throwing direction (cf. Wood et al., 2007).
Despite individual differences, Table 4 shows that most throws
were performed from a tripedal posture (75.9%), as opposed to bipedal (21.7%) and sitting postures (2.4%). Only two individuals,
a young female and a growing male, maintained a bipedal posturealmost as often as a tripedal posture while throwing. The only twooverhand throws were performed from a sitting posture. Most
throwing events occurred from a position located on the ground (77out 83 throws, i.e., 92.8%) where the subjects spent about threequarters of their time (72.7% for the Takh. troop: see Leca et al., 2008b).
Four throwing variants. In their comprehensive list of the 45 SH
patterns performed by Japanese macaques, Leca et al. (2007a)distinguished four throwing variants. Here, we provide a moredetailed description of each of these variants: 1) throw and jump:
the stone-throwing behavior is accompanied (preceded and/or
followed) by repeated vertical leaps performed from a tripedal
stance; 2) throw and sway: the stone-throwing behavior is accompanied (preceded and/or followed) by a rapid and exaggerated
swaying (i.e., standing and shifting body weight from side to side)or tossing (i.e., rocking head and upper torso back and forth in thevertical plane while the hindlimbs remain stationary); 3) throw andrun: the stone-throwing behavior is accompanied (preceded and/or
followed) by a rapid backward running while scattering about otherstones or pieces of food present on the ground; and 4) throw: throwa stone without jumping, swaying, or running.
The four throwing variants were observed several times in the
Takh. troop (Table 4), with a large majority of ‘throw and jump’ (64.7%

994

J.-B. Leca et al. / Journal of Human Evolution 55 (2008) 989–998

Table 4
Distribution of stone-throwing events and quantiﬁcation of throwing form in throwers from the Takh. troop according to age, sex, dominance class, and ranked in chronologicalorder of their ﬁrst observed throwing behavior (date in month/day/year)a
Individual Age (yr)/ sex Dom. class First obs.b No. throwsb Throwing variantb

Sora
TsuyudHaiiro
Kakoo
Taked
Peke
Yama
Sakura
Kaede
Aod
Mizu
Taiyo
Oka
Kiro

16/F
19/F
5/M
3/F
15/F
6/M
12/F
2/F
2/F
22/M
1/M
3/M
2/M
8/M

Uncertain –
Total

LR
HR
HR
MR
HR
MR
HR
MR
LR
HR
LR
MR
MR
HR

08/04/03
09/01/03
09/04/03
09/10/03
09/10/03
10/12/03
10/19/03
10/26/03
10/28/03
11/13/03
11/14/03
12/11/03
06/14/04
08/05/04

–

–

2
9
7
30
30
12
1
9
2
6
1
2
3
2

Throwing posturec

Throwing directionc

Throwing distancec (m)Handednessb

TH

TJ

TS

TR

Tp

Bp

Sit

Fw

Bw

Uw

Sw

<1

1–3

3–5

>5

L

0
5
0
14
1
1
0
0
2
0
1
2
1
0

2
2
4
15
29
9
1
9
0
6
0
0
0
0

0
0
2
1
0
2
0
0
0
0
0
0
0
2

0
2
1
0
0
0
0
0
0
0
0
0
2
0

1
8
5
9
20
7
–
2
2
5
0
1
–
–

0
0
1
12
0
5
–
0
0
0
0
0
–
–

0
0
0
0
0
0
–
0
0
0
1
1
–
–

0
0
1
0
0
2
–
0
0
0
0
1
–
–

1
6
3
4
20
0
–
0
0
0
0
0
–
–

0
0
1
11
0
4
–
2
1
5
0
1
–
–

0
2
1
6
0
6
–
0
1
0
1
0
–
–

0
0
0
7
0
2
–
1
2
0
1
1
–
–

0
1
4
10
0
10
–
1
0
0
0
1
–
–

1
1
1
4
1
0
–
0
0
5
0
0
–
–

0
6
1
0
19
0
–
0
0
0
0
0
–
–

0 2 unk
9 0 LH (.004)
0 6 RH (.031)
3 21 RH (< .001)
0 22 RH (< .001)
12 0 LH (< .001)– – unk
0 2 unk
2 0 unk
5 0 unk
1 0 unk1 1 unk–
1 unk
2 0 unk

R

3

3

0

0

0

3

0

0

0

0

3

0

2

0

1

0

–

119

30

77

7

5

63

18

2

4

34

28

17

16

27

14

26

35 55

–

HP (p)unka
TH: throw, TJ: throw and jump, TS: throw and sway, TR: throw and run; Tp: tripedal, Bp: bipedal, Sit: sitting; Fw: forward, Bw: backward, Uw: upward, Sw: sideways; L:number of left-handed throws, R: number of right-handed throws, HP (p): hand preference (and p-value obtained with binomial tests), LH: left-handed, RH: right-handed,
unk: unknown.Uncertain: regarding the thrower identity, there was an uncertainty between two individuals but some elements of the throwing behavior could be recorded.
b
Data sets #1 and 2.
c
Data set #1 only.
dIndividual who was observed throwing before but the exact date is not available.

of the 119 throwing events collected in data sets #1 and 2), and toa lesser extent, ‘throw’ (25.2%). The variants ‘throw and sway’ and‘throw and run’ were notably less frequent at 5.9% and 4.2%, respectively. Six members of the Takh. troop performed at least two
different throwing variants, and among them, four individuals
displayed three different throwing variants. In contrast, only thesimple ‘throw’ variant was performed in the two throwing events
recorded in the Wak.A troop. Out of the two throwing events recorded
in JMC, one ‘throw’ and one ‘throw and run’ were displayed.
Ballistic motion and stones thrown. The stones thrown were propelled through the air according to four different directions: forward, backward, upward, or sideways (Table 4). A stone thrownforward or backward was released more or less horizontally or
followed a slightly curved trajectory. A stone thrown upward was
released more or less vertically (i.e., at about a 45 degree angle orgreater), whereas a stone thrown sideways was released at abouta 45 degree angle or less. Three quarters of throws were directedbackward (41.0% of the 83 throwing events collected in data set #1)
or upward (33.7%), whereas only one quarter of throws were displayed sideways (20.5%) or forward (4.8%). When a stone wasthrown backward, it seemed to be propelled with greater velocity
and force than when thrown forward, upward, or sideways.
Throwing distances ranged from about half a meter (n ¼ 16
throws) to approximately 15 meters (n ¼ 12). To test whether
throwing distance was related to throwing direction, posture, orvariant, we conducted chi-square tests of independence based oncontingency tables representing the frequency of throws at distances of less than 1 m, 1–3 m, 3–5 m, or greater than 5 m among 1)
backward throws versus throws in other directions; 2) throws
performed from a tripedal posture versus throws performed frombipedal and sitting postures; and 3) throws accompanied by jumps,
swaying, and running versus simple throws. We found a signiﬁcantassociation between throwing direction and throwing distance(n ¼ 83 throws, c2 ¼ 60.9, df ¼ 3, p < 0.001). As suggested above,
post-hoc examination of adjusted standardized residuals showedthat backward throws were associated with signiﬁcantly longer
distance projections (more than 5 m) than throws performed inother directions.

We also found a signiﬁcant association between throwing posture and throwing distance (c2 ¼ 25.8, df ¼ 3, p < 0.001), withlonger throws performed from a tripedal posture than from bipedal
and sitting postures. Finally, throwing variant and throwing distance were signiﬁcantly linked (c2 ¼ 10.2, df ¼ 3, p ¼ 0.017), withthrows accompanied by jumps, swaying, and running associatedwith longer distance projections than simple throws.
Out of the 119 throwing events collected in data sets #1 and 2,
one stone was thrown in 113 throws (95.0%) and two stones werethrown in 6 throws (5.0%). In the latter, the two stones were throwniteratively during two successive throwing events. We compared
the size of the stones thrown with the size of the stones used insome of the most representative SH patterns in the Takh. troop (cf.
Leca et al., 2008b) and drawn from a same-sized data subset. The
stones thrown were signiﬁcantly bigger than the stones used toperform the following SH patterns: ‘‘cuddle’’ (n ¼ 83 throws,c2 ¼ 35.6, df ¼ 3, p < 0.001); ‘‘grasp with hands’’ (c2 ¼ 41.2, df ¼ 3,
p < 0.001); ‘‘roll in hands’’ (c2 ¼ 44.5, df ¼ 3, p < 0.001); ‘‘rub/roll on
surface’’ (c2 ¼ 49.9, df ¼ 3, p < 0.001); and ‘‘sniff’’ (c2 ¼ 29.3, df ¼ 3,
p < 0.001). Post-hoc examination of adjusted standardized residuals showed that S3 stones were more often thrown than usedduring these SH patterns, whereas S2 stones were more often usedin these SH patterns than thrown.
Handedness. In all throwing events, only one hand was used. No
two-handed throws were observed. Among the ﬁve throwers forwhich hand preferences could be statistically evaluated, two individuals were categorized as left-handed (moreover, both werealways left-handed, i.e., they used their left hand for 100% ofthrows) and three individuals were categorized as right-handed(among which two were always right-handed). There were no
ambilateral subjects (Table 4). With only ﬁve lateralized subjects
the troop could not be statistically tested for lateralization. However, an overall comparison of the distributions of left-handed
versus right-handed throws was not consistent with a clear grouplevel handedness. When throwing from a bipedal posture, righthanded throws were twice as many as left-handed throws (12versus 6 throws, respectively), but this difference was not statistically signiﬁcant (binomial test, p ¼ 0.238, two-tailed).
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Stone-throwing as a display behavior
Context of throwing. We found a statistically signiﬁcant effect of thecontext on the throwing frequency (Friedman test, n ¼ 12, df ¼ 4,
c2 ¼ 12.9, p ¼ 0.012). Multiple paired comparisons based on meanranks showed that an individual was signiﬁcantly more likely tothrow a stone immediately after being engaged in disturbance-related vigilance activity than after being engaged in resting/grooming, locomoting, and stone handling activities (p < 0.05).
Figure 1 shows that throwing was also more frequent under vigilance circumstances than in playing contexts, although the latter
difference did not reach statistical signiﬁcance (p > 0.05).
Despite individual behavioral differences, stone-throwing wasseemingly performed as part of a response to various sources ofdisturbance, including loud noise produced by Japanese military
aircrafts ﬂying very low over the Primate Research Institute inpractice maneuvers, and intra-group aggressive interactions. Under
such circumstances, the thrower showed obvious signs of excitement. However, stone-throwing was never accompanied by vocalizations and never recorded in individuals directly involved in an
aggressive interaction (i.e., the initiator or the recipient of anaggression).
Unaimed throwing. Several elements drawn from the observations
support the view that stone-throwing in the Takh. troop was
unaimed in the sense that stones were not thrown directionally: 1)
the stone was generally not propelled in the direction of what may
be perceived to be a potential danger: there was no signiﬁcantassociation between throwing direction (upward versus roughly
horizontal [i.e., forward, backward, and sideways]) and the generallocation of the disturbance source (above the ground [i.e., aircrafts]
versus on the ground [i.e., aggressive interactions]) (n ¼ 39 throws
associated with external disturbances, c2 ¼ 0.2, df ¼ 1, p ¼ 0.863);
2) the percentage of forward throws was small (4.8%); 3) thethrower generally threw a stone from the spot where the stone waspicked up, and was not often observed carrying a stone from one
place to another before using it for throwing; 4) there was no apparent preparation phase and the thrower seldom looked up orback at a possible target before or after throwing (Leca, pers.
observ.); and 5) no thrown stones ever hit a monkey.
Intra-group diffusion of the stone-throwing tradition
Age, sex, and social status of the throwers. There was no signiﬁcanteffect of age, sex, and dominance classes on the distribution ofthrowers and non-throwers in the Takh. troop (N ¼ 46 individuals,
age: c2 ¼ 1.2, df ¼ 2, p ¼ 0.551; sex: c2 ¼ 1.5, df ¼ 1, p ¼ 0.379;*

45

Number of throws

40

*

*

30
25
20
15
10
5
0
Locomotion

Stone handlingdominance: c2 ¼ 1.4, df ¼ 2, p ¼ 0.490). Although the number ofthrowing events observed per subject ranged from 1 to 30, the 14
throwers recorded in the Takh. troop belonged to all classes, males
or females, low-, middle- or high-ranks, and were from one to 22
years of age (Table 4). Therefore, stone-throwing was not limited toparticular individuals based on these life history features or social
status.
Despite striking individual differences in the frequency ofthrowing events, this frequency was not signiﬁcantly affected by
the age and sex of throwers (age: Kruskal-Wallis test, c2 ¼ 0.3,
df ¼ 2, p ¼ 0.861; sex: Mann-Whitney test, z ¼ -0.778, p ¼ 0.456).
Although throwing frequencies in middle- and high-ranking individuals (mean  SD ¼ 11.2  11.3 and 9.2  10.6, respectively)
were higher than in low-ranking individuals (1.7  0.6), this difference did not reach statistical signiﬁcance (Kruskal-Wallis test,
c2 ¼ 4.0, df ¼ 2, p ¼ 0.133).
Propagation over time of the throwing behavior. The exact date andcircumstances of appearance of the stone-throwing behavior in the
Takh. troop are unknown. Based on 492 hours of data collected inthis troop during another study conducted from July 2002 throughJuly 2003, throwing events were very rare and only observed invery few older-aged individuals: Take (13–15 years), Tsuyu (17–19
years), and Ao (20–22 years; Rizaldi, pers. comm.). According to the
137 hours of observation done by CADN between May and July
2003, stone-throwing was not observed in the other troop members before August 4th, 2003. Table 4 shows the extent and chronology of observed propagation of the throwing behavior from thisdate.
Within a 12-month period, stone-throwing had been acquiredby 11 more troop members in other age classes. Even if we do notconsider the three individuals who were observed throwing before
August 2003, the acquisition of the behavior seemed to occur
within strongly afﬁliated dyads, and in ﬁts and starts (i.e., at least
two new stone-throwers could be recorded during short periods oftime punctuated with longer periods during which no new thrower
was recorded). For instance, Haiiro and Kakoo, as well as Peke andYama, who had relatively high afﬁliation scores (36.4 and 23.6 min,respectively), were ﬁrst observed throwing during the same week,
respectively. Sakura and Kaede, who were peer playmates (afﬁliation score ¼ 36.9 min), were ﬁrst observed throwing within a twoday period. Moreover, the performance of the rare ‘throw and run’variant by a mother (Tsuyu) and her offspring (Oka, afﬁliation
score ¼ 35.7 min) is suggestive of vertical transmission. Finally,stone-throwing appears to be a long-enduring SH variant that was
still maintained in the Takh. troop in 2007 (Nahallage, pers.
observ.).
Discussion

35

Inactive (resting,grooming)

995

Social/locomotor play

Disturbancerelated vigilance

Throwing context (thrower's activity within 15 sec before throwing)
Fig. 1. Effect of the context on the number of stone-throwing events recorded in Takh.
(*: p < 0.05).

215

Our descriptive and quantitative data on the form and contexts
of stone-throwing in Japanese macaques show that throws weremainly underarm, performed on the ground from a tripedal posture, and often accompanied by repeated vertical leaps. Generally,
one relatively big (50–100 mm) stone was thrown at a time, andpreferentially projected backward or upward and to heights of 15
meters. We found marked individual hand preferences for throwing, but no consistent handedness at the group level. Although
there was no evidence for aimed throwing, stone-throwing eventswere more likely to occur during periods of disturbance than inother contexts, and throws were probably performed as part ofa display sequence.
Even though a larger sample size would allow further analyses at
the individual level, our data suggest that stone-throwing in Japanese macaques meets several criteria which represent evidence fora behavioral tradition (cf. Perry and Manson, 2003): 1) based on the996

J.-B. Leca et al. / Journal of Human Evolution 55 (2008) 989–998

lack of previous reports on spontaneous stone-throwing in a socialgroup of Japanese macaques and according to the present comparative evidence, we consider this behavior to be speciﬁc to thecaptive Takahama troop housed at the Kyoto University Primate
Research Institute, although it is ecologically possible at other sites(cf. Leca et al., 2008b); 2) there were individual preferences in someof the four stone-throwing variants (i.e., similar behaviors withminor alterations in their form; 3) stone-throwing is conspicuousand attention getting, and naı̈ve individuals are likely to have intently observed others performing the behavior before ﬁrst exhibiting it themselves; 4) the behavior was observed to spread within
the group from one age class to another (here vertically from older
to young); 5) the transmission of the behavior seems to be sociallymediated since its dissemination happened in accordance withlinks via maternal kinship and social proximity; and 6) stonethrowing behavior has been maintained in the Takahama troop
over a number of years and has even passed from one generation to
the next. It should be noted that evidence for the last three criteria
were based on case studies of few individuals rather than systematic analysis.
With regards to the form of stone-throwing, our results support
the hypotheses relating body posture, throwing style, and handedness in throwing (Calvin, 1983; Fifer, 1987; Knüsel, 1992; Hopkins
et al., 2005). Like most non-human primates reported to throw
objects, and particularly other terrestrial cercopithecines, such as
chacma baboons (Papio ursinus: Hamilton et al., 1975), Japanesemacaques mainly exhibited underarm throwing from a tripedal
posture. When a tripedal monkey performs stone-throwing, thehand is placed on the stone palm down and the stone can be tossed
in different directions (mainly backward in our case). Froma structural point of view, such underarm scooping is an action very
close to ‘‘normal locomotion,’’ being only a minor change from theusual swing of the limb in walking (Washburn and Jay, 1967).
During the throwing action, there is little movement at the shoulder, the propulsive force being generated mainly by the hand, wrist,and forelimb. According to Washburn and Jay (1967), overhand
throwing is impossible for most primates because they maintaina tripedal rather than a bipedal posture. Interestingly, we foundthat occasional overhand throws from an erect stance can occur inJapanese macaques. Likewise, in chimpanzees, body posture wasrelated to throwing style, with most subjects standing bipedally
while throwing overhand, whereas most underarm throws occurred from a tripedal stance (Hopkins et al., 2005).
The marked individual hand preferences for unaimed throwing
found in this study are consistent with those reported in three
Japanese macaques trained to throw stones directionally into a pipe
to obtain food as part of an instrumental conditioning experiment(Tanaka et al., 2001). Strong individual hand preferences for aimed
stone-throwing were also found in capuchins (Westergaard andSuomi, 1994, 1995), chimpanzees (Hopkins et al., 1993), and humans(Calvin, 1983). Our results on the lack of clear group-level handedness in Japanese macaques are in agreement with those obtainedin capuchins and chimpanzees (Westergaard et al., 2000; McGrew
and Marchant, 2001). In contrast, the strong right-hand bias foundin human populations is often explained by the specialization of theleft brain for the sequential-movement skills needed to ﬁnely
control facial and hand muscles used in language and throwing,
respectively (Calvin, 1983; Annett, 2002; Hopkins et al., 2005).
Regarding the functional aspects of the behavior, throwing objects randomly as part of an agonistic display is considered the mostcommon tool-use in non-human primates according to Beck’s(1980) deﬁnition. As predicted by Huffman (1996), and unlike mostother SH patterns performed by Japanese macaques, unaimed
stone-throwing observed in the Takahama troop during periods of
disturbance and in conjunction with agonistic signals typical of thisspecies (e.g., bouncing or swaying; cf. Modahl and Eaton, 1977) canbe regarded as a spontaneous tool-using behavior. Although it is
difﬁcult to quantify the outcome of stone-throwing performances
during agonistic displays (in terms of intimidation effectiveness or
dominance assertion), we consider two direct beneﬁts. First, due tothe sight of a stone propelled through the air and the sound generated by a stone hitting against the concrete surfaces of the enclosure walls and ﬂoor, the stone thrown can be characterized asa ‘‘technological ampliﬁer’’ (cf. Guilmet, 1977) or bimodal (visualand auditory) extension of the non-vocal display. As suggested forcapuchins and chimpanzees (Nishida et al., 1999; Moura, 2007), theincorporation of stones into agonistic display is likely to be an effective means of capturing the attention of an otherwise inattentive
social audience and augmenting the effect of the behavior. Second,since stone-throwing is often part of display sequences, there islittle doubt that this behavior is ‘‘emotionally loaded’’ (Boesch andBoesch, 1981) and an expression of general excitement that may
serve as a mechanism of tension reduction linked to disturbances.
There are at least two other possible explanations for this behavior. First, as observed in young chimpanzees (Goodall, 1986), ourdata suggest that stone-throwing by young members of the Takahama troop may serve to initiate social play by attracting theattention of peer playmates (but see Shimada, 2006). Second, whenno obvious context (i.e., resting or grooming) could be reliably related to stone-throwing, we cannot rule out the possibility that themonkeys may simply enjoy performing this behavior and the soundassociated with it. The idea of throwing as a pleasurable activity inanimals and humans has often been discussed (Darlington, 1975;
Calvin, 1983). Although pleasure is difﬁcult to isolate and measure,the possible emotional process involved in throwing behavior may
have physiological, hormonal, or neurological correlates that canreasonably be considered reinforcing components of the behavior.
We currently have no additional data that would further support
the latter interpretations. Nevertheless, all these explanations ofstone-throwing are not mutually exclusive. As suggested by thecross-site observations of the leaf-clipping behavior in chimpanzees, the same behavior can have different functions depending on
the context in which it is performed in different groups (Nishida,1980; Boesch, 1995, 1996).
Although we did not ﬁnd obvious behavioral patterns of stoneselection before throwing, the apparent preference for relatively
large stones for throwing (as opposed to other typical SH patterns)
is congruent with the tendency of stone-tool selectivity previously
suggested in Japanese macaques (Weinberg and Candland, 1981;
Tanaka et al., 2001). The preferential use of large stones forthrowing or banging has also been observed in brown capuchins,chacma baboons, and chimpanzees (Hamilton et al., 1975; Nishida
et al., 1999; Moura, 2007). The ability to categorize stone-tools
according to their physical characteristics and functional properties
has been attributed to several non-human primate species (Boesch
and Boesch, 1983; Cleveland et al., 2003; Evans and Westergaard,2004). Whether the stones used are modiﬁed or not (like in percussive or throwing behaviors, respectively), stone-selectivity is
widespread among animals, and may be regarded as the ﬁrst
evolutionary steps to primate tool-making in general, and hominid
stone-technology in particular (cf. Kortlandt and Kooij, 1963; Isaac,
1987; McGrew, 1992; Mercader et al., 2007).
Although throwing behavior is a component of the Japanesemacaque repertoire (Torigoe, 1987), spontaneous throwing is
generally not reported, even in studies focusing on object manipulation and social play in this species (e.g., Menzel, 1966; Shimada,2006). In the rare reports of throwing in Japanese macaques, thisbehavior was either idiosyncratic or its performance was restricted
to a very few group members. In another semi-free ranging Oregon
troop, a male incorporated unaimed throwing of stones into his
courtship displays, but stone-throwing never spread to otherindividuals (Eaton, 1972). Despite the invention by a female
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Japanese macaque of the stone-throwing technique as a food-getting solution in an instrumental task, the behavior spread to only
four group members during the following years (Tanaka et al.,2001). In contrast, stone-throwing in the Takahama troop waslargely distributed among group members of all classes rather than
exclusively restricted to a particular subset of the group (e.g.,dominant adult males or juveniles).
How can we explain the speciﬁcity of stone-throwing prevalence in the Takahama troop, as opposed to the absencedor idiosyncratic presencedof this behavior in other troops of Japanesemacaques? Among environmental factors, stone availability andfood provisioning are not likely to account for such a difference (cf.
Leca et al., 2008a,b). Instead, the existence of a group-speciﬁcstone-throwing tradition may reﬂect possible inter-troop variationin 1) the likelihood of behavioral innovations, 2) the social constraints on the early dissemination and long-term maintenance ofsuch inventions, and 3) appropriate social and/or environmental
reinforcement for continued practice and spread of an innovation(cf. Huffman and Hirata, 2003).
First, it is acknowledged that captive conditions may provide themonkeys with more free time than free-ranging conditions. Moretime available could lead to more opportunities for the explorationof stone by individuals, which in turn may result in a greater diversity in SH patterns, some potentially implanted in tool-use(Huffman and Quiatt, 1986). This interpretation is supported by thepresent results showing that the three troops in which stonethrowing was observed at least once were housed in captive settings, and previous ﬁndings showing that the troop with thehighest rates of stone-throwing, namely the Takahama troop, wasalso the troop exhibiting the most diverse SH repertoire (Leca et al.,2007a). The performance of bouncing, swaying, or tossing patterns
as behavioral responses to external disturbances was observed inseveral captive troops of Japanese and rhesus macaques (Modahl
and Eaton, 1977; Nahallage, pers. observ.). Such forms of display
seem to be common traits to these two macaque species. However,
our results suggest that, although stones are available in all of thesetroops, they seem only to be incorporated into agonistic displays bytroops in which SH is already an established behavioral tradition.
Second, chance may account for a good number of behavioral
innovations (Reader and Laland, 2003). Thus, the following isa reasonable scenario: since a Takahama troop member spends, on
average, more time with stones in its hands than a member of othercaptive troops (Leca et al., 2007a), it is more likely to have at least
once accidentally released and propelled a stone through the air
during an agonistic interaction or a playing episode. When stones
are thrown, individuals in the line of trajectory will often moveaside to avoid being inadvertently hit (Nahallage, pers. observ.).
This reaction of others to stone-throwing, if recognized by thedisplayer, may encourage it to repeat the behavior for the same
effect in the future. This would in turn make this individual likely to
become a stone-throwing initiator for others.
Third, although social inﬂuence on the dissemination of stonethrowing was not quantiﬁed in this study, it is possible to imagine
that, once invented, social conditions particular to the Takahama
troop, such as a relatively relaxed dominance style, may haveallowed numerous group members to perform stone-throwing
even when higher-ranking individuals were nearby. With moreavailable stone-throwing demonstrators, naı̈ve individuals werelikely to have more opportunities to observe and learn the novel
behavior, thereby facilitating its spread within the group. On theother hand, previous ﬁndings suggest that when a behavioral
practice is restricted to very few group members or individuals
with a particular social status, the behavior is likely to disappear at
the group level (Candland et al., 1978; Nishida et al., 1999; Lecaet al., 2007c). Because younger individuals have been observed tointegrate throwing into playful stone handling contexts, it is likely
217

997

to spread more widely within the group. Unfortunately, since we
did not witness the appearance and initial dissemination of thestone-throwing behavior, we can only speculate about the emergence of the stone-throwing tradition. Further investigation, including experimentally-elicited stone-throwing, may help todetermine the learning process by which this behavior is transmitted within the group.
To our knowledge, this is the ﬁrst study to report a stone-tooluse tradition in Japanese macaques, and to address a single type of
behavior in a non-human primate species, by taking a multi-troop
comparative approach, presenting analyses borrowed from physical anthropology (in terms of motor patterns, body postures,
handedness, and ballistic motion), exploring a psychological perspective (motivational aspects of throwing behavior), and discussing a longitudinal view (dissemination over time of the throwing
tradition). Overall, our ﬁndings are consistent with the comparative
data using modern non-human primate species to model thestructural processes and functional aspects of throwing evolution
in early hominids.
Our results and interpretations also support the view that tooluse evolves in stages from initially non-functional behaviors, suchas object play (Beck, 1980; Huffman and Quiatt, 1986), a categorization that perfectly suits the SH activity (Huffman, 1984). Foodprovisioning and captivity have relaxed selective pressures on
foraging and created favorable environmental conditions underwhich SH may simply serve the function of maintaining in some
populations a set of behaviors that could evolve into tool-use ina different environment. As an unselected but eventually beneﬁcial
trait, the SH tradition would be an exaptation (cf. Gould and Vrba,
1982). Given the lack of information on spontaneous use of stonetools by macaques (Beck, 1980; but see Malaivijitnond et al., 2007),
this report is of direct relevance to questions regarding the evolution of stone technology in hominids.
Acknowledgments
JBL was supported by a Lavoisier Grant, Ministère des Affaires
Etrangères, France, and a fellowship from the Japan Society for the
Promotion of Science (P 07421). CADN was supported by a scholarship from the Japanese Ministry of Education, Science and Culture
for graduate studies. NG was supported by a National Science
Foundation grant (BCS-0352035). This study would not have beenpossible without the contribution of many people, researchers,
students, staff, and friends, who helped in many ways during thecourse of this research. We wish to thank particularly A. Kato, T.
Matsuzawa, H. Ohsawa, and H. Takemoto (Primate Research Institute), M. Nakamura and Y. Takenoshita (Japan Monkey Centre), F.
Kanchi, A. Mori, and T. Suzumura (Koshima Field Station), K.
Watanabe (Koshima Field Station and Wild Monkey Park, Shodoshima), S. Asaba, S. Hanamura, J. Hashiguchi, T. Kawashima, S.
Kobatake, M. Shimada (Iwatayama Monkey Park, Arashiyama), andH. Kurita (Takasakiyama Natural Zoo). We also thank Rizaldi forproviding valuable information on the Takahama troop. We are
grateful to S. Antón, W.C. McGrew, and G.C. Westergaard for insightful comments on a previous version of the manuscript.
References
Altmann, J., 1974. Observational study of behaviour: sampling methods. Behaviour
49, 227–267.
Annett, M., 2002. Handedness and Brain Asymmetry: The Right Shift Theory.
Psychology Press, Hove, UK.
Beck, B.B., 1980. Animal Tool Behavior: The Use and Manufacture of Tools by Animals. Garland Press, New York.
Boesch, C., 1995. Innovation in wild chimpanzees. Int. J. Primatol. 16, 1–16.
Boesch, C., 1996. Three approaches for assessing chimpanzee culture. In: Russon, A.
E., Bard, K.A., Parker, S.T. (Eds.), Reaching into Thought: The Minds of the Great
Apes. Cambridge University Press, Cambridge, pp. 404–429.

998

J.-B. Leca et al. / Journal of Human Evolution 55 (2008) 989–998

Boesch, C., Boesch, H., 1981. Sex differences in the use of natural hammers by wild
chimpanzees: a preliminary report. J. Hum. Evol. 10, 585–593.
Boesch, C., Boesch, H., 1983. Optimization of nut-cracking with natural hammers bywild chimpanzees. Behaviour 83, 265–286.
Calvin, W.H., 1983. The Throwing Madonna: Essays on the Brain. McGraw-Hill, NewYork.
Calvin, W.H., 1993. The unitary hypothesis: a common neural circuitry for novel
manipulations, language, plan-ahead, and throwing? In: Gibson, K.R., Ingold, T.
(Eds.), Tools, Language, and Cognition in Human Evolution. Cambridge University Press, Cambridge, pp. 230–250.
Candland, D.K., French, J.A., Johnson, C.N., 1978. Object-play: test of a categorized
model by the genesis of object-play in Macaca fuscata. In: Smith, E.O. (Ed.),
Social Play in Primates. Academic Press, New York, pp. 259–296.
Churchill, S.E., Schmitt, D., 2002. Biomechanics in palaeoanthropology: engineering andexperimental approaches to the study of behavioural evolution in the genus Homo.
In: Harcourt, C.S., Sherwood, B.R. (Eds.), New Perspectives in Primate Evolution and
Behaviour. Linnaean Society, Westbury, London, West Yorkshire, pp. 71–102.
Cleveland, A., Rocca, A.R., Wendt, E.L., Westergaard, G.C., 2003. Throwing behavior
and mass distribution of stone selection in tufted capuchin monkeys (Cebus
apella). Am. J. Primatol. 61, 159–172.
Cohen, J., 1960. A coefﬁcient of agreement for nominal scales. Educ. Psychol. Meas.
20, 37–46.
Darlington Jr., P.J., 1975. Group selection, altruism, reinforcement, and throwing inhuman evolution. Proc. Natl. Acad. Sci. U. S. A. 72, 3748–3752.
Dennell, R., 1997. The world’s oldest spears. Nature 385, 767–768.
Eaton, G., 1972. Snowball construction by a feral troop of Japanese macaques(Macaca fuscata) living under seminatural conditions. Primates 13, 411–414.
Evans, T.A., Westergaard, G.C., 2004. Discrimination of functionally appropriate andinappropriate throwing tools by captive tufted capuchins (Cebus apella). Anim.
Cogn. 7, 255–262.
Fa, J.E., Lindburg, D.G., 1996. Evolution and Ecology of Macaque Societies. Cambridge
University Press, Cambridge.
Fifer, F.C., 1987. The adoption of bipedalism by the hominids: a new hypothesis.
Hum. Evol. 2, 135–147.
Goodall, J., 1964. Tool-using and aimed throwing in a community of free-living
chimpanzees. Nature 201, 1264–1266.
Goodall, J., 1986. The Chimpanzees of Gombe: Patterns of Behaviour. Harvard
University Press, Cambridge.
Gould, S.J., Vrba, E.S., 1982. Exaptation–a missing term in the science of form. Paleobiology 8, 4–15.
Guilmet, G.M., 1977. The evolution of tool-using and tool-making behaviour. Man
12, 33–47.
Hall, K.R.L., 1963. Tool-using performances as indicators of behavioural adaptability.
Curr. Anthropol. 4, 479–494.
Hamilton, W.J., Buskirk, R.E., Buskirk, W.H., 1975. Defensive stoning by baboons.
Nature 255, 488–489.
Hopkins, W.D., Bard, K.A., Jones, A., Bales, S.L., 1993. Chimpanzee hand preference inthrowing and infant cradling: implication for the origins of human handedness.
Curr. Anthropol. 34, 786–790.
Hopkins, W.D., Russell, J.L., Cantalupo, C., Freeman, H., Schapiro, S.J., 2005. Factors
inﬂuencing the prevalence and handedness for throwing in captive chimpanzees (Pan troglodytes). J. Comp. Psychol. 119, 363–370.
Huffman, M.A., 1984. Stone-play of Macaca fuscata in Arashiyama B troop: transmission of a non-adaptive behavior. J. Hum. Evol. 13, 725–735.
Huffman, M.A., 1996. Acquisition of innovative cultural behaviors in non-humanprimates: a case study of stone handling, a socially transmitted behavior inJapanese macaques. In: Galef Jr., B., Heyes, C. (Eds.), Social Learning in Animals:
The Roots of Culture. Academic Press, Orlando, FL, pp. 267–289.
Huffman, M.A., Hirata, S., 2003. Biological and ecological foundations of primate
behavioral tradition. In: Fragaszy, D.M., Perry, S. (Eds.), The Biology of Tradition:
Models and Evidence. Cambridge University Press, Cambridge, pp. 267–296.
Huffman, M.A., Quiatt, D., 1986. Stone handling by Japanese macaques (Macaca
fuscata): implications for tool use of stone. Primates 27, 427–437.
Isaac, B., 1987. Throwing and human evolution. Afr. Archaeol. Rev. 5, 3–17.
Knüsel, C.J., 1992. The throwing hypothesis and hominid origins. Hum. Evol. 7, 1–7.
Kortlandt, A., Kooij, M., 1963. Protohominid behaviour in primates (preliminary
communication). Symp. Zool. Soc. Lond. 10, 61–88.
Leakey, L.S.B., 1948. The Bolas in Africa. Man 48, 48.
Leca, J.-B., Gunst, N., Huffman, M.A., 2007a. Japanese macaque cultures: inter- andintra-troop behavioural variability of stone handling patterns across 10 troops.
Behaviour 144, 251–281.
Leca, J.-B., Gunst, N., Huffman, M.A., 2007b. Age-related differences in the performance, diffusion, and maintenance of stone handling, a behavioral tradition in
Japanese macaques. J. Hum. Evol. 53, 691–708.
Leca, J.-B., Gunst, N., Huffman, M.A., 2008b. Of stones and monkeys: testing ecological constraints on stone handling, a behavioral tradition in Japanesemacaques. Am. J. Phys. Anthropol. 135, 233–244.
Leca, J.-B., Gunst, N., Huffman, M.A., 2008a. Variability of food provisioning regimes
and stone handling tradition in Japanese macaques: a comparative study of ten
troops. Am. J. Primatol. 70, 803–813.
Leca, J.-B., Gunst, N., Watanabe, K., Huffman, M.A., 2007c. A new case of ﬁsh-eatingin Japanese macaques: implications for social constraints on the diffusion of
feeding innovation. Am. J. Primatol. 69, 821–828.
Malaivijitnond, S., Lekprayoon, C., Tandavanitj, N., Panha, S., Cheewatham, C.,
Hamada, Y., 2007. Stone-tool usage by Thai long-tailed macaques (Macaca fascicularis). Am. J. Primatol. 69, 227–233.

Martin, P., Bateson, P., 1993. Measuring Behaviour: An Introductory Guide. Cambridge University Press, Cambridge.
McGrew, W.C., 1992. Chimpanzee Material Culture: Implications for Human Evolution. Cambridge University Press, Cambridge.
McGrew, W.C., Marchant, L.F., 1997. On the other hand: current issues in and metaanalysis of the behavioral laterality of hand function in nonhuman primates.
Yearb. Phys. Anthropol. 40, 201–232.
McGrew, W.C., Marchant, L.F., 2001. Ethological study of manual laterality in the
chimpanzees of the Mahale mountains, Tanzania. Behaviour 138, 329–358.
Menzel Jr., E.W., 1966. Responsiveness to objects in free-ranging Japanese monkeys.
Behaviour 26, 130–150.
Mercader, J., Barton, H., Gillespie, J., Harris, J., Kuhn, S., Tyler, R., Boesch, C., 2007.
4,300-year-old chimpanzee sites and the origins of percussive stone technology. Proc. Natl. Acad. Sci. U. S. A. 104, 3043–3048.
Modahl, K.B., Eaton, G.G., 1977. Display behaviour in a conﬁned troop of Japanesemacaques (Macaca fuscata). Anim. Behav. 25, 525–535.
Moura, A.C.de A., 2007. Stone banging by wild capuchin monkeys: an unusual
auditory display. Folia Primatol. 78, 36–45.
Nahallage, C.A.D., Huffman, M.A., 2007a. Age-speciﬁc functions of stone handling,a solitary-object play behavior, in Japanese macaques (Macaca fuscata). Am. J.
Primatol. 69, 267–281.
Nahallage, C.A.D., Huffman, M.A., 2007b. Acquisition and development of stone
handling behavior in infant Japanese macaques. Behaviour 144, 1193–1215.
Nakamichi, M., 1998. Stick throwing by gorillas (Gorilla gorilla gorilla) at the San
Diego Wild Animal Park. Folia Primatol. 69, 291–295.
Nishida, T., 1980. The leaf-clipping display: a newly-discovered expressive gesturein wild chimpanzees. J. Hum. Evol. 9, 117–128.
Nishida, T., Kano, T., Goodall, J., McGrew, W.C., Nakamura, M., 1999. Ethogram andethnography of Mahale chimpanzees. Anthropol. Sci. 107, 141–188.
Perry, S., Manson, J.H., 2003. Traditions in monkeys. Evol. Anthropol. 12, 71–81.
Reader, S., Laland, K.N., 2003. Animal Innovation. Oxford University Press, Oxford.
Savage-Rumbaugh, S., Fields, W.M., Tagliatela, J.P., 2001. Language, speech, tools andwriting: a cultural imperative. J. Conscious. Stud. 8, 273–292.
Schaller, G.B., 1963. The Mountain Gorilla: Ecology and Behavior. The University of
Chicago Press, Chicago.
Schmitt, D., Churchill, S.E., Hylander, W.L., 2003. Experimental evidence concerning
spear use in Neandertals and early modern humans. J. Archaeol. Sci. 30, 103–114.
Shimada, M., 2006. Social object play among young Japanese macaques in Arashiyama, Japan. Primates 47, 342–349.
Siegel, S., Castellan, N.J., 1988. Nonparametric Statistics for the Behavioral Sciences.
McGraw-Hill, Singapore.
Struhsaker, T., 1975. The Red Colobus Monkey. The University of Chicago Press,
Chicago.
Tanaka, I., Tokida, E., Takefushi, H., Hagiwara, T., 2001. Tube test in free-ranging
Japanese macaques: use of sticks and stones to obtain fruit from a transparent
pipe. In: Matsuzawa, T. (Ed.), Primate Origins of Human Cognition and Behavior.
Springer-Verlag, Tokyo, pp. 509–518.
Thierry, B., Singh, M., Kaummans, W., 2004. Macaque Societies: A Model for the
Study of Social Organization. Cambridge University Press, Cambridge.
Tokida, E., Tanaka, I., Takefushi, H., Hagiwara, T., 1994. Tool-using in Japanesemacaques: use of stones to obtain fruit from a pipe. Anim. Behav. 47, 1023–1030.
Torigoe, T., 1985. Comparison of object manipulation among 74 species of nonhuman primates. Primates 26, 182–194.
Torigoe, T., 1987. Object manipulation in a captive troop of Japanese monkeys(Macaca fuscata): a developmental analysis. Primates 28, 497–506.
Visalberghi, E., 1993. Tool use in a South American monkey species: an overview of
the characteristics and limits of tool use in Cebus apella. In: Berthelet, A.,
Chevaillon, J. (Eds.), The Use of Tools by Human and Non-human Primates.
Clarendon Press, Oxford, pp. 118–135.
de Vries, H., 1995. An improved test of linearity in dominance hierarchies containing unknown or tied relationships. Anim. Behav. 50, 1375–1389.
de Vries, H., Netto, W.J., Hanegraaf, P.L.H., 1993. Matman: a program for the analysis
of sociometric matrices and behavioural transition matrices. Behaviour 125,157–175.
Washburn, S.L., Jay, P.C., 1967. More on tool-use among primates. Curr. Anthropol. 8,
253–257.
Watson, N.V., 2001. Sex differences in throwing: monkeys having a ﬂing. Trends
Cogn. Sci. 5, 98–99.
Weinberg, S.M., Candland, D.K., 1981. ‘‘Stone-grooming’’ in Macaca fuscata. Am. J.
Primatol. 1, 465–468.
Westergaard, G.C., Kuhn, H.E., Babitz, M.A., Suomi, S.J., 1998. Aimed throwing asa means of food transfer between tufted capuchins (Cebus apella). Int. J.
Primatol. 19, 123–131.
Westergaard, G.C., Liv, C., Haynie, M.K., Suomi, S.J., 2000. A comparative study of
aimed throwing by monkeys and humans. Neuropsychologia 38, 1511–1517.
Westergaard, G.C., Suomi, S.J., 1994. Aimed throwing of stones by tufted capuchinmonkeys (Cebus apella). Hum. Evol. 9, 323–329.
Westergaard, G.C., Suomi, S.J., 1995. Stone-throwing by capuchins (Cebus apella):a model of throwing capabilities in Homo habilis. Folia Primatol. 65, 234–238.
Whiten, A., Goodall, J., McGrew, W.C., Nishida, T., Reynolds, V., Sugiyama, Y., Tutin, C.E.G.
, Wrangham, R.W., Boesch, C.,1999. Cultures in chimpanzees. Nature 339, 682–685.
Wittiger, L., Sunderland-Groves, J.L., 2007. Tool use during display behavior in wildcross river gorillas. Am. J. Primatol. 69, 1307–1311.
Wood, J., Glynn, D.D., Hauser, M.D., 2007. The uniquely human capacity to throw
evolved from a non-throwing primate: an evolutionary dissociation between
action and perception. Biol. Lett. 3, 360–364.

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Int J Primatol (2008) 29:795–806
DOI 10.1007/s10764-008-9268-3

Environmental and Social Factors Associatedwith the Occurrence of Stone-Handling Behavior
in a Captive Troop of Macaca fuscata
Charmalie A. D. Nahallage & Michael A. Huffman

Received: 14 June 2007 / Accepted: 1 September 2007 /Published online: 6 June 2008
# Springer Science + Business Media, LLC 2008

Abstract Stone-handling, a documented behavioral tradition in Japanese macaques(Macaca fuscata), occurs in both captive and provisioned free-ranging troops. We
utilize data systematically collected as part of a broader investigation of stonehandling behavior in a captive troop to elucidate the environmental and social factors
responsible for its occurrence. We analyzed contexts of stone-handling over 18 mo
to determine under what conditions individuals most often perform it. There is clear
seasonal variation in the occurrence of stone-handling. The lowest number andshortest duration of stone-handling bouts were in winter, gradually increasing to apeak in summer, and again decreasing toward autumn. Monkeys stone-handled more
on clear sunny days than on cloudy or rainy ones. They displayed the behavior lessunder stressful conditions caused by human intervention or by aggression among
troop members. Such stressful social conditions appeared to decrease individual
motivation for stone-handling. In other words, individuals most frequently
performed stone-handling under more relaxed environmental and social conditions.
The findings are consistent with the hypothesis that stone-handling is a form ofsolitary object play behavior in macaques.
Keywords behavioral tradition . Macaca fuscata . object play . stone-handling

Introduction
Animals acquire new behaviors via innovation and learning. Two well-known
examples of behavioral innovation are sweet-potato washing in Japanese macaques(Macaca fuscata: Kawai 1965) and milk bottle opening by British titmice (Fisher
and Hinde 1949). The behaviors spread among other group members to become
long-lived behavioral traditions. Tradition is a behavioral practice that is relatively
C. A. D. Nahallage (*) : M. A. Huffman
Section of Ecology, Department of Ecology and Social Behavior, Primate Research Institute,
Kyoto University, 41–2 Kanrin, Inuyama Aichi 484–8506, Japane-mail: nahallag@pri.kyoto-u.ac.jp

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long lasting, i.e., performed repeatedly over time, and is shared among members of agroup in part via social learning (Perry and Manson 2003).
From the perspective of cultural primatology, it is of interest to understand thefactors that influence a change in the occurrence of a behavioral tradition over time
because it may inform something about the nature or function of the behavior itself.
For example, after acquisition, does an individual perform the behavior at the same
frequency all the time or does it vary according to the age or sex of the individual, agroup’s ranging condition (captive vs. wild), or different seasonal or otherenvironmental conditions? Bernstein (1972, 1975, 1976, 1980) and Bernstein and
Baker (1988) reported the influence of diurnal, temperature, and other weather
conditions on the activity patterns of captive primates. Hanya (2004), Isbell andYoung (1993), Maruhashi (1981), Vasey (2005), Rasoazanabary (2006), Watanuki
and Nakayama (1993), and Yotsumoto (1976) conducted similar research on thevariation of activity patterns under different environmental conditions of freeranging primates. Several factors may affect an individual’s performance of abehavior, which may change with time of day or season. Thus, overlooking suchinformation by sampling a behavior for only a short duration, or looking at it from alimited age/sex/class subgroup of the population, can bias our interpretation of abehavior’s function or the reason for its occurrence.
Individual or social characteristics such as age, sex, and stress caused byaggression among troop members or by human interference can contribute tochanges in the frequency with which a behavior is performed. For example, in all
forms of play —solitary, object, social— the frequency of occurrence changes due toage, sex, habitat, feeding conditions, season, and weather condition (Baldwin and
Baldwin 1977; Fedigan 1972; Hall 1998; Kummer 1971; Nahallage and Huffman
2007a; Pellis 1991, 2002; Poirier and Smith 1974; Poirier et al. 1978; Starin 1990).
In addition, animals experiencing stress are less likely to engage in play-related
activities (Aldis 1975; McCune 1992; Poole and Fish 1975). Knowing the effects ofthese factors should make it easier to understand the function or proximate
motivation for practicing the behavior.
We tested environmental and social factors affecting stone-handling, a form ofsolitary object play behavior in Macaca fuscata (Huffman 1984). Stone-handling is aform of object play in Candland’s terminology (1978), and Fagen (1981) defines
object play as “divertive interactions with an inanimate object… including
exploratory manipulation” (p. 45). Stone-handling occurs in 4 captive troops and
11 provisioned free-ranging troops across Japan (Leca et al. 2007; Nahallage andHuffman 2007a). Stone-handling is the repetitive manipulation of stones in many
ways, e.g., gather, clack, strike together, scatter, etc. (Huffman 1984, 1996). Thoughstone-handling has no obvious immediate survival value, primates have practiced it
in Arashiyama and Takasakiyama since 1979 (Huffman 1984, 1996; Huffman and
Hirata 2003) and in Takahama for ca. 25 yr (Nahallage 2005). There are significant
group- and age-related behavioral differences in stone-handling (Huffman 1996;
Leca et al. 2007; Nahallage and Huffman 2007a). Infants acquire the behavior fromtheir mothers within the first 6 mo of their lives, and the presence of inter- andintratroop variations in the occurrence, frequency, prevalence, and form of stonehandling has led researchers to consider it a behavioral tradition in Macaca fuscata(Huffman 1996; Leca et al. 2007; Nahallage and Huffman 2007b).
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In long-term surveys of the provisioned free-ranging Arashiyama and Takasakiyama
troops, Huffman (1984, 1996) described stone-handling as object play that occurs underrelaxed environmental and social conditions. Conversely, Nishie (2002) proposed thatthe emotional conflict between feeding and aggression avoidance at feeding time werethe main proximate factors for stone-handling. However, in captive groups there is no
association between feeding time and the occurrence of stone-handling (Leca et al.
2004; Nahallage and Huffman 2007a). Clearly, stress during feeding of provisioned
food is not a consistent proximate factor inducing stone-handling by macaques.
We systematically investigated the effects of environmental and certain social
factors on the occurrence of stone-handling behavior. We tested the prediction thatstone-handling occurs under relaxed environmental and social conditions and notstressful ones.

Methods
Focal GroupWe conducted our study at the Kyoto University, Primate Research Institute, Inuyama.
We selected a captive stone-handling troop of Macaca fuscata for ease of detailed
systematic observations. The captive Takahama troop live in a 960-m2 outdoor
enclosure. The troop comprised 48 monkeys of different age-sex classes (Table I).
They ate monkey chow daily between 1000 h and 1100 h; sweet potatoes twice perweek; and occasionally fruits, grains, and vegetables whenever available. They could
drink water ad libitum. The enclosure contained climbing structures, swings, andaluminum sleeping boxes (Nahallage 2005; Nahallage and Huffman 2007a). Of the48 subjects, 45 handled stones and we used them all in analyses (Table I).
Data Collection
We used 2 sampling methods for data collection: continuous focal individual
sampling and instantaneous scan sampling (Altmann 1974). Before starting a focal
observation or a scan, we noted the weather condition as sunny, cloudy, or rainy. We
recorded temperature and humidity via a digital thermometer that automaticallyrecorded the data every 30 min. We recorded each focal session for 15 min via aTable I Age –sex distributionof Takahama groupAge-class category

Number ofindividuals

Number of verified
stone handlers

Adult males (>10 yr)
Adult females (>7 yr)
Adolescent males (5–9 yr)
Adolescent females(5–6 yr)
Juvenile males (1–4 yr)
Juvenile females (1–4 yr)
Infant males (0–1 yr)
Infant females (0–1 yr)

1
18
5
0

1
15
5
0

9
7
3
5

9
7
3
5

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digital video camera (Sony Digital Handycam). Before and after each focal session,
we performed scans to record the major behavioral activities of the troop as a control
for average troop activity patterns at that time of the day: prefocal and postfocal
scans. We recorded resting, feeding, foraging, locomotion, grooming, playing, object
handling, stone-handling, aggression, and other. We recorded all other observations
ad libitum.
We started data collection of the troop in June 2003 and continued until
November 2004. We observed all members of the group equally during all seasons(spring: March–May; summer: June–August; autumn: September–November;
winter: December–February) to determine possible seasonal effects on stonehandling. The daily observation time depended on daylight length, which varied
according to season (spring: 0700–1800 h, 11 focals/individual; summer: 0700–
1900 h, 12 focals/individual; autumn: 0700–1800 h, 11 focals/individuals; winter:
0700–1600 h, 9 focals/individual). We divided the daily observation schedule into
1-h time blocks and sampled individuals randomly in each block. We collected equal
numbers of focal samples for each individual in all time periods of the day in every
month of each season to avoid sampling bias of certain age-sex classes and possible
seasonal differences. We sampled each individual 43 times and obtained 878
observation hours (Nahallage 2005). Our analyses are based on 578 stone-handlingbouts recorded from 45 individuals. A bout is the continuation of the behavior withpauses of ≤120 s, which is the duration after which further stone-handling issignificantly less likely to recur (Huffman 1996). If stone-handling resumed after>120 s, we treated it as a separate bout.
Data Analysis
We analyzed video focal records of stone-handling and noted the time and day of thestone-handling bout, weather conditions, duration and frequency of stone-handlingbouts, activities of a stone handler immediately before and after a stone-handlingbout, and the troop activity budget during a bout. We performed 2-tailed
nonparametric tests via SPSS (version 10), and set significance at p≤0.05.

Results
Effect of Season and Daily Weather Conditions
There is a significant seasonal difference in the number of stone-handling bouts
performed by individuals (Friedman: χ2 =26.57, df=3, p<0.001, n=45). Multiple
pairwise comparisons between seasons (Siegal and Castellan 1988) show asignificant difference between summer and winter (p<0.05), but not between
autumn and spring, autumn and summer, autumn and winter, spring and summer, or
spring and winter. The lowest numbers of stone -handling bouts occurred in winterand the highest in summer (Table II).
The average duration of stone-handling bouts varied across seasons (Table II).
There is a statistically significant seasonal difference in the duration of bouts(Friedman: χ2 =26.48, df=3, p<0.001, n=45). In winter, with the lowest average
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799

Table II Average temperature, humidity, and stone-handling bouts in each season

Temperature (°C)
Humidity
Total number of bouts
Frequency of bouts/h
Average time per bout (s)WinterSpringSummerAutumn2.96(–4.1–4.6)
72.35(24.6–100)
74
0.69
90.12

15.19
(2.8–26.9)
60.99(15.4–100)
150
1.11
116.7627.89(22.8–34.4)
71.74(44.2–94.2)
200
1.34
138.0615.73(6.6–24.4)
71.48(23.8–100)
154
1.14
103.88temperatures (min., –4.1°C; max., 14.6°C), the number of total stone-handling bouts
were the lowest and short in duration, while the number of bouts and durations werehighest in summer when average temperatures were highest (min., 22.8°C; max.,
34.4°C). There is a statistically significant positive correlation between the average
daily temperature and the number of bouts (Spearman ρ rS=0.150, p=0.037, n=195).
Daily weather conditions also appear to influence directly the frequency of stone
handling activity. Regardless of season, there is a statistically significant differencein the number of an individual’s stone-handling bouts in different weather conditions(Friedman: χ2 =68.96, df=2, p<0.001, n=45). Multiple pairwise comparisonsamong 3 weather conditions show a significant difference between sunny andrainy and sunny and cloudy (p<0.05), but not between rainy and cloudy. Individuals
handled stones more frequently on sunny (84%, 487/578 bouts) than on cloudy(12%) or rainy (4%) days.
Effect of Seasonal Variation on Troop Activity Budget
When we analyzed the overall troop activity budget by seasons, there were statisticallysignificant differences in each activity (resting/grooming: Friedman: χ2 =81.03, df=3,
ρ<0.001, n=627; object play: Friedman: χ2 =51.84, df=3, p<0.001, n=627;
locomotion: Friedman: χ2 =371.43, df=3, p<0.001, n=627; aggression: Friedman:
χ2 =25.83, df=3, ρ<0.001, n=627; Fig. 1). Multiple pairwise comparisons for resting/grooming between the seasons show significant differences between summer andautumn, summer and winter, autumn and spring, and winter and spring (p<0.05), but
not between summer and spring or autumn and winter. For object manipulation there
is a significant difference only between summer and winter (p<0.05). For locomotion,
there are significant differences between all 6 combinations of season (summer:
autumn, summer: winter, summer: spring, autumn: winter, autumn: spring and winter:spring; p<0.05). In contrast, there is no significant difference for aggression between
the seasons. Resting/grooming and object handling were lowest in winter and highest
in summer, whereas activities such as locomotion and aggression were highest in
winter and lowest in spring (Fig. 1).
Activity of Focal Stone-handling Individuals Immediately Before
and After Stone-handling
We analyzed the activities each individual performed immediately before astone-handling bout (pre-SH activity) and just after a bout (post-SH activity) to
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C.A.D. Nahallage, M.A. Huffman
Locomotion
Troop activity budget

Troop activity budget

Resting and Grooming
50
45
40
35
30
25
20
15
10
5
0
SummerAutumnWinter

50
45
40
35
30
25
20
15
10
5
0
SummerSpringAutumnWinter50

Object Handling

SpringAggression

Troop activity budget

Troop activity budget

45
50
45
40
35
30
25
20
15
10
5
0

40
35
30
25
20
15
10
5
0

SummerAutumnWinterSpringSummerAutumnWinterSpringFig. 1 Comparison of troop activity budgets in 4 seasons.

determine the possible proximate cause of stone-handling (Fig. 2). There is asignificant difference between the activities individuals performed before starting astone handling bout (Friedman: χ2 =172.50, df=6, p<0.001, n=45; Fig. 2). Multiple
pairwise comparisons between activities show significant differences between
resting and aggression and resting and object manipulation (p<0.05), but not
between any other activity. Resting (55%) was the most common activity in which
an individual engaged just before starting a stone-handling bout. The othermost common activities displayed were foraging (17%) and social play (11%).
The least common activity was aggression (0.6%; Fig. 2). Resting (49%) was again
the most common activity that an individual displayed immediately after stonehandling and foraging (17%), and playing (14%) followed resting (Fig. 2).
60
50
Pre SH Activity
Post SH Activity

40
30
20
10

Behavior

224

ObjectManipulation

Locomotion

Grooming

Aggression

Foraging

FeedingPlay

0
Resting

Percentage frequency

Fig. 2 Activity an individual
performed before and immediately after a stone-handling bout.

Stone-handling in Macaca fuscata
60

Percentage activity

Fig. 3 Troop activity budget
during focal stone-handling boutbased on prefocal and postfocal
scans of the troop.

801

50

Pre Focal Scans

40

Post Focal Scans

30
20
10

Aggression

Object Hn

Stone Hn

Feeding

Foraging

Playing

Walking

Grooming

Resting

0

activity

Effect of Other Troop Members and External Disturbances
We used prefocal and postfocal scans to describe the overall activity of troop members
when a focal individual was handling stones (Fig. 3). Stone-handling occurred mostoften when >50% of the other troop members were resting (Fig. 3). The 2 other mostcommon behaviors at the time were grooming (9%) and feeding (10%). Aggressive
encounters among other troop members in prefocal scans were also relatively
infrequent versus other activities (15%, 351/2361 total focal observations of stone
handlers). There is no statistically significant relationship between prefocal scan troop
aggression and the occurrence of stone-handling in subsequent focal observations (χ2with Yates correction = 2.6887, 2 sided; p=0.1011).
Conversely, drastic external disturbances such as the capture of the whole troop
for their annual health checkup had a profound effect on stone-handling. We
calculated the percentage of occurrence of stone-handling over total focal sessions
per week after the October 2003 medical checkup. A return to normal stone-handlinglevel is gradual, starting with a nearly total absence of stone-handling in the firstweek after capture and release on October 7. The percentage frequencies of stonehandling for the 3 wk after a medical examination are: wk 1: 8% (October 8–14); wk
2: 25% (October 15–21); wk 3: 45% (October 22–30).

Discussion
Environmental and social factors are associated with variation in the occurrence ofstone-handling in Takahama troop. Individuals tended to handle stones more under
milder climatic and less under stressful social conditions. Our findings are consistent
with previous reports from less systematic, albeit long-term surveys of stone-handlingin 2 free-ranging troops at Arashiyama and Takasakiyama (Huffman 1984, 1996).
Environmental factors can be important determinants of when and how frequently
stone-handling occurs. Monkeys handled stones more in summer, when thetemperature was warmer, than in winter; thus, the significant positive correlation
between daily temperature and number of bouts further supports our results.
Similarly, the frequency of stone-handling in our study troop was lowest on rainydays and more frequent in sunny weather conditions. Therefore, our results support
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previous studies of object manipulation by Bernstein, who revealed that object
manipulation rates were higher in hot than in cold weather (geladas; monkeys:
Bernstein 1975; stumptailed macaques: Bernstein 1980; mangabeys: Bernstein
1976; pig-tailed macaques: Bernstein 1972). Likewise, the studies also noted that in
wet or rainy weather conditions, individual proximity to others and inactivity
increased while object manipulation rate decreased noticeably (Bernstein 1975;
Bernstein and Baker 1988). Other activities also show clear seasonal variation,suggesting that not only object manipulation is affected by season and weather
conditions. For example, resting was highest in summer and lowest in winter,indicating that they become less active in hot weather conditions, which is supportedby the low rates of locomotion in summer (Fig. 1). Bernstein (1972, 1980) reported asimilar pattern for captive stump-tailed and pig- tailed macaques. In our focal troops,
aggression was high in both winter and autumn, and low in summer and spring. Low
aggression during summer could partly be a result of inactivity during hot weather
conditions. In Takahama troop, like the Arashiyama and Takasakiyama troops, themating season starts in November and continues until the end of January when many
aggressive encounters occur in the troop, undoubtedly increasing tension among its
members. Social aggression during autumn and winter could also influence the low
rates of object manipulation and high rates of locomotion in the troop (Fig. 1).
Environmental factors, in combination with social factors, clearly can play a key rolein when and how frequently individual macaques handle stones.
Takahama troop’s overall activity budget while individuals displayed stonehandling, and the activities that individuals performed just before starting a stonehandling bout, indicate that they handle stones under relaxed social conditions andnot as a result of aggressive encounters with others or because of other stress-related
conditions. The activity monkeys performed most before stone-handling was resting,with aggression occurring at very low levels. A gradual increase in stone–handlingeach week after the annual medical examination, which entails capture andanesthesia to record body mass and to collect blood samples, further supports theidea that individuals display the behavior less under stressful conditions. It takes a
few weeks for behavioral normality to return, during which individuals are sensitive
to the slightest sounds caused by human activities outside their enclosure. Wheneverthey hear such a sound, they stop what they are doing and walk together around theedge of the enclosure.
Our results are in sharp contrast to conclusions based on the analysis of 21 focal
sessions (30 min each) on 21 adult females at Arashiyama during 2.5 mo in the fall
and winter of 2000–2001 (Nishie 2002). Of the 21 focal adult females, 13 handledstones and 8 did not. Based on analyses of feeding time, aggression directed toothers, self-scratching, and the subjects’ relative rank, Nishie (2002) suggested
emotional conflict between feeding and aggression avoidance by lower-ranking
females as the main proximate factors for the occurrence of stone-handling.
However, there are limits to the inferences that one can draw from that study
because there was a highly skewed age-sex class in subjects (adult females),restricted seasonal data collection (mating season, colder fall and winter months), a
small focal sample size (1 focal observation/individual), and an inflated data baseusing 5 s of stone-handling inactivity instead of the standardized 120 s used in allother systematic studies of stone-handling to quantify bouts (Huffman 1996; Leca et
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al. 2007; Nahallage and Huffman 2007a). Clearly the factors lead to potential biases
that one cannot ignore and limit the potential of any conclusion derived therefrom to
explain proximate factors responsible for stone-handling in general from the data.
Our data are not directly compatible with those of Nishie, making a direct test of his
hypothesis from the results of our study impossible. Nonetheless in 578 stonehandling bouts, we found no relationship between feeding or aggression and theoccurrence of stone-handling. In addition, the fact that in both Arashiyama and
Takahama, >85% and 93% of troop members, respectively, perform stone-handling(Huffman 1996; Nahallage and Huffman 2007a; Huffman and Quiatt 1986), and that
all infants acquire the behavior within the first 6 mo postpartum (Huffman 1996;
Nahallage and Huffman 2007b) contradicts the suggestion that lower-ranking
individuals perform it (Nishie 2002).
A short 5-d study (38 h, 52 focal individuals) in Takasakiyama troop examining theduration of stone-handling by individuals receiving aggression during feeding showedthat they do not handle stones or do so (do not handle stones, n=2/23; handle stones,
n=21/23) for statistically significantly shorter durations (56 s±39.82, range 0–144 s)
than nonaggressed stone handlers did (n=29, 165 s±117.42, range 0–422 s)(Nahallage, unpub. data). Further, the latency period before starting stone-handlingwas significantly greater in aggressed (105 s±100.55, range 7–421 s) versus
nonaggressed (21 s±31.36, range 1–149 s) stone-handlers (Nahallage, unpub. data).
The negative impact of aggression on duration and latency of stone-handling in the
Takasakiyama free-ranging troop and the lack of a relationship between feeding andaggression on stone-handling in our captive in the Takahama troop strongly support
the idea that such object play is most likely to occur under nonstressful conditions.
There are differences in the occurrence of stone-handling between captive andprovisioned free-ranging troops. In captive troops, stone-handling occurs throughout
the day (Nahallage 2005; Nahallage and Huffman 2007a), and in provisioned freeranging troops it occurs soon after provisioning (Huffman 1984, 1996; Leca et al.
2007; Nahallage 2005). For provisioned free-ranging troops, one could reason that
due to a large troop size and less food availability per individual at regular timeintervals, a monkey’s main concern is to gather as much food as possible into its
cheek pouches over the short period it remains in the feeding ground. Once monkeys
gather enough food, they move away from the provisioning ground to start chewing
on the food and to handle stones. No doubt the provisioning situation is stressful, but
it is not proof that individuals handle stones because they are stressed, only that the
behavior occurs more often in provisioned troops after they have obtained food. In
natural situations, when monkeys feed or forage they simultaneously use both theirhands and mouth. However, provisioned free-ranging troops first gather food into
the cheek pouches because of competition and later chew slowly, for which they use
only their mouth. Therefore, they may want to engage in some form of activity with
their hands while they chew. This is one interpretation for why macaques continue tohandle stones until they finish the food in their cheek pouches (Huffman and Quiatt1986), but does not explain the situation for captive troops because there is no
relationship with feeding. An alternative explanation for the occurrence of stonehandling in adults of free-ranging troops, which is consistent with results of bothfree-ranging (Huffman 1984, 1996) and captive troops (Nahallage and Huffman
2007a; this study), is that under the daily routine of gathering food in the restricted
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C.A.D. Nahallage, M.A. Huffman

space of the provisioning grounds, once they have filled their cheek pouches,monkeys disassociate themselves from feeding competition and move away to aquieter place. The relaxed state could heighten their motivation to handle stones,
while they finish the food in their cheek pouches before moving on to forage on
natural vegetation or to socialize with other individuals.
Overall, one can interpret our results as an indication that monkeys perform stonehandling most often under climatically favorable and socially relaxed conditions, as
expected for any form of play behavior. We found no evidence that stone-handlingoccurs as a result of stressful conditions alone. In troops where stone-handling isclosely linked to provisioning of food, it is important to investigate systematicallyand in detail the possible effects of provisioning frequency and food type on theoccurrence and form of stone-handling (Leca et al. in press). Stone–handling occurs
at 11 sites across Japan, in both captive and provisioned free-ranging troops, andfurther extensive investigation and comparison of all factors likely to affect stonehandling is needed that would further clarify the function and nature of stonehandling and the effects of different ecological and social factors responsible forintersite variation in this and other behavioral traditions.
Acknowledgments We conducted the research in accordance with PRI’s Rules and Guidelines for
Animal Health and Welfare. The Japanese Ministry of Education, Science and Culture supported C. A. D.
Nahallage’s graduate studies, of which this study is a part.. We received travel funds from the HOPE
Project, a core-to-core program sponsored by JSPS (Japan Society for the Promotion of Science), topresent this and related work at the 2006 IPS Congress in Entebbe, Uganda and the Social Learning
Conference in St. Andrews Scotland where we benefited from many fruitful comments and criticisms bycolleagues. We thank Drs. J.-B. Leca, A. D. Hernandez, and Andrew MacIntosh for their comments ondata analysis and for commenting on the manuscript. We also thank the faculty and supporting veterinary
staff of the Center for Human Evolution Modeling Research, PRI for facilitating the research and forcaring for the captive monkey troops. We thank the faculty, friends, and students of the Department of
Ecology and Social Behavior for their valuable advice and guidance. Last but not least, we thank the chief
editor and 2 anonymous reviewers for their fruitful comments.

References
Aldis, O. (1975). Play fighting. New York: Academic Press.
Altmann, J. (1974). Observational study of behavior: Sampling method. Behavior, 49, 227–67.
Baldwin, J. D., & Baldwin, J. I. (1977). The role of learning phenomena in the ontogeny of exploration andplay. In S. Chevalier-Skolnikoff, & F. E. Poirier (Eds.), Primate Bio-social Development (pp. 343–406).
New York: Garland.
Bernstein, I. S. (1972). Daily activity cycles and weather influences on a pigtail monkey group. Folia
Primatologica, 18, 390–415.
Bernstein, I. S. (1975). Activity patterns in a gelada monkey group. Folia Primatologica, 23, 50–71.
Bernstein, I. S. (1976). Activity patterns in a sooty mangaby group. Folia Primatologica, 33, 20–45.
Bernstein, I. S. (1980). Activity patterns in a stumptail macaque group (Macaca arctoides). Folia
Primatologica, 33, 20–45.
Bernstein, I. S., & Baker, S. C. (1988). Activity patterns in a captive group of celebus black apes (Macaca
nigra). Folia Primatologica, 51, 61–75.
Candland, D. G., French, D. K., & Johnson, C. N. (1978). Object play: Test of a categorize model by thegenesis of object play in Macaca fuscata. In E. O. Smith (Ed.), Social play in primates (pp. 259–296).
New York: Academic Press.
Fagen, R. (1981). Animal play behavior. New York: Oxford University Press.

228

Stone-handling in Macaca fuscata

805

Fedigan, L. (1972). Social and solitary play in a colony of vervet monkeys (Cercopithecus aethiops).
Primates, 13, 347–64.
Fisher, J., & Hinde, R. A. (1949). The opening of milk bottles by birds. British Birds, 42, 347–57.
Hall, S. L. (1998). Object play by adult animals. In M. Bekoff, & J. A. Byers (Eds.), Animal play:
Evolutionary, comparative and ecological perspectives (pp. 45–60). Cambridge, U.K.: Cambridge
University Press.
Hanya, G. (2004). Seasonal variations in the activity budget of Japanese macaques in the Coniferous forestof Yakushima: Effects of food and temperature. American Journal of Primatology, 63, 165–77.
Huffman, M. A. (1984). Stone play of Macaca fuscata in Arashiyama B troop: Transmission of a nonadaptive behavior. Journal of Human Evolution, 13, 725–735.
Huffman, M. A. (1996). Acquisition of innovative cultural behaviors in nonhuman primates: A case studyof stone handling, a socially transmitted behavior in Japanese macaques. In B. G. Galef Jr., & C.
Heyes (Eds.), Social learning in animals: Roots of culture (pp. 267–289). Orlando, FL: Academic
Press.
Huffman, M. A., & Hirata, S. (2003). Biological and ecological foundations of primate behavioral
tradition. In D. M. Fragaszy, & S. Perry (Eds.), The biology of traditions: Models and evidence (pp.
267–296). Cambridge, U.K.: Cambridge University Press.
Huffman, M. A., & Quiatt, D. (1986). Stone handling by Japanese macaques (Macaca fuscata):
Implication of tool use of stones. Primates, 27, 413–423.
Isbell, L. A., & Young, T. P. (1993). Social and ecological influences on activity budgets of vervet
monkeys and their implications for group living. Behavioral Ecology Sociobiology, 32, 337–385.
Kawai, M. (1965). Newly-acquired pre-cultural behavior of the natural troop of Japanese monkeys on
Koshima islet. Primates, 6, 1–30.
Kummer, H. (1971). Primate societies: Group techniques of ecological adaptations. Chicago: Aldine.
Leca, J.-B., Gunst, N., & Huffman, M. A. (2007). Japanese macaque cultures: Inter- and intra-troop
behavioral variability of stone handling patterns across 10 troops. Behavior, 144, 251–281.
Leca, J.-B., Gunst, N., & Huffman, M. A. (in press). Food provisioning and stone handling tradition in
Japanese macaques: A comparative study of ten troops. American Journal of Primatology DOI
10.1002/ajp.20551
Leca, J.-B., Gunst, N., Nahallage, C. A. D., & Huffman, M. A. (2004). Stone handling as a behavioural
tradition: A comparative study in nine troops of Japanese macaques. In 20th Congress of Primate
Society of Japan (Supplement abstract). Primate Research, 20, 63.
Maruhashi, T. (1981). Activity patterns of a troop of Japanese monkeys. Primates, 22, 1–14.
McCune, S. (1992). Temperament and the welfare of caged cats. Ph.D thesis. University of Cambridge.
Nahallage, C. A. D. (2005). Object Play with Stones in the Captive Takahama Troop of Japanese
Macaques (Macaca fuscata): The Effect of Environmental Factors on Its Occurrence, the Acquisition
Process, Development and Transmission. Master’s dissertation, Kyoto University, Primate ResearchInstitute, Japan.
Nahallage, C. A. D., & Huffman, M. A. (2007a). Age specific functions of stone handling, a solitary object
play behavior in Japanese macaques (Macaca fuscata). American Journal of Primatology, 69, 267–81.
Nahallage, C. A. D., & Huffman, M. A. (2007b). Acquisition and development of stone handling behavior
in infant Japanese macaques. Behaviour, 144, 1193–1215.
Nishie, H. (2002). The proximate factors of stone handling behaviour of Japanese macaques (Macaca
fuscata) in Arashiyama E troop. Primate Research, 18, 225–32 (in Japanese with English abstract).
Pellis, S. M. (1991). How motivationally distinct is play? A preliminary case study. Animal Behavior, 42,
851–3.
Pellis, S. M. (2002). Sex differences in play fighting revisited: Traditional and nontraditional mechanismsof sexual differentiation in rats. Archives of Sexual Behavior, 31, 17–26.
Perry, S., & Manson, J. H. (2003). Traditions in monkeys. Evolutionary Anthropology, 12, 71–81.
Poirier, F. E., & Smith, E. O. (1974). Socializing function of animal play behavior. American Zoologist,
14, 275–87.
Poirier, F. E., Bellisari, A., & Haines, L. (1978). Functions of primate play behavior. In E. O. Smith (Ed.),
Social play in primates (pp. 143–168). New York: Academic Press.
Poole, T. B., & Fish, J. (1975). An investigation of playful behavior in Rattus norvegicus and Mus
musculus (Mammalia). Journal of Zoology London, 175, 61–71.
Rasoazanabary, E. (2006). Male and female activity patterns in Microcebus murinus during the dry season
at Kirindy forest, Western Madagascar. International Journal of Primatology, 27, 437–64.
Siegal, S., & Castellan Jr., N. J. (1988). Nonparametric statistics for the behavioral sciences (pp. 180–183,
2nd ed.). New York: McGraw-Hill.

229

806

C.A.D. Nahallage, M.A. Huffman

Starin, E. D. (1990). Object manipulation by wild red colobus monkeys living in the Abuko Nature
Reserve, The Gambia. Primates, 31, 385–91.
Vasey, N. (2005). Activity budgets and activity rhythms in red ruffed lemurs (Verecia rubra) on the
Masoala Penninsula, Madagascar: Seasonality and reproductive energetics. American Journal ofPrimatology, 66, 23–44.
Watanuki, Y., & Nakayama, Y. (1993). Age differences in activity patterns of Japanese monkeys: Effects
of temperature, snow and diet. Primates, 34, 419–30.
Yotsumoto, N. (1976). The daily activity rhythem in a troop of wild Japanese monkeys. Primates, 17,
183–204.

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American Journal of Primatology 70:1124–1132 (2008)

Research Article
Comparison of Stone Handling Behavior in Two Macaque Species: Implications
for the Role of Phylogeny and Environment in Primate Cultural Variation
CHARMALIE AD NAHALLAGE1,2 AND MICHAEL A. HUFFMAN1
1
Primate Research Institute, Kyoto University, Inuyama, Japan2
Department of Sociology and Anthropology, University of Sri Jayawardenepura, Gangodawela, Nugegoda, Sri Lanka

This study describes the stone handling (SH) behavior of captive rhesus macaques and compares it withthat of a captive troop of Japanese macaques with reference to the relative contributions of phylogenydriven behavioral propensities, environmental differences and socially facilitated learning to theformation of culture. These systematically collected data demonstrate for the first time that two closely
related macaque species might share a common cultural behavior, SH. The rhesus troop displayed SH
behavioral patterns that was already described in Japanese macaque troops. The one exception was a
new pattern not yet seen in any Japanese macaque troop. Differences in the physical environment of thetwo study enclosures may be responsible for some of the variation in observed SH behavioral patterns inthese two troops. These data support the idea that environmental factors can be important for theformation of cultural variation, when the key materials needed to perform the behavior are present inboth habitats (stones). Our results are consistent with the prediction made by Huffman and Hirata [Thebiology of tradition: Models and evidence. Cambridge: Cambridge University Press. p 267–296] that aninteractive triad of phylogenetic, environmental and social factors can be responsible for the formationof cultural variation in primates. Am. J. Primatol. 70:1124–1132, 2008. c 2008 Wiley-Liss, Inc.
Key words: M. fuscata; M. mulatta; behavioral predisposition; object play; environment
gical foundations of culture. Based on the studies ofself-medication in the African great apes and stone
handling (SH) in Japanese macaques, Huffman and
Hirata [2003] predicted that cultural behaviors couldbe ‘‘shared’’ by different populations, between which
cultural transmission is not physically possible,
regardless of whether they are the same species,different subspecies or even closely related species.
They argued that if there is evidence for social
learning in the acquisition and diffusion of aparticular behavior within a group (or species), andthat behavior is present across groups of the same orclosely related species, then phylogeny-driven behavioral propensities and environmental factors (habitat structure, season) could have a positive role in
the occurrence of cultural variation in that behavior.
Very few studies, however, have looked at
putative cultural behaviors shared by two different

INTRODUCTION
Many studies have used inter-population behavioral variation within a species and between subspecies to search for culture in primates [e.g. Galef,
2003; Hohmann & Fruth, 2003; Itani, 1958; Lecaet al., 2007a; McGrew, 1992; Perry et al., 2003; van
Schaik et al., 2003; Whiten et al., 1999, 2001]. Someemphasize that inter-troop cultural differences inbehavior are based solely on social processes [Janson& Smith, 2003; McGrew, 1992; van Schaik et al.,
2003; Whiten et al., 1999, 2001]. It is often difficult,however, to demonstrate the contribution of social
learning in wild populations to the acquisition andtransmission of a specific behavior across generations. In the absence of clear evidence for social
learning in most field studies, caution about attributing culture to behavioral variation has been
voiced, noting that ecological influences (i.e. absenceof conditions for the behavior to occur), genetics orindividual trial and error learning are more parsimonious explanations for observed variation [Galef,
1992; Janik, 2001; Laland & Janik, 2006; Tomasello,
1994]. Perry and Manson [2003] state that the
influence of ecological and genetic factors need not
be completely eliminated for behavioral patterns to
be defined as culture, as long as social influences canbe demonstrated in the acquisition of the behavior.
Others too have discussed the biological and ecolo-r 2008 Wiley-Liss, Inc.

Contract grant sponsor: Japanese Ministry of Education, Science
and Culture.
Correspondence to: Charmalie AD Nahallage, Primate Re-

search Institute, Kyoto University, 41-2 Kanrin, Inuyama, Aichi
484-8506, Japan. E-mail: nahallag@pri.kyoto-u.ac.jp
Received 8 April 2008; revised 21 July 2008; revision accepted 21
July 2008
DOI 10.1002/ajp.20610
Published online 2 September 2008 in Wiley InterScience (www.
interscience.wiley.com).

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Cross Species Comparison of SH / 1125

but phylogenetically close primate species [Hohmann& Fruth, 2003: bonobo-chimpanzees; Huffman and
Hirata, 2003: African great apes, Japanese and longtailed macaques]. To date, no systematic behavioral
study has compared a putative cultural behavior
present in two species to appraise these predictions.
Here, we evaluate this prediction with SH, a known
cultural behavior in Japanese macaques.
SH is one of the best-studied cultural behaviors
in Japanese macaques [Huffman, 1984, 1996; Huffman & Hirata, 2003; Huffman & Quiatt, 1986; Lecaet al., 2007a,b; Nahallage & Huffman, 2007a,b,
2008]. SH is a solitary object play behavior consistingof the manipulation of stones in different ways, e.g.
gather, clack, strike together and scatter [Huffman,
1984, 1996]. Appearance of SH, its initial transmission among other troop members and long-term
diffusion across generations spanning three decades
are well documented for the Arashiyama troop,
where the behavior was first observed in 1979
[Huffman, 1996]. SH consists of a suite of behavioral
patterns that has significant individual as well asinter-group level variation [Leca et al., 2007a;
Nahallage & Huffman, 2007a]. To date, 45 behavioral patterns of SH have been recorded from ten
different populations. Troops that live in close
proximity to each other displayed similar SH
patterns compared with the troops that live apart,
indicating the existence of cultural zones in populations living in close proximity [Leca et al., 2007a].
Furthermore, no major difference was found in theoccurrence and form of SH between the two
Japanese macaque subspecies (Macaca fuscata fuscata and Macaca fuscata yakui) [Leca et al., 2007a].
Socially biased learning plays an important rolein the initial acquisition of SH by infants in bothfree-ranging and captive troops [Huffman, 1996;
Nahallage & Huffman, 2007b]. In a systematic 18month study in the captive Takahama troop at thePrimate Research Institute, Kyoto University, thetiming of acquisition of SH by infants was shown todepend on the level of proximity to the mother, thefrequency of SH performed by the mother and theprior attention paid to the mother’s SH [Nahallage &Huffman, 2007b]. If the mother did not display SH,
the infant only began to do so after proximity to SH
peers increased from around 4–5 months of age[Nahallage & Huffman, 2007b]. Together, the abovementioned studies of SH in Japanese macaques
support Huffman and Hirata’s [2003] predictions
about the interplay of phylogeny, environmental andsocial factors.
In this article, we analyze for the first time SH
behavior in rhesus macaques and compare it with the
Takahama troop of Japanese macaques. We investigated whether there were similarities in the type of
behavioral patterns displayed by the individuals ofthese two species and investigate the possible role ofenvironment for group-level behavioral variation.

METHODS
Subjects and Housing Conditions
Our study was conducted at Kyoto University’sPrimate Research Institute, Inuyama. This research
was approved by and conducted in accordance with
the Primate Research Institute’s Rules and Guidelines for Animal Health and Welfare. The Takahama
captive Japanese macaque troop was housed in a
960 m2 outdoor enclosure. This troop consisted of 48
monkeys of different age–sex classes; the oldest
individual was 30 years of age (Fig. 1). Out of these48 monkeys, 45 were observed to stone handle andthese were all used in our analyses [Nahallage &Huffman, 2007a]. The captive rhesus troop washoused in a 680 m2 outdoor enclosure. The troop
consisted of 29 monkeys of different age–sex classes,
the oldest individual was 11 years of age and thetroop consists of relatively young individuals compared with the Japanese macaque troop (Fig. 1).
Except for four adult monkeys, all rhesus troop
members’ stone handled during their focal sessions
and were used for the analysis. The four adults notincluded were rare stone handlers. We had ad
libitum recordings only to verify that they exhibited
SH. We define young as individuals from newborn to
up to 4 years of age and adult as individuals over 5
years of age [Nahallage & Huffman, 2007a].
The Japanese macaque enclosure was equippedwith metal climbing structures, swings and aluminum sleeping boxes (Fig. 2). Total climbing structurearea was 82.56 m2 (9% of the enclosure) consisting of
118 metal pipes (diameter 5 cm, length 3 to 4 m)
constructed about 30 cm above the ground. The
climbing structures of the rhesus enclosure consistedof wide flat wooden walking structures and logs built
2 m above the ground and connected by bolts andjoints (Fig. 2). Total climbing structure area for therhesus enclosure was 406.88 m2 (60% of the enclosure), consisting of 267 wooden logs (diameter
18–25 cm, length 4–5 m) and 42 flat wooden planks(height  width 5 cm  12 cm, length 3 to 5 m).
Monkeys used these pathways for locomotion, playing, resting, feeding, SH, etc. The ground of theJapanese macaque enclosure had three flat terrace
areas at different elevations separated by two cement
slopes. Stones could only be found on the flat areas(ranging 8  10  7 mm to 92  62  41 mm in size)[Nahallage & Huffman, 2007b]. Although for safety
reasons we did not enter the rhesus enclosure, visualinspection from outside allowed us to conclude that
there was no obvious difference in stone size oravailability between the two study enclosures.
We out rule the possibility of inter-species
observation of SH between these two groups, because
they were located on the opposite sides of theinstitute campus. The possibility that the rhesus
macaques observed other neighboring groups of SH
Japanese macaques cannot be completely out ruled.
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Am. J. Primatol.

1126 / Nahallage and Huffman

A

5

4

3
2
Females
n=30

1

30
29
28
27
26
25
24
23
22
21
20
19
18
17
16
15
14
13
12
11
10
9
8
7
6
5
4
3
2
1
0
Age

B

1

2

3
4
males
n = 18

5

6

3

2
1
females
n=20

11
10
9
8
7
6
5
4
3
2
1
0
Age

1

2
3
males
n= 9

Fig. 1. Histogram of the age sex distribution of the two troops; (A) Japanese macaque troop; (B) rhesus macaque troop (black: verified
stone handlers, gray: verified nonstone handler.

number of observations were made on all membersof the group in all seasons of the year (spring:
March–May; summer: June–August; autumn: September–November; winter: December–February).
Each individual was sampled 43 times, and a totalof 878 observation hours were obtained [Nahallage &Huffman, 2007a]. The analyses presented below forJapanese macaques are based on a total of 578 SH
bouts recorded from 45 individuals. A SH bout isdefined as the occurrence of the behavior with pausesof no longer than 120 sec, the duration after whichfurther SH is significantly less likely to resume[Huffman, 1996]. If SH resumed after more than
120 sec, it was treated as a separate bout.
Data collection of the rhesus group was conducted from December 2003 to August 2004. We
collected data for three seasons (excluding autumn,
owing to the disturbance caused by construction
work on the adjacent enclosure). Each individual was
sampled 30 times on average (SD 5 1.43) and a totalof 363 observation hours were obtained. The analyses presented below for rhesus macaques are basedon a total of 103 SH bouts recorded from 25
individuals.

However, the nearest SH Japanese macaque enclosure is about 5 m away, and the high walls of theenclosures make direct observations of SH in otherneighboring Japanese macaques unlikely. Furthermore, the appearance of SH in the rhesus group has
been suggested by primate care staff Mr. Kiyonori
Kumazaki as coinciding after the construction of theenclosure’s pond in 1998 when stones used in its
construction were left in the enclosure (personalcommunication).
Data Collection
We used continuous focal animal sampling fordata collection [Altmann, 1974]. Each focal session
was video recorded for 15 min using a digital video
camera (Sony Digital Handycam, China). The focal
session was extended if SH was still in progress or
started toward the end of the session. The session
was continued for 5 min after the last contact withstones and terminated thereafter, if there was nofurther contact with stones [Huffman, 1996].
We collected data on the Takahama troop from
June 2003 through November 2004. An equal

Am. J. Primatol.

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Cross Species Comparison of SH / 1127

members and (5) ‘‘absent’’ instead of ‘‘unknown’’,for 0%, considering that we spent 878 and 368 hr
observing Takahama and rhesus groups, respectively. For statistical analysis, we performed twotailed nonparametric tests using SPSS (version 10),and a was set at Pr0.05.
RESULTS
Comparison of Behavioral Patterns Between
Species
There was a difference in the total number of SH
behavioral patterns displayed by the two species. The
rhesus macaque troop displayed 23 patterns,
whereas the Japanese macaque troop displayed 45
patterns. All but one of the 23 rhesus SH behaviors
were displayed by the Japanese macaques (Table I).
In addition, the rhesus macaques had a statisticallysignificant lower SH rate in relation to Japanesemacaques (Mann–Whitney, U 5 304.00, N1 5 45,
N2 5 25, P 5 0.002). Mean SH rate for rhesus andJapanese macaques is 0.5770.44 bouts/hr and1.1870.78 bouts/hr, respectively.
Rhesus macaques displayed a behavioral variant
that has not been observed in any of the ten
Japanese macaque troops studied so far. We called
this behavioral pattern ‘‘insert into a cavity’’ (IC);where a monkey repeatedly inserts and takes out astone from a cavity or the open end of a pipe. Only
five individuals were observed to exhibit this behavior.
When we grouped the 46 behavioral patterns
displayed by one or both macaque species according
to the frequency of occurrence, Japanese macaques
had seven customary behavioral patterns (pick, hold,bite, grasp walk, carry, rub on surface and roll inhand) and five habitual ones (lick, sniff, cuddle, put
in mouth, scatter) (Table I). In rhesus macaques
three behavioral patterns were customary (hold,carry and rub on surface) and five were habitual(pick, bite, lick, put in mouth and grasp walk)(Table I). As the total number of behavioral patterns
displayed was different for each species, we compared the proportions of behaviors displayed. The
proportion of customary behaviors displayed by
Japanese and rhesus species were 13.04 and15.55%, respectively. The proportion of habitual
behaviors displayed by Japanese and rhesus species
were 21.74 and 24.44%, respectively (Table I). Even
though the behaviors ‘‘hold,’’ ‘‘carry’’ and ‘‘rub on
surface’’ were customary in both species, expressedas the mean percentage of behaviors performed byeach troop, they were more common in the rhesus
macaques (rhesus: 23, 11 and 25%, respectively,
Japanese macaques: 15, 3 and 12%, respectively)(Fig. 3(a)). One of the most conspicuous differences
between the two troops was the high percentage of‘‘rub on surface’’ behavior displayed by both young
and adult rhesus macaques (Fig. 3(a, c)).

Fig. 2. Two enclosure structures; (a) Takahama Japanesemacaque enclosure (b) rhesus macaque enclosure.

Data Analysis
From video focal records we calculated theduration and frequency of SH bouts, frequency of
behavioral patterns in each bout, whether SH was asolitary or communal activity (sitting within 1–2 m toa another stone handler or within that individuals
visibility range) and whether it occurred on or off
ground. We grouped the SH behaviors into fivecategories according to their basic motor pattern: (i)investigatory, (ii) locomotion, (iii) collecting/gathering (iv) sound production and (v) combine with
objects and other complex behaviors [Nahallage &Huffman, 2007a]. For the purpose of comparison, wegrouped investigatory, locomotion and collecting/gathering as simple activities, and sound production
and other complex patterns as complex activities [seealso Leca et al., 2007a]. To assess behavioral variantsof SH in each group, we adopted and modified thedefinitions used by Whiten et al. [1999, 2001] andLeca et al. [2007a]. The definitions of occurrence
were (1) ‘‘customary’’ if exhibited by more than 70%
of group members, (2) ‘‘habitual’’ if exhibited by
50–70% of group members, (3) ‘‘present’’ if exhibitedby 25–50% of members, (4) ‘‘rare’’ when exhibited byless than 25% but more than 0% of the group

234

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1128 / Nahallage and Huffman

TABLE I. Frequency of Occurrence of the Stone Handling Behaviors According to Two Species and Age-class. C:
Customary, H: Habitual, P: Present, R: Rare, (–): Absent
Behavioral pattern
Investigative
Pick (PI)
Hold (H)
Bite (B)
Lick (L)Sniff (SN)
Cuddle (CD)Put in mouth (PIM)
Move in mouth (MIM)
Locomotive
Move and push (MP)Grasp walk (GW)
Carry (CA)Carry in mouth (CIM)
Toss walk (TW)
Collecting/gathering
Insert into cavity (IC)Gathering (GA)Pick up (PU)
Pick up small stones (PUS)
Pick up and drop (PUD)
Grasp with hands (GH)Sound producing activities
Rub on surface (ROS)
Roll in hands (RIH)
Rub together (RT)
Scatter (SC)Clacking (CL)
Rub with hands (RWH)
Pound on surface (POS)
Slapping (SL)Rub with mouth (RWM)
Rub in mouth (RIM)
Tap in mouth (TIM)
Flinting (FL)
Flip (F)Swiping (SW)
Flint in mouth (FIM)
Combination with other objects and complex activities
Put in water (PIM)
Wrap in leaves (WIL)
Rub on fur (ROF)
Combine with objects (COO)
Throw (TH)Stone groom (SGR)
Shake in hand (SIH)
Wash (W)
Spin (SP)Throw and sway (TS)Jump and throw (JT)Run and throw (RAT)
Total number
No. of simple behaviors
No. of complex behaviors

Am. J. Primatol.

MacacamulataMacacafuscata

Adult
(M.m)

Adult
(M.f)

Young
(M.m)

Young
(M.f)

H
C
H
P
H
R
H
R

C
C
C
H
H
H
H
P

P
C
P
H
H
–
P
R

C
C
C
H
H
R
H
P

C
C
C
P
H
R
H
R

C
C
C
H
H
C
C
R

R
H
C
P
R

R
C
C
P
P

–
P
P
R
–

–
H
P
P
R

P
H
C
P
R

P
C
C
H
P

R
–
–
R
R
–

–
P
R
R
R
R

R
–
–
–
–
–

–
P
P
R
R
R

R
–
–
R
R
–

C
R
R
R
R
–
–
–
–
R
–
–
–
–
–

C
C
R
H
R
R
R
R
R
R
R
R
R
R
R

H
R
R
R
–
–
–
–
–
R
–
–
–
–
–

H
H
R
P
R
P
R
R
–
–
R
P
R
R
R

C
P
P
R
R
–
–
–
–
R
–
–
–
–
–

C
C
P
H
P
R
R
R
R
R
R
P
R
–
–

–
–
–
R
–
–
–
–
–
–
–
–
23
16
7

R
R
R
R
R
R
R
R
R
R
R
R
45
18
27

–
–
–
–
–
–
–
–
–
–
–
–
16
11
5

–
–
–
R
–
–
R
R
R
R
R
R
37
17
20

–
–
–
R
–
–
–
–
–
–
–
–
23
16
7

R
R
R
P
R
R
R
R
–
–
R
–
39
17
22

235

–
P
R
R
R
–

Mean percentage of behaviors
displayed40

aM. fuscata25

M. mulatta

20
15
10
5

PI
H
B
L
SN
CD
PIM
MIM
MP
GW
CA
CIM
TW
IC
GA
PU
PUS
PUD
GH
ROS
RIH
RT
SC
CL
RWH
POS
SL
RWM
RIM
TIM
FL
F
SW
FLM
PIW
WIL
ROF
COO
TH
SGR
SIH
W
SP
TS
JT
RAT

0

b

35

M.f. young

30

M.f. adult

25
20
15
10
5

c
M.m young
M.m. adult

ROS
RIH
RT
SC
CL
RWH
POS
SL
RWM
RIM
TIM
FL
F
SW
FLM
PIW
WIL
ROF
COO
TH
SGR
SIH
W
SP
TS
JT
RAT

90
80
70
60
50
40
30
20
10
0

ROS
RIH
RT
SC
CL
RWH
POS
SL
RWM
RIM
TIM
FL
F
SW
FLM
PIW
WIL
ROF
COO
TH
SGR
SIH
W
SP
TS
JT
RAT

PI
H
B
L
SN
CD
PIM
MIM
MP
GW
CA
CIM
TW
IC
GA
PU
PUS
PUD
GH

0

PI
H
B
L
SN
CD
PIM
MIM
MP
GW
CA
CIM
TW
IC
GA
PU
PUS
PUD
GH

Mean percentage of
behaviors displayed

30

Mean percentage of behaviors
displayed

Cross Species Comparison of SH / 1129

Behavioral variants

Fig. 3. Mean percentage of stone handling behaviors displayed by (a) two macaque species; (b) adults and young of Japanese macaques;(c) adults and young of rhesus macaques.

the rhesus SH patterns with those of Japanesemacaques below 11 years of age. The outcome wassimilar: Japanese macaques displayed significantly
more complex behaviors than rhesus macaques (25complex behaviors; Mann–Whitney, U 5 179.50,
N1 5 34, N2 5 25, Po0.001).
When we exclude the two most common
complex behaviors (‘‘rub on surface’’ and ‘‘rollin hand’’) displayed by adults and young, there
is a significant difference between the frequency
of complex behaviors displayed by young andadultJapanese
macaques(Mann–Whitney,
U 5 159.50, N1 5 25, N2 5 20, P 5 0.038), withadults displaying complex behaviors more frequently(Fig. 3(b)).

Simple and Complex Behavioral Patterns
This analysis was done to find out how demographic factors might affect SH. There were 19
simple behaviors and 27 complex behaviors in the SH
repertoire of macaques (Table I). When we calculate
the percentage of complex behaviors over the sum ofcomplex and simple behaviors for each individual,
Japanese macaques displayed more complex behaviors than rhesus macaques (Mann–Whitney,
U 5 250.00, N1 5 45, N2 5 25, Po0.001). The numbers of simple and complex behaviors performed byrhesus macaques were 16 and 7, respectively, and forJapanese macaques 18 and 27, respectively. As theoldest rhesus were 11 years of age, we also compared
236

Am. J. Primatol.

1130 / Nahallage and Huffman

stones are readily available for all troops [Leca et al.,2008], ruling out an ecological difference.
All customary behaviors and some of thehabitual SH behaviors displayed by the rhesus andJapanese macaques studied here are common object
manipulative behaviors of many Old-World Monkeys[Torigoe, 1985]. SH behavior has also been observedin a few troops of M. fascicularis (Florida Monkey
Jungle—A.
Zeller;Ubud,
Bali-Indonesia—A.
Fuentes; Thailand—K. Bauer, Myanmar—Aye Mi
San personal communication). All of these troops
were captive or provisioned free ranging. It has not
yet been reported in M. cyclopis another member ofthis species group. This may reflect the paucity of
research on captive or provisioned troops of thisspecies. So far, no other macaque taxonomic groups,
i.e. sylvana, silenus, sinica or arctoides have beenreported to SH. It will be of interest to see just how
widely SH occurs among other macaque species.

SH Activity on the Ground, Above the Ground,and Solitary Vs. Communal
Concerning the percentage of individuals’ SHtime spent above the ground, there was a significant
difference
betweentroops(Mann–Whitney,
U 5 125.50, N1 5 45, N2 5 25, Po0.001). Rhesus
macaques spent more SH time above the ground,on the climbing structure, than Japanese macaques.
Japanese monkeys spent 85% of time SH on the
ground and 15% on the climbing structures above
the ground. Rhesus monkeys spent 67% SH on thewooden structures compared with 33% on the
ground. Furthermore, rhesus macaques displayed
more communal SH than Japanese macaques(Mann–Whitney, U 5 333.50, N1 5 45, N2 5 25,
P 5 0.004).
DISCUSSION
Shared Behavioral Propensity for SH

Socio-Demographic Factors Influencing
Behavioral Variation of SH

The occurrence of SH behavior in rhesus
macaques confirms the prediction that these two
closely related macaque species share a behavioral
propensity for SH. There is no compelling evidence
to suggest that observed differences are owing to theinherent species differences. With the exception of
one behavior, ‘‘insert into cavity,’’ all behaviors
displayed by the rhesus macaques are typical SH
behavioral patterns of Japanese macaques. It should
be noted that among all Japanese macaques troops
studied to date, Takahama troop exhibits the greatest number of SH behaviors, in fact all the behaviors
known for Japanese macaques. Even though therhesus macaque troop exhibited a lower SH rate anddisplayed fewer SH patterns than the Takahama
troop, both rate of occurrence and patterns exhibited
fall within the recorded range observed in Japanesemacaque troops [Leca et al., 2007a]. The SH rate forten captive and free-ranging Japanese macaquetroops ranged from 0.1 to 5.9 per hour and theoverall number of SH patterns exhibited per troop
ranged from 17 to 45 [Leca et al., 2007a]. The rhesus
macaque troop falls above the captive PRI Arashiyama troop and the free-ranging Koshima troop in bothSH rate and the number of behaviors displayed(Arashiyama: SH rate 0.2/hr, 17 behaviors; Koshima:
SH rate 0.1/hr, 16 behaviors; Leca et al., 2007a).
Interestingly, a similar trend was reported fortool use behavior in chimpanzees and bonobos.
Hohmann and Fruth [2003] stated that the extent
of tool use by bonobos appears to be at the lower endof the range for chimpanzees, resembling that of thechimpanzee populations of Kibale and Budongo. This
was attributed to the differences in the evolution ofmaterial culture in these two Pan species [Hohmann& Fruth, 2003]. Bonobos’ lack of need to engage intool use for food acquisition is another possibility[McGrew et al., 1997]. In the case of SH, however,Am. J. Primatol.

Demographic structure and the duration forwhich these cultures have been present in each troop
may also contribute to the quantitative differences
between SH in the rhesus and Japanese macaquetroops. In Japanese macaques, a troop’s SH repertoire increases over time, and the newly emerging
behavioral patterns become more specialized. At
Arashiyama in 1983, 5 years after the behavior’s
innovation, the troop displayed eight SH behavioral
patterns. By 1989–1990, Arashiyama and Takasakiyama troops displayed 17 and 16 behavioral
patterns, respectively [Huffman, 1984, 1996]. In
2004, almost 21 years later, the SH repertoire had
increased in number to 32 and 31, respectively [Lecaet al., 2007a].
Infant Japanese macaques start SH with a few
basic patterns, then the number and complexity of
behaviors gradually increases with age, peaking at
3–4 years [Nahallage & Huffman, 2007b]. In the
Takahama troop most of the complex behaviors weredisplayed by the individuals over 15 years of age[Nahallage & Huffman, 2007a]. The absence of older
adults may therefore be one reason for the lack ofmore complex behaviors in the PRI rhesus troop’s
repertoire.
SH first begun in the rhesus troop about 10
years ago in 1998 (see Methods), much more recently
than in the Takahama troop, which is thought tohave started SH around 25–30 years ago [Nahallage& Huffman, 2007a]. The rhesus macaque troop’s
current demography, behavioral profile (mostly
simple, nonspecialized behaviors) and the small
number of SH patterns displayed are all consistent
with this relatively recent emergence of SH.
It has recently been demonstrated that social
learning plays a key role in the acquisition of SH
237

Cross Species Comparison of SH / 1131

influencing the processes and mechanisms of acultural behavior.

behavior by infant Japanese macaques [Nahallage &Huffman 2007b]. The age of acquisition of SH varied
from infant to infant (6–31 weeks) and was closely
related to the frequency of SH exhibited by an
infant’s mother. When we started our observation on
the rhesus macaque troop the infants that year werealready older than six months and they were allobserved to SH. Our comparison with Japanesemacaques leads us to conclude that SH can beconsidered a cultural behavior in rhesus macaques.
We assume that this troop has at least reached the
tradition phase, at which the behavior is now passed
down from mother to offspring and/or other multigenerational lines.

ACKNOWLEDGMENTS
This research was approved by and conducted inaccordance with the Primate Research Institute’s
Rules and Guidelines for Animal Health and Welfare. CADN’s graduate studies, of which this study isapart, were supported by the Japanese Ministry of
Education, Science and Culture. We sincerely thankDrs. J.-B. Leca, A. D. Hernandez for commenting on
the manuscript. We also thank the faculty andsupporting veterinary staff of the Center for Human
Evolution Modeling Research, PRI for facilitating
this research and for taking care of the captivemonkey troops. Our sincere thanks to Kiyonori
Kumazaki for his information about the time-period
and possible cause for the beginning of stone
handling in the Indian rhesus troop. We thankexecutive editor Paul Garber and review editor
James Anderson and two anonymous reviewers fortheir helpful comments on the manuscript.

Environmental Factors Influencing Cultural
Behavioral Variation
Another possible reason for the behavioral
variation between two troops is the physical environment of their enclosures, especially the climbing
structure areas. These structures constitute 60% of
the rhesus macaques and only 9% of Japanesemacaques’ enclosures. The rhesus often rub stoneson the metal bolts of the climbing structures,presumably for the sound it produces. The loudsound that results appears to draw others attention
to the behavior. Several individuals, irrespective ofage, may then pick up a stone(s) and carry it (them)on to the wooden walkways and start rubbing themagainst the iron bolts. The bolted junctures of thesewalkways are close together, bringing SH individuals
into close proximity with each other. The synchronization of SH in rhesus macaques could thus be
explained by the contagious nature of play behavior[Huffman, 1984; Leca et al., 2007b].
As a direct consequence of these environmental
factors, rhesus macaques displayed the ‘‘rub on
surface’’ pattern more, and SH more on thesewooden structures, above the ground. This also
explains the high percentage of communal SH in
rhesus compared with Japanese macaques. The
Japanese macaque enclosure does not have wooden
walkways. When they perform ‘‘rub on surface’’ they
do so on the ground on the cement passageway, andthe sound produced does not appear to stimulate SH
in other troop members. They perform more solitary
SH bouts, mainly on the ground, and the frequencyof ‘‘rub on surface’’ is lower than in the rhesus troop.
All the above factors support the view that SH in
the two species studied is owing to the combinationof shared phylogenetic behavioral propensities, andenvironmental and social factors. Other factors may
also contribute to the cultural variation seen in otherbehavioral contexts. Further studies of inter-species
cultural variation in animals within the frameworkof the predictions evaluated here are encouraged.
Such work promises to provide insight into theinterface of phylogenetic and ecological factors

REFERENCES
Altmann J. 1974. Observational study of behavior: sampling
methods. Behaviour 49:227–267.
Galef Jr BG. 1992. The question of animal culture. Hum Nat
3:157–178.
Galef Jr BG. 2003. Social learning: promoter or inhibitor ofinnovation? In: Reader SM, Laland KN, editors. Animal
innovation. Oxford: Oxford University Press. p 137–152.
Hohmann G, Fruth B. 2003. Culture in bonobos? Between
species and within species variation in behaviour. Curr
Anthropol 44:563–571.
Huffman MA. 1984. Stone-play of Macaca fuscata in Arashiyama B troop: transmission of a non-adaptive behavior. J Hum
Evol 13:725–735.
Huffman MA. 1996. Acquisition of innovative cultural behaviors in non-human primates: a case study of stone
handling, a socially transmitted behavior in Japanesemacaques. In: Galef Jr B, Heyes C, editors. Social learningin animals: the roots of culture. Orlando: Academic Press.
p 267–289.
Huffman MA, Hirata S. 2003. Biological and ecologicalfoundations of primate behavioral tradition. In: Fragaszy
DM, Perry S, editors. The biology of tradition: models andevidence. Cambridge: Cambridge University Press.
p 267–296.
Huffman MA, Quiatt D. 1986. Stone handling by Japanesemacaques (Macaca fuscata): implications for tool use ofstone. Primates 27:427–437.
Itani J. 1958. On the acquisition and propagation of a new food
habit in the troop of Japanese monkeys at Takasakiyama.
Primates 1:84–98.
Janik VM. 2001. Is cetacean social learning unique? Behav
Brain Sci 24:337–338.
Janson CH, Smith EA. 2003. The evolution of culture: newperspective and evidence. Evol Anthropol 12:57–60.
Laland KN, Janik VM. 2006. The animal cultures debate.
Trends Ecol Evol 21:542–547.
Leca J-B, Gunst N, Huffman MA. 2007. Japanese macaquecultures: inter- and intra-troop behavioural variability ofstone handling patterns across 10 troops. Behaviour
144:251–281.

238

Am. J. Primatol.

1132 / Nahallage and Huffman

Leca J-B, Gunst N, Huffman MA. 2007b. Age-related differences in the performance, diffusion, and maintenance ofstone handling, a behavioral tradition in Japanese macaques. J Hum Evol 53:691–708.
Leca J-B, Gunst N, Huffman MA. 2008. Of stones andmonkeys: testing ecological constraints on stone handling,a behavioral tradition in Japanese macaques. Am J Phy
Anthropol 135:233–244.
McGrew WC. 1992. Chimpanzee material culture: implications
for human evolution. Cambridge: Cambridge University
Press.
McGrew WC, Ham RM, White LJT, Tutin CGE, Fernandez M.
1997. Why don’t chimpanzees in Gabon crack nuts? Int J
Primatol 18:353–374.
Nahallage CAD, Huffman MA. 2007a. Age-specific functions ofstone handling, a solitary-object play behavior, in Japanesemacaques (Macaca fuscata). Am J Primatol 69:267–281.
Nahallage CAD, Huffman MA. 2007b. Acquisition and development of stone handling behavior in infant Japanesemacaques. Behaviour 144:1193–1215.
Nahallage CAD, Huffman MA. 2008. Proximate factors
associated with the occurrence of stone handling behavior
in a captive troop of Japanese macaques. Int J Primatol.
DOI 10.1007/s10764008.9268-3.

Am. J. Primatol.

Perry S, Manson JH. 2003. Traditions in monkeys. Evol
Anthropol 12:71–81.
Perry S, Baker M, Fedigan L, Gros-Louis J, Jack K, McKinnon
KC, Manson JH, Panger M, Pyle K, Rose L. 2003. Social
conventions in wild white-faced capuchin monkeys. Curr
Anthropol 44:241–268.
Tomasello M. 1994. The question of chimpanzee culture. In:
Wrangham RW, McGrew WC, de Waal FBM, Heltne PG,
editors. Chimpanzee cultures. Cambridge: Harward University Press. p 301–318.
Torigoe T. 1985. Comparison of object manipulation among 74
species of non-human primates. Primates 26:182–194.
van Schaik CP, Ancrenaz M, Borgen G, Galdikas B, Knott CD,
Singleton I, Suzuki A, Utami SS, Merill M. 2003. Orangutan
cultures and the evolution of material culture. Science
299:102–105.
Whiten A, Goodall J, McGrew WC, Nishida T,
Reynolds V, Sugiyama Y, Tutin CEG, Wrangham RW,
Boesch C. 1999. Cultures in chimpanzees. Nature 339:
682–685.
Whiten A, Goodall J, McGrew WC, Nishida T, Reynolds V,
Sugiyama Y, Tutin CEG, Wrangham RW, Boesch C. 2001.
Charting cultural variation in chimpanzees. Behaviour
138:1481–1516.

239

11. CULTURED JAPANESE MACAQUES - A MULTIDISCIPLINARY APPROACH TO STONE HANDLINGBEHAVIOR AND ITS IMPLICATIONS FOR THE
EVOLUTION OF BEHAVIORAL TRADITIONS IN NONHUMAN PRIMATES

Michael A HUFFMAN1, Jean-Baptiste LECA2, Charmalie AD
NAHALLAGE3

1: Section of Social Systems Evolution, Primate Research Institute, Kyoto University, 41-2 Kanrin, Inuyama, Aichi 484-8506,
Japan
Email: huffman@pri.kyoto-u.ac.jp
2: Section of Social Systems Evolution, Primate Research Institute, Kyoto University, 41-2 Kanrin, Inuyama, Aichi 484-8506,
Japan
Email: leca@pri.kyoto-u.ac.jp
3: Department of Sociology and Anthropology, University of Sri Jayewardenepura, Gangodawila, Nugegoda, Sri Lanka
Email: charmalie2@hotmail.com

Corresponding author: Michael A HUFFMAN, Section of Social Systems Evolution, Primate Research Institute, Kyoto
University, 41-2 Kanrin, Inuyama, Aichi 484-8506, Japan
Email: huffman@pri.kyoto-u.ac.jp

Huffman MA, Leca JB, Nahallage CAD. In press. Cultured Japanese macaques – A multi-disciplinary approachto stone handling behavior and its implications for the evolution of behavioral traditions in non-humanprimates. In: N. Nakagawa, M. Nakamichi & H. Sugiura (eds). The Japanese macaques. Springer, Tokyo.

24011.1. Abstract
Japanese primatologists have paid attention to cultural phenomena in non-human primates since its
earliest stage. The most famous example of behavioral traditions in Japanese macaques is probably sweet potato
washing behavior. After being innovated by a young female on Koshima Islet, this behavior was sociallytransmitted from the innovator to most other group members. More recently, stone handling (SH) behavior, aform of solitary object play, also became a well-known example of culture in this species. A longitudinal study
allowed following the appearance, subsequent transmission, and transformation processes over 30 years andacross multiple generations in a provisioned group at Arashiyama, Kyoto. Also under more controlled conditionsof captivity, we assessed how the individual acquisition, expression, and possible functional aspects of SH
behavior may be influenced by specific environmental factors, access to demonstrators by naïve individuals(typically within mother-infant dyads), and neuro-motor developmental constraints. Finally, a 10 troop inter-sitecomparison of this behavior was carried out to investigate the genetic, ecological, and socio-demographic factorsthat may affect the innovation, spread, and maintenance of the SH culture. This research on SH is the mostextensive and systematic survey focused on the intra- and inter-group variability of a single type of behavior inmonkeys to date.

11.2 Introduction
The concept of culture (also referred to as behavioral tradition) in animals was first proposed in 1952 by thefounder of primatology in Japan, Kinji Imanishi, who predicted that culture should be present in all sociallyliving animals. By the early 1950s, provisioning and individual recognition of all members of several Japanesemacaque (Macaca fuscata) troops across Japan were accomplished, including Koshima, Takasakiyama,
Arashiyama, and Minoo. Thus started the practice of long-term comparative and collaborative research, one of
the many early contributions by Japanese scientists to the field of primatology (Huffman 1991; Yamagiwa andHill 1998; Takahata et al. 1999). Provisioning provided the first outdoor laboratory situation for recording theprocess of behavioral innovation and diffusion of behaviors in a novel environment and research at these sites
has contributed much to our understanding of the patterns of diffusion of innovative behavior in primates(reviewed in Itani and Nishimura 1973; Nishida 1987; Thierry 1994; Huffman and Hirata 2003).
Perhaps the most widely cited evidence for culture in animals is the innovation and transmission of sweet
potato washing behavior in the Japanese macaques on Koshima Island, Miyazaki Prefecture, Kyushu (Kawai
1965). More recent work in Japanese macaques has focused specifically on the innovation and diffusion of new
behaviors across individuals and the establishment of group-specific behavioral traditions in free-ranging
provisioned troops (Huffman 1984, 1996; Huffman and Quiatt 1986; Watanabe 1994; Leca et al. 2007a).
Extensive collaborative field studies of socially learned behaviors among the great apes, have also documented
complex behavioral traditions in chimpanzees (Tomasello 1990; Whiten et al. 1999) and orangutans (van Schaik
et al. 2003a).
Evidence for socially mediated learning and culture in many species now exists, including the great apes,
New World monkeys, rats, cetaceans, birds and fish (see Fragaszy and Perry 2003). These examples range fromthe opening of milk bottle caps by British tit birds (Fisher and Hinde 1950, 1952) and pinecone stripping byIsraeli black rats (Aisner and Terkel 1992; Terkel 1996) to examples including transmission of behaviors
sometimes leading to social traditions as diverse as mate choice in guppies (Dugatkin 1996), new vocalizations
in ravens (Enggist-Dueblin and Pfister 2002), feeding techniques of Tonkean macaques (Drapier and Thierry2002), abnormal behaviors of captive rhesus macaques (Hook et al. 2002) and prey capture by killer whales(Rendell and Whitehead 2001). All of these studies have looked at determinants of cultural behavior, including
innovation, transmission, acquisition, developmental constraints thereof, long-term maintenance and inter-groupvariation. However, none have considered the role of all of these factors into an integrated framework of social
learning.
There are two basic approaches to the study of social learning, the underpinnings of culture. The first
focuses on underlying mechanisms, i.e. ‘how’ the information is transferred between two individuals. Under acontrolled experimental setting, a naïve subject, faced with a problem solving task, is given the opportunity toobserve an experienced subject and learn from its behavioral strategies (Custance et al. 1999). The second
focuses on the pathway of behavioral diffusion under natural conditions in a stable social group, i.e. from‘whom’ the information is transferred (Biro et al. 2003). Inter-individual tolerance allowing spatial proximity,
frequency of the behavior performed, and the attention paid to the behavior are essential factors to predict the
speed of diffusion of a novel behavior and the pathway of transmission (Coussi-Korbel and Fragaszy 1995;
Huffman and Hirata 2003; van Schaik et al. 2003a). However, not only social, but also environmental,
demographic, and developmental constraints can affect the efficiency and speed of acquisition and diffusion of aparticular behavior (Huffman and Hirata 2003). Thus far, only the study of stone handling (SH) behavior inJapanese macaques has embraced all of these determinants into the understanding of a single cultural behavior.

241

Our long-term study supports the idea of SH culture and provides insights into the nature of social learning, itsrole in the spread of behavioral innovations, the factors influencing inter-group behavioral variation, theemergence and transformation of culture, and the potential importance of culture in the process of biologicalevolution.

11.3 Stone handling behavior
SH is a seemingly non-adaptive solitary object play activity (Huffman 1984, 1996; but see Nahallage andHuffman 2007a and section 11.6.8 below). SH consists of manipulation of stones in various ways including
rubbing or clacking them together, pounding them onto other hard surfaces, picking up and rolling them together
in the hands, cuddling, carrying, pushing or throwing them (Fig. 11.1; Table 11.1). Currently 45 different
behavioral patterns are documented in Japanese macaques (Leca et al. 2007a).
SH is reported to occur in four captive troops and six provisioned free-ranging troops across Japan, and stillother sites are known but have not yet been systematically investigated. This behavior has been followed for 30
years across multiple generations in the Arashiyama troop, Kyoto, Japan beginning from its innovation(Huffman 1984, 1996; Leca et al. 2007a). Unlike potato washing, SH was first transmitted horizontally among
playmates. Transmission began to occur vertically from elder to younger individuals around 1984. Since then,SH has been acquired by every infant in the group, but never by individuals over five years of age.

11.4 Long-term observation of the Arashiyama troop
11.4.1 Innovation
Japanese macaques have been studied at Arashiyama since 1954, after monkeys were enticed to narrow
down their wide seasonal ranging patterns when provisioning was successfully initiated at the Iwatayama
Monkey Park (Huffman 1991). In spite of the intense history of research at the site by many scientists insuccession, SH was not noted until December 7, 1979 (Huffman 1984). The first individual recognized toperform this behaviors was the three-year-old, middle ranking female Glance-6476 (Fig. 11.2). She had brought
several flat stones from the forest and was gathering them together and scattering them about with the palms ofher hands on the open ground of the provisioning site. This was the first and the last time that SH was observedby Huffman during a 14-month study lasting up to September 1980.

11.4.2 Transmission
In October 1983, when Huffman returned again to Arashiyama to resume research, SH had alreadydiffused to many members of the troop and had become a daily occurrence. SH was classified into 8 basic
behavioral patterns: gathering, pick up, scatter, roll in hands, rubbing stones, clacking, carry and cuddle(Huffman 1984). By 1985, an additional 9 behavioral patterns were also recognized, with 6 of those patterns
being variations of the original 8 (pick up and drop, rub of surface, flinting, pick up small stones, rub with hands,
and grasp with hands). The 3 new behaviors were toss walk, move and push, and grasp walk, all behaviorsconsidered to reflect an increasing familiarity with stones in general as the practice of SH spread and became asubstantial part of the individual and the troop daily activity.
In June of 1984, 49% (115/236) of the troop exhibited SH and by June of 1985, 60% (142/236) of thetroop members born before June 1984 were verified to be new SH handlers. Eighty percent (92/115) of theindividuals observed were born between 1980 and 1983, after the first record of SH was made in 1979. The
remaining 20% were young adult males (N= 6, 4.5 – 8.5 years old), young adult females (N= 6, 4 years old), andadult females (N= 11, 5 plus years old).
The evidence strongly suggests that SH originated from the Glance kin group, given that other thanGlance-6476, the first female observed to SH in 1979, the only older individuals noted to SH were her two
female cousins, Glance-6775 and Glance 6774, and a lower ranking female Blanche-596475. Unlike potato
washing and wheat washing behavior, two of the earliest examples of cultural traditions in Japanese macaques,
no individuals have ever been noted to acquire SH behavior after they reached the age of 5 years. This supports
our observations that SH was not likely innovated earlier than 1978 or 1979, otherwise we should expect to havefound older stone handlers during these early surveys. Eleven years on into the study in 1991, every individual
under the age of 10 was observed to SH. Thus, unlike other examples of cultural behavior reported in Japanesemacaques, SH first spread laterally among young individuals of the same age, and only began to be transmitted
from adults to offspring, when the first female stone handlers began to have offspring of their own.
The route of transmission of a novel behavior is in part determined by the nature of the behavior and thesocial networks in which it normally occurs. Those most likely to be together while engaging in a particular242

kind of behavior, whether it be play, foraging, grooming or sleeping, should be more likely to learn variants ofthese behaviors from one another (Huffman 1996).

11.5 Environmental versus social influences of a demonstrator, and the role ofdevelopmental constraints in the acquisition and expression of stone handling
The long-term study at Arashiyama allowed us to determine the general pathways of diffusion of SH
and evaluate the factors that may have contributed to the spread of SH within the group. One the one hand,mothers were presumed to be the primary source of an infant’s early exposure to SH (Huffman 1984, 1996). On
the other hand, we believe that there are atypical environmental conditions, such as the concomitant presence ofprovisioned foods and numerous stones, sometimes artificially brought by humans around the open space offeeding areas, under which the innovation and initial diffusion of SH could be facilitated (Huffman 1996; Leca etal. 2008a; Nahallage and Huffman 2008a,b).
However, only through controlled captive conditions, are we able to systematically evaluate the possible
contributions of environmental, social and developmental factors to behavioral acquisition. Nahallage andHuffman (2007b) studied the SH behavior of a captive group of 48 Japanese macaques at the Primate ResearchInstitute, Kyoto University, for 24 months spanning two breeding seasons between 2003-2005, during which 14
infants were born.

11.5.1 Environmental factors
Based on a detailed analysis on the exposure of infants to specific areas of an outdoor enclosure withvarying stone availability, we failed to validate the environmental stimuli hypothesis, stating that the total timespent in areas with high stone availability and, therefore, exposure to more stones, increases the likelihood thatan infant acquires SH behavior. We found no significant correlations between the age of SH acquisition and therate of stones encountered from birth to acquisition.

11.5.2 Access to demonstrators by naïve individuals and the acquisition of behaviors
We investigated the effect of pivotal individuals as demonstrators on the initial acquisition anddevelopment of SH behavior by focusing on inter-individual interactions, in particular mother-infant dyads. In
the 14 mother-infant dyads born during the study, all but one infant started SH within the first 6 months after
birth. There was great variability among them in the age SH was first displayed (6-31 weeks). During their first
three months of life, infants spent 75% of the time within one-meter of their mother, significantly more than theyspent with other individuals. This high level of proximity to the mother had a significant impact on the age at
which SH was acquired. Infants of mothers with higher SH frequencies exhibit the behavior earlier than infantsof less frequent SH mothers. Two infants, born in consecutive years, to the same non-SH mother were the last toacquire the behavior. These results suggest that the acquisition of SH behavior in infants was strongly
influenced by the amount of time spent in proximity to a stone handler and the frequency of the behavior
displayed by that model (Nahallage and Huffman 2007b). Infants of frequent SH mothers spent proportionally
twice as much time (83%) watching their mothers when she was SH than did infants whose mother showed low
SH frequency (42%). The former tried to take stones away from their mothers in 75% of the SH bouts whereas
the latter tried to do so in only 33% of these bouts, resulting in a difference in the amount of time an infant took
part in its mother’s activity. Differences in mothers’ SH frequency could affect their infant’s exposure to SH,
opportunities to handle stones, and practice SH.

11.5.3 Constraints of neuro-motor development on the expression of SH behaviors
Few longitudinal studies have been conducted on the ontogeny of specific cultural behaviors, but rather
most tend to deduce development from cross-sectional observations (Lonsdorf 2005). Furthermore, neuro-motor
development has rarely been considered as a constraint in the expression of matched behavioral patterns between
experienced and naïve individuals. Our study showed that though mothers had a strong influence on the initialacquisition of SH behavior in infants, infants did not perform the same behavioral patterns as adults mainly
because of developmental constraints in the kinds of behaviors they could perform (Nahallage and Huffman
2007b). There was a gradual increase in the number and complexity of SH patterns displayed by infants, which
revealed a neuro-motor developmental phase of this behavior. The infants we studied acquired the basic SH
behaviors at around 2-3 months. Common to other behavioral traits observed during the early stages of infantdevelopment in macaques, stone manipulation patterns were quite simple actions, mainly pick up, cuddle, lick orbite a stone and typically short in duration. Infants did not perform any complex manipulative action with stones

243during this time. The average number of patterns performed by an individual up to 6 months of age was 3.75 ±1.90. At around 6 months, individuals started to perform more complex stone-directed actions such as clacking
or rubbing two stones together or on a substrate. On average they displayed 8.85 ± 2.26 patterns from six to 12
months of age. According to neuromotor studies on macaques, the earliest sign of relative independent finger
movement (RIFM) occurred at 2-3 months, with mature patterns occurring at 7-8 months (Bortoff and Strick1993). Galea and Darian-Smith (1995) reported that performance on a reach and grasp test by a group of young
macaques approached adult levels by 6 months. This agrees with our study showing infants starting the behavior
between 2 to 3 months and performing activities that require firm grasp of the stones around 6 months. Even
though the motoneuronal projections responsible for finger movement develop rapidly in the first neonatalmonths, they do not mature until the second year of life. This explains the increase in the number of SH patterns
up to 3-4 years of age. Older juveniles displayed the highest number of patterns among all age classes (18.14 ±5.38), whereas the number of patterns displayed decreased into adulthood, which might reveal the appearance ofindividual preferences or behavioral routines over the years (Nahallage and Huffman 2007b).
We concluded that at the time of acquisition, infants acquired a rudimentary form of SH, but wereconstrained from matching specific behaviors from the demonstrator due to their level of neuro-motor
development. Our findings support developmental theories on juvenile primates (Pereira and Fairbanks 1993).
Later on however, this kind of matching did occur, and was particularly noticeable for rare behaviors displayedby the mother, which were then being seen to diffuse among offspring and others. A good example for this is thethrow and run behavior displayed by the alpha female of the troop. Her son first started throwing stones when he
was one and half years old but was not able to perform the run and throwing together, but by around 3 years ofage he was seen performing the throw and run behavior just like his mother. They were the only individuals who
displayed this behavior in the troop (Nahallage and Huffman 2007b; Leca et al. 2008c).

11.6 Exploring and explaining inter-group behavioral differences
11.6.1 The method of elimination
Recently, primatologists have found evidence of inter-group behavioral variation in several non-humanprimate taxa including capuchins, macaques, and great apes (Whiten et al. 1999; Huffman and Hirata 2003;
Perry et al. 2003; van Schaik et al. 2003b; Leca et al. 2007a). The ‘method of elimination’ is a multi-stepdecision procedure that may be used to assess whether a geographically variable behavior is or is not traditionalor cultural (van Schaik 2003; see also Boesch 1996). First a patchy geographical distribution of the behavior
must be demonstrated. Within the same (sub)species, a given behavioral pattern can be customary or at least
habitual in some groups and rare or even absent in others although it is ecologically possible. Like someethnographic research in human social sciences or like the powerful comparative method used in ethology, thisgroup-contrast approach to cultural primatology has been widely used by field primatologists as a first step toidentify candidates for cultural behaviors, particularly in primate stone-tool cultures (e.g., Whiten et al. 1999).
Second, inter-group behavioral differences are typically attributed to genetic, environmental or cultural
factors (Goldberg and Wrangham 1997; Whiten et al. 1999; Yamakoshi 2001). By elimination, when obvious
genetic and ecological causations can be ruled out, or at least when the effects of genetic and ecological factors
are likely to be minimal, then inter-group behavioral variation is largely considered cultural. Third, the behavior
should meet a set of criteria, such as being observed in at least two members of one group, showing pathways of
diffusion within age structures, affiliated networks, or along matrilineages, being largely dependent on social
means for its diffusion and maintenance, and being persistent across generations, or at least over a number ofyears (Fragaszy and Perry 2003). As more elements congruent with the concept of tradition are provided, thelikelihood of alternative interpretations decreases (van Schaik 2003). Accordingly, if a behavior shows ageographically patchy distribution unlikely attributed to genetic or ecological differences between sites, and if it
is long-lasting and socially-transmitted, then a cultural phenomenon can be inferred (McGrew 2003).

11.6.2 Exploring genetic, ecological, demographic and social factors
To better understand how the SH tradition in Japanese macaques may appear, spread, and be maintained
within the group over generations, we used the method of elimination to investigate the roles of genetic,
ecological, demographic, and social factors in explaining inter-group similarities and differences in SH (Leca etal. 2007a,b, 2008a,b,c). Our main goal was to test several hypotheses proposing that SH variability reflects moredemographic and social constraints than genetic and ecological factors. Our specific objectives were: 1) toestablish the comprehensive repertoire of SH local variants in Japanese macaques; 2) to provide a systematic andbroad inter-group comparison of the frequency, form, and context of occurrence of SH; 3) to address the possible
role of genetic determinants in SH variation, through a comparison of the behavior in the two subspecies of244

Japanese macaques, Macaca fuscata fuscata, widely distributed in the Japanese archipelago, and M. f. yakui
endemic to Yakushima, a small island at the southern limit of distribution of the species (cf. Fooden and Aimi
2005); 4) to evaluate three major environmentally-based hypotheses invoked to account for inter-groupdifferences in SH; 5) to consider the influence of various socio-demographic constraints on the appearance,
diffusion, and maintenance of SH; 6) to test the association between geographic proximity and culturalsimilarity, as a way to infer a phenomenon of cultural zone; 7) to explore the transformation over time in theform of SH from the perspective of stone-tool use in non-human primates.
We conducted a systematic comparison of SH in ten troops of Japanese macaques. Nine troops belonged
to the M. f. fuscata subspecies and one troop was M. f. yakui. Four captive troops were housed in large outdoor
enclosures at the Kyoto University Primate Research Institute, and Japan Monkey Centre, Inuyama, and six freeranging provisioned troops lived at four geographically isolated sites in Japan, namely Arashiyama,
Takasakiyama, Koshima, and Shodoshima (Fig. 11.3). The comparison represented a total of 2,328 individuals
and included two long-term studied troops at Arashiyama and Takasakiyama. We used the same observation
procedure in all troops studied: continuous focal-animal sampling interspersed with instantaneous group scansampling, and occasionally supplemented with ad libitum sampling (Altmann 1974). We analyzed a total of
1,950 hours of observation, including 1,280 video-recorded SH bouts (Leca et al. 2007a). We provided arigorous documentation of the local environmental context of SH occurrence, such as site-specific stone
availability and the conditions of food provisioning (Leca et al. 2008a,b).

11.6.3 Inter-group variation in SH
We listed a total of 45 different behavioral patterns in the SH repertoire of Japanese macaques (Leca et al.
2007a; Nahallage and Huffman 2007a). By taking a group-contrast approach to chart inter-group diversity in SH,
Leca et al. (2007a) showed substantial variability in the frequency of occurrence and form of SH among the ten
study troops. We found major inter-group differences in the frequency of occurrence and the prevalence of mostof the 45 SH patterns, with local variants being customary in some troops, and rare or even absent in others
although they were ecologically possible, and performed by a majority of individuals in some troops, or only
idiosyncratically in others (Leca et al. 2007a,b; see Table 11.2 for definitions).
The frequency of occurrence of SH patterns were highly variable according to the pattern and troop inquestion. Very few patterns were unique to any troop, as most were shared between two or more troops. Even
though most simple SH patterns (corresponding to investigative, locomotion, and collection activities) could beobserved in most study troops, their frequency of occurrence varied from being present or to being a customary
practice. The frequent occurrence of more complex SH patterns (flint, combine with object), corresponding topercussive, rubbing and other complex manipulative activities was even more restricted to particular troops, but
again highly variable depending on the pattern. Finally, a few complex SH patterns were specific to one troop,such as tap in mouth, spin, and wrap in leaf in the Takahama troop, and stone groom in the Shodoshima A troop.
Following Whiten (2005), we defined a ‘tradition’ as a local behavioral variant, showing different
frequencies of occurrence across the study sites, i.e. being customary or habitual in at least one site, but absent
elsewhere. We defined a ‘culture’ as a package of multiple related traditions, and ‘cultures’ as distinctive arraysof clustered traditions. Almost all SH patterns showed geographically patchy distributions, i.e. had different
profiles of frequency of occurrence across the study sites, and were referred to as local variants or SH traditions.
In terms of behavioral complexity, we found three levels of SH culture, each level being defined by troopdependent clusters of SH traditions (Leca et al. 2007a).
In summary, our results revealed a significant inter-troop variability in the form of SH, consistent with theextensive and multiple inter-site behavioral differences recorded in chimpanzees, and interpreted as culturalvariation (cf. Whiten et al. 1999).

11.6.4 No major evidence for genetic determinants in SH variation
First, our comparative study revealed that M. f. yakui did not notably differ from M. f. fuscata in the SH
repertoire, as well as the occurrence, form, and context of SH. We found that SH patterns varied as much
between seven troops of the same subspecies (M. f. fuscata in Wak.A, Takh., Ara.E, Sho.A, Sho.B, Tak.B, andTak.C) as between subspecies themselves (M. f. fuscata versus M. f. yakui) (Leca et al. 2007a).
Second, the occurrence of SH behavior in rhesus macaques (Macaca mulatta) and long-tailed macaques(M. fascicularis) confirmed the prediction that closely related macaque species shared a behavioral propensity
for SH (Huffman and Hirata, 2003; Nahallage and Huffman 2008a). With the exception of one variant, all theSH patterns displayed by the rhesus macaques were typical of Japanese macaques. We found no compelling
evidence to suggest that the observed differences could be attributed to differences inherent to these two species(Nahallage and Huffman 2008a). Therefore, we can assume that most SH patterns are macaque ‘universals’. All245

the basic motor actions involved in every SH pattern are shared behavioral predispositions, i.e. they are alreadypresent in the repertoire of the genus Macaca (Huffman and Hirata 2003; Nahallage and Huffman 2008a).
Third, Fooden and Aimi (2005) provided information about the geographic distribution of extant
populations of Japanese macaques, including continuities and discontinuities, migration, and genetic variability.
There was evidence for geographic variation in mitochondrial DNA of Japanese macaques (Hayasaka et al.
1991). Although it is acknowledged that genes determine the occurrence of general behavioral categories withina given species, such as the ability to handle stones or use tools, we suggest that intraspecific genetic differences
are negligible in terms of possible implications for local behavioral variants, such as the manual dexterity toclack rather than rub stones together.
In sum, based on comparative analyses at the subspecies and species levels, common behavioral
predispositions in phylogenetically close taxa, and knowledge of genetic determinism, it is reasonable toconsider that genetic and phylogenetic factors may not be key to explaining the observed inter-troop variability
in the form of SH in macaques (Leca et al. 2007a; Nahallage and Huffman 2008a).

11.6.5 Role of ecological factors in SH variation between troops
SH is a behavior particularly well-suited for the method of elimination. Its apparent lack of direct
adaptive consequences and the arbitrariness of its behavioral variants make it easier to rule out ecological factors
as potential causes of inter-group variation (Leca et al. 2008b). Among the most obvious ecological differences
which could affect SH, we addressed site-specific availability in stone number and size, the degree ofterrestriality of individuals, and food provisioning constraints.
11.6.5.1 Stone availability and terrestriality
Although we demonstrated that SH is almost exclusively a terrestrial activity, our comparative analyses
showed that the number of stones readily available and the relative amount of time spent on the ground by themacaques were not significantly associated with the inter-troop differences in the occurrence of SH. Moreover,the size of stones handled was not associated with the size of stones available (Leca et al. 2008b). The absence ofevidence supporting the stone availability and terrestriality hypotheses suggests that the performance of SH andthe motivation to engage in this activity are both more diverse and more complex than the direct links to timespent on the ground or the number of stones readily available in the local environment.
However, this does not imply that any dramatic local change in the availability of stones or substrates(such as vertical structures) would not affect the chance of SH to occur or the form of SH in a particular troop.
We believe that there are favorable environmental circumstances under which the innovation and initial diffusionof SH could be facilitated (Leca et al. 2008a; Nahallage and Huffman 2008a,b).
11.6.5.2 Food provisioning
Food provisioning undoubtedly affects the animals’ activity budget (Huffman 1991; Huffman and
Hirata 2003; Leca et al. 2008a; Jaman and Huffman 2008). Feeding monkeys gives them ‘free’ time since they
can devote less time to foraging. Moreover, attracting monkeys to the open space of feeding areas, where stones
occur and many individuals can gather and observe each other, may result in increased behavioral coordination
at the group-level and contagion-like processes. In this context, the occurrence of an individual starting tomanipulate stones could enhance the probability for a neighboring group member to exhibit SH. In turn, thelatter stone handler could enhance the probability for another neighboring group member to exhibit SH, and soon. Therefore, food provisioning is likely to increase the chances for SH to emerge and diffuse, or at least to be
expressed.
We found that food provisioning constraints, including provisioning frequency, duration of foodavailability, and the size of food items considerably influenced a troop’s food-related activities and feeding style,which in turn could affect several aspects of SH. In troops provisioned several times a day, SH was more
frequent, longer, and more prevalent during provisioning than non-provisioning periods. These effects ofprovisioning were not significant in troops provisioned less frequently. Moreover, SH was more frequently
integrated with food-related activities in troops supplied with food several times a day than in the other troops.
Thus, we argued that the context of occurrence, frequency, and form of SH in a given troop were directly
influenced by provisioning parameters (Leca et al. 2008a). Food provisioning may be a key factor in theinnovation and transformation phases of the SH tradition in Japanese macaques. However, evidence forrelationships between SH and food provisioning does not argue against a cultural interpretation of SH, since thislong-enduring behavior is socially transmitted (Huffman 1984, 1996; Nahallage and Huffman 2007b), whichsome authors suggest is sufficient evidence of a behavioral tradition (Perry and Manson 2003).

246

11.6.6 Demographic constraints on the emergence, transmission, and maintenance of SH
By both facilitating and limiting the expression of particular behaviors, demographic factors may
influence the likelihood of individual innovation, the subsequent diffusion of a novel behavior within a group,
and its long-term maintenance (Huffman and Hirata 2003). Group size and composition can be regarded as major
constraints to the appearance, spread, and transformations over time of traditional behaviors. Here, we evaluated
how group size, the age structure of the group may account for the substantial inter-troop variations in SH
reported in Japanese macaques. The ten study troops varied greatly both in size and proportion of individuals
belonging to the different age classes (Leca et al. 2007b).
11.6.6.1 Group size
We found that troop size was positively correlated with the percentage of troop members exhibiting SH
simultaneously. The larger the group, the higher the proportion of individuals performing SH at the same time
(Leca et al. 2007b). The effect of troop size on the synchronized performance of SH may reveal the contagious
nature of play. Seeing group members playing is a reliable cue for more individuals that the current
environmental conditions are safe enough to engage in play. The sight of nearby stone handlers and even the
loud noise generated by percussive patterns may increase the individual probability to start handling stones. This
stimulation effect may be amplified by an increasing number of troop members and eventually result in a form of“hysterical contagion”. This may help to explain the increase in number of SH individuals (synchronizedoccurrence) around feeding time in free-ranging provisioned troops, as this is the only time when most troop
members are all together in the same location.
11.6.6.2 Age structure
Another demographic factor, age class composition of the group may also affect the diffusion andmaintenance of SH. We verified that a group with abnormal age structure (e.g., missing age classes) showed
lower proportion of stone handlers and lower frequency of SH than more normally age structured groups. Thevery low occurrence and frequency of SH in the captive Arashiyama A troop, with no subadults and young
adults, strongly supported the view that a group’s age structure might affect the diffusion and maintenance of SH
behavior. We suggested that the age gap in the Arashiyama A troop might have constrained the diffusion of SH
from the young to the older group members (Leca et al. 2007b). The restricted practice of SH by young
individuals and only very occasional practice by older troop members may not be sufficient to maintain the
behavior in this troop in the long-term.
These findings are consistent with long-term field observations conducted at Arashiyama and describedabove, suggesting that 1) after initial innovation by youngsters, SH behavior first spreads among young
individuals, probably peer playmates, 2) there is a critical period after which SH cannot be acquired by anindividual (> 5 years), and 3) when a behavioral practice is restricted to a particular class of group members, its
propagation should be slow and its maintenance may be jeopardized (Huffman 1996; Leca et al. 2007b,c, inreview).
In sum, the present findings supported the hypothesis that patterns of variation in SH across troops
reflected variability in group size and composition in age classes.

11.6.7 Social influences and observational learning in SH
11.6.7.1 Cultural zones
We found a positive correlation between geographic proximity and cultural similarity in SH between
troops. In other words, there were significantly greater similarities in SH patterns in the troops living at the same
site, compared to other troops. The numbers of patterns showing the same occurrence in the two troops living at
Shodoshima (Sho.A and Sho.B) and in the two troops living at Takasakiyama (Tak.B and Tak.C) were 26 and25, out of 33 respectively. These neighboring troops had similar sets of SH patterns and their total numbers ofpatterns observed were close (23 and 22 at Shodoshima, and 27 and 31 at Takasakiyama; Leca et al. 2007a).
The geographic distribution of clear troop-dependent clusters of SH variants and the similarities in the
SH repertoires between the free-ranging troops living at the same site were suggestive of the phenomenon ofcultural zones, since any alternative explanation is hard to imagine. Although food provisioning schedules weredifferent, neighboring troops had overlapping home ranges and came into occasional contact around theprovisioning site, where SH activity most often occurs.
The notion of cultural zones is based on the possibility of 1) inter-troop observation when monkeys
come into occasional contact around the feeding sites where most SH activity occurs and 2) males transferring247

SH patterns when migrating from one troop to another. When such inter-troop social influences do not exist(e.g., troops separated by substantial geographic distance in natural situations or by artificial barriers like
concrete walls in captive conditions), the troops showed more differences in their SH repertoires: their mean
number of behaviors showing the same frequency of occurrence was only 12.1 ± 7.3. Inter-troop culturaltransmission in wild chimpanzees has been inferred from the geographical distribution of certain tool-using
behaviors and social conventions (Boesch et al. 1994; McGrew et al. 1997, 2001), and suggested from field
experiments (Biro et al. 2003).
In Japanese macaques, food provisioning provokes several times a day the gathering of most troop
members around feeding sites. Attracting monkeys to the open space of feeding areas, where small-sized foods(cereal grains) are scattered on the ground among stones, increases considerably their chances to encounter theseobjects, and spatial proximity among individuals represents opportunities to observe others handling stones.
Although SH is a primarily solitary activity, non-SH individuals are very likely to observe performances of SH
by other group members, and often show close interest in others’ stones (Huffman and Quiatt 1986; Quiatt andHuffman 1993; Leca et al. 2008b).
11.6.7.2 Social tolerance and spatial cohesion
To test the hypothesis that SH will be more prevalent in more cohesive groups, we calculated, for the 10
study troops, a group-level index of social tolerance, defined as the mean percentage of group members within 1
m of each other. This typical index of group-level social tolerance was not significantly correlated with thefrequency and rate of diffusion of SH (Leca, unpublished data). In other words, the troops showing higher levelsof positive social interactions (such as grooming and playing) were not necessarily the troops with more frequentepisodes of SH and higher percentages of stone handlers. Instead, group size and group spatial cohesion after
food provisioning was positively correlated with the prevalence of SH. Larger troops characterized by closer
physical proximity among individuals feeding on provisioned food also showed higher percentages of troop
members exhibiting SH simultaneously (Leca et al. 2007b).
Therefore, inter-group differences in SH prevalence and cultural similarity in SH between neighboring
troops were better explained by inter-group transfers, as well as opportunities for observational learning andbehavioral coordination both within and between troops rather than intra-group social tolerance alone.
11.6.7.3 Transformation of the SH tradition
The transformation phase of the SH tradition is defined as the late period in which long-enduring
practice and acquired familiarity with the behavior and the stones are gained through the integration of SH withother daily activities (Huffman and Quiatt 1986; Huffman and Hirata 2003). By using similar methods of datacollection for about 15 years of continued observation at Arashiyama and Takasakiyama, we found that themonkeys have almost doubled the size of their SH repertoire and largely diversified the contexts in which SH
activity was practiced (Leca et al. 2007a).
The late emergence of SH patterns not recorded before involved complex manipulative actions, such as
combine with object, rub/put on fur, stone groom, and wash revealed an increased diversity in the combination ofstones with other objects or substrates. The appearance of variants combining the use of hands and mouth (e.g.,
carry in mouth, move inside mouth, bite, and lick) suggested that SH had become more integrated with foraging
and feeding activities. The integration of SH with food-related activities and the emergence of food-directed SH
patterns were more frequent in free-ranging troops where food provisioning strongly influenced the activity
budget.
In human material culture, the “ratchet effect” is referred to as the cumulative modifications andincremental improvements resulting in increasingly elaborate technologies (Tomasello 1999). Our longitudinal
data suggested that the long-term cultural transformation of SH might result in a generational ratchet effect,defined as an increase in the diversity and complexity of SH patterns compared to earlier generations of stone
handlers.
From a functional viewpoint, almost all the 45 SH patterns currently observed in Japanese macaques are
regarded as a non-instrumental manipulation of stones, with no obvious survival value (Huffman 1984; Leca etal. 2007a; but see Nahallage and Huffman 2007a for a possible ultimate function of SH). When combined withother objects, the stones handled by Japanese macaques were never used as tools to achieve an overt goal.
However, when practiced on a daily basis and by most members of a group, the non-instrumental
manipulation of stones could be considered as a behavioral precursor to the possible use of stones as tools(Huffman and Quiatt 1986; Huffman 1996; Leca et al. 2008a). The gradual transformation of the SH tradition,
associated with a generational ‘ratchet effect’ could ultimately result in future stone-tool use, as stone-related
behaviors become more deeply ingrained into the behavioral landscape of these monkeys at the population level.

248

For example, the persistence of SH in food-related contexts may eventually turn into the instrumental use ofstones as foraging tools by Japanese macaques (Huffman and Quiatt 1986; Leca et al. 2008a).
This prediction was eventually verified. Until recently, there was no optimal SH pattern and no local
survival advantage in performing a particular SH pattern rather than another. However in 2004, we witnessed theemergence of the first example of a possible adaptive transformation in the spontaneous practice of SH. Unlike
all other SH patterns performed by Japanese macaques, unaimed stone-throwing exclusively observed in thecaptive Takahama troop during periods of disturbance and in conjunction with agonistic signals typical of thisspecies could be regarded as a spontaneous tool-using behavior (Leca et al. 2008c). Based on the analysis of thecontexts that may elicit the behavior, we inferred that stone-throwing might serve to augment the effect ofagonistic displays. The Takahama troop was the only one to show a complexity level-3 SH culture. This troop
also exhibited the most diverse SH repertoire (44 patterns out of a total of 45), and showed the highest
frequencies of occurrence in SH patterns (28 habitual or customary patterns) among all troops. These findings
suggest that, although SH was observed in the ten studied troops, the transformation of SH into an adaptive
behavior is more likely in troops where SH is a well established behavioral tradition showing diverse andcomplex patterns performed in various contexts.
This study of stone-throwing also supports the view that tool-use evolves in stages from initially nonfunctional behaviors, such as object play (Beck 1980; Huffman and Quiatt 1986; Leca et al. 2008c), a
categorization that perfectly suits the SH activity (Huffman 1984). Food provisioning and captivity have relaxed
selective pressures on foraging and created favorable environmental conditions under which SH may simply
serve the function of maintaining in some populations a set of behaviors that could evolve into tool-use provided
particular environmental circumstances exist. As an unselected but eventually beneficial trait, the SH tradition
would be an exaptation (cf. Gould and Vrba 1982).

11.6.8 Possible functions of stone handling behavior
While not every socially learned behavior needs to be adaptive, the propensity to learn and adopt new
behaviors certainly is. In the immediate sense, SH appears to be rewarding in itself, rather than the means to anend (Huffman 1996). Why the behavior persists in troops over many generations, despite the lack of any obvious
direct adaptive value or function to those who practice SH, has long been an elusive question.
Two hypotheses regarding the occurrence of other types of object play in animals are the misdirected
foraging behavior hypothesis and the motor training hypothesis. According to the misdirected foraging
hypothesis, play in captive or domesticated animals is motivationally directed to objects as if they were food(Hall 1998; Pellis 1991; Pellis et al. 1998). However, SH as described here is not consistent with the misdirected
foraging behavior hypothesis (pseudo-feeding behavior) proposed by Pellis (1991). Even in provisioned freeranging troops, SH occurs predominantly after feeding, not before. Thereby we conclude that this behavior is
not elicited by the anticipation of food as described for captive otters and other zoo animals (Hediger 1964;
Pellis 1991).
Though many theories have been proposed for the function of play behavior (Smith 1978), no single one
can be applied across the board to all play behaviors in all species. Indeed, there are differences of play
activities exhibited by the same species living under different environmental conditions (Ramsey and McGrew
2005). SH is no exception, as evidenced by the contrasts and similarities of the behavior between free-ranging
and captive provisioned troops, and age class differences within the same troop reported here.
The underlying function of play is expected to vary according to the content of the behavior itself, potential
motivational differences brought about by differences in the social and natural environment, and by species’level characteristics. This is confirmed for Takahama macaques also, in that the frequency of SH is significantly
greater on clear sunny days versus cloudy or rainy days as well as during warmer seasons of the year than in thecolder months, and that monkeys suppress SH for days following periods of externally induced intense stress, i.e.
capturing the entire troop for annual check-ups, moving a group temporarily into a new enclosure (Nahallage andHuffman 2008b).
When we compare age-class differences in SH, the possible motivations for performing the behavior appear
to be different for young and adults (Nahallage and Huffman 2007a). This is of particular interest to us, giventhat the behavior is only acquired by individuals when young. This leads us to speculate that unlike other play
behaviors that disappear from the repertoire of most primates when they reach adulthood, presumably because
they no longer serve a function, biological and cultural selective forces may be acting on individuals who haveacquired SH, to maintain the practice throughout life.
The immediate motivation for young to handle stones, like any other form of object play, is most likely to bethat it is intrinsically an enjoyable activity (Hall 1998). They are naturally curious about what others are doing
and have the desire to play with an object made ‘popular’ by others’ use of it (Huffman 1984). At the functional
level, playing with stones allows them to develop and practice the interactive use of motor and perceptual skills
supportive of physical and neurophysiological development. In macaques, a surge of synaptogenesis occurs

249

roughly 2 months before birth and continues up to 3 years of age (Rakic et al. 1986; Bourgeois et al. 1994). The
overall trend in the increasing complexity of SH behaviors (pattern and number of behaviors) over time from
infancy into the juvenile period is consistent with this increase in neural-motor developmental activity. Thesefindings are consistent with Fairbanks’ (2000) model describing the heightened frequency of object manipulationin correlation with synaptic development in juvenile vervets and rhesus macaques (Rakic et al. 1986). We feelthat this model is the best functional explanation for SH in young Japanese macaques.
For adults, the immediate motivation to SH appears to be different from that of young. With age,
adults exhibit fewer bouts of longer duration, involving relatively more complex behavioral patterns than young(Nahallage and Huffman 2007a). They concentrate on these more demanding manipulative activities, withseemingly intense concentration. They carry stones to their individually preferred locations to stone handle in an
unhurried, seemingly ‘leisurely’, manner. Sometimes older individuals sit nearby their preferred location,
waiting for others to leave, before going there to SH and performed the behavior most often in the afternoon. We
suggest that SH may allow adults to temporarily divert their attention away from the social interactive networkof associations with others by concentrating on this solitary activity. Since adults have already acquired thenecessary motor skills during early life, we propose that the ultimate function of SH is also different from that ofyoung. However, an equally important neurophysiological benefit may be gained by them from its practice. As
macaques grow older, a decline in memory and cognitive impairment and associated pathology (senile plaque,synapse loss) of the prefrontal cortex occurs (Hof and Duan 2001 for a review). Recently, a number of clinicalstudies have shown the benefits for elderly humans in significantly reducing the risk of acquiring such disease
through regular leisure activities involving concentrated mental activity (reading, playing board games, cards andmusical instruments) (e.g. Verghese et al. 2003). It has been suggested that the mental exercise of such leisureactivities may stimulate new neural growth around damaged parts of the brain caused by aging (Coyle 2003). A
shift in the role of SH activity from neural-motor development when young to basic maintenance in adults andre-generation of neurophysiological pathways in aging adults may be the prominent functions behind thesustained practice of this seemingly non-adaptive behavior in macaques.

11.7 Conclusions and future directions
In Japanese macaques, the individual acquisition and expression of SH behavior, the appearance,
diffusion, and maintenance of the SH culture, as well as inter-troop variation in the frequency, form, and context
of occurrence of SH were better explained by neuro-motor developmental constraints, socio-demographic factors(namely group size, age structure, inter-group transfers, opportunities for observational learning in mother-infant
dyads and among peer-playmates, and behavioral coordination at the group level), and environmental factors thatwere not stone-related (food provisioning) than by genetic differences, stone availability, or terrestriality. We
presented what may be the most extensive and systematic survey focused on the intra- and inter-group variabilityof a single type of behavior in monkeys to date. Through the combination of the method of elimination, crosssectional and longitudinal analyses, evidence for social transmission and durability of SH, and the view of
behavioral predispositions, we drew an overall picture of rich cultural diversity in a particular type of object play
behavior in Japanese macaques. Amongst the rare non-adaptive proposed traditional behaviors (see also ‘leafpile pulling’ in chimpanzees: Nishida and Wallauer 2003), SH is the most thoroughly documented.
To further explore the proximate causes of SH and the constraints on its propagation and long-termtransformation, our findings call for experimental approaches 1) to test the strength of the connection between
SH and feeding activities, 2) to assess the influence of the physical characteristics of the stones on stone
selectivity, 3) to examine the effect of the contagion process on the synchronized performance of SH, 4) toinvestigate how visual and auditory stimulus enhancement may help trigger SH behavior at the individual level,and 5) to evaluate the distinct effects of various social learning processes, such as social enhancement, social
facilitation, or imitation on the individual acquisition of SH. Such experiments could involve respectively: 1) the
manipulation of food provisioning schedule, 2) the introduction into the environment of new stones varying insize, shape, weight, and chemical properties, 3) the manipulation of size of subgroups from a social group held in
captive conditions, 4) the setting up of particular stone arrangements, such as piles of stones, to simulate SH byproducts and the playback of sounds produced during SH activity, and 5) the introduction of stones to semiisolated individuals or into caged-groups under the controlled conditions of captive settings.
Field studies on geographic variation in the occurrence of numerous behavioral patterns, supported bylongitudinal and experimental investigations of whether and how these behaviors are socially learned, canprovide extensive evidence for behavioral traditions in several primate species (Huffman et al. 2008).

11.8 Acknowledgments
The authors' are particularly grateful to the following sources that funded much of the research work
presented here. In particular, a Grant-In-Aid for scientific research (No. 1907421 to M.A. Huffman) sponsored250

by the Ministry of Education, Science, Sports and Culture, Japan, a Lavoisier postdoctoral Grant, Ministère desAffaires Etrangères, France and a JSPS (Japan Society for the Promotion of Science) postdoctoral fellowship(No. 07421 to J.-B. Leca), a 5.5 year scholarship from the Japanese Ministry of Education, Science and Culture
for graduate studies at Kyoto University’s Primate Research Institute to , and by travel funds to all three authors
from the HOPE Project, a core-to-core program sponsored by JSPS at different times to present work at
international meetings and to conduct related field research overseas.

11.9 References
Aisner R, Terkel J (1992) Ontogeny of pine cone opening behaviour in the black rat, Rattus rattus. Anim Behav 44:327–336.
Altmann J (1974) Observational study of behavior : Sampling methods. Behaviour 49:227–265.
Beck BB (1980) Animal tool behavior: The use and manufacture of tools by animals. Garland Press, New York.
Biro D, Inoue-Nakamura N, Tonooka R, Yamakoshi G, Sousa C, Matsuzawa T (2003) Cultural innovation and transmission of tool
use in wild chimpanzees: Evidence from field experiments. Anim Cogn 6:213–223.
Boesch C (1996) Three approaches for assessing chimpanzee culture. In : Russon AE, Bard KA, Parker ST (eds) Reaching intothought : The minds of the great apes. Cambridge University Press, Cambridge, p. 404–429.
Boesch C, Marchesi P, Fruth B, Joulian F (1994) Is nut cracking in wild chimpanzees cultural behavior? J Hum Evol 26:325–338.
Bortoff GA, Strick PL (1993) Corticospinal terminations in two New World primates: Further evidence that corticoneuronalconnections provide part of the neural substrate for manual dexterity. J Neurosci 13:5105–5118.
Bourgeois JP, Goldman-Rakic PS, Pakic P (1994) Synaptogenesis in the prefrontal cortex of rhesus monkeys. Cereb Cortex 4:78–96.
Coussi-Korbel S, Fragaszy DM (1995) On the relationship between social dynamics and social learning. Anim Behav 50:1441–1453.
Coyle JT (2003) Use it or lose it–do effortful mental activities protect against dementia? New Engl J Med 348:2489–2490.
Custance D, Whiten A, Fredman T (1999) Social learning of an artificial fruit task in capuchin monkeys (Cebus apella). J Comp
Psychol 113:13–23.
Drapier M, Thierry B (2002) Social transmission of feeding techniques in Tonkean macaques? Int J Primatol 23:105–122.
Dugatkin LA (1996) Interface between culturally based preferences and genetic preferences: Female mate choice in Poecilia
reticulata. Proc Nat Acad Sci USA 93:2770–2773.
Enggist-Dueblin P, Pfister U (2002) Cultural transmission of vocalizations in ravens. Anim Behav 64:831–841.
Fairbanks LA (2000) The developmental timing of primate play: a neural selection model. In: Parker ST, Langer J, McKinney ML(eds) Biology, brains and behavior: The evolution of human development. Oxford: School of American Research Press. p 131–
158.
Fisher J, Hinde RA (1950) The opening of milk bottles by birds. Brit Birds 42:347–357.
Fisher J, Hinde RA (1952) Further observations on the opening of milk bottles by birds. Brit Birds 44:393–396.
Fooden J, Aimi M (2005) Systematic review of Japanese macaques, Macaca fuscata (Gray, 1870). Field Zool 104:1–200.
Fragaszy DM, Perry S (2003) Towards a biology of traditions. In: Fragaszy DM, Perry S (eds) The biology of traditions: Models andevidence. Cambridge University Press, Cambridge, p. 1–32.
Galea MP, Darian-Smith I (1995) Postnatal maturation of the direct corticospinal projections in the macaque monkey. Cereb Cortex
5:518–540.
Goldberg TL, Wrangham RW (1997) Genetic correlates of social behaviour in wild chimpanzees: evidence from mitochondrialDNA. Anim Behav 54:559–570.
Gould SJ, Vrba ES (1982) Exaptation – a missing term in the science of form. Paleobiol 8:4–15.
Hall SL (1998) Object play by adult animals. In: Bekoff M, Byers JA (eds) Animal play: evolutionary, comparative and ecologicalperspectives. Cambridge: Cambridge University Press. p 45–60.
Hayasaka K, Ishida T, Horai S (1991) Heteroplasmy and polymorphism in the major noncoding region of mitochondrial DNA in
Japanese monkeys: Association with tandemly repeated sequences. Mol Biol Evol 8:399–415.
Hediger H (1964) Wild animals in captivity. New York: Dover Publications.
Hof PR, Duan H (2001) Age-related morphologic alteration in the brain of Old World and New World anthropoid monkeys. In: Hof
PR, Mobbs CV (eds) Functional neurobiology of aging. San Diego: Academic Press. p 435–445.
Hook MA, Lambeth SP, Perlman JE, Stavisky R, Bloomsmith MA, Schapiro SJ (2002) Inter-group variation in abnormal behaviourin chimpanzees (Pan troglodytes) and rhesus macaques (Macaca mulatta). Appl Anim Behav Sci 76:165–176.
Huffman MA (1984) Stone-play of Macaca fuscata in Arashiyama B troop: Transmission of a non-adaptive behavior. J Hum Evol
13:725–735.
Huffman MA (1991) History of Arashiyama Japanese Macaques in Kyoto, Japan. In: Fedigan LM, Asquith PJ (eds) The Monkeys of
Arashiyama: Thirty-five Years of Research in Japan and the West. Albany: SUNY Press. p 21–53.
Huffman MA (1996) Acquisition of innovative cultural behaviors in non-human primates: A case study of stone handling, a sociallytransmitted behavior in Japanese macaques. In: Galef B Jr, Heyes C (eds) Social Learning in Animals: The Roots of Culture.
Orlando: Academic Press. p 267–289.
Huffman MA, Quiatt D (1986) Stone handling by Japanese macaques (Macaca fuscata): Implications for tool use of stones.
Primates 27:413–423.
Huffman MA, Hirata S (2003) Biological and ecological foundations of primate behavioral tradition. In: Fragaszy DM, Perry S (eds)
The biology of tradition: Models and evidence. Cambridge: Cambridge University Press. p 267–296.
Huffman MA, Nahallage CAD, Leca JB (2008) Cultured monkeys, social learning cast in stones. Curr Dir Psychol Sci 17:410–414.
Itani J, Nishimura A (1973) The study of infrahuman culture in Japan. In: Menzel EW Jr (ed) Symposia of the Fourth International
Congress of Primatology, Vol 1. Karger, Basel, pp 26–60.
Jaman MF, Huffman MA (2008) Enclosure environment affects the activity budgets of captive Japanese macaques (Macaca fuscata)
Am J Primatol 70:1133–1144.
Kawai M (1965) Newly-acquired pre-cultural behaviour of the natural troop of Japanese monkeys on Koshima islet. Primates 6:1–
30.

251

Leca JB, Gunst N, Huffman MA (2007a) Japanese macaque cultures: Inter- and intra-troop behavioural variability of stone handling
patterns across 10 troops. Behaviour 144:251–281.
Leca JB, Gunst N, Huffman MA (2007b) Age-related differences in the performance, diffusion, and maintenance of stone handling,a behavioral tradition in Japanese macaques. J Hum Evol 53:691–708.
Leca JB, Gunst N, Watanabe K, Huffman MA (2007c) A new case of fish-eating in Japanese macaques: Implications for social
constraints on the diffusion of feeding innovation. Am J Primatol 69:821–828.
Leca JB, Gunst N, Huffman MA (2008a) Variability of food provisioning regimes and stone handling tradition in Japanesemacaques: a comparative study of ten troops. Am J Primatol 70:803–813.
Leca JB, Gunst N, Huffman MA (2008b) Of stones and monkeys: Testing ecological constraints on stone handling, a behavioral
tradition in Japanese macaques. Am J Phys Anthropol 135:233–244.
Leca JB, Nahallage CAD, Gunst N, Huffman MA (2008c) Stone-throwing by Japanese macaques: form and functional aspects of agroup-specific behavioral tradition. J Hum Evol 55:989–998.
Leca JB, Gunst N, Huffman MA (In review in Primates) A first case of dental flossing in Japanese macaques (Macaca fuscata):
implications for the determinants of behavioral innovation and the constraints on social transmission.
Lonsdorf EV (2005) Sex differences in the development of termite-fishing skills in the wild chimpanzees, Pan troglodytes
schweinfurthii of Gombe National Park, Tanzania. Anim Behav 70:673–683.
McGrew WC (2003) Ten dispatches from the chimpanzee culture wars. In de Waal FBM, Tyack PL (eds) Animal Social
Complexity. Intelligence, Culture and Individualized Societies. Cambridge: Harvard University Press, pp. 419–439.
McGrew WC, Ham RM, White LJT, Tutin CEG, Fernandez M (1997) Why don’t chimpanzees in Gabon crack nuts? Int J Primatol
18:353–374.
McGrew WC, Marchant LF, Scott SE, Tutin CEG (2001) Intergroup differences in a social custom of wild chimpanzees: Thegrooming hand-clasp of the Mahale mountains. Curr Anthrop 42:148–153.
Nahallage CAD, Huffman MA (2007a) Age-specific functions of stone handling, a solitary-object play behavior, in Japanesemacaques (Macaca fuscata). Am J Primatol 69:267–281.
Nahallage CAD, Huffman MA (2007b) Acquisition and development of stone handling behavior in infant Japanese macaques.
Behaviour 144:1193–1215.
Nahallage CAD, Huffman MA (2008a) Comparison of stone handling behavior in two macaque species: Implications for the role ofphylogeny and environment in primate cultural variation. Am J Primatol 70:1124–1132.
Nahallage CAD, Huffman MA (2008b) Environmental and social factors associated with the occurrence of stone-handling behavior
in a captive troop of Macaca fuscata. Int J Primatol 29:795–806.
Nishida T (1987) Local traditions and cultural transmission. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, StruhsakerTT (eds) Primate Societies, University of Chicago Press, Chicago, pp 462–474.
Nishida T, Wallauer W (2003) Leaf-pile pulling: an unsual play pattern in wild chimpanzees. Am J Primatol 60:167–173.
Pellis SM (1991) How motivationally distinct is play? A preliminary case study. Anim Behav 42:851–853.
Pellis SM, O’Brion DP, Pellis VC, Teitelbaum P, Wolgin DL, Kennedy S (1988) Escalation of feline predation along a gradient fromavoidance through ‘‘play’’ to killing. Behav Neurol Sci 102:760–777.
Pereira, ME, Fairbanks LA (1993) Juvenile Primates: Life History, Development and Behavior. University of Chicago Press,
Chicago.
Perry S, Manson JH (2003) Traditions in monkeys. Evol Anthropol 12:71–81.
Perry S, Panger M, Rose LM, Baker M, Gros-Louis J, Jack K, MacKinnon KC, Manson J, Fedigan L, Pyle K (2003a) Traditions inwild white-faced capuchin monkeys. In: Fragaszy DM, Perry S (eds) The Biology of Traditions: Models and Evidence,
Cambridge University Press, Cambridge, pp 391–425.
Quiatt D, Huffman MA (1993) On home bases, nesting sites, activity centers, and new analytic perspectives. Curr Anthropol 34:68–
70.
Rakic P, Bourgeois JP, Eckenhoff MF, Zecevic N, Goldman-Rakic PS (1986) Concurrent over- production of synapses in diverse
regions of the primate cerebral cortex. Science 232:232–235.
Ramsey JK, McGrew WC (2005) Object play in great apes. Studies in nature and captivity. In: Pellegrini AD, Smith PK (eds) The
nature of play–great apes and humans. Guilford Press, New York, p 89–112.
Rendell L, Whitehead H (2001) Culture in whales and dolphins. Behav Br Sci 24:309–382.
Smith EO (1978) A historical view on the study of play statement of the problem. In: Smith EO (ed) Social play in primates.
Academic Press, New York, p 1–32.
Takahata Y, Huffman MA, Suzuki S, Koyama N, Yamagiwa J (1999) Male-female reproductive biology and mating strategies inJapanese macaques. Primates 40:143–158.
Terkel J (1996) Cultural transmission of feeding behaviour in the black rat (Rattus rattus). In: Heyes CM, Galef BG Jr (eds) Social
Learning in Animals: The Roots of Culture, Academic Press, San Diego, pp 17–47.
Thierry B (1994) Social transmission, tradition and culture in primates: From the epiphenomenon to the phenomenon. Techn Cult
23/24:91–119.
Tomasello M (1990) Cultural transmission in chimpanzee tool use and signaling? In: Parker ST, Gibson KR (eds) “Language” andIntelligence in Monkeys and Apes, Cambridge University Press, Cambridge, pp 274–311.
Tomasello M (1999) The Cultural origins of Human Cognition. Cambridge: Harvard University Press.
van Schaik CP (2003) Local traditions in orangutans and chimpanzees: social learning and social tolerance. In: Fragaszy DM, Perry
S (eds) The biology of tradition: Models and evidence. Cambridge: Cambridge University Press. p 297–328.
van Schaik CP, Fox EA, Fechtman LT (2003a) Individual variation in the rate of use of tree-hole tools among wild orang-utans:
Implications for hominin evolution. J Hum Evol 44:11–23.
van Schaik CP, Ancrenaz M, Borgen G, Galdikas B, Knott CD, Singleton I, Suzuki A, Utami SS, Merill M (2003b) Orangutan
cultures and the evolution of material culture. Science 299:102–105.
Verghese J, Lipton RB, Hall CB, Kuslansky G, Katz MJ (2003) Low blood pressure and the risk of dementia in very old individuals.
Neurol 61:1667–1672.
Watanabe K (1994) Precultural behaviour of Japanese macaques: Longitudinal studies of the Koshima troops. In: Gardner RA,
Chiarelli AB, Gardner BT, Plooij XF (eds) The Ethological Roots of Culture, Kluwer Academic Publishers, Dordrecht, pp 81–
94.

252

Whiten A (2005) The second inheritance system of chimpanzees and humans. Nature 437:52–55.
Whiten A, Goodall J, McGrew WC, Nishida T, Reynolds V, Sugiyama Y, Tutin CEG, Wrangham RW, Boesch C (1999) Cultures inchimpanzees. Nature 399:682–685.
Yamagiwa J, Hill D (1998) Intraspecific variation in the social organization of Japanese macaques: Past and present scope of fieldstudies in natural habitats. Primates 39:257–273.
Yamakoshi G (2001) Ecology of tool use in wild chimpanzees: Toward reconstruction of early hominid evolution. In: Matsuzawa T(ed) Primate origins of human cognition and behavior. Springer, Tokyo, pp. 537–556.

Fig. 11.1. Five SH patterns. (a) cuddle, (b) rub together, (c) rub on surface, (d) clack, (e) carry, and (f) a motherinfant dyad performing SH simultaneously. Credit: photos (a), (c), and (f) by JB Leca, photo (b) by N Gunst, andphotos (d) and (e) by MA Huffman.

Fig. 11.2. Glance-6476 (three-year-old, middle ranking female): First individual recognized to perform SH on
December 7, 1979.

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Fig. 11.3. Map of the sites in Japan where SH has been studied or reported. Sources: Arashiyama,
Funakoshiyama, Gagyusan, Takagoyama, Takasakiyama, Yakushima (Huffman & Hirata, 2003), Arashiyama,
Inuyama (Primate Research Institute and Japan Monkey Centre), Koshima, Shodoshima, Takasakiyama (Leca etal., 2007a), Tsubaki (Leca, unpublished data), Miyajima (Watanabe, pers. comm.).

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CategoryName

Definition

Investigative activities
Bite
Hold
Lick
Move inside mouth
Pick
Put in mouth
Sniff

Bite a stone
Pick up a stone in one's hand and hold on to it, away from the body
Lick a stone
Make a stone move inside one's mouth with tongue or hands
Pick up a stone
Put a stone in one's mouth and keep it sometime
Sniff a stone

Locomotion activities
Carry
Carry in mouth
Grasp walkMove and push/pull
Toss walk

Carry a stone cuddled in hand from one place to another
Carry a stone in mouth while locomoting
Walk with one or more stones in the palm of one or both hands
Push/pull a stone with one or both hands while walking forward/backward
Toss a stone ahead (repeatedly) and pick it up while walking

Collection or gathering activities
CuddleGather
Grasp with hands
Pick up
Pick and drop
Pick up small stones

Take hold of, grab or cradle a stone against the chest
Gather stones into a pile in front of oneself
Clutch a stone or a pile of stones gathered and placed in front of oneself
Pick up a stone and place it into one's hand
Pick up a stone and drop it repeatedly
Pick up small stones and hold them between fingertips (like the picking up of
wheat grains)

Percussive or rubbing sound producing activities
Clack
Clack stones together (both hands moving in a clapping gesture)
Combine with object
Combine (rub or strike) a stone with an object different from a stone (fooditem, piece of wood, metal, etc.)
Flint
Strike a stone against another held stationary
Flint in mouth
Strike a stone against another held in mouth
Pound on surface
Pound a stone on a substrate
Rub in mouth
Rub a stone against another held in mouth
Rub/roll on surface
Rub or roll a stone on a substrate
Rub stones together
Rub stones together
Rub with mouth
Rub a surface with a stone held in mouth
Scatter
Scatter stones about, on a substrate, in front of oneself
Shake in hands
Take stones in one's open palm hand and shake the stones with the handmoving back and forth
Slap
Slap, tap or pound a stone with one’s fingertips or palm of hand
Swipe
Swipe stones together (both hands moving in a sweeping gesture)
Tap in mouth
Tap a stone held in mouth with fingertips or palm of hand
Other complex manipulative activities
Flip
Put in water
Roll in hands
Rub/put on fur
Rub with hands
Spin
Stone-groom
Throw
Throw and jump
Throw and run
Throw and sway
Wash
Wrap in leaf

Turn a stone over with both hands
Put a stone in water
Roll a stone in one's hands
Rub or put a stone on one’s fur while self-grooming
Hold a stone in one hand and rub it with the other (like potato-washing)Spin a stone around on the ground using two fingers of one hand or both
hands (one moving forward and the other backward)
Allo-groom with a stone
Throw a stone without jumping or running
Throw a stone and jump (or vice versa)
Throw a stone and run (or vice versa)
Throw a stone and sway (or vice versa)
Put a stone in water or pick up a stone from water and rub it with hands
Wrap a stone in a leaf (or wrap a leaf around a stone)

Table 1. Forty five SH patterns performed by Japanese macaques and categorized according to general activity
patterns (after Leca et al., 2007a).

255

Captive troops_________________________
SH pattern

Ara.A Wak.A Takh.

Investigative activities
Lick
P
H
C
Move inside mouth
H
H
Pick
C
P
P
Put in mouth
P
H
H
Locomotion activities
Carry
C
H
Carry in mouth
H
C
Move and push/pullC
H
Toss walkP
PC
Collection (gathering) activities
Pick and dropP
Pick up small stones
H
Percussive or rubbing sound producing activities
Clack
P
P
H
Combine with object
P
C
Flint
H
C
Flint in mouth
P
P
Pound on surfaceP
H
Rub in mouthPP
Rub stones together
HC
Rub with mouth
P
P
Shake in hands
P
Slap
H
Swipe
P
P
Tap in mouth
P
Other complex manipulative activities
FlipPH
Put in waterP
Rub/put on fur
H
P
Spin
P
Stone groom
Throw
P
P
Throw and jumpH
Throw and run
PThrow and swayP
Wash
P
Wrap in leaf
H
No. pattern occurrence

5

20

32

Free-ranging troops_________________________________________JMC* Kosh.

Ara.E

Sho.A Sho.B Tak.B Tak.C

P
P
P
P

P
P
-

P
P
P
P

(-)
(-)
P
H

(-)
(-)
(-)
P

P
P
(-)
P

P
P
P
P

H
P
P
P

P
P
-

C
P
H
H

H
P
P
(-)

H
P
P
(-)

H
P
P
P

H
P
P
P

-

-

P
H

P
(-)

(-)
(-)

P
P

H
P

H
P
P
H
P
P
P
-

-

H
P
P
C
P
P
-

P
(-)
P
(-)
P
(-)
P
(-)
(-)
(-)
(-)
(-)

P
P
P
(-)
(-)
(-)
P
(-)
P
(-)
(-)
(-)

P
(-)
P
(-)
(-)
(-)
H
(-)
P
(-)
P
(-)

P
P
H
P
H
P
H
(-)
P
(-)
H
(-)

P
P
P
P
-

-

P
P
P
H
-

(-)
(-)
(-)
(-)
P
(-)
(-)
(-)
(-)
(-)
(-)

(-)
(-)
P
(-)
(-)
(-)
(-)
(-)
(-)
(-)
(-)

P
(-)
(-)
(-)
(-)
(-)
(-)
(-)
(-)
(-)
(-)

(-)
(-)
(-)
(-)
(-)
(-)
(-)
(-)
(-)
(-)
(-)

19

4

20

11

10

15

19

Table 2. Frequency of occurrence of the 33 SH patterns that are not observed in all the ten studied troops of Japanesemacaques, four captive (PRI Arashiyama = Ara.A, Wakasa = Wak.A, Takahama = Takh., and Japan Monkey Center = JMC)
and six free-ranging troops (Koshima = Kosh., Arashiyama E = Ara.E, Shodoshima = Sho.A and Sho.B, Takasakiyama =Tak.B and Tak.C); No asterisks: Macaca fuscata fuscata troops, asterisk: M. f. yakui troop; C: Customary: Exhibited by atleast 90% of the sampled individuals in at least one age class, or at least 70% of the sampled individuals in at least two age
classes, H: Habitual: Not customary but observed at least three times in several individuals, consistent with some degree ofsocial transmission, P: Present: Not customary or habitual, but observed at least once, -: Absent: Not observed despite
sufficient observation time (at least 90 hours of total observation time), (-): Unknown: Not observed but absence uncertain
because of insufficient observation time (less than 90 hours of total observation time); No. pattern occurrence: Number of SH
patterns scoring at least the Present status; Neighboring troops living at the same site (respectively two troops at Shodoshima
and two troops at Takasakiyama) are represented inside a dotted-line frame.

256Primates
DOI 10.1007/s10329-009-0159-9

ORIGINAL ARTICLE

The first case of dental flossing by a Japanese macaque (Macaca
fuscata): implications for the determinants of behavioral
innovation and the constraints on social transmission
Jean-Baptiste Leca Æ Noëlle Gunst Æ Michael A. Huffman

Received: 1 April 2009 / Accepted: 20 June 2009
Ó Japan Monkey Centre and Springer 2009

Keywords Behavioral variant  Constraint  Innovation 
Tradition  Tool-use

Abstract We report the first case of dental flossing
behavior by a Japanese macaque. We used cross-sectional
data to assess the presence of this novel tool-use behavior
at the group-level. Although this behavior was performed
frequently by a central middle-ranking middle-aged female
during her grooming interactions, and appeared at least
four years ago, it remained idiosyncratic to its innovator,
and until now has not spread to other group members. We
examined the factors that may have favored this innovation, including the environmental context, the individual
characteristics of the innovator, and the structural andfunctional aspects of the behavior. Group size, kinship, anddominance are socio-demographic factors that are likely tolimit the opportunities for any group member to observe
the innovator, and thus constrain the diffusion of thispotential candidate as a new behavioral tradition. This is
one of the rare studies to document the spontaneous
appearance of tool-use behavior in primates under natural
conditions. Identifying the determinants of innovations andthe constraints on their diffusion within social groups of
non-human primates is of special interest to understanding
cultural evolution.

Introduction
Innovation is defined as the discovery of novel information,
the emergence of new behavioral patterns, or the performance of existing behaviors in a novel context (Reader andLaland 2003). When a novel behavioral practice, initiallyinvented by an individual—the innovator—spreads to othergroup members, and is dependent on social means for
its diffusion and maintenance, it becomes a tradition(Fragaszy and Perry 2003). Various factors may enhance orlimit the likelihood of innovation and subsequent propagation within a group, including individual attributes (age,sex, social rank, personality), social relationships (dominance, affiliation, kinship), group size and cohesiveness,and structural, contextual, and functional aspects of the
new behavior (Huffman and Hirata 2003).
Innovations and traditions can be found in various animal
taxa (reviewed by Laland and Hoppitt 2003). Identifying
the determinants of the spontaneous appearance of new
behavioral patterns and the constraints on their diffusion
within social groups of non-human primates is of special
interest to understanding cultural evolution in hominids(McGrew 1992). On the one hand, there are numerous
examples of socially-transmitted behavioral innovations inseveral non-human primate species (Huffman 1996; Whiten
et al. 1999; Perry et al. 2003; van Schaik et al. 2003).
However, little is known about the initial process by whichnovel behavioral patterns emerge spontaneously and thevarious factors influencing the rate, speed, and route of theirsubsequent transmission within a group (but see Kummer
and Goodall 1985; Tanaka 1998; Huffman and Hirata 2003;

J.-B. Leca (&)  M. A. Huffman
Section of Social Systems Evolution, Primate Research Institute,
Kyoto University, 41-2 Kanrin,
Inuyama, Aichi 484-8506, Japane-mail: jbtleca@yahoo.com
M. A. Huffman
e-mail: huffman@pri.kyoto-u.ac.jp
N. Gunst
Odum School of Ecology, University of Georgia,
Athens, GA 30602-2202, USAe-mail: noelle.gunst@gmail.com

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Bonnie and de Waal 2006; Leca et al. 2007a; for a few
notable exceptions).
On the other hand, only a subset of innovations
becomes traditions. Many new behaviors have beenreported to appear in primate troops, but were either
idiosyncratic, or independently adopted by very few
individuals, or their performance was restricted to a smallclass of the population, and for some reason, they neverspread widely within the group by social means. Wild
chimpanzees (Pan troglodytes) show a variety of spontaneous tool-use innovations (sensu Beck 1980) peculiar to
one individual and bound to disappear after the death oftheir unique performers (reviewed by Nishida et al. 2009).
Health maintenance, a sub-division of self-medicative
behavior (sic Huffman 2007), in the form of the use oftwigs as ‘‘toothpicks’’ by one or very few individuals has
been reported in great apes, including chimpanzees(McGrew and Tutin 1972, 1973), bonobos, Pan paniscus(Ingmanson 1996), and orang-utans, Pongo pygmaeus(Russon et al. 2009). Although macaques are not frequenttool-users (Beck 1980; but see Malaivijitnond et al. 2007;
Leca et al. 2008a), dental flossing behavior has beenreported in long-tailed macaques, Macaca fascicularis(Watanabe et al. 2007). The spontaneous and idiosyncratic
use of tools in hygiene contexts, such as stones in allogrooming and sticks as vaginal probes have been occasionally reported in this genus (Weinberg and Candland
1981; Sinha 1997).
The role of the importance of these behaviors to theperformers themselves in the likelihood to innovate hasreceived little attention (Kummer and Goodall 1985).
Surprisingly, few attempts have been made to address thefactors that would constrain or even impede the spread ofcertain novel behavioral patterns (Reader and Laland2003). As Huffman (1996) pointed out, it is critical toknow the history of a behavioral innovation in order toassess how environmental factors and social influences
may enhance or limit its propagation within a group.
In an effort to encourage the compilation of relevant
data on the determinants of behavioral innovations in nonhuman primates and stimulate general interest in the constraints on their diffusion within social groups, we report
the first case of dental flossing (DF) behavior in a freeranging group of Japanese macaques (Macaca fuscata). We
systematically documented the frequent use, by an adultfemale, of hair as dental floss to remove food remains stuck
between her teeth. We used cross-sectional data to assess
the presence of this novel tool-use behavior at the grouplevel. We examined the initial conditions that may havefavored this innovation and evaluated the various constraints that may account for the lack of diffusion within
the group of this potential candidate for a new behavioral
tradition in Japanese macaques.

Methods
Study group
The following observations were made on the free-ranging Arashiyama E troop of Japanese macaques at the
Iwatayama Monkey Park, Arashiyama, Kyoto Prefecture,
Japan. Japanese macaques have been provisioned andstudied since 1954 at Arashiyama (Huffman 1991; see
Leca et al. 2008b for details on provisioning conditions).
All group members were individually identified, and theirages and kin relations through maternal lineages were
known. The study group contained 145 individuals of 15
separate matrilines. All age/sex classes were present,
including 56 old adults, aged 16 years and more (52females and four males), 25 middle-aged adults, between
11 and 15 years old (21 females and four males), 15 young
adults, between 7 and 10 years old (14 females and onemale), 22 subadults, between 4 and 6 years old (14 females
and eight males), 13 juveniles, between 2 and 3 years old(six females and 7 males), and 14 yearlings and infants(six females and eight males) (Leca et al. 2007b).
Data collection
To garner detailed data on the DF behavior performed by
the innovator, JBL collected 15-min video-recorded focalanimal samples (Altmann 1974) of subject Chonpe-69-8594 with a Sony DCR-HC48 digital camera. This focal
subject was sampled independently of its activity,
throughout the day, but not twice in the same hour-block.
The typical duration of a focal session was 15 min. If the
focal subject performed DF during the final 2 min, theobservation was extended for 5 min, or longer if DF was
still in progress. A DF event (or DF behavior) was considered to occur any time an individual:
1.

2.

stretched one or a few pieces of its own hair or anotherindividual’s hair, by either grasping the tip(s) of thehair with one or both hands, or by clutching its lips
from the basal to the distal end of the hair; andinserted the hair between the upper or lower front teeth(incisors or canines) by performing repeated teethchattering to remove food remains stuck between theteeth.

Subjects were never encouraged to floss for the purposeof this study (by providing them with hair, for example: cf.
Watanabe et al. 2007), but instead observations were madeon spontaneous DF behaviors. Because DF may serve to
remove food remains stuck between the teeth, we tested theeffect of feeding activity on DF by sampling the innovator
within 1 h after provisioning time (post-feeding focals) andany other time throughout the day (non-feeding focals).

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6.

To assess the DF prevalence at the group-level (percentage of individuals performing the DF behavior), JBL
and NG collected continuous 15 min pen-and-paper focalanimal samples on the other group members (Altmann1974). We selected the focal individual independently of
its activity and by using a semi-random procedure (Lecaet al. 2007b, c, 2008a, b, c). However, preliminary analysis
on the context of occurrence of DF in Chonpe-69-85-94
showed that all DF behaviors were performed duringgrooming activity. Therefore, during the last 10 days of thestudy period, and in order to supplement the data set andreach a threshold of 30 min of grooming patterns in a
maximum number of group members, we also collected aseries of 2-min pen-and-paper focal-animal samples in anordered list of temporarily undersampled subjects. In thisseries, an individual was eligible as the next focal subject if
it was engaged in self-grooming activity or involved as
participant in an allo-grooming interaction, and the subject
with least cumulative data was given priority. We recorded
the following activities: self-grooming, allo-grooming,
dental flossing, feeding, foraging, locomoting, resting,agonistic interaction (avoidance or aggression), and other.
We defined grooming as the activity consisting of combing
and/or picking through its own or another individual’s hair(self-grooming and allo-grooming, respectively) with thehands or mouth. Given the potential risk of being aggressedby dominant flossing recipients, we established the dominance hierarchy within the group by recording ad libitum
data (Altmann 1974) on the direction of dyadic agonistic
interactions.
Visibility was excellent. The observers could approachand sample the subjects within 2–5 m. The following
observations were made between 0800 and 1600 hours,
from June 10 to July 31 and from September 9 to October30, 2008.

As for the DF patterns, we distinguished three different
variants or DF techniques. First, the ‘‘stretching withmouth’’ technique was a behavioral sequence lastingaround 5 s and consisting of stretching its own hair or
another individual’s hair (typically several long hairpieces)by clenching its lips on to the basal part of the hair,inserting the hair between the front teeth by slightly pullingits head downwards, and pulling the head backwards while
gradually moving the lips to the distal end of the hair andperforming repeated teeth-chattering (Fig. 1a). Second, the‘‘stretching with hand’’ technique consisted of stretching its
own hair or another individual’s hair by grasping andpulling the tip(s) of the hair between the thumb and forefinger of one hand, moving the mouth to the hair, andinserting the hair between the front teeth by performing
repeated teeth-chattering (Fig. 1b). Third, the ‘‘plucking’’
technique consisted of pulling out its own hair with one
hand, holding the hair horizontally by grasping and pulling
the tips of the hair between the thumb and forefinger ofboth hands, taking the hair to the mouth, and inserting thehair between the front teeth by performing repeated teethchattering (Fig. 1c).
We arbitrarily defined a DF bout as the display of DF
activity with possible pauses of no longer than 120 s. If theindividual resumed DF within 120 s after pausing, then the
two DF episodes were considered as a single DF bout. If
DF was resumed more than 120 s after pausing, this would
mark the start of a new DF bout. A DF bout could consistof several DF events interspersed with pauses of no longer
than 120 s.
To assess the prevalence of DF, we ascribed each groupmember to one of three DF categories: verified flosser,
verified non-flosser, or non-verified individual. An individual was labeled a verified flosser if at least one DF event
had been recorded during its total focal time. We labeled an
individual as a verified non-flosser if it was sufficiently
sampled during grooming activity (at least 30 min of focal
data) but was never observed performing DF. When an
individual was not observed performing DF, but wasinsufficiently sampled during grooming activity (between 6
and 30 min of focal data), it was labeled as non-verified
individual. Because individuals aged one year and lessseldom groom, they were not included in the analyses. Of
the 17 non-sampled group members (with no focal data),
15 were peripheral males and two were peripheral females.
We verified the linearity of the dominance hierarchy
for 87 adult females, including the innovator Chonpe-6985-94 (h0 = 0.25, directional consistency index = 0.96,
p \ 0.001; cf. de Vries 1995). We distinguished three

Data analysis
We collected a total of 170.7 h of focal data, including
17.8 h on Chonpe-69-85-94 and 152.9 h on 113 othergroup members. These data comprised 5.8 and 64.4 h ofgrooming activity, respectively. From the video samples,
NG recorded:
1.
2.
3.
4.

5.

whether or not the focal subject licked off the foodremains mixed with saliva and attached to the hairafter each DF event.

the duration of the same activities as for paper-andpaper samples;the identity of the focal subject’s grooming partners;
the number and duration of the DF events;from which body part the hair was used to floss (head/neck, chest, belly, back, ano-genital region, arm, andlegs);
whether the focal subject used the same or different
hair in the successive DF events within a DF bout; and

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Fig. 1 a ‘‘Stretching withmouth’’ technique.
b ‘‘Stretching with hand’’technique during self-grooming(left) and during allo-grooming(right). c ‘‘Plucking’’ techniqueclasses of individuals according to their dominance rank:
high-ranking, middle-ranking, and low-ranking individuals (N = 29 for each dominance class). Inter-observer
reliability kappa coefficients were k = 0.89 for individual
identities and 0.94 for all activities and behaviors
including DF. Intra-coder reliability kappa coefficient was
k = 0.87 (cf. Martin and Bateson 1993).
We reported percentages on number of events or durations and mean values ± the standard deviation (SD). To
compare the observed frequencies of the two categories of
dichotomous variables (e.g., use of same hair vs. use ofdifferent hair) to the frequencies expected under a binomial
distribution with a probability parameter of 0.5, we used
two-tailed binomial tests. To test the effect of dominanceon the choice of flossing recipients, we used a two-tailed
Mann–Whitney U test to compare the cumulative durationsof DF events on lower-ranking and higher-ranking recipients. Statistical analyses were performed using the SPSS
13.0 analytical program. Significance levels were set at
a = 0.05.

Results
Social profile of the innovator: status, kinship,
and partners
The innovator Chonpe-69-85-94 was a central-troop (cf.
Leca et al. 2007b) middle-aged (14 year-old) female. She
was middle-ranking, and ranked 42 out of 87 adult females.
She had no offspring and only two close kin: her mother(Chonpe-69-85) and her younger brother (Chonpe-69-8506). The 12 other living members of the Chonpe matriline
were distant kin (Leca, unpublished data).
Out of 130 potentially available grooming partners,
Chonpe-69-85-94 had grooming interactions with 11 individuals. She devoted 71.9% of her grooming to her two
close kin, including 43.1% to her mother and 28.8% to her
younger brother. The nine other grooming partners totaled
28.1% of grooming interactions, ranging from 0.4 to 5.3%.
Among them, five individuals were dominant over Chonpe69-85-94. The next results relate to Chonpe-69-85-94 only.

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The dental flossing innovation

350
Self-grooming

300

Number of DF events

Frequency and duration of DF activity and DF behavior
The DF behavior occurred in 41 out of 70 focal samples(58.6%) collected on Chonpe-69-85-94. We recorded 63
DF bouts in 17.8 h of focal samples. Thus the DF frequency was 3.5 bouts per hour. The mean duration of DF
bouts was 2.1 ± 3.0 min, ranging from 0.1 to 11.8 min.
The mean number of DF events per bout was 9.3 ± 16.0,
ranging from 1 to 81. The mean duration of DF events was
5.0 ± 2.4 s and the DF activity represented 4.6% of thetotal activity budget of Chonpe-69-85-94.

Allo-grooming

250
200
150
100
50
0

Stretch with mouth

Stretch with hand

Pluck

DF techniqueFig. 2 Distribution of DF events according to the three DF
techniques and the type of grooming activity

seconds selecting and removing several hairpieces from thefirst tuft clutched before using the remaining ones to floss.
Such patterns to select the number and/or types of hair wasless frequent when the ‘‘stretching with mouth’’ and the‘‘stretching with hand’’ techniques were performed (31.8
and 59.3%, respectively). Overall, video close-ups showedthat the number of pieces of hair used as floss ranged from
one to about five or six pieces. In the successive DF events
within a DF bout, the focal subject used significantly moredifferent hairs than the same hairs (210 vs. 142 events,
respectively; two-tailed binomial test (0.5), p \ 0.001).
After flossing, the focal subject very occasionally discarded
the hair immediately; usually, however, she almost systematically looked at the hair and then licked off saliva(presumably mixed with food remains) attached to the hair
before discarding it (18 vs. 571 events, respectively; twotailed binomial test (0.5), p \ 0.001). Although there werepreferred flossing sites on the flossing recipient’s body, thehair used to floss came from every body part (back 221
events, chest 96 events, arm 83 events, belly 79 events, leg
74 events, ano-genital region 25 events, and head/neck 11
events).
When DF was associated with allo-grooming, Chonpe69-85-94 had flossing interactions with 7 of her 11
grooming partners. She devoted 88.9% of her flossing
interactions to her two close kin, including 74.9% to hermother and 14.0% to her younger brother. We found asignificant effect of dominance on the choice of flossing
recipients among the grooming partners: after excluding
the two close kin from the analysis, the duration of DF
events on higher-ranking recipients was significantly lower
than on lower-ranking recipients (Mann–Whitney U test:
Nlower-ranking = 4, Nhigher-ranking = 5; z = -2.56; p =0.011). In other words, the flosser spent less time flossing
on dominant than on subordinate individuals. It should also
be noted that during the three cases of DF bouts ending
with aggression directed from the flossing recipients to theflosser (having its hair stretched is presumably painful), theformer were dominant over the latter.

Context of occurrence of the DF behavior
The DF behavior was always associated with grooming
activity, either starting the grooming sequence (9.5%),
ending it (15.9%), or being interspersed within (74.6%).
Out of 589 DF events, 167 (28.4%) were recorded during
self-grooming activity with a frequency of 1.3 events per
minute, whereas 422 (71.6%) occurred during allogrooming interactions, with a frequency of 1.9 events per
minute. Out of 63 DF bouts, 27 (42.9%) were associatedwith self-grooming activity at a frequency of 0.2 bout per
minute, whereas 36 (57.1%) occurred during allo-groominginteractions, with a frequency of 0.2 bouts per minute.
Overall, there were 1.7 DF events and 0.2 DF bouts
per minute devoted to grooming activity. In terms oftime budget, the DF activity represented 10.8% of timespent self-grooming, 15.6% of time spent allo-grooming,and 13.9% of time devoted to grooming in general.
There was no significant difference in the occurrenceof DF behavior between post-feeding and non-feeding
focals (Nwith DF = 20 and 21, Nwithout DF = 15 and 14,
respectively, v2 = 0.06, df = 1, p = 0.808).
Form and recipients of the DF behavior
In 100% of DF events, Chonpe-69-85-94 used hair to floss
her teeth and never used any other object or her fingers
alone. Among the 589 DF events, the ‘‘stretching withhand’’ technique was the most frequently performed(65.4%), followed by the ‘‘stretching with mouth’’ technique (28.7%), and the ‘‘plucking’’ technique (5.9%). For
the ‘‘stretching with mouth’’ and ‘‘stretching with hand’’techniques, most of DF events were performed during allogrooming (62.1 and 82.3%, respectively), whereas the
opposite occurred for the ‘‘plucking’’ technique, with 35
DF events recorded during self-grooming and none duringallo-grooming interactions (Fig. 2).
In almost all the DF events where the ‘‘plucking’’
technique was performed (90.9%), the flosser spent a few

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Age
OlAd
MdAd
YgAd
SuAd
Juv

50

45

40

35

30

25

20

15

10

5
Nf = 107

Ntot = 131

5
Nm = 24

10

Fig. 3 Age and sex distribution of verified flosser (observed
performing DF at least once: black areas), verified non-flossers(sampled at least 30 min during grooming activity and in which DF
was not observed: white areas), non-verified individuals (in which DF
was not observed, but individuals were undersampled—less than
30 min—during grooming activity: grey areas), and non-sampledindividuals (horizontal lines) according to age and sex classes. Juv
juvenile, SuAd subadult, YgAd young adult, MdAd middle-aged adult,
OlAd old adult. The left part of the distribution represents the numberof females (Nf), and the right part represents the number of males(Nm), Ntot: total number of individuals

Current prevalence of the DF behavior
at the group-level

Individual characteristics of the DF innovator
Because DF is always grooming-related, the behavior ismore likely to appear in frequent groomers, i.e. central
group members, than in individuals less involved ingrooming interactions, i.e. peripheral group members (cf.
Nakamichi and Shizawa 2003). Thus, it is not surprisingthat the innovator was a central individual. We could notassess whether the social status of the innovator—middleranking—was consistent with other findings, because mostreports broadly classified innovators as either high or lowranking, with no intermediate dominance rank (Reader andLaland 2001).
As an adult female, the current age of the innovator wasconsistent with most studies, whereas the sex was not. It
has been found that innovators were more frequently males
and adults than females and non-adults (reviewed byReader and Laland 2001). However, the innovator may
have been younger when she first performed the DF
behavior. This is consistent with previous research showingthat most Japanese macaque innovators are juvenile
females (Kawai 1965; Itani and Nishimura 1973; Huffman
1984; Kawai et al. 1992).
Finally, Chonpe-69-85-94 might have temperamental
traits that made her prone to behavioral innovation.
Despite extensive observation of most troop members in astudy of stone handling behavior, she was the only individual observed repeatedly rolling small stones on thepalm of her hand while intensively grooming her palm
and presumably trying to remove a spine stuck in it(Leca, personal observation). This first report of Japanesemacaques seeming to attempt to use stones in a healthmaintenance context is suggestive of a generally inventive
temperament. Sinha (2005) suggested the role of temperament in bipedal begging innovation by bonnet
macaques (Macaca radiata).

From 152.9 h of this focal data on 113 other central groupmembers, we obtained 103 verified non-flossers and ten
non-verified individuals. Therefore, the DF behavior was
reasonably declared absent from the rest of the group andthe prevalence of DF at the group-level was one verified
flosser out of 113 central-troop individuals, i.e. around
0.01% (Fig. 3).

Discussion
Determinants of the DF innovation
Environmental opportunities to start flossing one’s teeth
Because they are provisioned with food several times aday, Arashiyama E troop members have ‘‘free time on theirhands’’, and this opportunity could lead them to further
explore various objects and incorporate them into feeding
activities (Huffman and Quiatt 1986; Leca et al. 2008b).
These artificial conditions are likely to enhance theappearance of food-related tool-use, such as the use of
dental floss. Provisioning has relaxed selective pressures on
foraging, and created favorable environmental conditions
under which various behavioral innovations by Japanesemacaques may occur (Leca et al. 2007a, 2008c).
Likewise, Watanabe et al. (2007) suggested that the DF
behavior exhibited by a troop of long-tailed macaquesliving around a Buddhist temple in Thailand, probably
originated from special anthropogenic circumstances:because the shrine visitors worshiped the monkeys, they
allowed them to climb up their shoulders and pull out somehair from their heads to use as dental floss.

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How and why inventing DF?

Emergence of new DF variants

Because chance may account for a good number ofbehavioral innovations (Reader and Laland 2003), andDF was always associated with grooming activity, wesuggest that the DF innovation is an accidental byproduct of grooming. Thus, the following is a reasonable
scenario: during regular grooming episodes, Japanesemacaques sometimes bite into hair or pull it throughtheir mouths to remove external parasites, such as louse
eggs (Tanaka and Takefushi 1993). Because of particular anatomical constraints such as diastema (i.e. gaps
between incisors), pieces of hair may accidentally havestuck between Chonpe-69-85-94’s teeth, and as she drew
them out, she may have noticed the presence of foodremains attached to them. The immediate reward oflicking the food remains off the hair may have encouraged her to repeat the behavior for the same effect in
the future, by actively inserting the hair between her
teeth.
Therefore, the DF innovation could be a transformationof grooming patterns via the running of hair between theteeth to remove louse eggs. These scenarios are consistent
with the ‘‘perception–action’’ perspective on the development of tool-use and foraging competence in monkeys,
apes, and humans, postulating that skilled actions are
acquired through the routine generation of species-typical
exploratory actions, coupled with learning about the outcomes and affordances of each action that generates
directly perceptible information (Lockman 2000; Gunst
2008).
Besides possible proximate causes, the problem arises
about why the DF behavior has been maintained by its
innovator for several years. A first parsimonious explanation of this behavior is that the flosser may simply
enjoy the interaction between the hair and its teeth, andapparent pleasurable feedback potentially gained fromthe activity may be an immediate reinforcement (cf.
Leca et al. 2007d). Second, DF could alleviate thepossible physical annoyance caused by a piece of foodstuck between the teeth. A third beneficial consequenceof DF could be an improvement in the teeth condition.
Flossing one’s teeth is a form of health maintenanceregarded as self-medication (Huffman 2007). Because all
self-medicative behaviors are driven by some quest for
comfort, these interpretations are congruent with theclassification of the tooth-pick behavior in orangutans asa ‘‘comfort innovation’’ (Russon et al. 2009). Because
DF was not more frequent in post-feeding than nonfeeding periods, we doubt that the DF innovation had
significant, or even any, survival value, through the verysmall amount of extra food the flosser can obtain fromits behavior.

Although these data did not allow us to accurately determine the order of appearance of the different DF techniques, past observations and comparative analysis of the
behavioral patterns support the view that the ‘‘plucking’’
technique was acquired later than the two other DF variants. First, previous long-term behavioral observations of
this group showed that Chonpe-69-85-94 had been using
the ‘‘stretching with hand’’ and the ‘‘stretching withmouth’’ techniques for at least four years (Leca, unpublished data; Vasey, personal communication). Although the‘‘plucking’’ technique was not noticed before 2008, its
absence remains speculative. Second, several elements
show a higher level of complexity in the ‘‘plucking’’
technique than in the two other variants:
1.

2.
3.
4.

the former consists in manipulation of a detachedobject (plucked hair) whereas hair is attached to theskin in the latter;the former requires both hands to be used whereas only
one hand is used in the latter;hair selection was more frequent in the former than in
the latter; andsince the former necessitates hair to be pulled out, it ismore invasive than the latter.

Likewise, the ‘‘stretching with hand’’ technique, that
requires the use of hand and mouth can be considered more
complex, in terms of sequence of actions, than the‘‘stretching with mouth’’ technique, in which only themouth is used. Although we cannot determine the exact
timeline, we propose the following order in the emergenceof DF techniques: first the ‘‘stretching with mouth’’ technique, then the ‘‘stretching with hand’’ technique, and lastthe ‘‘plucking’’ technique. In long-tailed macaques, there
was a generalization of the DF behavior with hair to the useof coconut shell fibers for the same purpose (Watanabe
et al. 2007). In Japanese macaques, even non-instrumental
object manipulation can undergo a major ‘‘transformation’’process over time, with an increase in the diversity andcomplexity of the behavioral patterns exhibited (Leca et al.
2007c, 2008a).
Constraints on the diffusion of the DF innovation
The first individual to display a novel behavior may do so
repeatedly and sometimes for long periods of time before it
starts diffusing within the group (Nishida et al. 2009).
However, it took less than four years for most behavioral
innovations reported in Japanese macaques to be transmitted to at least a second group member (Kawai 1965;
Itani and Nishimura 1973; Huffman 1984; Watanabe 1989;
Nakamichi et al. 1998). Therefore, it is reasonable to

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aggressive reactions from flossing recipients. The risk ofbeing aggressed by dominant flossing recipients may
account for the innovator spending less time flossing on
higher-ranking than lower-ranking partners. If the expression of the DF innovation is restricted by dominancerelationships, it may limit its chance of spread to groupmembers of all social status. In dominance-structured
groups, social status may constrain behavioral innovations,
their subsequent propagation, and long-term maintenance(Leca et al. 2007a).

consider the DF innovation as being not particularly prone
to diffusion.
Socio-demographic features at the group level
Group size and number of grooming partners available With 145 individuals, the Arashiyama E troop is alarge troop of Japanese macaques. However, the innovator
had grooming interactions with relatively few partners(11 individuals), and among them a large proportion ofgrooming time (71.9%) was allocated to two individuals.
This is consistent with findings from another group ofJapanese macaques, comparable in terms of number ofadult females, maternal kin-groups, and environmental
conditions (both are free-ranging provisioned troops),
showing that in large groups, most females had groominginteractions with a small subset of females (Nakamichi andShizawa 2003). Because DF was grooming-related, thesmall grooming network of the innovator may constrain the
diffusion of the behavior. Large-sized groups comprisemany uninformed bystanders who could slow down the
diffusion (Lefebvre and Giraldeau 1994). Not only groupsize but also group composition in age classes may affectthe diffusion and performance of some behaviors in thisspecies, like stone handling (Leca et al. 2007b).

Structural and functional aspects of the DF behavior
Depending on their form, function, or context of performance, some types of behavior may be more or less prone
to spread within a group (Tanaka 1998).
Form First, the innovator’s dependence on object use
was shown by the fact that in all DF episodes she usedhair to floss her teeth and never used her fingers alone.
However, as opposed to feeding innovations whose
propagation can be constrained by access to andmonopolization of the novel food source (cf. Leca et al.
2007a), the lack of diffusion of the DF innovation cannot
be explained by the opportunity to get access to theflossing tool—the number of hairs on its own body or onothers’ bodies is countless. Second, mathematical models
predict that the expected proportion of naive individuals
learning the new skill will decrease as skill complexity
increases (Cavalli-Sforza and Feldman 1981). This
explanation may not hold for DF either. The behavioral
patterns involved in the performance of the three DF
techniques (e.g., stretching with hand, plucking, holding,repeated teeth-chattering) are simple enough to be
exhibited by all but the very young individuals inJapanese macaques, a species also known for complex
object manipulation (cf. Leca et al. 2007c).
A third possibility could be that individuals are not able
to make the discrimination between the novel behavior(i.e. using hair as dental floss) and regular grooming
patterns. In their form, the ‘‘stretching with mouth’’ and‘‘stretching with hand’’ techniques are close to somegrooming variants such as ‘‘combing’’ and ‘‘pinching’’ (cf.
Tanaka 1998). As for the ‘‘plucking’’ technique, which
differs from regular grooming, it was only performed during
self-grooming activity, thereby limiting the opportunity forsocial influence, and its frequency could be too low to makethis variant noticeable by others. In other words, the DF
behavior, as currently practiced by its innovator, would not
be conspicuous enough to be reliably noticed and learnt by
naive group members. The anthropogenic circumstances of
DF innovation in long-tailed macaques (see above) could
make the behavior more attractive to naive individuals andKinship The innovator had only two close kin: her motherand only one sibling, a 2 year-old brother. She had nooffspring. Since the pathways of diffusion of most behavioral innovations by Japanese macaques involve at somepoint the spread among siblings and the downward verticaltransmission from mother to offspring (Huffman 1984;
Nahallage and Huffman 2007), this paucity in individuals
closely related to the innovator may limit opportunities for
diffusion of DF. Long-tailed macaque mothers exaggerated
their DF actions in the presence of their offspring, which
could facilitate the learning of the behavior by infants(Masataka et al. 2009). Another channel of diffusion of
innovations in this species is the upward vertical transmission from offspring to mother (Huffman 1984). However,the nature of the behavior (see below) may explain the lackof transmission of DF from the innovator to her mother,
despite their close social proximity.
Dominance Among the few non-related grooming partners of the innovator, most were higher-ranking. In despotic macaque species, for example Japanese macaques,grooming is mainly directed up a hierarchy (Koyama
1991). Our data suggest that when associated with allogrooming interactions, the DF behavior is not risk-free.
Stretching others’ hair to make it suitable for flossing islikely to be more painful for others than regular allogrooming patterns, thereby exposing the flosser to

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Primatesby Ministry of Education, Culture, Sports, Science and Technology,
Japan, by a JSPS (Japan Society for the Promotion of Science)
postdoctoral fellowship to J.-B. Leca (no. 07421), and by travel funds
from the HOPE Project, a core-to-core program sponsored by JSPS.
We thank S. Asaba, J. Hashiguchi, S. Kobatake, and S. Tamada from
Iwatayama Monkey Park for helping us during the course of thestudy. For occasional assistance with data collection, we thank N.
Tworoski. We thank P. Vasey for providing us with longitudinal dataon the study group. We thank T. Nishida, W.C. McGrew, and two
anonymous reviewers for fruitful comments on the manuscript.

could account for the spread of this innovation within thegroup (Watanabe et al. 2007).
Context, innovation-related risk, and function The more
specialized the context and function of the behavior, themore limited will be the subgroup of individuals that will
acquire it (Huffman and Hirata 2003). In Japanese macaques,
DF behavior occurs mainly during allo-grooming, a social
interaction involving a certain amount of risk to one or bothprotagonists (cf. Zahavi 1977). Aversive flossing recipients’reaction to harmful behaviors may explain why the ‘‘plucking’’ technique was not observed during allo-groominginteractions. The social transmission of certain behavioral
variants may be constrained by the risk of aggression(cf. Tanaka 1998). In a group of long-tailed macaques where
DF has spread widely, the behavior was self-directed andperformed solitarily (Watanabe et al. 2007). Observing eachother at a distance with a lower risk of aggression may havefacilitated the diffusion of the behavior.
The low adaptive value of the DF innovation may also
partly account for the lack of propagation. Such object
manipulation may not spread simply because of the narrowwindow of its applicability (cf. Sinha 2005; but see Huffman
1984). Comfort innovations may also be less likely to diffuse
than those that are related to subsistence or socio-sexual
communication (van Schaik et al. 2006).

References
Altmann J (1974) Observational study of behavior: sampling
methods. Behaviour 49:227–267
Beck BB (1980) Animal tool behavior: the use and manufacture oftools by animals. Garland Press, New York
Bonnie KE, de Waal FBM (2006) Affiliation promotes the transmission of a social custom: handclasp grooming among captive
chimpanzees. Primates 47:27–34
Cavalli-Sforza LL, Feldman MW (1981) Cultural transmission andevolution: a quantitative approach. Princeton University Press,
Princetonde Vries H (1995) An improved test of linearity in dominancehierarchies containing unknown or tied relationships. Anim
Behav 50:1375–1389
Fragaszy DM, Perry S (2003) Towards a biology of traditions. In:
Fragaszy DM, Perry S (eds) The biology of traditions: models
and evidence. Cambridge University Press, Cambridge, pp 1–
32
Gunst N (2008) The ontogeny of foraging skills in wild brown
capuchins (Cebus apella): developmental perspective on theacquisition of ecological competence. PhD Dissertation, The
University of Georgia, USA
Huffman MA (1984) Stone-play of Macaca fuscata in Arashiyama B
troop: transmission of a non-adaptive behavior. J Hum Evol
13:725–735
Huffman MA (1991) History of Arashiyama Japanese macaques in
Kyoto, Japan. In: Fedigan LM, Asquith PJ (eds) The monkeys of
Arashiyama: thirty-five years of research in Japan and the West.
SUNY Press, Albany, pp 21–53
Huffman MA (1996) Acquisition of innovative cultural behaviors in
non-human primates: a case study of stone handling, a sociallytransmitted behavior in Japanese macaques. In: Galef B, Heyes
C Jr (eds) Social learning in animals: the roots of culture.
Academic Press, Orlando, pp 267–289
Huffman MA (2007) Primate self-medication. In: Campbell CJ,
Fuentes A, MacKinnon KC, Panger M, Bearder SK (eds)
Primates in perspective. Oxford University Press, New York,
pp 677–690
Huffman MA, Hirata S (2003) Biological and ecological foundationsof primate behavioral tradition. In: Fragaszy DM, Perry S (eds)
The biology of tradition: models and evidence. Cambridge
University Press, Cambridge, pp 267–296
Huffman MA, Quiatt D (1986) Stone handling by Japanese macaques(Macaca fuscata): implications for tool use of stone. Primates
27:413–423
Ingmanson EJ (1996) Tool-using behavior in wild Pan paniscus:
social and ecological considerations. In: Russon AE, Bard KA,
Parker ST (eds) Reaching into thought: the minds of the great
apes. Cambridge University Press, New York, pp 190–210
Itani J, Nishimura A (1973) The study of infra-human culture in
Japan. In: Menzel E (ed) Precultural primate behaviour. Karger,
Basel, pp 26–50

Conclusions and future directions
This is one of the rare studies to document the spontaneous
appearance of tool-use behavior in Japanese macaques
under natural conditions (see also Leca et al. 2008a). The
lack of report on DF in other troops of Japanese macaques
and the idiosyncratic presence of the behavior in this troop
may reflect possible intra-troop and inter-troop variations in:
1.
2.
3.

the likelihood of behavioral innovation;
the social constraints on the early dissemination andlong-term maintenance of such inventions; andappropriate social and/or environmental reinforcement
for the emergence, propagation, and continued practiceof this behavior.

When a behavior is restricted to one or very few groupmembers, it is likely to disappear at the group level (Lecaet al. 2007a; Nishida et al. 2009). Further investigation,
including experimentally-elicited DF, may help to determine more accurately the conditions of appearance of thisnovel behavior, and to elucidate why it has not spread within
the group (cf. Watanabe et al. 2007; Leca et al. 2008a).
Acknowledgments The authors’ work was funded by a Grant-InAid for scientific research (no. 1907421 to M.A. Huffman) sponsored

123
265

Primates
Nahallage CAD, Huffman MA (2007) Acquisition and developmentof stone handling behavior in infant Japanese macaques.
Behaviour 144:1193–1215
Nakamichi M, Shizawa Y (2003) Distribution of grooming among
adult females in a large, free-ranging group of Japanesemacaques. Int J Primatol 24:607–625
Nakamichi M, Kato E, Kojima Y, Itoigawa N (1998) Carrying andwashing of grass roots by free-ranging Japanese macaques at
Katsuyama. Folia Primatol 69:35–40
Nishida T, Matsusaka T, McGrew WC (2009) Emergence, propagation or disappearance of novel behavioral patterns in the
habituated chimpanzees of Mahale: a review. Primates 50:23–36
Perry S, Panger M, Rose LM, Baker M, Gros-Louis J, Jack K,
McKinnon KC, Manson J, Fedigan L, Pyle K (2003) Traditions
in wild white-faced capuchins. In: Fragaszy DM, Perry S (eds)
The biology of traditions: models and evidence. Cambridge
University Press, Cambridge, pp 391–423
Reader SM, Laland KN (2001) Primate innovation: sex, age andsocial rank differences. Int J Primatol 22:787–805
Reader S, Laland KN (2003) Animal innovation: an introduction. In:
Reader S, Laland KN (eds) Animal innovation. Oxford University Press, Oxford, pp 3–35
Russon AE, van Schaik CP, Kuncoro P, Ferisa A, Handayani DP,
van Noordwijk MA (2009) Innovation and intelligence inorangutans. In: Wich SA, Utami Atmoko SS, Mitra Setia T(eds) Orangutans: geographic variation in behavioral ecology
and conservation. Oxford University Press, New York, pp 279–
298
Sinha A (1997) Complex tool manufacture by a wild bonnet macaque.
Folia Primatol 68:23–25
Sinha A (2005) Not in genes: phenotypic flexibility, behavioural
traditions and cultural evolution in wild bonnet macaques.
J Biosci 30:51–64
Tanaka I (1998) Social diffusion of modified louse egg-handlingtechniques during grooming in free-ranging Japanese macaques.
Anim Behav 56:1229–1236
Tanaka I, Takefushi H (1993) Elimination of external parasites (lice)is the primary function of grooming in free-ranging Japanesemacaques. Anthropol Sci 101:187–193
van Schaik CP, Ancrenaz M, Borgen G, Galdikas B, Knott CD,
Singleton I, Suzuki A, Utami SS, Merill M (2003) Orangutan
cultures and the evolution of material culture. Science 299:102–
105
van Schaik CP, van Noordwijk MA, Wich SA (2006) Innovation inwild Bornean orangutans (Pongo pygmaeus wurmbii). Behaviour
143:839–876
Watanabe K (1989) Fish: a new addition to the diet of Koshimamonkeys. Folia Primatol 52:124–131
Watanabe K, Urasopon N, Malaivijitnond S (2007) Long-tailed
macaques use human hair as dental floss. Am J Primatol 69:940–
944
Weinberg SM, Candland DK (1981) ‘‘Stone-grooming’’ in Macaca
fuscata. Am J Primatol 1:465–468
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
Zahavi A (1977) The testing of a bond. Anim Behav 25:246–247

Kawai M (1965) Newly acquired pre-cultural behavior of a natural
troop of Japanese monkeys on Koshima Island. Primates 6:1–30
Kawai M, Watanabe K, Mori A (1992) Pre-cultural behaviors
observed in free-ranging Japanese monkeys on Koshima islet
over the past 25 years. Primate Rep 32:143–153
Koyama N (1991) Grooming relationships in the Arashiyama groupof Japanese monkeys. In: Fedigan LM, Asquith PJ (eds) The
monkeys of Arashiyama: thirty-five years of research in Japanand the West. State University of New York Press, Albany,
pp 211–226
Kummer H, Goodall J (1985) Conditions of innovative behaviour inprimates. Philos Trans R Soc Lond B Biol Sci 308:203–214
Laland KN, Hoppitt W (2003) Do animals have culture? Evol
Anthropol 12:150–159
Leca JB, Gunst N, Watanabe K, Huffman MA (2007a) A new case offish-eating in Japanese macaques: implications for social
constraints on the diffusion of feeding innovation. Am J
Primatol 69:821–828
Leca JB, Gunst N, Huffman MA (2007b) Age-related differences in
the performance, diffusion, and maintenance of stone handling, abehavioral tradition in Japanese macaques. J Hum Evol 53:691–
708
Leca JB, Gunst N, Huffman MA (2007c) Japanese macaque cultures:inter- and intra-troop behavioural variability of stone handling
patterns across 10 troops. Behaviour 144:251–281
Leca JB, Gunst N, Petit O (2007d) Social aspects of fur rubbing in
Cebus capucinus and C. apella. Int J Primatol 28:801–817
Leca JB, Nahallage CAD, Gunst N, Huffman MA (2008a) Stonethrowing by Japanese macaques: form and functional aspects ofa group-specific behavioral tradition. J Hum Evol 55:989–998
Leca JB, Gunst N, Huffman MA (2008b) Variability of foodprovisioning regimes and stone handling tradition in Japanesemacaques: a comparative study of ten troops. Am J Primatol
70:803–813
Leca JB, Gunst N, Huffman MA (2008c) Of stones and monkeys:
testing ecological constraints on stone handling, a behavioral
tradition in Japanese macaques. Am J Phys Anthropol 135:233–
244
Lefebvre L, Giraldeau LA (1994) Cultural transmission in pigeons isaffected by the number of tutors and bystanders present. Anim
Behav 47:331–337
Lockman J (2000) A perception-action perspective on tool use
development. Child Dev 71:137–144
Malaivijitnond S, Lekprayoon C, Tandavanitj N, Panha S, Cheewatham C, Hamada Y (2007) Stone-tool usage by Thai long-tailed
macaques (Macaca fascicularis). Am J Primatol 69:227–233
Martin P, Bateson P (1993) Measuring behaviour: an introductory
guide. Cambridge University Press, Cambridge
Masataka N, Koda H, Urasopon N, Watanabe K (2009) Free-ranging
macaque mothers exaggerate tool-using behavior when observedby offspring. PLoS ONE 4:e4768
McGrew WC (1992) Chimpanzee material culture: Implications forhuman evolution. Cambridge University Press, Cambridge
McGrew WC, Tutin CEG (1972) Chimpanzee dentistry. J Am Dent
Assoc 85:1198–1204
McGrew WC, Tutin CEG (1973) Chimpanzee tool use in dental
grooming. Nature 241:477–478

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Animal Behaviour xxx (2009) 1–10

Contents lists available at ScienceDirect

Animal Behaviour
journal homepage: www.elsevier.com/locate/anbehav

Indirect social inﬂuence in the maintenance of the stone-handling tradition in
Japanese macaques, Macaca fuscata
Jean-Baptiste Leca*, Noëlle Gunst 1, Michael A. Huffman
Primate Research Institute, Kyoto University

a r t i c l e i n f o
Article history:
Received 3 July 2009
Initial acceptance 17 September 2009
Final acceptance 25 September 2009
Available online xxx
MS. number: 09-00449
Keywords:
artefact
cultural maintenanceﬁeld experimentindirect social inﬂuence
Japanese macaque
Macaca fuscata
niche construction
stimulus/local enhancementstone handlingtraditional behaviour

Comparative and longitudinal studies have shown that stone-handling (SH) behaviour, deﬁned as thenoninstrumental manipulation of stones by performing various behavioural patterns, is socially transmitted across generations as a cultural behaviour in Japanese macaques. We investigated experimentally
how stimulus/local enhancement, a form of indirect social inﬂuence through the physical traces typicallyleft in the environment by previous stone handlers, might trigger SH behaviour at the individual level,
and thus could contribute to the maintenance of the SH tradition at the group level. Through thesemicontrolled conditions of ﬁeld experiments, conducted in the free-ranging provisioned Arashiyama E
troop, in which the SH tradition has been well established for nearly three decades, our results supported
the stimulus/local enhancement hypothesis. Most group members preferentially directed their SH
behaviour towards typical physical traces of SH activity (piles of stones) over randomly scattered stones.
Encountering SH artefacts enhanced the use of these particular stones for performing SH in thatparticular part of the environment. The common occurrence of such ‘play stations’ may favour thefrequent reuse of the same stones over time and explain the transport of stones between and around SH
artefacts. We provided evidence for the role of indirect social inputs on the long-term persistence of theSH tradition in Japanese macaques, through SH by-products, the stimulating effect of which can bedelayed in time and separate in space from others. We discuss our ﬁndings from the perspective ofsocially mediated behaviours, conformity-enforcing responses and niche construction.
Ó 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

In the quest for cultural versus alternative explanations of
behavioural variation within and between groups of the same
animal species, there has been a heated conceptual and methodological debate among ﬁeld and laboratory researchers. Before such
behavioural variability can be regarded as cultural, it is acknowledged that the effects of genetic and ecological factors should be
minimal. However, depending on the environmental conditions of
the study, the species’ attributes and the behavioural domain underinvestigation, the questions addressed and the methods used toanswer them vary considerably. Three major approaches have beentaken to assess whether intra- and intergroup behavioural diversity
in a given species can be considered evidence for culture (oftenlabelled ‘behavioural tradition’ by ethologists; reviewed in Caldwell& Whiten 2007).

* Correspondence: J.-B. Leca, Primate Research Institute, Kyoto University, 41-2
Kanrin, Inuyama, Aichi 484-8506, Japan.
E-mail address: jbtleca@yahoo.com (J.-B. Leca).
1
N. Gunst is now at Kyodai Syokuin Syukusha 142, Tonoji Ooguro 178-44,
Inuyama, Aichi 484-0094, Japan.

First, the ‘group contrast’ approach (see Fragaszy & Perry 2003a)
consists of examining variation in the frequency of behaviouralvariants between groups (often sampled from geographicallyseparate populations; Whiten et al. 1999; Rendell & Whitehead
2001; Hunt & Gray 2003; Perry et al. 2003; Leca et al. 2007a).
Second, the longitudinal approach relies on the social context ofdiffusion and maintenance over time of a novel behaviour withina group, as a way to assess whether social or individual learning ismore likely to be involved (Coussi-Korbel & Fragaszy 1995; Lefebvre
1995).
However, from a conceptual viewpoint, the very notion ofculture is debatable until there is empirical evidence that thetransmission and maintenance of the novel behaviour within thegroup are socially mediated (Fragaszy & Perry 2003b; Galef 2004).
Therefore, the third approach consists of conducting experimental
studies to determine whether ‘socially biased learning’ processes(Fragaszy & Visalberghi 2001, 2004) could support the putative
cultural behaviours observed in the wild. Social learning is any formof learning inﬂuenced by the presence of, observation of or interaction with another individual (typically a conspeciﬁc) or its
products (Galef 1988). The various ‘social inﬂuences supporting thelearning of novel behaviours’ (Fragaszy & Visalberghi 2004, page0003-3472/$38.00 Ó 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.anbehav.2009.09.035

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27) or the performance of species-speciﬁc behaviours can thus bedivided into two broad categories, namely direct social inﬂuences
and indirect social inﬂuences (Galef 1988; Tomasello et al. 1993;
Whiten 2000; Visalberghi & Fragaszy 2002).
Among the forms of direct social inﬂuences, the probability of anindividual performing a behaviour may increase in the presence ofa conspeciﬁc performing the behaviour, which is already in theobserver’s behavioural repertoire (social facilitation), or in the mere
presence of a conspeciﬁc resulting in a behavioural disinhibition by
reduction of isolation-induced fear (social enhancement). An
individual’s behaviour may also be triggered by the synchronizedperformance of a similar behaviour by several conspeciﬁcs, as partof an ampliﬁcation process (contagion). Finally, an individual may
learn to copy some part of the form of the behaviour performed bya demonstrator or may learn from a model the goal to pursue(imitation/emulation). Most studies on social-learning processes
have focused on direct social inﬂuence through the necessarypresence of other group members (reviewed in Zentall & Galef
1988; Fragaszy & Perry 2003a).
By contrast, indirect social inﬂuence assumes that an individual’s behaviour may result from directing its attention to a ‘limited
aspect of the total stimulus situation to which the response is to be
made’ (Spence 1937, page 821), without necessarily interacting
directly with a conspeciﬁc. If stimulus/local enhancement isinvolved in the acquisition, transmission or maintenance of a habit,
then individuals should tend to focus their attention on, or aim
their responses towards, particular objects or places in the environment after observing conspeciﬁcs’ actions in conjunction withthose objects or at that place (Thorpe 1963; Byrne & Russon 1998).
Through the stimulating effect of the physical traces (or artefacts)
left behind by previous individuals, indirect social inﬂuences aredelayed in time and separate in space from others. For example,
residual olfactory cues left on foraging trails by ants and rodents
affect the selection of feeding sites (Hölldobler & Wilson 1991;
Galef & Buckley 1996). As opposed to some of the complex learning
processes mentioned above, the role of stimulus/local enhancement offers a more parsimonious explanation for the acquisition of
foraging techniques by immatures in various taxa such as birds,
rodents and primates (Denny et al. 1988; Tomasello et al. 1993;
Huber et al. 2001; Gunst et al. 2008). However, to date, indirect
social inﬂuence on the acquisition, performance or long-term
maintenance of behaviours has not received the formal attention it
deserves.
One reason for this could be the lack of experimental dataobtained from the spontaneous behaviours in free-ranging andsocially living groups of animals. Most experimental studies ofsocial learning have used artiﬁcial tasks and were conducted in theunnatural social conditions of laboratory settings (reviewed in
Galef & Laland 2005). Recent criticisms about the ecological validityof these studies has led to recommendations for ﬁeld experiments
using biologically relevant tasks and allowing individuals tointeract spontaneously with each other and with test stimuli, withno human-imposed outcomes for the successful completion of thetask (Matsuzawa 1994; Galef 2004; Huffman et al. 2008; Watson &Caldwell 2009).
Here, we took a ﬁeld experimental approach to test the indirect
social inﬂuence of lithic artefacts on the enduring performance ofstone-handling (SH) behaviour in Japanese macaques. The SH activity
is the noninstrumental and seemingly playful manipulation ofstones, such as repeatedly pounding a stone on a substrate, clacking
two stones together, or gathering several stones into a pile (Huffman
1984). SH is the longest studied and best-documented cultural
behaviour in monkeys to date (reviewed in Huffman et al. 2008).
Research on SH has already beneﬁted from a comparative approachrevealing substantial variation in SH between troops of Japanesemacaques, and from long-term observational studies conducted atseveral points in time over a 30-year period to address the inﬂuenceof environmental, sociodemographic and developmental constraints
on the emergence, diffusion and maintenance of the SH tradition(Huffman 1984, 1996; Huffman & Quiatt 1986; Huffman & Hirata
2003; Leca et al. 2007a, b, 2008a, b, in press a). For example, thecontinuous study of mothers and infants during the ﬁrst 6 months oflife, in the semicontrolled conditions of an outdoor enclosure,showed that (1) the mother was the primary source of an infant’s
early exposure to SH, (2) the acquisition of SH behaviour by young
individuals may involve direct social inﬂuences (social facilitation)
through the observation by naı̈ve infants of their mothers as SH
demonstrators, and (3) some intragroup variability in the performance of SH patterns could be interpreted from the viewpoint ofdevelopmental constraints (Nahallage & Huffman 2007a, b).
However, the maintenance of the SH tradition across generations may involve not only direct social inﬂuences but also indirect
social inputs through the stimulating effect of SH artefacts (Quiatt &Huffman 1993). Through the enduring practice of SH behaviour,acquired familiarity with the stones and occasional integration of
SH with other daily activities, Japanese macaques often carry stones
about and leave them behind when engaging in another activity. As
a result of these regular transports, small piles of stones areconspicuously deposited on grassy patches, stone slabs or at thebase of large trees (Huffman & Quiatt 1986). The common occurrence of such SH artefacts or ‘play stations’ around the feeding
ground, and sometimes in the forest, may favour the frequent reuseof the same stones over time (Quiatt & Huffman 1993). However,
the hypothesis that encountering physical traces of previous SH
activity affects subsequent SH activity has not yet been tested.
The present work is the ﬁrst to use a ﬁeld experimental
approach to examine the environmental and social conditions, atleast partially reconstructed, under which the SH tradition may be
maintained within troops of Japanese macaques. We studied thefree-ranging provisioned Arashiyama E troop, in which the SH
tradition has been well established for nearly three decades(Huffman 1984, 1996; Leca et al. 2008b). Therefore, it is beyond thescope of this study to address the social-learning processes
involved in the initial establishment of the SH tradition. Our main
goal was to investigate experimentally how the physical traces
typically left in the environment by previous stone handlers might
help, through a stimulus enhancement process, trigger SH behaviour in individuals on a daily basis, and thus contribute to the longterm maintenance of the SH tradition at the group level.
We tested the ‘stimulus/local enhancement hypothesis’ on theperformance of SH, proposing that individuals should preferentiallydirect their SH activity towards the places where previous stone
handlers left conspicuous physical traces of their SH activity, andmore speciﬁcally towards piles of stones. Our speciﬁc objective wasto test two predictions derived from the ‘stimulus/local enhancement hypothesis’. Prediction 1 stated that the frequency andduration of SH behaviour should be signiﬁcantly higher when
directed to a pile of stones than when directed to randomly scattered stones for all individuals entering the experimental area,
including the ﬁrst one to do so, that is, when any possible direct
social inﬂuence had been removed. Prediction 2 stated that if thelocation of the piles of stones changed during consecutive visits tothe same area, a given stone handler should be more attracted to
the new locations (where the piles of stones are) than the previous
locations. Rejection of the ‘stimulus/local enhancement hypothesis’
could suggest that the persistence of the SH tradition and the
motivation to engage in this activity are better explained by direct
social inﬂuences such as social facilitation or social enhancement.
To explore further the environmental factors underlying themaintenance of the SH tradition, (1) we tested the possible spatial

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preferences for SH at the group and individual levels, (2) we evaluated the number and relative locations of the piles of stones used,and (3) we documented the transport of stones between andaround piles of stones. Finally, to assess how social constraints mayeither promote or inhibit the daily performance of stone-directedbehaviours, and thus the long-term persistence of the SH tradition,
we investigated the role of age, kinship and dominance relationships in the use of SH artefacts.
METHODS
Study GroupThe following observations were made on the free-ranging
Arashiyama E troop of Japanese macaques at the Iwatayama
Monkey Park, Arashiyama, Kyoto Prefecture, Japan. Japanesemacaques have been provisioned and studied at Arashiyama since1954 (Huffman 1991). At the time of our observations, the study
group was provisioned with wheat grains four times a day by thepark staff. This type of food was eaten by the monkeys without any
processing whatsoever other than chewing. Visitors were also
allowed to give a small amount of extra food to the monkeys (seeLeca et al. 2008b for details on provisioning conditions). Water wasavailable ad libitum around the provisioning site. All groupmembers were individually identiﬁed, and their ages and kin
relations through maternal lineages were known. The study groupcontained 145 individuals of 15 separate matrilines. All age/sex
classes were present, including 56 old adults, aged 16 or more years(52 females and four males), 25 middle-aged adults, between 11
and 15 years old (21 females and four males), 15 young adults,
between 7 and 10 years old (14 females and one male), 22
subadults, between 4 and 6 years old (14 females and eight males),13 juveniles, between 2 and 3 years old (six females and sevenmales) and 14 yearlings and infants (six females and eight males;
see Leca et al. 2007b for details on age classiﬁcation).

Data Collection
We deﬁned an experimental area as a 24 m2 surface (2  12 m)
located on the ground and within 60 m around the feeding ground,
where SH activity most visibly occurs (Huffman 1984; Leca et al.
2008b). We used only natural and already present landmarks(bushes, trees, rocks) to form the boundary of the area. To investigate local enhancement, we established four experimental areas
located in different directions from the feeding ground and inplaces rarely disturbed by visitors and staff (Fig. 1a). There was no
signiﬁcant difference in stone availability within the four areas(Leca et al. 2008a). We randomly determined the area where eachsession took place, provided that the distribution of sessions in thefour areas was homogeneous.
To investigate stimulus/local enhancement, we discreetly set
out stones according to two speciﬁc spatial arrangements (called
SH spots) within the chosen area, and before each experimental
session. We deﬁned an SH spot as a particular place with several
stones placed on the ground, and where SH activity may occur. We
distinguished two categories of SH spots: SH stations and SH zones.
We deﬁned an SH station as a set of 12 stones that we gathered intoa small pile (Fig. 1b). We deﬁned an SH zone as another set of 12
stones that we randomly scattered over a 1  1 m surface arounda centralized SH station, and previously cleared of other stones. The
stones used for the experiments were collected around the feeding
ground and were typically used by the monkeys for performing SH.
The number and spatial arrangement of stones used in a SH station
were based on the average number and layout of stones found ina sample of 54 pictures of SH stations spontaneously set out by thegroup members (J.-B. Leca, unpublished data).
Within an experimental area, there were seven SH stations andseven SH zones, each numbered from 1 to 7. In an attempt todiscriminate between stimulus and local enhancement, and when
two consecutive sessions took place in the same area, we moved,
during the second session, each SH station 2 m away from its

Area 3

Original spot

3

Area 4
Area 1(c)
SH station

New location

SH zoneNext session
12 m

2 adjacent
SH stations

Feedingground2mArea 2
(b)

(a)
Trail
0

30 m

Pond
Building

Figure 1. (a) Study site (map after Nishie 2002), (b) photo of a stone-handling (SH) station, and (c) spatial arrangement of SH stations within an experimental area during two
consecutive sessions.

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original spot during the ﬁrst session (Fig. 1c). We conducted eachexperimental session during the 20 min period immediately
following food provisioning because it was the time when most SH
activity occurs at the group level (Leca et al. 2008b). To ensure
independence between sessions, we conducted only one session
per postprovisioning period.
Each experimental session was continuously videorecorded byeither J.-B.L (N ¼ 33 sessions) or N.G. (N ¼ 15 sessions) with a DCRHC48 Sony digital camera from a position overhanging the experimental area. They used the focal-place sampling method (Lecaet al. 2007c; Vogel & Janson 2007), focused on the experimental
area, and videorecorded all individuals entering and staying within
the area. The typical duration of an experimental session was
20 min. If an individual performed SH within the experimentalzone during the ﬁnal 2 min, the observation was extended until
2 min after this individual had stopped performing SH (Leca et al.
2007a).
Visibility during the experiments was excellent. The observers
could sample the subjects within 5–10 m. We conducted a total of
48 experimental sessions between 0800 and 1500 hours, during
two different periods: 26 sessions in autumn 2008 (10 September–
3 October) and 22 sessions in spring 2009 (4–10 May). We conducted 15 sessions in area 1, and 11 sessions in each of the threeother areas (see detailed analyses below). To establish the dominance hierarchy within the group, we recorded ad libitum data
(Altmann 1974) on the direction of dyadic agonistic interactions.
Data Analysis
For each videorecorded session, N.G. continuously transcribedto the second (1) the number, identity and activity (locomoting,feeding, foraging, grooming, resting and SH) of all individuals
entering and present within the experimental area, (2) whether
individuals were engaged in SH activity on SH stations or SH zones,
and their respective numbers, (3) all occurrences of individualchanges in SH spots, and possible transport of stones between SH
spots, and (4) all occurrences of supplanting interactions over SH
stations or SH zones. Although we could not identify all individuals
passing through the experimental areas, we could identify all
individuals engaged in SH activity within these areas. We deﬁned
an SH phase as the individual performance of SH activity on a given
SH spot. Each change of SH activity between SH spots marked thestart of a new SH phase.
For most analyses, we report percentages of events or durations
and mean values  SD. Since our raw and transformed data violated
the parametric assumptions, we conducted nonparametric tests(Siegel & Castellan 1988). To demonstrate stimulus/local enhancement, we used a Wilcoxon signed-ranks test to compare, for eachindividual involved in SH activity within the experimental areas,
the frequency and duration of SH phases performed on SH stations
versus on SH zones. Since the direction of the difference was predicted, the region of rejection was one tailed. A given individual wascategorized as more attracted to SH stations, more attracted to SH
zones or equally attracted to both SH spots, if the cumulated
frequency or duration of its SH phases was higher on SH stations
than on SH zones, higher on SH zones than on SH stations or equal
for both SH spots, respectively. We also used Wilcoxon signedranks tests (one tailed) to compare (1) the SH frequency on the newversus the previous locations of SH stations during two consecutive
sessions, and (2) the frequency of supplanting interactions over SH
stations versus over SH zones.
To examine further the magnitude of stimulus/local enhancement and provide more information than the conventional statistical signiﬁcance (P value), upon which we make a dichotomous
decision (reject or fail to reject), we used the effect size statistic. To

assess the effect size and calculate its conﬁdence interval (95% CI),
we used, respectively, the Cohen’s d statistic and its related standard error (SEd) for two dependent groups (Nakagawa & Cuthill2007). We considered d values of 0.2, 0.5 and 0.8 as benchmarks for‘small’, ‘medium’ and ‘large’ effects, respectively, and we qualiﬁed
the effect size as statistically signiﬁcant (at an a level of 0.05) if its CI
did not include zero (Cohen 1988).
To compare the frequency of presence and SH frequency ofgroup members in the four experimental areas, we used a Friedman
test followed by multiple paired comparisons based on mean ranks.
Compared with the 11 sessions conducted in areas 2, 3 and 4, thefour additional sessions in area 1, an area frequented by many groupmembers, were only used in the analyses of stimulus/local
enhancement (comparing the types of SH spots used within anexperimental area), not in the analyses of spatial preferences(comparing the frequency of presence and SH between experimental areas). When comparing the number of stone handlers
recorded in the four areas, we drew lots for 11 sessions in area 1 toobtain data directly comparable with the three other areas.
We used chi-square goodness-of-ﬁt tests to compare (1) the
number of individuals recorded performing SH in one, two, threeand four areas, (2) the number of SH stations used by stone
handlers during the same session, and (3) the frequency of transport of stones between two SH stations, from an SH station to an SH
zone, and from an SH zone to an SH station. For post hoc examination of chi-square tests, we calculated the adjusted standardized
residuals, and considered statistically signiﬁcant those values of
Z scores that were j1.96j.
We recorded 592 avoidances and dyadic unidirectional acts ofaggression (see Leca et al., in press b). We used the Matman
program edited by Noldus Information Technology (1998) to verify
the linearity of the dominance hierarchy for 91 group members,that is, 87 adult females and the four top-ranking adult males(h0 ¼ 0.27, directional consistency index ¼ 0.97, P < 0.001; de Vries
et al. 1993; de Vries 1995). We distinguished three classes of individuals according to their dominance rank: high-ranking, middleranking and low-ranking individuals (N ¼ 30, 31 and 30,
respectively).
Interobserver reliability kappa coefﬁcients were k ¼ 0.89 forindividual identities and 0.94 for all activities and behaviours
including SH. To measure the extent to which a single observer
obtained consistent results when transcribing the same videorecorded behaviours on different occasions, N.G. transcribed twotimes a sample of ﬁve experimental sessions, involving a total of
670 sample points. A good intracoder reliability kappa coefﬁcient
was also obtained: k ¼ 0.85 (Martin & Bateson 1993). Statisticalanalyses were performed using the SPSS 13.0 analytical program(SPSS Inc., Chicago, IL, U.S.A.). Signiﬁcance levels were set at
a ¼ 0.05.
RESULTS
Number and Activity of Group Members Involved in Sessions
The number of identiﬁed group members entering the areas atleast once during the experimental sessions was 116 (i.e. 80.0% ofgroup members), among which 82 were engaged in SH activity (i.e.
56.6% of group members). Of 48 sessions, we recorded a total of 448
entrances, among which 247 (55.1%) were followed by SH activity,
whereas 201 (44.9%) were not. The average number of entrances
per session was 9.3, among which 5.1  3.9 were followed by SH
activity. The average duration of presence of an individual within anexperimental area per session was 4.9 min, among which
0.8  1.9 min were devoted to SH (Table 1). The activity budget of
the individuals present in the experimental areas shows that the

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Table 1Frequency and duration of presence of individuals within the experimental areas,according to the type of activity performed (stone handling, SH, versus otheractivity)
Presence within the experimental areas

Activity

Total

SH

Other

5.1
3.9
0
15

4.2
4.6
0
19

9.3
7.4
0
30

Mean duration (min)SD
Minimum
Maximum

0.8
1.9
0.0
18.9

4.0
5.5
0.0
37.3

4.9
6.6
0.0
39.1

All sessions
Total frequency(%)
Total duration (hours)
(%)

247
55.1
6.3
17.3

201
44.9
30.2
82.7

448
100.0
36.6
100.0

Per session
Mean frequency
SD
Minimum
Maximum

two most represented activities were locomoting and SH on SH
stations (Fig. 2). In sum, most individuals entering an experimental
area either walked across it, or stopped to perform SH on SH
stations. A slight majority of group members were engaged in thelatter activity.
Stimulus/Local Enhancement
Before pooling the data obtained from all the experimental
sessions, we veriﬁed that the attraction to SH stations was signiﬁcantly higher than the attraction to the SH zones during each of thetwo study periods and in each of the four areas (Table 2). Therefore,
in the following analyses, we pooled the data obtained from all theexperimental sessions. When considering all sessions, we foundthat stone handlers were signiﬁcantly more frequently attracted to
SH stations than to SH zones, and spent signiﬁcantly more timehandling stones from SH stations than from SH zones (Table 2).
Regarding the effect sizes, we found that d ¼ 0.86 with 95%
CI ¼ 0.6 to 1.1 for the frequency of SH on SH stations versus on SH
zones, and d ¼ 0.65 with 95% CI ¼ 0.3 to 1.0 for the duration of SH
on SH stations versus on SH zones. These results show that theeffect sizes can be considered ‘large’ in terms of frequency, and5

between ‘medium’ and ‘large’ in terms of duration, and are both
statistically signiﬁcant (at an a level of 0.05) because the CIs do notinclude zero.
Whether we considered each session or all sessions, and eachstone handler or all stone handlers, the mean, total frequency andduration of SH phases were systematically higher on SH stations
than in SH zones (Table 3). We compared SH frequency on bothtypes of SH spots only for the individual ﬁrst entering the experimental area in each session, the strongest test of prediction 1
because the stone handler could not be affected by the behaviour oreven the mere presence of a conspeciﬁc, and thus any possible
direct social inﬂuence was removed. We also found that thefrequency of SH behaviour was signiﬁcantly higher when directed
to SH stations than when directed to SH zones (17 individuals more
attracted to SH stations, one more attracted to SH zones, and two
equally attracted to both SH spots; Wilcoxon signed-ranks test:
Z ¼ 3.581, N ¼ 20, P < 0.001). In sum, we have shown that thefrequency and duration of SH behaviour were signiﬁcantly higher
when directed to piles of stones (SH stations) than when directed torandomly scattered stones (SH zones), for all individuals entering
the experimental areas, including the ﬁrst one to do so, thereby
verifying prediction 1.
During two consecutive sessions, the same individuals entering
the same experimental area where the SH stations had been moved
2 m away from their previous spots were signiﬁcantly more
attracted to the new locations of the SH stations than the previous
spots to perform SH (Wilcoxon signed-ranks test: Z ¼ 3.473,
N ¼ 17, P ¼ 0.001). Thus, we veriﬁed prediction 2.

Spatial Preferences for SH at Group and Individual Levels
We found signiﬁcant differences in the frequency of presence
and SH frequency of group members in the four experimental areas(Friedman tests: presence: c23 ¼ 88.88, N ¼ 116, P < 0.001; SH:
c23 ¼ 50.28, N ¼ 82, P < 0.001). Multiple paired comparisons
showed that the frequency of presence was signiﬁcantly higher inareas 1 and 3 than in areas 2 and 4 (P < 0.05) and SH frequency wassigniﬁcantly higher in area 1 than in area 4 and in area 3 than inareas 2 and 4 (P < 0.05). The other differences did not reachstatistical signiﬁcance (P > 0.05). These results were consistent
with the number of group members recorded present and engaged
in SH activity at least once in the four experimental areas (Table 4).

7060% Time

50
40
30
20
10
0

Locomoting Feeding

Foraging

Grooming

Resting

SH on SHstations

SH on SH
zones

Activity
Figure 2. Mean percentage  SD of time devoted to different activities by individuals present in the experimental areas.

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Table 2Comparison of the number of individuals more attracted to stone-handling (SH) stations, more attracted to SH zones, and equally attracted to both SH spots, based on thefrequency and duration of SH phases on SH stations versus on SH zones
PeriodAutumn 2008
Spring 2009
Area
1
2
3
4

VariableNZ*

P (one tailed)

2
0
5
0

46
46
68
68

5.616
5.3706.347
6.159<0.001<0.001<0.001<0.001

1
2
5
6
4
4
3
3

2
0
4
0
2
0
0
0

46
46
31
31
54
54
18
18

5.722
5.709
2.761
3.175
5.953
5.928
2.658
2.592<0.001<0.001
0.006
0.002<0.001<0.001
0.008
0.010

3
6

6
0

82
82

7.455
7.307<0.001<0.001

No. of individuals
More attracted to
SH stations

More attracted to
SH zones

Equally attracted toboth SH spots

Frequency
Duration
Frequency
Duration

42
43
57
61

2
3
6
7

Frequency
Duration
Frequency
Duration
Frequency
Duration
Frequency
Duration

43
44
22
25
48
50
15
15

Frequency
Duration

73
76

All sessions*

Wilcoxon signed-ranks test.

Therefore, at the group level, some areas were more attractive thanothers in terms of presence and SH activity.
Of 82 group members engaged in SH activity during theexperimental sessions, there was a signiﬁcant difference in thenumber of individuals recorded performing SH in only one area
(N ¼ 40, i.e. 48.8%), in two areas (N ¼ 21, i.e. 25.6%), in three areas(N ¼ 16, i.e. 19.5%) and in the four areas (N ¼ 5, i.e. 6.1%; chi-square
test: c23 ¼ 31.27, P < 0.001). Post hoc examination of residuals
showed that there were signiﬁcantly more individuals recorded
performing SH in only one area than in two, three and four areas.
Thus we found, at the individual level, differential spatial preferences to engage in SH activity.
Number and Relative Location of SH Stations Used
We found a signiﬁcant difference in the number of SH stations
used by a given stone handler during the same session, namely only
one SH station (N ¼ 130, i.e. 56.6% of sessions), two SH stations(N ¼ 58, i.e. 25.2%), three SH stations (N ¼ 24, i.e. 10.4%) and fromfour to seven SH stations (N ¼ 18, i.e. 7.8%; chi-square test:
c23 ¼ 138.07, P < 0.001). Post hoc examination of residuals showedthat the use of one SH station was signiﬁcantly more frequent than

Table 3
Mean  SD frequency and duration (in min) of stone-handling (SH) phases
performed on SH stations and SH zones
SH stations

the use of two, three and four to seven SH stations. When a given
stone handler used more than one SH station per session (N ¼ 100),it used adjacent SH stations in a majority of cases (59.7  44.1%).
Transport of Stones between SH Spots
We found that 68 of 559 SH phases (i.e. 12.2%) started witha transport of stones between SH spots. We did not record any
transport of stones between two SH zones. There was a signiﬁcantdifference in the frequency of the three other categories of transport, namely between two SH stations (N ¼ 14), from an SH station
to an SH zone (N ¼ 21), and from an SH zone to an SH station(N ¼ 33; chi-square test: c22 ¼ 8.15, P ¼ 0.017). Post hoc examination of residuals showed that the transport of stones from an SH
zone to an SH station was signiﬁcantly more frequent than thetransport of stones between two SH stations.
Use of SH Artefacts across Age Classes
Across all age classes, stone handlers were signiﬁcantly more
frequently attracted to SH stations than to SH zones (Wilcoxon
signed-ranks tests: infants and yearlings: Z ¼ 2.944, N ¼ 11,
P ¼ 0.003; juveniles: Z ¼ 2.536, N ¼ 10, P ¼ 0.011; subadults:
Z ¼ 3.426, N ¼ 16, P ¼ 0.001; young adults: Z ¼ 1.992, N ¼ 9,
P ¼ 0.046; middle-aged adults: Z ¼ 2.887, N ¼ 13, P ¼ 0.004; oldadults: Z ¼ 4.018, N ¼ 23, P < 0.001) and spent signiﬁcantly moretime handling stones from SH stations than from SH zones (infants
and yearlings: Z ¼ 2.934, P ¼ 0.003; juveniles: Z ¼ 2.599,
P ¼ 0.009; subadults: Z ¼ 3.516, P < 0.001; young adults:

SH zones

Total

Per session and per stone handler
Mean frequency
2.01.8
Mean duration
1.52.4

0.40.8
0.10.4

2.42.0
1.62.4

Per session and for all stone handlers
Mean frequency
12.87.5
Mean duration
9.68.1

2.33.1
0.71.3

15.17.9
10.38.1

For all sessions and per stone handler
Mean frequency
5.86.7
Mean duration
4.48.5

1.01.9
0.81.0

6.87.5
4.68.5

Area

For all sessions and for all stone handlers
Total frequency
473(%)(84.6)
Total duration
5.9(%)(93.1)

86(15.4)
0.4
(6.9)

559
(100.0)6.3(100.0)

1
2
3
4

Table 4
Number and percentage of identiﬁed group members recorded present andperforming stone handling (SH) at least once in the four experimental areas
Number (%) of identiﬁed group membersrecorded at least once
Present

SH

81 (55.9)33 (22.8)
79 (54.5)
35 (24.1)

46 (31.7)
32 (22.1)
54 (37.2)
18 (12.4)

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Z ¼ 1.982, P ¼ 0.048; middle-aged adults: Z ¼ 2.760, P ¼ 0.006;
old adults: Z ¼ 4.106, P < 0.001).
Role of Kinship in the Use of SH Artefacts
Twelve group members aged 1 year and less entered the areas atleast once during the experimental sessions (i.e. 85.7% of infants
and yearlings), among which 11 were engaged in SH activity (i.e.
78.6% of infants and yearlings). We recorded a total of 29 entrancesof infants and yearlings, among which 27 (93.1%) occurred in thepresence of the mother. We recorded a total of 12 coactions of two
individuals performing SH simultaneously on the same SH spot, allof which occurred on SH stations (not on SH zones), and all ofwhich involved close kin (six involved three mother–infant dyads,
three involved one mother–yearling dyad, one involved a motherand her 2-year-old daughter, one involved a mother and her 8-yearold daughter, and one involved an infant and her 2-year-old sister).
In the 13 other cases when two close kin performed SH simultaneously in the same area, they did it on two adjacent SH stations in
10 cases (i.e. 76.9%).
Role of Dominance Relationships in the Use of SH Artefacts
Low- and middle-ranking stone handlers were signiﬁcantly
more frequently attracted to SH stations than to SH zones(Wilcoxon signed-ranks tests: low-ranking: Z ¼ 4.296, N ¼ 25,
P < 0.001; middle-ranking: Z ¼ 3.054, N ¼ 14, P ¼ 0.002), andspent signiﬁcantly more time handling stones from SH stations
than from SH zones (low-ranking: Z ¼ 4.211, P < 0.001; middleranking: Z ¼ 3.233, P ¼ 0.001). We did not ﬁnd such signiﬁcantdifferences in high-ranking stone handlers (N ¼ 5, frequency:
Z ¼ 0.707, P ¼ 0.480; duration: Z ¼ 0.674, P ¼ 0.500). The latter
result may be explained by the small sample size: only ﬁve highranking group members were engaged in SH activity during theexperimental sessions. Supplanting interactions were signiﬁcantly
more frequent over SH stations than over SH zones (59 interactions(i.e. 96.7%) versus 2 (i.e. 3.3%), respectively; Wilcoxon signed-ranks
test: Z ¼ 4.873, N ¼ 33 individuals, P < 0.001).
DISCUSSION
Through the semicontrolled conditions of ﬁeld experiments, weaimed to simulate the context under which SH might be sociallymaintained in the wild, and infer which form(s) of social inﬂuence
might support the persistence of the SH culture in Japanesemacaques. Our results supported the ‘stimulus/local enhancement
hypothesis’ that individuals preferentially direct their SH behaviour
towards typical physical traces of SH activity (piles of stones) overrandomly scattered stones. In other words, encountering SH artefacts enhanced the use of these particular stones to perform SH
activity in that particular part of the environment. Therefore, wehave provided the ﬁrst experimental evidence for the role of indirect social inﬂuence in the daily performance of SH behaviour by
most group members, and thus the maintenance of the SH tradition. By supporting the view that SH is a socially inﬂuenced
behaviour, this study helps validate the concept of SH culture (seealso Huffman 1984, 1996; Leca et al. 2007b, 2008c; Nahallage &Huffman 2007b).
Some authors have argued for a formal difference between
stimulus enhancement (Spence 1937) and local enhancement(Thorpe 1963); the former would refer to an individual aiming its
responses towards particular objects, whereas the latter wouldrefer to an individual focusing its attention towards particularplaces in the environment. However, in practice, it is difﬁcult tomake an operational distinction between the two mechanisms.

7

This may explain why they are often associated in the literature asa single stimulus/local enhancement process (Tomasello et al. 1993;
Byrne & Russon 1998; Visalberghi & Adessi 2001; Visalberghi &Fragaszy 2002). Some of our results were more consistent withstimulus enhancement, such as (1) the preferential attraction to the
new locations (where the piles of stones were) over the original
locations (from when the piles of stones were removed), (2) thegeneralized attraction for SH artefacts, found in all experimental
areas, and (3) the fact that most stone handlers mainly used one
pile of stones during the same session. Other results rather supported local enhancement, such as (1) clear spatial preferences for
SH at the group and individual levels, and (2) the use of adjacentpiles of stones by the same stone handler. The relatively frequenttransport of stones between SH spots could be interpreted as
stimulus or local enhancement. The two processes are apparently
not mutually exclusive, and they both inﬂuence the relative probability of encountering stones.
In our case, local and stimulus enhancement could even occur
sequentially. We argue that prospective stone handlers ﬁrst aim fora particular area where stones are usually available, and then they
may preferentially direct their SH behaviour towards alreadygathered stones, if any, rather than randomly scattered stones.
During our experiments, some individuals were ﬁrst seen walking
across the entire experimental area, visually scanning all the local
piles of stones, occasionally touching some of them, and thencoming back to one particular artefact to start performing SH (J.-B.
Leca, personal observation).
From an evolutionary perspective, the niche construction
process refers to the environmental alterations caused by organisms, and their consequences for their community members,
including cultural changes (Odling-Smee 1996). As typical SH byproducts, the occurrence of multiple piles of stones left in particularplaces by previous stone handlers are attention getting and could
be considered conspicuous visual cues of SH activity even between
SH events. As they become more deeply ingrained into the
behavioural landscape of the monkeys, these ‘play stations’ (Quiatt& Huffman 1993) could ensure a baseline level of visual persistenceof this form of material culture in Japanese macaques. This isparticularly true for free-ranging provisioned troops, characterized
by an increased sedentary lifestyle, with most group members
staying around feeding grounds, that is, open areas with stones(Leca et al. 2008b). Smaller home ranges are likely to increase anindividual’s probability of encountering SH artefacts, which, inturn, may enhance SH activity. Moreover, we showed that piles ofstones are frequently reused and constantly modiﬁed by themonkeys themselves through the transport of stones between andaround SH artefacts. The frequent transport of randomly scatteredstones to already gathered stones suggests cumulative environmental modiﬁcations. Therefore, through the ever-changing physical traces they leave in the environment, their subsequent
stimulating effect on other group members and across generations,and their possible role in the maintenance of the SH tradition, we
argue that stone handlers can be considered niche constructors.
Our study suggests that a niche construction process could
underlie the cultural maintenance of SH behaviour in Japanesemacaques. Niche construction, through the creation of enduringphysical artefacts, occurs in other taxa as well. As extractive anddestructive foragers, capuchin monkeys can be labelled as‘ecosystem engineers’ (Fragaszy et al. 2004). When wild brown
capuchins, Cebus apella, forage on invertebrates embedded inbamboo stalks, they leave in the environment speciﬁc physicaltraces, that is, numerous holes in bamboo segments previously
ripped apart for larvae. These conspicuous foraging artefacts are
attractive visual cues for young individuals (Gunst et al. 2007).
Through drawing their attention to a particular foraging spot, even

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after the original forager had left the site, stimulus enhancement
may contribute to naı̈ve foragers becoming more familiar with thefood items and substrates, learning the characteristics of appropriate substrates, acquiring speciﬁc detection techniques, andmaintaining them at the group level (Gunst et al. 2008, in press). In
capuchins, learning can also be delayed in time and separate inspace from others, and in this sense, niche construction has anextended time frame and lesser dependence on copresence withothers (Gunst et al. 2008).
Similar indirect social inﬂuences are likely to occur in theacquisition and maintenance of tool use behaviours in wild chimpanzees, Pan troglodytes, and brown capuchins, through the stimulating effect of nut-cracking by-products (nutshells, stones) left byskilled foragers around nut-cracking ateliers (Tomasello et al. 1993;
Inoue-Nakamura & Matsuzawa 1997; Visalberghi et al. 2009).
Situations in which artefacts of others’ activity promote practice of
relevant behaviours and may foster learning effectively can also befound in nonprimate taxa, as shown by experimental studies ofbirds learning to open the lids on milk bottles (Sherry & Galef 1984,1990), a behaviour observed to occur spontaneously (Fisher &Hinde 1949), as well as bower birds’ nests that can be considered
artefactual niches (Odling-Smee et al. 2003). In general, conspeciﬁcs provide ‘tools’ (sensu sociocultural learning theory: Forman
et al. 1993) for the individual acquisition, as well as the diffusion
and maintenance, of behaviours at the group level.
From a developmental perspective, constant exposure to various
artefacts could increase individual attention to some relevant
environmental features, as suggested by Furlong et al. (2008) withrespect to young chimpanzees reared in a human socioculturalenvironment. For young Japanese macaques growing up in a troop
where the SH tradition is well established and has reached its
transformation phase (deﬁned as the late period of cultural transmission during which the behaviour is consolidated through integration with other daily activities: Huffman & Hirata 2003),
resulting in a stimulating environment enriched in SH artefacts,
a form of ‘SH enculturation’ process may facilitate their earlyacquisition of the behaviour. This argument is all the more relevant
as we found a preferential use of piles of stones for SH across all age
classes, including infants and yearlings.
The ﬁnding that the ﬁrst individual to enter an experimental
area preferred the piles of stones to scattered stones (prediction 1)
provides evidence that a pile of stones per se is a sufﬁcient
stimulus to enhance the performance of SH activity in any individual, and without any direct social inﬂuence from other groupmembers. It is beyond the scope of this study to evaluate thepossible role of other social inﬂuences supporting the persistenceof SH activity within Japanese macaque troops over decades.
However, our results on the positive role of kinship in the use of
SH artefacts, and particularly the common occurrence of mother–
infant dyads around SH artefacts, sometimes coacting on the same
pile of stones, are consistent with the view that the motivation foryoung individuals to engage in SH activity on a daily basis, andthus the maintenance of the SH tradition across generations, canalso be explained by direct social inﬂuence such as social facilitation or social enhancement.
Through the controlled study conditions of a captive group ofJapanese macaques, Nahallage & Huffman (2007b) showed thatsocial facilitation, involving the observation by naı̈ve infants of
their mothers as SH demonstrators, may better explain theacquisition of SH during the ﬁrst 6 months of life than merely the
infant’s early exposure to stones. Leca et al. (2008c) recently
suggested that the early diffusion of stone-throwing behaviour,a particular SH pattern, may be socially mediated within strongly
afﬁliated dyads. An intertroop comparative study suggested thatsociodemographic constraints such as group size and compositionin age classes, as well as group spatial cohesion, might impact thesynchronized performance of SH at the group level, thereby
conﬁrming the contagious nature of play behaviours (Leca et al.
2007b, 2008b). Overall, the conformity-enforcing hypothesis,
which proposes that culturally nonconforming individuals may bediscriminated against (Lachlan et al. 2004), predicts that immature individuals should adopt the same type of stone-directed
activities as most of the older group members. Our ﬁndings showthat even traditional behaviours with no obvious function and noapparent adaptive value, such as SH, can be practised on a daily
basis and maintained over several years within a large proportionof group members via indirect social inﬂuences. By contrast, whena behavioural practice is restricted to a particular class of groupmembers, it is supposed to spread very slowly and its maintenance may be jeopardized (Huffman & Hirata 2003; Leca et al.
2007b, c, in press b).
Our result on supplanting interactions being more frequent
over piles of stones than randomly scattered stones is consistent
with previous observations showing that once particular stones,
or sets of stones, are involved in an SH episode, they seem tobecome valuable objects for the handler who may pick them up
and carry them to different places rather than leave them behind,and they appear to trigger great interest from others who try tosnatch them away from the handler as if they were the only
stones available (Huffman & Quiatt 1986; Leca et al. 2008b). These
reports suggest the existence of a rudimentary form of ‘possession’ in monkeys, also reported in chimpanzees at Bossou, Guinea,
where some individuals seem to have their favourite stone tool
(Matsuzawa 1999). However, the present results cannot be
exclusively interpreted from the viewpoint of competition forstones, social status and dominance relationships, since theattraction for SH artefacts was higher for low-ranking than highranking individuals.
We have provided evidence for the role of indirect social inputs
on the maintenance of the SH tradition in Japanese macaques,
through the stimulating effect of SH artefacts. To some extent, ourﬁndings allowed us to reconstruct some elements of the environmental and social contexts underlying the SH culture. We clearlyfound that where an individual was likely to handle stones wasaffected by the distribution of the stones manipulated by others. To
claim unequivocally that piles of stones induce SH activity, further
experiments should show that SH frequency is higher in areas withpiles than in areas with no piles. Our study emphasizes the utility ofﬁeld experiments as a way to explore further the determinants ofthe diffusion of novel behaviours and their long-term persistence infree-ranging animal populations (see also Heberlein & Turner 2009;
Thornton & Malapert 2009a, b). Future experiments will investigate
the stimulating effect of different sizes of SH artefacts, and will test
auditory stimulus enhancement via the playback of sounds generated by percussive SH patterns.

Acknowledgments
Our work was funded by a Grant-In-Aid for scientiﬁc research(No. 1907421 to M.A.H.) sponsored by Ministry of Education,
Science, Sports and Culture, Japan, by a JSPS (Japan Society for the
Promotion of Science) postdoctoral fellowship to J.-B.L. (No. 07421),
and by travel funds from the HOPE Project, a core-to-core programme sponsored by JSPS. We are grateful to S. Asaba, J. Hashiguchi, S. Kobatake and S. Tamada from Iwatayama Monkey Park forhelping us during the course of the study. For occasional assistancein data collection, we thank N. Tworoski. We also thank Diego Gil
and two anonymous referees for fruitful comments on the
manuscript.

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References
Altmann, J. 1974. Observational study of behavior: sampling methods. Behaviour,49, 227–267.
Byrne, R. W. & Russon, A. E. 1998. Learning by imitation: a hierarchical approach.
Behavioral and Brain Sciences, 21, 667–721.
Caldwell, C. A. & Whiten, A. 2007. Social learning in monkeys and apes: cultural
animals? In: Primates in Perspective (Ed. by C. J. Campbell, A. Fuentes,
K. C. Mackinnon, M. Panger & S. K. Bearder), pp. 652–664. Oxford: Oxford
University Press.
Cohen, J. 1988. Statistical Power Analysis for the Behavioral Sciences, 2nd edn. Hillsdale, New Jersey: L. Erlbaum.
Coussi-Korbel, S. & Fragaszy, D. M. 1995. On the social relation between social
dynamics and social learning. Animal Behaviour, 50, 1441–1453.
Denny, M. R., Clos, C. F. & Bell, R. C. 1988. Learning in the rat of a choice responseby observation of S–S contingencies. In: Social Learning: Psychological and Biological Perspectives (Ed. by T. R. Zentall & B. G. Galef), pp. 207–223. Hillsdale,
New Jersey: L. Erlbaum.
Fisher, J. & Hinde, R. A. 1949. The opening of milk bottles by birds. British Birds, 42,
347–357.
Forman, E., Minick, N. & Stone, C. A. 1993. Contexts for Learning: Sociocultural
Dynamics in Childrens’ Development. Oxford: Oxford University Press.
Fragaszy, D. M. & Perry, S. 2003a. The Biology of Traditions: Models and Evidence.
Cambridge: Cambridge University Press.
Fragaszy, D. M. & Perry, S. 2003b. Towards a biology of traditions. In: The Biology ofTraditions: Models and Evidence (Ed. by D. M. Fragaszy & S. Perry), pp. 1–32.
Cambridge: Cambridge University Press.
Fragaszy, D. M. & Visalberghi, E. 2001. Recognizing a swan: socially-biased
learning. Psychologia, 44, 82–98.
Fragaszy, D. M. & Visalberghi, E. 2004. Socially biased learning in monkeys.
Learning and Behavior, 32, 24–35.
Fragaszy, D. M., Visalberghi, E. & Fedigan, L. M. 2004. The Complete Capuchin: theBiology of the Genus Cebus. Cambridge: Cambridge University Press.
Furlong, E. E., Boose, K. J. & Boysen, S. T. 2008. Raking it in: the impact of
enculturation on chimpanzee tool use. Animal Cognition, 11, 83–97.
Galef, B. G. Jr. 1988. Imitation in animals: history, deﬁnitions and interpretation of
the data from the psychological laboratory. In: Social Learning: Psychological andBiological Perspectives (Ed. by T. R. Zentall & B.G. Galef Jr.), pp. 3–28. Hillsdale,
New Jersey: L. Erlbaum.
Galef, B. G. Jr. 2004. Approaches to the study of traditional behaviors of free-living
animals. Learning and Behavior, 32, 53–61.
Galef, B. G. Jr. & Buckley, L. L. 1996. Use of foraging trails by Norway rats. Animal
Behaviour, 51, 765–771.
Galef, B. G. Jr. & Laland, K. N. 2005. Social learning in animals: empirical studies
and theoretical models. BioScience, 55, 489–499.
Gunst, N., Boinski, S. & Fragaszy, D. M. 2007. Studying how social context aids
acquisition of foraging skills in wild brown capuchins (Cebus apella) in
Suriname (Abstract). American Journal of Primatology, 69 (Supplement 1), 76.
Gunst, N., Boinski, S. & Fragaszy, D. M. 2008. Acquisition of foraging competence
in wild brown capuchins (Cebus apella), with special reference to conspeciﬁcs’
foraging artefacts as an indirect social inﬂuence. Behaviour, 145, 195–229.
Gunst, N., Boinski, S. & Fragaszy, D. M. In press. Development of skilled detectionand extraction of embedded preys by wild brown capuchin monkeys (Cebus
apella apella). Journal of Comparative Psychology.
Heberlein, M. & Turner, D. C. 2009. Dogs, Canis familiaris, ﬁnd hidden food byobserving and interacting with a conspeciﬁc. Animal Behaviour, 78, 385–391,
doi:10.1016/j.anbehav.2009.05.012.
Hölldobler, B. & Wilson, E. O. 1991. The Ants. Berlin: Springer-Verlag.
Huber, L., Rechberger, S. & Taborsky, M. 2001. Social learning affects object
exploration and manipulation in keas, Nestor notabilis. Animal Behaviour, 62,
945–954, doi:10.1006/anbe.2001.1822.
Huffman, M. A. 1984. Stone-play of Macaca fuscata in Arashiyama B troop:transmission of a non-adaptive behavior. Journal of Human Evolution, 13,725–735.
Huffman, M. A. 1991. History of Arashiyama Japanese macaques in Kyoto, Japan. In:
The Monkeys of Arashiyama: Thirty-ﬁve Years of Research in Japan and the West
(Ed. by L. M. Fedigan & P. J. Asquith), pp. 21–53. Albany, New York: SUNY Press.
Huffman, M. A. 1996. Acquisition of innovative cultural behaviors in non-humanprimates: a case study of stone handling, a socially transmitted behavior inJapanese macaques. In: Social Learning in Animals: the Roots of Culture (Ed. by
B. G. Jr & C. Heyes), pp. 267–289. Orlando: Academic Press.
Huffman, M. A. & Hirata, S. 2003. Biological and ecological foundations of primate
behavioral tradition. In: The Biology of Tradition: Models and Evidence (Ed. by
D. M. Fragaszy & S. Perry), pp. 267–296. Cambridge: Cambridge University
Press.
Huffman, M. A. & Quiatt, D. 1986. Stone handling by Japanese macaques (Macaca
fuscata): implications for tool use of stones. Primates, 27, 413–423.
Huffman, M. A., Nahallage, C. A. D. & Leca, J.-B. 2008. Cultured monkeys, social
learning cast in stones. Current Directions in Psychological Science, 17, 410–414.
Hunt, G. R. & Gray, R. D. 2003. Diversiﬁcation and cumulative evolution in New
Caledonian crow tool manufacture. Proceedings of the Royal Society, B, 270,
867–874.
Inoue-Nakamura, N. & Matsuzawa, T. 1997. Development of stone tool use by wild
chimpanzees (Pan troglodytes). Journal of Comparative Psychology, 111, 159–173.

9

Lachlan, R. F., Janik, V. M. & Slater, P. J. B. 2004. The evolution of conformityenforcing behaviour in cultural communication systems. Animal Behaviour, 68,
561–570, doi:10.1016/j.anbehav.2003.11.015.
Leca, J.-B., Gunst, N. & Huffman, M. A. 2007a. Japanese macaque cultures: interand intra-troop behavioural variability of stone handling patterns across 10
troops. Behaviour, 144, 251–281.
Leca, J.-B., Gunst, N. & Huffman, M. A. 2007b. Age-related differences in theperformance, diffusion, and maintenance of stone handling, a behavioral
tradition in Japanese macaques. Journal of Human Evolution, 53, 691–708,
doi:10.1016/j.jhevol.2007.05.009.
Leca, J.-B., Gunst, N., Watanabe, K. & Huffman, M. A. 2007c. A new case ofﬁsh-eating in Japanese macaques: implications for social constraints on
the diffusion of feeding innovation. American Journal of Primatology, 69,
821–828.
Leca, J.-B., Gunst, N. & Huffman, M. A. 2008a. Of stones and monkeys: testing
ecological constraints on stone handling, a behavioral tradition in Japanesemacaques. American Journal of Physical Anthropology, 135, 233–244.
Leca, J.-B., Gunst, N. & Huffman, M. A. 2008b. Variability of food provisioning
regimes and stone handling tradition in Japanese macaques: a comparative
study of ten troops. American Journal of Primatology, 70, 803–813.
Leca, J.-B., Nahallage, C. A. D., Gunst, N. & Huffman, M. A. 2008c. Stone-throwing
by Japanese macaques: form and functional aspects of a group-speciﬁcbehavioral tradition. Journal of Human Evolution, 55, 989–998, doi:10.1016/
j.jhevol.2008.06.004.
Leca, J. -B., Gunst, N. & Huffman, M. A. In press a. Principles and levels of laterality
in unimanual and bimanual stone handling patterns by Japanese macaques.
Journal of Human Evolution.
Leca, J. -B., Gunst, N. & Huffman, M. A. In press b. The ﬁrst case of dental ﬂossing
by a Japanese macaque (Macaca fuscata): implications for the determinants of
behavioral innovation and the constraints on social transmission. Primates. doi:
10.1007/s10329-009-0159-9.
Lefebvre, L. 1995. Culturally-transmitted feeding behaviour in primates: evidence
for accelerating learning rates. Primates, 36, 227–239.
Martin, P. & Bateson, P. 1993. Measuring Behaviour: an Introductory Guide. Cambridge: Cambridge University Press.
Matsuzawa, T. 1994. Field experiments on use of stone tools by chimpanzees in thewild. In: Chimpanzee Cultures (Ed. by R. W. Wrangham, W. C. McGrew, F. B. M. de
Waal & P. G. Heltne), pp. 351–370. Cambridge, Massachusetts: Harvard
University Press.
Matsuzawa, T. 1999. Communication and tool use in chimpanzees: cultural andsocial context. In: The Design of Animal Communication (Ed. by M. Hauser &M. Konishi), pp. 645–671. Cambridge, Massachusetts: MIT Press.
Nahallage, C. A. D. & Huffman, M. A. 2007a. Age-speciﬁc functions of stone
handling, a solitary-object play behavior, in Japanese macaques (Macaca fuscata). American Journal of Primatology, 69, 267–281.
Nahallage, C. A. D. & Huffman, M. A. 2007b. Acquisition and development ofstone handling behavior in infant Japanese macaques. Behaviour, 144,
1193–1215.
Nakagawa, S. & Cuthill, I. C. 2007. Effect size, conﬁdence interval andstatistical signiﬁcance: a practical guide for biologists. Biological Reviews,
82, 591–605.
Nishie, H. 2002. The proximate factors of stone handling behaviour of Japanesemacaques (Macaca fuscata) in Arashiyama E troop (in Japanese with English
abstract). Primate Research, 18, 225–232.
Noldus Information Technology 1998. Matman Reference Manual. Version 1.0 for
Windows. Wageningen, The Netherlands: Noldus Information Technology.
Odling-Smee, F. J. 1996. Niche construction, genetic evolution and cultural change.
Behavioural Processes, 35, 195–205.
Odling-Smee, F. J., Laland, K. N. & Feldman, M. 2003. Niche Construction: theNeglected Process in Evolution. Princeton. New Jersey: Princeton University
Press.
Perry, S., Panger, M., Rose, L. M., Baker, M., Gros-Louis, J., Jack, K.,
McKinnon, K. C., Manson, J., Fedigan, L. & Pyle, K. 2003. Traditions in wild
white-faced capuchins. In: The Biology of Tradition: Models and Evidence (Ed. by
D. M. Fragaszy & S. Perry), pp. 391–423. Cambridge: Cambridge University
Press.
Quiatt, D. & Huffman, M. A. 1993. On home bases, nesting sites, activity centers,
and new analytic perspectives. Current Anthropology, 34, 68–70.
Rendell, L. & Whitehead, H. 2001. Culture in whales and dolphins. Behavioral andBrain Sciences, 24, 309–382.
Sherry, D. & Galef, B. G. 1984. Cultural transmission without imitation: milk bottle
opening by birds. Animal Behaviour, 32, 937–938.
Sherry, D. & Galef, B. G. 1990. Social learning without imitation: more about milkbottle opening by birds. Animal Behaviour, 40, 987–989.
Siegel, S. & Castellan, N. J. 1988. Nonparametric Statistics for the Behavioral Sciences.
Singapore: McGraw-Hill.
Spence, K. W. 1937. Experimental studies of learning and higher mental processes
in infra-human primates. Psychological Bulletin, 34, 806–850.
Thornton, A. & Malapert, A. 2009a. The rise and fall of an arbitrary tradition:
an experiment with wild meerkats. Proceedings of the Royal Society B, 276,
1269–1276.
Thornton, A. & Malapert, A. 2009b. Experimental evidence for social transmissionof food acquisition techniques in wild meerkats. Animal Behaviour, 78, 575–592,
doi:10.1016/j.anbehav.2009.04.021.
Thorpe, W. H. 1963. Learning and Instinct in Animals. London: Methuen.

Please cite this article in press as: Leca, J.-B., et al., Indirect social inﬂuence in the maintenance of the stone-handling tradition in Japanese...,Animal Behaviour (2009), doi:10.1016/j.anbehav.2009.09.035

ARTICLE IN PRESS
276

10

J.-B. Leca et al. / Animal Behaviour xxx (2009) 1–10

Tomasello, M., Cale Kruger, A. & Horn Ratner, H. 1993. Cultural learning. Behavioural and Brain Sciences, 16, 495–552.
Visalberghi, E. & Adessi, E. 2001. Acceptance of novel foods in capuchin monkeys:
do speciﬁc social facilitation and visual stimulus enhancement play a role?
Animal Behaviour, 62, 567–576, doi:10.1006/anbe.2001.1787.
Visalberghi, E. & Fragaszy, D. M. 2002. Do monkeys ape? Ten years after. In:
Imitation in Animals and Artifacts (Ed. by K. Dautenhahn & C. L. Nehaniv),
pp. 471–499. Cambridge, Massachusetts: MIT Press.
Visalberghi, E., Spagnoletti, N., Ramos da Silva, E. D., Andrade, F. R. D., Ottoni, E.,
Izar, P. & Fragaszy, D. 2009. Distribution of potential suitable hammers andtransport of hammer tools and nuts by wild capuchin monkeys. Primates, 50,
95–104.
Vogel, E. R. & Janson, C. H. 2007. Predicting the frequency of food-related agonism
in white-faced capuchin monkeys (Cebus capucinus), using a novel focal-tree
method. American Journal of Primatology, 69, 533–550.

de Vries, H. 1995. An improved test of linearity in dominance hierarchies containing
unknown or tied relationships. Animal Behaviour, 50, 1375–1389.
de Vries, H., Netto, W. J. & Hanegraaf, P. L. H. 1993. Matman: a program for the
analysis of sociometric matrices and behavioural transition matrices. Behaviour,
125, 157–175.
Watson, C. F. I. & Caldwell, C. A. 2009. Understanding behavioral traditions inprimates: are current experimental approaches too focused on food? International Journal of Primatology, 30, 143–167.
Whiten, A. 2000. Primate culture and social learning. Cognitive Science, 24,
477–508.
Whiten, A., Goodall, J., McGrew, W. C., Nishida, T., Reynolds, V., Sugiyama, Y.,
Tutin, C. E., Wrangham, R. W. & Boesch, C. 1999. Cultures in chimpanzees.
Nature, 399, 682–685.
Zentall, T. R. & Galef, B. G. Jr. 1988. Social Learning: Psychological and Biological
Perspectives. Hillsdale, New Jersey: Erlbaum.

Please cite this article in press as: Leca, J.-B., et al., Indirect social inﬂuence in the maintenance of the stone-handling tradition in Japanese...,Animal Behaviour (2009), doi:10.1016/j.anbehav.2009.09.035

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Journal of Human Evolution xxx (2009) 1–11

Contents lists available at ScienceDirect

Journal of Human Evolution
journal homepage: www.elsevier.com/locate/jhevol

Principles and levels of laterality in unimanual and bimanual stone handling
patterns by Japanese macaquesJean-Baptiste Leca*, Noëlle Gunst, Michael A. Huffman
Section of Social Systems Evolution, Primate Research Institute, Kyoto University, 41-2 Kanrin, Inuyama, Aichi 484-8506, Japana r t i c l e i n f o

a b s t r a c t

Article history:
Received 28 April 2009
Accepted 22 September 2009
Available online xxx

The preferential use of one hand over the other is considered the primary behavioral expression of
structural and functional asymmetry in cerebral structures, which is a decisive factor in human evolution. We present the ﬁrst analysis of manual laterality in a form of object playdstone handling (SH)behaviordin a free-ranging group of Japanese macaques. Deﬁned as a stone-directed manipulative
activity, and comprised of multiple one-handed SH patterns (e.g., grabbing a stone in one hand andcradling it against its chest), as well as coordinated two-handed SH patterns with manual role differentiation (e.g., holding a stone with one hand and rubbing it with the other), SH behavior is a goodcandidate for the study of hand lateralization. We systematically followed the methodological framework
developed by McGrew and Marchant (1997) to measure and analyze the presence, strength, anddirection of manual preference in the performance of SH behavior and in various SH patterns, both at theindividual and group level. Some individuals showed a signiﬁcant manual lateral bias on a single SH
pattern (hand preference), whereas others showed consistency in laterality across all or most of the SH
patterns they performed (hand specialization). At the group level, we found that, although their collective
distribution of left versus right remained random, most subjects were either signiﬁcantly but incompletely lateralized, or completely lateralized within particular SH patterns (pattern specialization), but not
across all SH patterns (no handedness for SH behavior as a whole). As predicted by the task-complexity
model, hand specialization and handedness were stronger in the coordinated bimanual SH patterns thanin the unimanual patterns. We discuss the implications of our ﬁndings for the evolution of manual
preferences in noninstrumental object manipulation versus stone tool use in nonhuman primates andhominins.
Ó 2009 Elsevier Ltd. All rights reserved.

Keywords:
Manual preference
Handedness
Role-differentiated actions
Object manipulation
Stone-tool use
Macaca fuscata

Introduction
Two main reasons may account for the interest in the nature,form, distribution, and possible function of manual laterality innonhuman primates (cf. MacNeilage et al., 1987; Ward and Hopkins, 1993; McGrew and Marchant, 1997; Papademetriou et al.,2005 for a review). First, the preferential use of one hand over theother is considered the primary behavioral expression of structuraland functional asymmetry in cerebral structures, the latter beinga decisive factor in human evolution (Corballis, 1983; Vallortigara
and Rogers, 2005). Different hypotheses propose that the translation of complex manipulative skills into a right-hand preference,linked to a specialization of the left hemisphere of the brain tocontrol it (cf. Corballis, 1983; Annett, 1985), are associated with the
emergence of bipedalism, object-throwing behavior, and elaborate* Corresponding author.
E-mail address: jbtleca@yahoo.com (J.-B. Leca).

cognitive processes such as tool use and language in early hominins(Frost, 1980; Calvin, 1982; Bradshaw and Rogers, 1993; Sharer,1993). Second, the search for a possible precursor of human manual
laterality in animals has primarily focused on nonhuman primates
because of their phylogenetic relatedness to humans (Homosapiens).
However, the evolution of hand lateralization has been a topic of
historical and contemporary debate (Warren, 1980; MacNeilage
et al., 1987; Fagot and Vauclair, 1991; Marchant and McGrew, 1991;
Hopkins, 1999; McGrew and Marchant, 1997; Palmer, 2002).
Despite a plethora of published studies, there was never anything
approaching a scientiﬁc consensus on that issue. The causes of suchcontroversy are both theoretical and methodological.
The most comprehensive evolutionary model of manual laterality to date was proposed by MacNeilage et al. (1987) and referred
to as ‘‘the postural origins theory’’ (MacNeilage, 1991). This model
advocates a phylogenetic continuity of hand lateralization within
the order Primates, originating from an adaptation to unimanual
predation in our primate ancestors, and whose evolutionary history0047-2484/$ – see front matter Ó 2009 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jhevol.2009.09.005

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Japanese macaques, J Hum Evol (2009), doi:10.1016/j.jhevol.2009.09.005

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Table 1
Principles of laterality in the performance of SH behavior (after Marchant and
McGrew, 1998)a
Subject(s)SH pattern(s)WithinAcrossWithinAcrossHand preference
Yes
Hand specialization
Yes(Sim-Comp > Uni)

Pattern specialization
Yes
HandednessNo(Sim-Comp > Uni)a
The results of the present study are in italics. Sim-Comp: coordinated bimanual
patterns where both hands operate simultaneously but complementarily; Uni:
unimanual patterns.

could be traceable through the pattern of manual laterality inmodern nonhuman primates. More than two decades later, anddespite an extensive database on manual laterality in various
primate taxa, there is scant support for the postural origins theory.
Overall, measures of hand preferences in prosimians, monkeys, andapes have yielded negative, inconsistent, contradictory, or far fromconclusive results (McGrew and Marchant, 1997). Many living
primates showed individual-level bias toward the left or right handin certain contexts and when performing particular behaviors.
However, signiﬁcance and directional consistency in manual
lateralization in free-ranging or semi-free-ranging populations of
nonhuman primates have not yet been found in any species and forany type of task (but see Hopkins [2006] in captive chimpanzees
and for speciﬁc tasks). Since Homo sapiens appears to be the only
species predominantly right-handed, the question arose as towhether the patterns of manual preferences in nonhuman primates
are more analogous than homologous to those observed in humans(Warren, 1980; Bradshaw and Rogers, 1993; McGrew and Marchant,1997).
Furthermore, the lack of methodological consensus among thestudies of laterality undoubtedly precludes systematic comparisonsand meaningful interpretations of the results obtained. Differencesin the way to measure manual preferences, the terminology used,
and the statistical procedures employed are also likely to explain
the considerable disagreement about the evolution of hand lateralization (McGrew and Marchant, 1997; Palmer, 2002). Moreover,various environmental, experiential, social, and biological factorsthat seem to inﬂuence directly or indirectly the development,
expression, and maintenance of manual laterality in individuals are
simply ignored in many studies. Intrinsic variables include themorphological and behavioral characteristics of the species understudy, life history traits such as age and sex, particular haplotypes,
individual experience and practice, and situational variables suchas emotional state, body posture, and positioning. Extrinsic variables include the complexity and novelty of the behavior measured,
procedural conditions, and habitat (see McGrew and Marchant,
1997 for a review). Finally, most data on manual laterality comefrom studies of captive primates, which may be problematic sincenotable differences in hand use patterns were found between
captive and free-ranging subjects (McGrew and Marchant, 1997).
The following example illustrates the need for both theoreticaland methodological considerations when tackling the issue ofmanual laterality. In the context of extractive foraging, most studies
showed that populations of wild chimpanzees were signiﬁcantly
lateralized for tool use (wadge-dipping: Boesch, 1991; nutcracking: Boesch, 1991; Matsuzawa et al., 2001; termite-ﬁshing:
McGrew and Marchant, 1996; Lonsdorf and Hopkins, 2005;
Strychnos fruit-pounding: McGrew et al., 1999; but see Marchantand McGrew, 2007 for ant-ﬁshing). This contrasts markedly withother food processing activities involving object manipulation but
not tool use, where no signiﬁcant lateral bias was found at thegroup level (food-reaching/picking: Boesch, 1991; Sugiyama et al.,
1993; food-plucking: Marchant and McGrew, 1996; McGrew andMarchant, 2001; eating: McGrew and Marchant, 2001; Saba fruitpeeling: Corp and Byrne, 2004).
The main reason that may account for this discrepancy isconceptual and is due to the fact that tool use behaviors are usuallymore complex than other object manipulation tasks (but see Byrne
and Byrne [1991, 1993] for complex food processing by mountaingorillas). According to the ‘‘task-complexity’’ model, complex tasks,
such as precise coordinated bimanual and sequential actions,should elicit a greater strength of manual laterality at the grouplevel than simple tasks, such as unimanual object reaching (cf.
Fagot and Vauclair, 1991 for a review). This model is supported by
an extensive database from several primate taxa (Cebus: Westergaard and Suomi, 1993a; Anderson et al., 1996; Cercopithecus:
Trouillard and Blois-Heulin, 2005; Lophocebus: Blois-Heulin et al.,2007; Pan: Hopkins and Rabinowitz, 1997; Papio: Vauclair et al.,2005). However, methodological ﬂaws could also explain the lack oflateralization found for object manipulation. In numerous studies,
two variables are often confounded: unimanual versus bimanual
manipulation, and simple versus complex tasks (cf. Marchant and
McGrew, 1991; McGrew and Marchant, 1997, for a review).
In the quest for uniformity in the empirical assessment ofmanual preference and for parsimony in the interpretations of theresults, the most extensive review on manual laterality innonhuman primates urged the systematic use of the ‘‘principles oflaterality’’ (sic McGrew and Marchant, 1997:215) that can besummarized in a 2  2 matrix representing the degree of variationof hand-use within and across subject(s), and within and acrosstask(s) (Marchant and McGrew, 1998:223). Unfortunately, theevaluation of the principles of laterality is difﬁcult because few
studies have systematically documented manual preference at theindividual and group levels for one and multiple behavioral
patterns (Fagot and Vauclair, 1991; Marchant and McGrew, 1991;
Papademetriou et al., 2005). To provide a better overall picture of
behavioral laterality of hand function in nonhuman primates, there
is a need for more data obtained from various behaviors spontaneously performed by several free-ranging group members to ﬁll
all four cells of the 2  2 matrix generated from the principles oflaterality (McGrew and Marchant, 1997; see also Table 1).
In particular, studies systematically testing the consistency of
manual preference in unimanual and bimanual object manipulative
patterns and across different levels of task complexity in freeranging groups of primates are lacking. Previous research on handuse in Japanese macaques (Macaca fuscata) showed some cases ofindividual manual preferences but no signiﬁcant group-level
lateralization for simple food reaching, foraging, or grooming
behaviors (Tokuda, 1969; Watanabe and Kawai, 1993; Takeda,
1994). However, some form of group-level lateralization appearedas the task increased in complexity, such as when carrying handfulsof wheat grains or when catching sweet potatoes in midair (Kawai,
1967; Watanabe and Kawai, 1993). Recently, Leca et al. (2008a)found marked individual hand preferences for spontaneous stone
throwing in a group of captive Japanese macaques but no consistentlateral bias across all throwers.
In this study, we present the ﬁrst analysis of manual laterality ina form of object playdstone handling (SH) behaviordin a freeranging group of Japanese macaques. SH is the longest studied andbest-documented cultural behavior in monkeys to date (Huffman,
1984, 1996; Huffman and Hirata, 2003; Leca et al., 2007a,b, 2008b,c;Nahallage and Huffman, 2007a,b). SH is a form of object play consisting of various non-instrumental stone-directed behavioral
patterns (Huffman, 1984), as illustrated in the following examples.
Some of the SH patterns are simple and unimanual, such as grabbing a stone in one hand and cradling it against the chest, orPlease cite this article in press as: Leca, J.-B., et al., Principles and levels of laterality in unimanual and bimanual stone handling patterns by
Japanese macaques, J Hum Evol (2009), doi:10.1016/j.jhevol.2009.09.005

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J.-B. Leca et al. / Journal of Human Evolution xxx (2009) 1–11

clutching with one hand a small pile of stones gathered and placing
the pile in front of oneself. Others are more complex in terms ofsequential-movement skills needed to ﬁnely control hand muscles
and may require asymmetric but coordinated bimanual hand use
with manual role differentiation, such as picking up a set of stones
with one hand and placing it into the other hand, or holding a stone
with one hand and rubbing it with the other (Leca et al., 2007a,b).
Therefore, SH behavior, deﬁned as an object manipulative behavior
comprised of multiple behavioral variants also called SH patterns, isa good candidate for the study of manual laterality.
Our main objective was to evaluate the principles of laterality inthe performance of SH behavior by documenting the presence,
strength, and direction of manual preference in SH behavior and invarious SH patterns, both at the individual level and group level. We
adapted the terminology used by McGrew and Marchant (1997) tothe particular case of SH. Thus, we deﬁned: 1) hand preference as
when an individual showed a signiﬁcant lateral bias on a single SH
pattern; 2) hand specialization as when an individual showeda signiﬁcant lateral bias across all SH patterns performed (i.e., theSH behavior as whole) or at least a range of SH patterns; 3) patternspecialization as when all (or at least a majority of) group members
showed a collective signiﬁcant lateral bias on a single SH pattern;
and 4) handedness as when all (or at least a majority of) groupmembers showed a collective signiﬁcant lateral bias across all SH
patterns performed (i.e., the SH behavior as whole) or at least
a range of SH patterns (see Table 1).
On the basis of the task-complexity model, and if we consider
that coordinated bimanual SH patterns are more complex than
one-handed patterns, then hand specialization, pattern specialization, and handedness should be stronger in the former than in thelatter (Prediction #1a, #1b, and #1c, respectively). In other words,
the strength of manual laterality, deﬁned as the absolute value of anindividual’s deviation from a random 50% hand usage, should besigniﬁcantly higher in all coordinated bimanual patterns than in all
unimanual patterns (Prediction #1a). We also predict that the
proportion of group members showing a signiﬁcant lateral bias on
any coordinated bimanual pattern should be higher than that on
any unimanual pattern (Prediction #1b). Finally, if any handedness(i.e., a group-level signiﬁcant lateral bias) should emerge acrosssome ranges of SH patterns, it should be higher in coordinatedbimanual patterns than in unimanual patterns (Prediction #1c).
However, since SH is not stone tool use, no signiﬁcant lateral bias
should emerge at the group level and across all SH patterns (i.e., nohandedness for the SH behavior as a whole is expected [Prediction#2]). If these predictions are conﬁrmed, our study will provide
further support for the ‘‘task-complexity’’ hypothesis and will add
to the arguments about the discrepancy between noninstrumental
object manipulation and tool use in the evolution of manual
preference.
Besides behavioral complexity, we also aimed to examine therelationship of hand preference to other major and most relevant
variables, such as the age, sex, and body posture of subjects, and totest the heritability of hand preference. We considered theremaining potentially inﬂuential variables either minor (e.g.,
emotional state, positioning) or irrelevant to SH (novelty of the
behavior, procedural conditions, habitat; Leca et al., 2007b, 2008b).
Materials and methods
Study group and data collection
We studied a free-ranging provisioned troop of Japanesemacaques (Arashiyama E troop) at the Iwatayama Monkey Park,
Arashiyama, Kyoto Prefecture. The group comprised 141 members,
among which 132 were sampled for SH behavior. Individual3

identities, exact age, and matrilineal membership were known for
all subjects. The study subjects could be approached and observed
within 3–5 m. None of the sampled individuals sustained obvious
hand injuries. From April 30 to August 28, 2004, between 08:00 and
17:00, JBL collected a total of 160.6 hours of continuous videorecorded focal-animal samples (Altmann, 1974). We selected focal
individuals by using a semi-random procedure: the focal target waschosen independently of its activity, and the subject with least
cumulative data was given priority. Whenever possible, they were
ﬁlmed from the front, within an area of 1 m2 (for details, see Lecaet al., 2007a).
Data analysis
We distinguished between two major categories of SH patterns,
namely the patterns performed unimanually, with only one hand
involved in a SH action while the other hand is either idle orinvolved in another activity (e.g., foraging, locomotion, or postural
support), and the patterns performed bimanually, with both hands
involved in SH activity (Table 2). Among the patterns performed
bimanually, we considered four categories (after McGrew andMarchant, 1997): 1) Sim-Id: both hands operate simultaneously andidentically on the same (set of) stone(s), e.g., rubbing the same stone
on a surface with both hands or using both hands to gather a pile ofstones in front of oneself; 2) Alt-Id: both hands operate alternately
but identically on the same (set of) stone(s), e.g., rubbing two stones
together with one stone in each hand; 3) Sim-Comp: both hands
operate simultaneously but complementarily on the same (set of)stone(s) with one hand (termed dominant hand) performing theﬁner, more skilful component, often a precision grip and the mostprecise movements of the ﬁngers, while the other hand (termed
subordinate hand) has a supportive role and is doing the more gross,less skilled component that involves less differentiation and accuracy of the ﬁngers, often with some form of power grip; there were
three Sim-Comp patterns: pick up with the dominant hand that picks
the stone from the ground and places it into the subordinate handthat receives it; ﬂint with the dominant hand that strikes a stone
against another held stationary in the subordinate hand; and rub
with hand with the dominant hand that rubs a stone held in thesubordinate hand; and 4) Sim-Diff: both hands operate simultaneously but perform different patterns on different (sets of) stones,e.g., one hand performing grasp with hand and the other cuddle.
For Sim-Id and Alt-Id patterns, no manual laterality is possible.
The Sim-Diff patterns were discarded from the analyses. Only
unimanual and Sim-Comp patterns were considered in the analysis
of manual laterality. The unimanual patterns were coded according to the hand useddnamely left or rightdto handle the stone(s).
The Sim-Comp patterns were coded according to the dominanthand. From all the video-recorded samples, NG scored a total of
13.7 hours of SH video-records onto an Excel spreadsheet, coding
to the second: 1) the SH pattern performed by the focal individual,
2) the (predominant) hand used, and the posture adopted by thestone handler (sitting, quadrupedal, bipedal, or lying). We
assessed intra-coder reliability for NG by measuring consistency intranscribing the same samples of SH video-records on two separate occasions and on a total of 146 data points (k ¼ 0.96; Martin
and Bateson, 1993).
For the analyses on the SH patterns performed unimanually, 83
individuals were taken into account. For the analyses on Sim-Comp
patterns, 31 individuals were considered. We categorized individuals according to seven age classes: Yrg ¼ yearling (1 yr),
Juv ¼ juvenile (2–3 yrs), SuAd ¼ subadult (4–6 yrs), YgAd ¼ young
adult (7–10 yrs), MdAd ¼ middle-aged adult (11–15 yrs), OlAd ¼ oldadult (16–20 yrs), Sen ¼ senescent (21 yrs and more; cf. Leca et al.,2007b).

Please cite this article in press as: Leca, J.-B., et al., Principles and levels of laterality in unimanual and bimanual stone handling patterns by
Japanese macaques, J Hum Evol (2009), doi:10.1016/j.jhevol.2009.09.005

ARTICLE IN PRESS
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4J.-B. Leca et al. / Journal of Human Evolution xxx (2009) 1–11

Table 2
List and deﬁnition of the 28 SH patterns sampled in the study group, with their categories, depending on whether they were performed unimanually (Uni) or bimanually
Name (code)

Deﬁnition

Categorya

Bite (B)
Carry (CA)Combine with object (COO)
Cuddle (CD)
Flint (FL)
Flip (FP)Gather (GA)
Grasp walk (GW)
Grasp with hands (GH)Hold (H)
Lick (L)Move and push/pull (MP)Move inside mouth (MIM)
Pick (P)Pick up (PU)
Pick up small stones (PUS)
Pound on surface (POS)
Put in mouth (PIM)
Roll in hands (RIH)
Roll on surface (ROS)
Rub on surface (RUS)
Rub stones together (RT)
Rub with hands (RWH)
Scatter (SC)
Sniff (SN)
Swipe (SW)Toss walk (TW)
Wash (W)

Bite a stone
Carry a stone cuddled in hand from one place to anotherCombine (mainly grasp or gather) a stone with an object different from a stone (mainly food item)
Take hold of, grab or cradle a stone against the chest
Strike a stone against another held stationary
Turn a stone over with both hands
Gather stones into a pile in front of oneself
Walk with one or more stones in the palm of one or both hands
Clutch a stone or a pile of stones gathered and placed in front of oneself
Pick up a stone in one’s hand and hold on to it, away from the body
Lick a stone held in one’s hand
Push/pull a stone with one or both hands while walking forward/backward
Make a stone move inside one’s mouth with hands
Pick up a stone
Pick up a stone and place it into one’s hand
Pick up small stones and hold them between ﬁngertips (like the picking up of wheat grains)
Pound a stone on a substrate
Put a stone in one’s mouth and keep it some time
Roll a stone in one’s hands
Roll a stone on a substrate
Rub a stone on a substrate
Rub stones together
Hold a stone in one hand and rub it with the other (like potato-washing)
Scatter stones about, on a substrate, in front of oneself
Sniff a stone held in one’s hand
Swipe stones together (both hands moving in a sweeping gesture)
Toss a stone ahead (repeatedly) and pick it up while walking
Put a stone in water or pick up a stone from water and rub it with hands

Uni or Sim-Diff
Uni or Sim-Diff
Uni or Sim-Diff
Uni or Sim-Diff
Sim-Comp
Alt-IdUni, Sim-Id, or Sim-Diff
Uni, Alt-Id, or Sim-Diff
Uni or Sim-Diff
Uni or Sim-Diff
Uni or Sim-Diff
Uni or Sim-Id
Uni, Sim-Id, or Sim-Diff
Uni or Sim-Diff
Sim-Comp
Uni or Sim-Diff
Uni or Sim-Diff
Uni or Sim-Diff
Alt-IdUni, Sim-Id, or Sim-Diff
Uni, Sim-Id, or Sim-Diff
Alt-IdSim-Comp
Uni or Sim-Diff
Uni or Sim-Diff
Alt-IdUni or Sim-Diff
Sim-IdaSim-Id: both hands operate simultaneously and identically on the same (set of) stone(s); Alt-Id: both hands operate alternately but identically on the same (set of) stone(s);Sim-Comp: both hands operate simultaneously but complementarily on the same (set of) stone(s) with manual role differentiation; Sim-Diff: both hands operate simultaneously but perform different patterns on different (sets of) stones.

We conformed to the methodological list of criteria by McGrew
and Marchant (1997): 1) we speciﬁed the age and species of thesubjects, 2) we sampled at least six subjects to allow binomial
testing of distribution of individuals in the group, 3) we recorded atleast six data points per subject to allow each subject to be categorized as lateralized by binomial test (two-tailed, p < .05), 4) we
presented raw data on manual preference to allow each subject to
be classiﬁed as AL (Always Left-preferent: uses left hand in 100% ofcases), SL (Signiﬁcantly Left-preferent: uses left hand signiﬁcantly
more often than right hand), A (Ambi-preferent: ratio of left to righthand usages does not differ from 50:50 or random), SR (Signiﬁcantly
Right-preferent: uses right hand signiﬁcantly more than left hand),or AR (Always Right-preferent: uses right hand in 100% of cases),and 5) we provided speciﬁcally-deﬁned behavioral categories (i.e.,
discrete SH patterns; cf. Table 2). Finally, we established the independence of behavioral data points (referred to as SH events, anddeﬁned as the occurrence of an individual hand use event must notbias the chances of the occurrence of another equivalent event, if
each is to be counted as a separate data point) when a different SH
pattern performed by the same hand intervened between two
instances of the same pattern (cf. McGrew and Marchant, 1997).
To express an individual’s direction of manual laterality, we used
the percentage of right-hand use, deﬁned as (R  100)/(R þ L) (e.g.,
Fagot and Vauclair, 1991). To calculate the strength of manual laterality, regardless of the direction, we took the absolute value of anindividual’s deviation from a random 50% hand usage, i.e.,
jdirection-50j (e.g., Corp and Byrne, 2004).
To investigate hand preference at the group level, we used
McGrew and Marchant’s (1997:216) classiﬁcation of ‘‘levels of laterality.’’ According to this classiﬁcation, a population of individuals
can be categorized as one of ﬁve levels: Level 1 is deﬁned as ‘‘when
the majority of individuals are ambi-preferent and the minority of
individuals are lateralized to either side to varying degrees’’; Level 2
is deﬁned as ‘‘when most of the subjects are signiﬁcantly but

incompletely (not 100%) lateralized, but their collective distribution
to left versus right does not depart from randomness’’; Level 3 isdeﬁned as ‘‘when most subjects use only one hand for a task, but
their distribution to left vs. right remains random’’; Level 4 isdeﬁned as ‘‘when the majority of individuals are signiﬁcantly but
incompletely lateralized, and when their distribution is signiﬁcantly skewed to the left, or the right’’; Level 5 is deﬁned as ‘‘when
the majority of individuals are completely lateralized, and when
their distribution is signiﬁcantly skewed to the left or the right.’’
In most analyses, we reported mean values  the standard
deviation (SD). To test the effect of posture on manual laterality, weused Wilcoxon tests to compare the direction and strength of handpreference when performing SH in a sitting versus a quadrupedal
posture. For this analysis, we considered only the SH patterns
performed unimanually and we discarded the individuals that did
not provide the required minimum number of six data points ineach posture. There were too few data to test a possible effect of thebipedal and lying postures on manual laterality. Regarding correlation tests, we used Spearman rank-order coefﬁcients when n < 30
and Pearson product-moment coefﬁcients when n was equal to or
more than 30 (Siegel and Castellan, 1988). Statistical analyses were
performed using the SPSS 12.0 analytical program. Signiﬁcancelevels were set at a ¼ 0.05.
Results
Lateral bias within subject and pattern: hand preference
Table 3 shows the hand preferences (labelled as AL, SL, A, SR,
and AR) of 70 individuals and for the 15 most frequent SH
patterns. To appear in the table, an individual should havea minimum of 6 data points for at least one SH pattern, and a SH
pattern should have been performed at least 6 times by one
individual or more. Of the 1050 generated cells, 873 had fewer

Please cite this article in press as: Leca, J.-B., et al., Principles and levels of laterality in unimanual and bimanual stone handling patterns by
Japanese macaques, J Hum Evol (2009), doi:10.1016/j.jhevol.2009.09.005

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J.-B. Leca et al. / Journal of Human Evolution xxx (2009) 1–11

5

Table 3
Hand preferences of 70 individuals (females and males ranked by descending age) for the 15 most frequent SH patternsa
Subject

Age class

Sex

Bl1
Bl2
Me1
Co2
Gl1
Bl3
Ku1
Mi1
Ai1
Op1
Bl4
Cho1
Ko1
Cho2
Ko2
Op2
Co3
Me2
Gl2
Mi2
Yun1
Bl5
Cho3
Ku2
Co4
Ku3
Co5
Gl3
Ra1
Ai2
Ko4
Mi3
Yun2
Cho4
Ra2
Cho5
Cho6
Me3
Ai3
Bl7
Gl4
Ku4
Me4
Shi1
Yun3
Yun4
Op3
Yun5
Ku5
Mi6
Mo1
Ai4
Gl5
Cho8
Ku6
Me5
Ra3
Shy1
Ai5
Co7
Co8
Yun6
Cho9
Cho10
Co9
Co10
Co11
Mi7
Shi2
Yun7

Sen
Sen
Sen
Sen
Sen
Sen
Sen
Sen
Sen
Sen
OlAd
OlAd
OlAd
OlAd
OlAd
OlAd
OlAd
OlAd
OlAd
OlAd
OlAd
OlAd
OlAd
OlAd
MdAd
MdAd
MdAd
MdAd
MdAd
MdAd
MdAd
MdAd
MdAd
MdAd
MdAd
YgAd
YgAd
YgAd
YgAd
YgAd
YgAd
YgAd
YgAd
YgAd
YgAd
YgAd
YgAd
YgAd
SuAd
SuAd
SuAd
SuAd
SuAd
Juv
Juv
Juv
Juv
Juv
Juv
Juv
Juv
Juv
Yrg
Yrg
Yrg
Yrg
Yrg
Yrg
Yrg
Yrg

F
M
F
F
M
F
F
F
F
M
M
F
F
F
F
M
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
M
M
F
F
F
F
F
M
F
F
F
F
M
F
F
F
M
M
F
F
F
F
F
F
M
M
M
M
F
F
M

SH pattern
CA

CD

COO

FL

GA

GH

GW

H

PU

PUS

ROS

RUS

RWH

SC

W

–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
AR
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
AR
–
–
–
–
–
–
–
–
–
–
AR
–
–
–
A
–
A
–
SL
–
–
A
A
SL

–
–
–
–
–
–
A
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
SR
–
–
–
–
–
AR
–
–
–
–
–
–
–
–
–
–
SR
–
–
–
–
–
A
–
A
–
A
–
A
SL

–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
A
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–

–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
AR
–
–
–
–
–
–
–
–

–
–
SR
–
–
–
–
–
A
A
A
–
A
–
–
–
–
A
–
–
–
–
–
–
–
A
A
SR
–
–
A
–
–
–
–
A
–
–
SL
–
–
–
–
SR
A
–
–
–
–
AR
–
A
–
–
–
A
–
–
–
–
–
–
–
–
–
–
–
–
–
A

SR
SL
SR
A
AL
AL
A
A
SR
A
AL
AL
SL
A
A
A
A
A
A
A
A
–
A
A
A
A
A
SR
A
A
–
A
A
A
A
A
A
A
A
–
A
–
A
SR
A
A
–
A
SR
AR
A
SR
A
–
–
A
A
–
A
A
–
A
–
–
A
A
A
A
A
A

–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
A
–
A
–
–
A
–
–
–
–
–
A
A
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
SR
–
–
–
SR
–
–
–
–
–
A
A
SR
A
A
A
A
–
A
A
–
A
A
A
A
A

–
–
–
–
–
–
A
–
–
–
–
–
–
–
–
AR
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
A
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
A
–
–
–

–
–
–
–
–
–
A
–
SR
–
–
–
–
AR
A
AL
–
–
–
–
–
–
–
SL
–
–
–
–
AL
–
–
A
SR
AR
A
–
–
–
–
–
AR
AR
–
–
–
AL
–
AR
–
–
–
–
–
AR
–
SR
AL
–
A
–
–
A
–
–
–
–
–
–
A
SR

–
–
–
–
–
AL
–
–
A
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–

–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
AR
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–

–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
A
–
–
–
–
–
–
–
–
–
–
A
–
–
–
–
–
–
–
–
–
A

–
–
–
SR
–
–
AR
–
–
–
–
–
–
–
–
A
–
–
AR
–
–
–
–
AL
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
A
–
–
–
–
SR

SR
–
–
A
AL
–
–
–
–
AL
A
–
A
–
–
AL
–
–
AR
–
–
–
–
–
–
–
A
A
–
–
–
–
–
–
–
A
–
–
–
–
–
–
–
AR
A
–
AL
–
–
–
–
–
–
–
–
A
–
–
–
–
–
–
–
–
–
–
–
–
–
A

–
–
–
–
–
–
–
–
–
–
AL
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
SR
–
–
–
–
SL
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
A
–
–
–
–
–
–
–
–
–
–

a
Each cell was assigned one of six outcomes: –, fewer than six data points (ignored since no valid statistical testing can be done); A, ambi-preference; SL, signiﬁcant left
preference; SR, signiﬁcant right preference; AL, systematic left preference; and AR, systematic right preference.

Please cite this article in press as: Leca, J.-B., et al., Principles and levels of laterality in unimanual and bimanual stone handling patterns by
Japanese macaques, J Hum Evol (2009), doi:10.1016/j.jhevol.2009.09.005

ARTICLE IN PRESS
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6

J.-B. Leca et al. / Journal of Human Evolution xxx (2009) 1–11

Table 4
Distribution of statistically signiﬁcantly (p < 0.05, two-tailed) lateralized individuals
for the 15 most frequent SH patterns (n ¼ 70 subjects)a
SH pattern

CA
CD
COO
FL
GA
GH
GW
H
PU
PUS
ROS
RUS
RWH
SC
W
Total

Manual laterality
AL

SL

A

SR

AR

0
0
0
0
0
4
0
0
4
1
0
0
1
4
1
15

2
1
0
0
1
2
0
0
1
0
0
0
0
0
1
8

4
5
1
0
13
45
18
3
7
1
0
3
2
9
1
112

0
2
0
0
3
7
3
0
4
0
0
0
2
1
1
23

3
1
0
1
1
1
0
1
6
0
1
0
2
2
0
19

Total

No. lat

% lat

9
9
1
1
18
59
21
4
22
2
1
3
7
16
4
177

5
4
0
1
5
14
3
1
15
1
1
0
5
7
3
65

55.6
44.4
0.0
100.0
27.8
23.7
14.3
25.0
68.2
50.0
100.0
0.0
71.4
43.8
75.0
36.7

a
No. lat ¼ number of signiﬁcantly lateralized individuals (AL þ SL þ SR þ AR); %lat ¼ percentage of signiﬁcantly lateralized individuals.

than 6 data points and so were ignored, since no valid statistical
testing could be done, and 177 cells could be statistically tested forhand preference. Among them, 112 cells indicated ambi-preference, 8 cells showed signiﬁcant left preference, 23 cells showedsigniﬁcant right preference, 15 cells showed systematic left preference, and 19 cells showed systematic right preference (Table 4).
Therefore, we found a total of 65 cases (36.7%) of hand preference
for particular SH patterns.
Lateral bias within subject and across patterns: hand specialization
SH behavior as a whole We analyzed the manual laterality of 84
individuals for all SH patterns (unimanual and Sim-Comp patternspooled together: n ¼ 3,740 SH events, mean ¼ 44.5  50.2 SH
events per individual, ranging from 6 to 312). We found that 18
individuals (45.0%) were signiﬁcantly biased toward the left hand(including 4 systematic left-preferent individuals), and 22 (55.0%)
toward the right hand (including 4 systematic right-preferent
individuals). Therefore, we recorded a total of 40 cases (47.6%) ofhand specialization for the SH behavior as a whole.
However, Table 3 shows that among the 14 individuals for which
statistical testing could be done in at least 4 patterns and with atleast one signiﬁcantly lateralized pattern (Ku1, Ai1, Bl4, Op2, Gl2,
Gl3, Cho5, Yun3, Yun4, Ku5, Me5, Ra3, Co9, and Yun7), none
exhibited a lateral bias in all these patterns. The 3 individuals
showing the highest number of lateralized outcomes (4 statistical
departures from 50 L:50 R) had mixed results, that is for none ofthem the lateral bias was toward the same side (Op2 was AL for 2
patterns and AR for 2 patterns, Yun7 was SL for 2 patterns and SR
for 2 patterns, and Ra3 was AL for one pattern, SR for 2 patterns, andAR for one pattern). Therefore, the type of SH pattern appeared toaffect the strength and direction of manual laterality in individuals.
Unimanual versus bimanual complementary SH patterns In the
30 testable individuals (subject Bl4 had too few data points for any
single Sim-Comp pattern), we compared the strength of manual
laterality in all unimanual patterns and in all Sim-Comp patterns.
We found that the latter was signiﬁcantly higher than the former(Wilcoxon signed rank test, n ¼ 30, z ¼ 3.363, p ¼ 0.001). This
result showed that hand specialization was stronger in coordinatedbimanual SH patterns than in unimanual patterns, thus verifying
Prediction #1a.

To determine whether each subject was consistent in its
lateral bias across unimanual SH patterns, we used Spearman
rank-order correlation tests between two SH patterns, using theindexes of direction and strength of manual laterality. We
restricted the analyses to the individuals with statisticallysigniﬁcant lateral bias for at least one pattern and to pairs ofunimanual SH patterns showing structural similarities in theirsequences of actions.
We found no consistency in manual laterality, neither in direction nor in strength 1) between two SH patterns involved in locomotion activities (carry and grasp walk, n ¼ 6; for direction, rs¼ .794, p ¼ 0.059, two-tailed; for strength, rs ¼ 0.000, p ¼ 1.000,
two-tailed), 2) between two SH patterns involved in collection
activities (cuddle and grasp with hand, n ¼ 7; for direction, rs¼ 0.649, p ¼ 0.115, two-tailed; for strength, rs ¼ 0.216, p ¼ 0.641,
two-tailed), and 3) between two SH patterns consisting of moving
several stones on the ground simultaneously (gather and scatter,n ¼ 10; for direction, rs ¼ 0.579, p ¼ 0.091, two-tailed; for strength,
rs ¼ 0.531, p ¼ 0.114, two-tailed). For example, Ra3 switched fromalways right-hand preferent for carry to signiﬁcant left-handpreferent for grasp walk; Yun4 switched from always right-handpreferent for cuddle to ambi-preferent for grasp with hand; Op1
switched from always left-hand preferent for scatter to ambipreferent for gather.
Lateral bias across subjects and within pattern: patternspecialization
With the exception of combine with object (only one individualwith sufﬁcient data points), each of the 15 most frequent SH
patterns showed at least one signiﬁcantly lateralized subject (Table4). When the sample size was more than two individuals classiﬁed
as AL, SL, A, SR, or AR, the group could be categorized as Level 1 forseven SH patterns (namely CD-cuddle, GA-gather, GH-grasp withhand, GW-grasp walk, H-hold, RUS-rub on surface, and SC-scatter, allperformed unimanually), Level 2 for two SH patterns (CA-carry and
W-wash, both performed unimanually), and Level 3 for two
patterns (PU-pick up and RWH-rub with hand, both bimanualcomplementary patterns). We found no evidence for a majority of
individuals being signiﬁcantly lateralized with their distribution
signiﬁcantly skewed to one side (Level 4), nor being completely
lateralized with their distribution signiﬁcantly skewed to one side
(Level 5).
When considering the nine unimanual patterns, we found that
only seven out of the 49 individuals with at least 10 data points (i.e.,
12.2%) were systematically lateralized. For grasp with hand, three
individuals were always left-preferent (Bl3 with 14L:0R, Gl1 with
11L:0R, and Cho1 with 10L:0R) and one individual was always
right-preferent (with Mi6 0L:13R). For gather, one individual wasalways right-preferent (Mi6 with 0L: 13R). For scatter, one individual was always left-preferent (Op3 with 11L:0R). For carry, one
individual was always right-preferent (Ra3 with 0L:14R).
By contrast, when considering the three Sim-Comp patterns, wefound that 11 out of the 23 individuals with at least 10 data points(i.e., 47.8%) were systematically lateralized. For pick-up, four individuals were always left-preferent (Op2 with 70L:0R, Ra3 with
23L:0R, Yun4 with 16L:0R, and Ra1 with 10L:0R) and four individuals were always right-preferent (Cho4 with 0L:38R, Cho8 with
0L:17R, Cho2 with 0L:14R, and Yun5 with 0L:10R). For rub withhand, one individual was AL (Ku2 with 30L:0R) and one individual
was AR (Ku1 with 0L:95R). For ﬂint, one individual was AR (Yun6with 0L:22R).
In sum, most group members showed a collective signiﬁcantlateral bias on a single SH pattern and especially for Sim-Comp
patterns. We found evidence for pattern specialization, and thisPlease cite this article in press as: Leca, J.-B., et al., Principles and levels of laterality in unimanual and bimanual stone handling patterns by
Japanese macaques, J Hum Evol (2009), doi:10.1016/j.jhevol.2009.09.005

ARTICLE IN PRESS
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J.-B. Leca et al. / Journal of Human Evolution xxx (2009) 1–11

Subject

Age class

Sex

L

R

Direction

Strength

p

Lat.

Bl1
Bl2
Co1
Me1
Co2
Gl1
Bl3
Ku1
Mi1
Ai1
Op1
Bl4
Cho1
Ko1
Cho2
Ko2
Op2
Co3
Me2
Gl2
Mi2
Yun1
Bl5
Cho3
Ku2
Co4
Ku3*
Co5
Gl3
Ra1
Ai2
Bl6
Ko3
Ko4
Ko5
Mi3
Yun2
Cho4
Ra2
Cho5
Cho6
Me3
Mi4
Mi5
Ai3
Bl7
Gl4
Me4
Shi1
Yun3
Yun4
Op3
Yun5
Co6
Ko6
Ku5
Mi6
Cho7
Mo1
Ai4
Gl5
Ko7
Cho8
Ku6
Me5
Ra3
Shy1
Ai5
Co7
Co8
Ku7
Yun6

Sen
Sen
Sen
Sen
Sen
Sen
Sen
Sen
Sen
Sen
Sen
OlAd
OlAd
OlAd
OlAd
OlAd
OlAd
OlAd
OlAd
OlAd
OlAd
OlAd
OlAd
OlAd
OlAd
MdAd
MdAd
MdAd
MdAd
MdAd
MdAd
MdAd
MdAd
MdAd
MdAd
MdAd
MdAd
MdAd
MdAd
YgAd
YgAd
YgAd
YgAd
YgAd
YgAd
YgAd
YgAd
YgAd
YgAd
YgAd
YgAd
YgAd
YgAd
SuAd
SuAd
SuAd
SuAd
SuAd
SuAd
SuAd
SuAd
SuAd
Juv
Juv
Juv
Juv
Juv
Juv
Juv
Juv
Juv
Juv

F
M
F
F
F
M
F
F
F
F
M
M
F
F
F
F
M
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
M
M
F
F
F
F
M
F
M
M
F
F
F
F
M
F
F
F
F
M
M
F
F
F
F
F
F

20
13
0
6
18
23
28
26
9
20
21
46
14
4
13
7
39
11
43
15
6
9
12
5
8
3
13
23
19
17
5
4
3
26
6
8
13
11
4
60
28
4
2
8
39
3
3
11
9
146
11
16
14
7
4
27
0
3
12
6
6
20
7
6
51
18
8
24
22
9
2
10

77
1
6
33
5
0
2
30
0
49
8
23
0
3
7
0
82
5
23
32
12
6
5
2
10
12
13
6
59
31
17
2
6
8
2
12
7
15
13
43
7
7
8
2
9
14
8
4
43
166
30
7
3
1
20
73
41
3
13
15
12
23
1
16
47
84
7
26
27
15
4
6

79.4
7.1
100.0
84.6
21.7
0.0
6.7
53.6
0.0
71.0
27.6
33.3
0.0
42.9
35.0
0.0
67.8
31.3
34.8
68.1
66.7
40.0
29.4
28.6
55.6
80.0
50.0
20.7
75.6
64.6
77.3
33.3
66.7
23.5
25.0
60.0
35.0
57.7
76.5
41.7
20.0
63.6
80.0
20.0
18.8
82.4
72.7
26.7
82.7
53.2
73.2
30.4
17.6
12.5
83.3
73.0
100.0
50,0
52,0
71,4
66,7
53,5
12,5
72,7
48,0
82,4
46,7
52,0
55,1
62,5
66,7
37,5

29.4
42.9
50.0
34.6
28.3
50.0
43.3
3.6
50.0
21.0
22.4
16.7
50.0
7.1
15.0
50.0
17.8
18.8
15.2
18.1
16.7
10.0
20.6
21.4
5.6
30.0
0.0
29.3
25.6
14.6
27.3
16.7
16.7
26.5
25.0
10.0
15.0
7.7
26.5
8.3
30.0
13.6
30.0
30.0
31.3
32.4
22.7
23.3
32.7
3.2
23.2
19.6
32.4
37.5
33.3
23.0
50.0
0,0
2,0
21,4
16,7
3,5
37,5
22,7
2,0
32,4
3,3
2,0
5,1
12,5
16,7
12,5

<0.001
0.002
0.031<0.001
0.011<0.001<0.001
0.689
0.004
0.001
0.024
0.008
<0.001
1.000
0.263
0.016
<0.001
0.210
0.019
0.019
0.238
0.607
0.143
0.453
0.815
0.035
1.000
0.002
<0.001
0.059
0.017
0.688
0.508
0.003
0.289
0.503
0.263
0.557
0.049
0.114
0.001
0.549
0.109
0.109
<0.001
0,013
0,227
0.118
<0.001
0.282
0.004
0.093
0.013
0.070
0,002
<0,001<0,001
1,000
1,000
0,078
0,238
0,761
0,070
0,052
0,762
<0,001
1,000
0,888
0,568
0,307
0,688
0,454

SR
SL
AR
SR
SL
AL
SL
A
AL
SR
SL
SL
AL
A
A
AL
SR
A
SL
SR
A
A
A
A
A
SR
A
SL
SR
A
SR
A
A
SL
A
A
A
A
SR
A
SL
A
A
A
SL
SR
A
A
SR
A
SR
A
SL
A
SR
SR
AR
A
A
A
A
A
A
A
A
SR
A
A
A
A
A
A

Table 5 (continued)
Subject

Age class

Sex

Cho9
Cho10
Cho11
Co9
Co10
Co11
Mi7
Shi2
Yun7
Yun8
Yun9

Yrg
Yrg
Yrg
Yrg
Yrg
Yrg
Yrg
Yrg
Yrg
Yrg
Yrg

F
M
F
M
M
M
F
F
M
F
F

L
23
8
1
28
16
23
23
26
86
6
0

R

Direction

Strength

12
12
5
11
9
42
10
35
46
4
7

34.3
60.0
83.3
28.2
36.0
64.6
30.3
57.4
34.8
40.0
100.0

15.7
10.0
33.3
21.8
14.0
14.6
19.7
7.4
15.2
10.0
50.0

p

Lat.

0.090
0.503
0.219
0.009
0.230
0.025
0.035
0.306
0.001
0.754
0.016

A
A
A
SL
A
SR
SL
A
SL
A
AR

a
L ¼ number of SH events performed with the left hand, R ¼ number of SH events
performed with the right hand, Direction ¼ direction of hand preference,Strength ¼ strength of hand preference, p ¼ probability obtained from binomial test
(two-tailed), Lat. ¼ manual laterality (A: ambi-preferent, SL: signiﬁcant left-preferent, SR: signiﬁcant right-preferent, AL: systematic left-preferent, and AR: systematic
right-preferent). * denotes subject with cleft hands (cf. text for detail).

principle of laterality was stronger in coordinated bimanual SH
patterns than in unimanual patterns, thereby conﬁrming Prediction#1b.
Lateral bias across subjects and patterns: handedness
First, we considered unimanual and Sim-Comp patterns separately. Table 5 shows the manual lateralization of 83 individuals for
the SH patterns performed unimanually. Since there were still moreambi-preferent individuals (n ¼ 46, i.e., 56.4%) than signiﬁcantly
lateralized individuals (n ¼ 37, i.e., 44.6%), the study group was also
categorized as Level 1 for unimanual SH patterns. The average
direction of manual laterality was 49.2  25.7 (ranging from 0.0 to
100.0) and the average strength of manual laterality was 21.8  13.4
(ranging from 0.0 to 50.0). Among individuals showing a statistically signiﬁcant preference for one hand, 18 (48.6%) were biased
toward the left hand and 19 (51.4%) toward the right hand. Manual
laterality was normally distributed, with a maximum number ofambi-preferent individuals and a minimum number of systematically biased individuals: 4.8% of individuals were AL, 16.9% were SL,
55.4% were A, 19.3% were SR, and 3.6% were AR (Fig. 1). It should be
noted that three out of the 69 individuals with at least 10 data
points (i.e., 4.3%) were systematically lateralized: Mi6 with 0L:41R,
Gl1 with 23L:0R, and Cho1 with 14L:0R.
However, a subanalysis on bimanual complementary SH
patterns revealed a slightly different picture of the manual laterality at the group level. Table 6 shows the manual lateralization of
31 individuals for Sim-Comp patterns. Contrary to the results on all
SH patterns and unimanual SH patterns, there were more

50

No. indivividuals

Table 5Manual lateralization of 83 individuals (females and males ranked by descendingage) for SH patterns performed unimanually.a7

45

Unimanual patterns

40

Sim-Comp patterns

35
30
25
20
15
10
5
0
AL

SL

A

SR

AR

Manual laterality
Fig. 1. Distribution of manual laterality across individuals and in two types of SH
patterns: unimanual patterns and coordinated bimanual patterns (Sim-Comp).

Please cite this article in press as: Leca, J.-B., et al., Principles and levels of laterality in unimanual and bimanual stone handling patterns by
Japanese macaques, J Hum Evol (2009), doi:10.1016/j.jhevol.2009.09.005

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J.-B. Leca et al. / Journal of Human Evolution xxx (2009) 1–11

Table 6Manual lateralization of 31 individuals (females and males ranked by descendingage) for Sim-Comp SH patterns.a
Subject

Age class

Sex

L

R

Direction

Strength

p

Lat.

Co2
Ku1
Ai1
Bl4
Cho2
Ko2
Op2
Gl2
Ku2
Co4
Ra1
Mi3
Yun2
Cho4
Ra2
Cho6
Gl4
Ku4
Yun4
Yun5
Ku5
Cho8
Me5
Ra3
Ai5
Yun6
Cho9
Co9
Co10
Shi2
Yun7

Sen
Sen
Sen
OlAd
OlAd
OlAd
OlAd
OlAd
OlAd
MdAd
MdAd
MdAd
MdAd
MdAd
MdAd
YgAd
YgAd
YgAd
YgAd
YgAd
SuAd
Juv
Juv
Juv
Juv
Juv
Yrg
Yrg
Yrg
Yrg
Yrg

F
F
F
M
F
F
M
F
F
F
F
F
F
F
F
F
M
F
F
F
F
F
M
M
F
F
F
M
M
F
M

1
5
2
4
0
7
77
0
49
5
10
6
2
1
9
3
0
0
16
0
4
0
4
24
5
3
2
7
3
12
23

27
102
36
3
14
1
2
8
4
1
0
1
26
42
12
3
6
6
0
10
2
18
16
0
2
31
5
5
6
6
52

96.4
95.3
94.7
42.9
100.0
12.5
2.5
100.0
7.5
16.7
0.0
14.3
92.9
97.7
57.1
50.0
100.0
100.0
0.0
100.0
33.3
100.0
80.0
0.0
28.6
91.2
71.4
41.7
66.7
33.3
69.3

46.4
45.3
44.7
7.1
50.0
37.5
47.5
50.0
42.5
33.3
50.0
35.7
42.9
47.7
7.1
0.0
50.0
50.0
50.0
50.0
16.7
50.0
30.0
50.0
21.4
41.2
21.4
8.3
16.7
16.7
19.3

<0.001<0.001<0.0011.000<0.0010.070<0.0010.008<0.001
0.219
0.002
0.125
<0.001<0.001
0.664
1.000
0.031
0.031
<0.001
0.002
0.688<0.001
0.012<0.0010.453<0.001
0.453
0.774
0.508
0.238
0.001

SR
SR
SR
A
AR
A
SL
AR
SL
A
AL
A
SR
SR
A
A
AR
AR
AL
AR
A
AR
SR
AL
A
SR
A
A
A
A
A

a

See Table 5 for legends.

signiﬁcantly lateralized individuals (n ¼ 18, i.e., 58.1%) than ambipreferent individuals (n ¼ 13, i.e., 41.9%). The average direction andstrength of manual laterality were stronger than for the SH patterns
performed unimanually: 57.9  38.1 (ranging from 0.0 to 100.0) and34.8  16.3 (ranging from 0.0 to 50.0), respectively. Among individuals showing a statistically signiﬁcant preference for one hand,ﬁve (27.8%) were biased toward the left hand and 13 (72.2%) toward
the right hand. Manual lateralization was still normally distributed,
but with a higher proportion of lateralized individuals than for theSH patterns performed unimanually, and slightly skewed to theright: 9.7% of individuals were AL, 6.4% were SL, 41.9% were A, 22.6%
were SR, and 19.4% were AR (Fig. 1). In sum, we found that handedness was stronger in coordinated bimanual SH patterns than in
unimanual patterns, thus verifying Prediction #1c.
When considering all SH patterns (unimanual and Sim-Comp
patterns pooled together), the study group showed a majority ofambi-preferent individuals (44 out of 84, i.e., 52.4%). It was categorized as Level 1 (i.e., unlateralized) for the SH behavior, according to
McGrew and Marchant’s (1997) classiﬁcation of ‘‘levels of laterality.’’
The average direction of manual laterality was 51.9  25.5 (ranging
from 0.0 to 100.0), and the average strength of manual laterality was
21.1 14.3 (ranging from 0.0 to 50.0). We found no handedness for SH
behavior as a whole, thus verifying Prediction #2.
Finally, when pooling only the signiﬁcantly lateralized individuals across the 15 SH patterns, we found a signiﬁcant bias toward theright hand (Binomial test, n ¼ 62, 20 L:42 R, p ¼ 0.007, two-tailed).
However, this overall effect could not be found on a SH pattern basis.

*

60
Average strength of manual laterality

8

*
50
40
30
20
10
0
Yrg

Juv

SuAd

YgAd

MdAd

OlAd

Sen

Age classes

Fig. 2. Effect of age on the strength of manual laterality. Yrg ¼ yearling (1 yr, n ¼ 11),Juv ¼ juvenile (2–3 yrs, n ¼ 10), SuAd ¼ subadult (4–6 yrs, n ¼ 9), YgAd ¼ young adult(7–10 yrs, n ¼ 15), MdAd ¼ middle-aged adult (11–15 yrs, n ¼ 14), OlAd ¼ old adult(16–20 yrs, n ¼ 14), Sen ¼ senescent (21 yrs and more, n ¼ 11). The lines at the top
indicate the two sets of paired comparisons (between age classes) that were signiﬁcant* p < 0.05; see text.

p ¼ 0.003). The analysis based on age classes conﬁrmed the overall
effect of age on the strength of lateralization (Kruskal-Wallis test,
df ¼ 6, c2 ¼ 16.1, p ¼ 0.013), and post-hoc paired comparisons
between age classes showed that senescent individuals weresigniﬁcantly more lateralized than yearlings and juveniles (p < 0.05;
Fig. 2). Other paired comparisons between age classes were notsigniﬁcant (p > 0.05).
Interestingly, we found: 1) a signiﬁcant negative correlation
between age and SH pattern diversity, deﬁned as the total number ofSH patterns observed in each individual (Pearson correlation test,n ¼ 84, r ¼ 0.229, p ¼ 0.036) and a signiﬁcant negative correlation
between SH pattern diversity and the strength of manual laterality(Pearson correlation test, n ¼ 84, r ¼ 0.304, p ¼ 0.004). Therefore,
extrapolating from the cross-sectional data, it appeared that asindividuals became older, they tended to perform a smaller range ofSH patterns and to become more lateralized for object manipulation.
We found no signiﬁcant effect of age on the direction of manual
laterality (Pearson correlation test, n ¼ 84, r ¼ 0.188, p ¼ 0.087;
Kruskal-Wallis test, df ¼ 6, c2 ¼ 7.5, p ¼ 0.277) and no signiﬁcantsex differences in the direction and strength of manual laterality(Mann-Whitney U tests, nfemale ¼ 66, nmale ¼ 18, direction:
U ¼ 443.5, p ¼ 0.101, strength: U ¼ 564.0, p ¼ 0.743).
Heritability of manual preference
To test the heritability of manual preference, we compared the
12 mother/offspring pairs that showed a statistically signiﬁcant
preference for one hand in all unimanual and Sim-Comp patterns. In
four pairs the manual preference was the same, and in eight pairs it
was opposite. Thus, there was no signiﬁcant concordance in laterality between mother and offspring (Binomial test, n ¼ 12,
p ¼ 0.388, two-tailed). We found the same negative result whencomparing the 6 mother/offspring pairs that showed a statisticallysigniﬁcant preference for one hand in at least one SH pattern. In
two pairs the manual preference was the same (Cho4/Cho8 with
0L:38R/0L:17R for pick up, and Yun2/Yun5 with 2L:22R/0L:10R for
pick up), and in four pairs it was opposite (Binomial test, n ¼ 6,
p ¼ 0.688, two-tailed). In the Ku1/Ku2 pair, the mother was always
right-preferent for rub with hand (0L:95R) where her daughter wasalways left-preferent for the same pattern (30L:0R).

Age, sex, and diversity in SH patterns
Body posture and a case of manual disability
When pooling unimanual and Sim-Comp patterns, we founda signiﬁcant positive correlation between age and the strength ofmanual laterality (Pearson correlation test, n ¼ 84, r ¼ 0.316,

We found no signiﬁcant effect of the posture of the stone
handler (sitting versus quadrupedal) neither in the direction nor in

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the strength of manual laterality (Wilcoxon test, n ¼ 32, direction:z ¼ 1.481, p ¼ 0.139; strength: z ¼ 0.584, p ¼ 0.559). Table 5shows that among the 69 individuals with at least 10 data points in
the SH patterns performed unimanually, Ku3 was the only one
exhibiting exactly the same number of left-hand and right-handusages (13L:13R). It should be noted that Ku3 was the only groupmember with a congenital hand malformation characterized by ananomaly in the digit morphology: she had cleft hands with only
two ﬁngers on each hand (cf. Homma, 1980 for further description).
Discussion
We evaluated the principles of laterality in the performance ofSH behavior in a troop of free-ranging Japanese macaques. For
individual subjects, we found evidence for manual lateral bias
within particular SH patterns (hand preference) and consistency inlaterality across SH patterns (hand specialization). At the grouplevel, we found evidence for manual lateral bias at Level 2 and Level
3 within particular SH patterns (pattern specialization) but not
across all SH patterns (no handedness for the SH behavior asa whole). As predicted by the task-complexity model, the type of SH
pattern signiﬁcantly affected the strength and direction of manual
laterality in individuals, since hand specialization and handedness
were stronger in the coordinated bimanual SH patterns than in theunimanual patterns. Our data allowed us to ﬁll the four cells of the2  2 matrix generated from the principles of laterality within andacross free-ranging Japanese macaque subjects, and within andacross various SH patterns (Table 1).
Complementary analyses on the factors that may inﬂuence handlateralization in the performance of SH showed that as individuals
became older, they tended to perform a smaller range of SH
patterns and to become more lateralized in their stone-directed
manipulative actions. We found no effect of age on the direction ofmanual laterality. Manual laterality was not signiﬁcantly affectedby sex and body posture (sitting versus standing quadrupedally).
Finally, we found no evidence for heritability of hand preference inthe performance of SH.
Our results on the principles of laterality are consistent withmost studies in nonhuman primates that often showed handpreference and task specialization (referred to as ‘‘pattern specialization’’ in the case of SH), sometimes hand specialization, and only
very occasionally handedness (cf. McGrew and Marchant, 1997 fora review). Within-individual consistency in laterality across several
behavioral measures, including simple and complex tasks, has beenfound in chimpanzees (Sugiyama et al., 1993; Colell et al., 1995).
However, individuals do not always show consistent lateral biases
across multiple complex tasks (Anderson et al., 1996; Spinozzi and
Truppa, 1999; Lilak and Phillips, 2008).
Likewise, our results on the levels of laterality are consistent
with the general pattern found in prosimians, monkeys, and apes.
At the group level, most nonhuman primate species were either
unlateralized (Level 1) or showed Level 2 laterality. The results
showing Level 3 and Level 4 laterality were often associated withpostural readjustments or complex motor tasks, whereas no clear
cases of true handedness (Level 5) were reported (McGrew andMarchant, 1997; but see Byrne and Byrne, 1991).
We found that some SH patterns elicited more lateralization
than others. More particularly, coordinated bimanual SH patterns
performed by the Arashiyama E troop members gave rise tosigniﬁcant manual preferences at the group level. This result
further supports the ‘‘task-complexity’’ hypothesis proposing thatlateralization increases with the complexity of the task (Fagot andVauclair, 1991). When considering coordinated bimanual SH
patterns, we found that the distribution of manual lateralization
across all group members was slightly skewed to the right hand.

9This ﬁnding is in agreement with the postural origins theory that
postulates, for nonhuman primates, a group-level right-handpreference for more complex tasks that require bimanual actions(MacNeilage et al., 1987). In the genus Macaca, strong evidence fora right-hand bias for complex tasks at the group level was found instump-tailed macaques, M. arctoides (Beck and Barton, 1972) and in
pig-tailed macaques, M. nemestrina (Rigamonti et al., 1998). Suchﬁndings suggest that manual laterality is labile and may emerge
only when the task demand is sufﬁciently high to involve motorand cognitive abilities that are speciﬁc to one hemisphere (Anderson et al., 1996).
The lack of signiﬁcant lateral bias at the group level and for SH
behavior as a whole is consistent with the view that populationlevel manual preference is less likely to emerge for non-instrumental object manipulation than for tool use (cf. Marchant and
McGrew, 2007; see also Westergaard and Suomi, 1996; Westergaard et al., 1998a). SH is typically deﬁned as a form of object playand, with the notable exception of stone-throwing, the 45 SH
patterns listed in the repertoire of Japanese macaques do not seemto serve any immediate function (Huffman, 1984; Leca et al., 2007a,
2008a; but see Nahallage and Huffman [2007a] for a possible
ultimate function of SH). Even the stone-throwing pattern, that
may serve to augment the effect of agonistic displays and can be
regarded as spontaneous tool use, did not show a group-level
lateral bias (Leca et al., 2008a).
Instead of cognitive and functional reasons, Corp and Byrne(2004) proposed that the temporal and spatial coordination of both
hands, with role-differentiated actions, may account for the strong
manual preference reported in tool use. If so, this argument would
also explain the increased lateralization observed in coordinatedbimanual SH patterns. Ethological analyses in humans also showedthat lateralization increases with the level of skill required for
manipulating objects, suggesting a marked distinction between
non-instrumental object manipulation and tool use in the evolution of manual preference. Marchant et al. (1995) found that inthree traditional societies, the most common non-tool use activities, including non-instrumental object manipulation, were unlateralized (Level 1 laterality), whereas gross tool use with power grip
and skilled tool use with precision grip were at Level 4 and 5,
respectively.
Given the gradual maturation of motor control during ontogeny,
age is one of the most signiﬁcant factors to be considered in relation
to manual laterality in nonhuman primates (cf. McGrew andMarchant, 1997 for a review; see Nahallage and Huffman [2007b]for ontogeny of SH motor development). The fact that older individuals became more lateralized for SH activity is consistent withprevious ﬁndings on Japanese macaques. In this species, adults
have greater strength of manual laterality than young individuals(Itani et al., 1963; Kubota, 1990; but see Takeda, 1994). Older infant
macaques even showed stronger hand preferences than younger
infants (Lehman, 1980). Most studies on the ontogeny of behavioral
laterality in humans and nonhuman primates show increased
lateralization with age (e.g., McManus et al., 1988; Bard et al., 1990;
Westergaard and Suomi, 1993b; Hopkins, 1995; Schaafsma et al.,2009; but see Boesch, 1991; McGrew and Marchant, 1992).
The lack of a sex effect on manual laterality is consistent withmost studies on nonhuman primates, including Japanese macaques(Itani et al., 1963; Tokuda, 1969; Kubota, 1990; Byrne and Byrne,
1993; Harigel, 1994; Colell et al., 1995). Likewise, no clear evidence
for the heritability of manual preference was found in most primate
species (Kubota, 1990; Boesch, 1991; Westergaard and Suomi, 1997;
but see Hopkins et al., 1993a). One reason for the lack of posturaleffect on manual preference could be that we only compared sitting
versus quadrupedal postures, whereas the majority of studies inmonkeys and apes showed that the direction and strength of

Please cite this article in press as: Leca, J.-B., et al., Principles and levels of laterality in unimanual and bimanual stone handling patterns by
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J.-B. Leca et al. / Journal of Human Evolution xxx (2009) 1–11

laterality was greater in bipedal or vertical clinging postures than ina quadrupedal posture (Olson et al., 1990; King and Landau, 1993;
Hopkins et al., 1993b; Westergaard et al., 1998b; Blois-Heulin et al.,2007).
In this study, our main goal was to provide an explicit andheuristic picture of the intrinsic and extrinsic variables that may
affect directly or indirectly the expression of manual laterality ina nonhuman primate species, for one or several manipulative tasks,
and at the individual and group levels. We systematically followed
the methodological framework developed by McGrew andMarchant (1997) to measure, label, and analyze manual preference
in a group of Japanese macaques. Overall, our results contribute to
the growing database of manual laterality in nonhuman primatesand provide additional evidence that Japanese macaques, like otherprimate species, display some form of group-level bias in manual
preference when performing asymmetric but coordinatedbimanual action involving role differentiation between hands.
Further study will focus on the inter-group comparison of handlateralization in SH by Japanese macaques, a cultural behavior withconsiderable geographical variation (Leca et al., 2007a). We
encourage similar detailed studies of manual laterality in primates
to shed further light upon the origins of functional laterality in theorder Primates and its implications for the evolution of tool use inearly hominins.

Acknowledgments
The authors’ work was funded by a Grant-In-Aid for scientiﬁc
research (No. 1907421 to M.A. Huffman) sponsored by Ministry of
Education, Science, Sports and Culture, Japan, by a JSPS (Japan
Society for the Promotion of Science) postdoctoral fellowship toJ.-B. Leca (No. 07421), and by travel funds from the HOPE Project,a core-to-core program sponsored by JSPS. We thank S. Asaba,
J. Hashiguchi, T. Kawashima, and S. Kobatake from Iwatayama
Monkey Park for helping us during the course of the study and forproviding us with valuable information on the study group. We areindebted to the Enomoto family for generously providing logistic
assistance at Arashiyama. We thank Dr. Susan Antón and theanonymous reviewers for fruitful comments on a previous versionof the manuscript.

References
Altmann, J., 1974. Observational study of behavior: sampling methods. Behaviour
49, 227–265.
Anderson, J.R., Degiorgio, C., Lamarque, C., Fagot, J., 1996. A multi-task assessment ofhand lateralization in capuchin monkeys (Cebus apella). Primates 37, 97–103.
Annett, M., 1985. Left, Right, Hand, and Brain: The Right Shift Theory. Erlbaum,
London.
Bard, K.A., Hopkins, W.D., Fort, C.L., 1990. Lateral bias in infant chimpanzees(Pan troglodytes). J. Comp. Psychol. 104, 309–321.
Beck, C.H.M., Barton, R.L., 1972. Deviation and laterality of hand preference inmonkeys. Cortex 8, 339–363.
Blois-Heulin, C., Bernard, V., Bec, P., 2007. Postural effect on manual laterality indifferent tasks in captive grey-cheeked mangabey (Lophocebus albigena).
J. Comp. Psychol. 121, 205–213.
Boesch, C., 1991. Handedness in wild chimpanzees. Int. J. Primatol. 12, 541–558.
Byrne, R.W., Byrne, J.M., 1991. Hand preferences in the skilled gathering tasks ofmountain gorillas (Gorilla g. beringei). Cortex 27, 521–546.
Byrne, R.W., Byrne, J.M.E., 1993. Complex leaf-gathering skills of mountain gorillas(Gorilla g. beringei): variability and standardization. Am. J. Primatol. 31, 241–261.
Bradshaw, J.L., Rogers, L.J., 1993. The Evolution of Lateral Asymmetries, Language,
Tool Use, and Intellect. Academic, San Diego.
Calvin, W.H., 1982. Did throwing stones shape hominid brain evolution? Ethol.
Sociobiol. 3, 115–124.
Colell, M., Segarra, M.D., Sabater Pi, J., 1995. Manual laterality in chimpanzees (Pantroglodytes) in complex tasks. J. Comp. Psychol. 109, 298–307.
Corballis, M.C., 1983. Human Laterality. Academic Press, New York.
Corp, N., Byrne, R.W., 2004. Sex difference in chimpanzee handedness. Am. J. Phys.
Anthropol. 123, 62–68.

Fagot, J., Vauclair, J., 1991. Manual laterality in nonhuman primates: A distinction
between handedness and manual specialization. Psychol. Bull. 109, 76–89.
Frost, G.T., 1980. Tool behavior and the origins of laterality. J. Hum. Evol. 9, 447–459.
Harigel, E.R., 1994. Hand preference in juvenile Japanese macaques (Macaca fuscata)
as a function of age, sex and rank. In: Anderson, J.R., Roeder, J.J., Thierry, B., Herrenschmidt, N. (Eds.), Current Primatology. Behavioral Neuroscience, Physiology
and Reproduction, vol. III. Universite Louis Pasteur, Strasbourg, pp. 23–30.
Homma, T., 1980. Sequential pattern of limb anomalies in Japanese monkeys on
Awajishima island. Primates 21, 20–30.
Hopkins, W.D., 1995. Hand preferences for a coordinated bimanual task in 110
chimpanzees (Pan troglodytes): cross-sectional analysis. J. Comp. Psychol. 109,291–297.
Hopkins, W.D., 1999. On the other hand: statistical issues in the assessment andinterpretation of hand preference data in nonhuman primates. Int. J. Primatol.
20, 851–866.
Hopkins, W.D., 2006. Comparative and familial analysis of handedness in great apes.
Psychol. Bull. 132, 538–559.
Hopkins, W.D., Rabinowitz, D.M., 1997. Manual specialization and tool-use incaptive chimpanzees (Pan troglodytes): the effect of unimanual and bimanual
strategies on hand preference. Laterality 2, 267–278.
Hopkins, W.D., Bales, S.A., Bennett, A.J., 1993a. Heritability of hand preference inchimpanzees (Pan). Int. J. Neurosci. 74, 17–26.
Hopkins, W.D., Bennett, A.J., Bales, S.L., Lee, J., Ward, J.P., 1993b. Behavioral laterality
in captive bonobos (Pan paniscus). J. Comp. Psychol. 107, 403–410.
Huffman, M.A., 1984. Stone-play of Macaca fuscata in Arashiyama B troop: transmission of a non-adaptive behavior. J. Hum. Evol. 13, 725–735.
Huffman, M.A., 1996. Acquisition of innovative cultural behaviors in nonhumanprimates: a case study of stone handling, a socially transmitted behavior inJapanese macaques. In: Galef Jr., B., Heyes, C. (Eds.), Social Learning in Animals:
The Roots of Culture. Academic Press, Orlando, FL, pp. 267–289.
Huffman, M.A., Hirata, S., 2003. Biological and ecological foundations of primate
behavioral tradition. In: Fragaszy, D.M., Perry, S. (Eds.), The Biology of Tradition:
Models and Evidence. Cambridge University Press, Cambridge, pp. 267–296.
Itani, J., Tokuda, K., Furuya, Y., Kano, K., Shin, Y., 1963. The social construction ofnatural troops of Japanese monkeys in Takasakiyama. Primates 4, 2–42.
Kawai, M., 1967. Catching behavior observed in the Koshima troop-a case of newly
acquired behavior. Primates 8, 181–186.
King, J.E., Landau, V.I., 1993. Manual preference in varieties of reaching in squirrel
monkeys. In: Ward, J.P., Hopkins, W.D. (Eds.), Primate Laterality: Current
Behavioral Evidence of Primate Asymmetries. Springer-Verlag, New York, pp.
107–124.
Kubota, K., 1990. Preferred hand use in the Japanese macaque troop, Arashiyama-R,
during visually guided reaching for food pellets. Primates 31, 393–406.
Leca, J.-B., Gunst, N., Huffman, M.A., 2007a. Japanese macaque cultures: inter- andintra-troop behavioural variability of stone handling patterns across 10 troops.
Behaviour 144, 251–281.
Leca, J.-B., Gunst, N., Huffman, M.A., 2007b. Age-related differences in the performance, diffusion, and maintenance of stone handling, a behavioral tradition in
Japanese macaques. J. Hum. Evol. 53, 691–708.
Leca, J.-B., Nahallage, C.A.D., Gunst, N., Huffman, M.A., 2008a. Stone-throwing by
Japanese macaques: form and functional aspects of a group-speciﬁc behavioral
tradition. J. Hum. Evol. 55, 989–998.
Leca, J.-B., Gunst, N., Huffman, M.A., 2008b. Of stones and monkeys: testing
ecological constraints on stone handling, a behavioral tradition in Japanesemacaques. Am. J. Phys. Anthropol. 135, 233–244.
Leca, J.-B., Gunst, N., Huffman, M.A., 2008c. Variability of food provisioning regimes
and stone handling tradition in Japanese macaques: a comparative study of ten
troops. Am. J. Primatol. 70, 803–813.
Lehman, R.A.W., 1980. Distribution and changes in strength of hand preference of
cynomolgus monkeys. Brain. Behav. Evol. 77, 209–217.
Lilak, A.L., Phillips, K.A., 2008. Consistency of hand preference across low-level andhigh-level tasks in capuchin monkeys (Cebus apella). Am. J. Primatol. 70,
254–260.
Lonsdorf, E.V., Hopkins, W.D., 2005. Wild chimpanzees show population-level
handedness for tool use. Proc. Natl. Acad. Sci. U S A 102, 12634–12638.
MacNeilage, P.F., 1991. The ‘‘postural origins’’ theory of primate neurobiologicalasymmetries. In: Krasnegor, N.A., Rumbaugh, D.M., Schiefelbusch, R.L. (Eds.),
Biological and Behavioral Determinants of Language Development. Lawrence
Erlbaum, Hillsdale, NJ, pp. 165–188.
MacNeilage, P.F., Studdert-Kennedy, M.G., Lindblom, B., 1987. Primate handedness
reconsidered. Behav. Brain. Sci. 10, 247–289.
Marchant, L.F., McGrew, W.C., 1991. Laterality of function in apes: a meta-analysis ofmethods. J. Hum. Evol. 21, 425–438.
Marchant, L.F., McGrew, W.C., 1996. Laterality of limb function in wild chimpanzees
of Gombe National Park: comprehensive study of spontaneous activities. J.
Hum. Evol. 30, 427–443.
Marchant, L.F., McGrew, W.C., 1998. Human handedness: an ethological perspective.
Hum. Evol. 13, 221–228.
Marchant, L.F., McGrew, W.C., 2007. Ant ﬁshing by wild chimpanzees is not lateralised. Primates 48, 22–26.
Marchant, L.F., McGrew, W.C., Eibl-Eibesfeldt, I., 1995. Is human handedness
universal? Ethological analyses from three traditional cultures. Ethology 101,
239–258.
Martin, P., Bateson, P., 1993. Measuring Behaviour: an Introductory Guide. Cambridge University Press, Cambridge.

Please cite this article in press as: Leca, J.-B., et al., Principles and levels of laterality in unimanual and bimanual stone handling patterns by
Japanese macaques, J Hum Evol (2009), doi:10.1016/j.jhevol.2009.09.005

ARTICLE IN PRESS
287

J.-B. Leca et al. / Journal of Human Evolution xxx (2009) 1–11
Matsuzawa, T., Biro, D., Humle, T., Inoue-Nakamura, N., Tonooka, R., Yamakoshi, G.,2001. Emergence of culture in wild chimpanzees: education by masterapprenticeship. In: Matsuzawa, T. (Ed.), Primate Origins of Human Cognition
and Behavior. Springer, Tokyo, pp. 557–574.
McGrew, W.C., Marchant, L.F., 1992. Chimpanzees, tools, and termites: hand preference or handedness? Curr. Anthropol. 33, 114–119.
McGrew, W.C., Marchant, L.F., 1996. On which side of the apes? In: McGrew, W.C.,
Marchant, L.F., Nishida, T. (Eds.), Great Ape Societies. Cambridge University
Press, Cambridge, pp. 255–272.
McGrew, W.C., Marchant, L.F., 1997. On the other hand: current issues in and metaanalyses of the behavioral laterality of hand function in nonhuman primates.
Yearb. Phys. Anthropol. 40, 201–232.
McGrew, W.C., Marchant, L.F., 2001. Ethological study of manual laterality in the
chimpanzees of the Mahale Mountains, Tanzania. Behaviour 138, 329–358.
McGrew, W.C., Marchant, L.F., Wrangham, R.W., Klein, H., 1999. Manual laterality inanvil use: wild chimpanzees cracking Strychnos fruits. Laterality 4, 79–87.
McManus, I.C., Sik, G., Cole, D.R., Mellon, A.F., Wong, J., Kloss, J., 1988. The development of handedness in children. Br. J. Dev. Psychol. 6, 257–273.
Nahallage, C.A.D., Huffman, M.A., 2007a. Age-speciﬁc functions of stone handling,a solitary-object play behavior, in Japanese macaques (Macaca fuscata). Am. J.
Primatol. 69, 267–281.
Nahallage, C.A.D., Huffman, M.A., 2007b. Acquisition and development of stone
handling behavior in infant Japanese macaques. Behaviour 144, 1193–1215.
Olson, D.A., Ellis, J.E., Nadler, R.D., 1990. Hand preferences in captive gorillas,orangutans and gibbons. Am. J. Primatol. 20, 83–94.
Palmer, A.R., 2002. Chimpanzee right-handedness reconsidered: evaluating theevidence with funnel plots. Am. J. Phys. Anthropol. 188, 191–199.
Papademetriou, E., Sheu, C.-F., Michel, G.F., 2005. A meta-analysis of primate handpreferences, particularly for reaching. J. Comp. Psychol. 119, 33–48.
Rigamonti, M.M., Previde, E.P., Poli, M.D., Marchant, L.F., McGrew, W.C., 1998.
Methodology of motor skill and laterality: new test of hand preference inMacaca nemestrina. Cortex 34, 693–705.
Schaafsma, S.M., Riedstra, B.J., Pfannkuche, K.A., Bouma, A., Groothuis, T.G.G., 2009.
Epigenesis of behavioural lateralization in humans and other animals. Phil.
Trans. R. Soc. B 364, 915–927.
Sharer, D.D., 1993. Patterns of handedness: comparative study of nursery school
children and captive gorillas. In: Ward, J.P., Hopkins, W.D. (Eds.), Primate Laterality: Current Behavioral Evidence of Primate Asymmetries. Springer-Vedag,
New York, pp. 267–283.

11

Siegel, S., Castellan, N.J., 1988. Nonparametric Statistics for the Behavioral Sciences.
McGraw-Hill, Singapore.
Spinozzi, G., Truppa, V., 1999. Hand preferences in different tasks by tufted capuchins (Cebus apella). Int. J. Primatol. 20, 827–849.
Sugiyama, Y., Fushimi, T., Sakura, O., Matsuzawa, T., 1993. Hand preference and tool
use in wild chimpanzees. Primates 34, 151–159.
Takeda, S., 1994. Hand specialization in social grooming behavior in Japanesemacaques (Macaca fuscata). In: Anderson, J.R., Roeder, J.J., Thierry, B.,
Herrenschmidt, N. (Eds.), Current Primatology. Behavioral Neuroscience, Physiology and Reproduction, vol. III. Universite Louis Pasteur, Strasbourg, pp. 31–35.
Tokuda, K., 1969. On the handedness of Japanese monkeys. Primates 10, 44–46.
Trouillard, E., Blois-Heulin, C., 2005. Manual laterality and task complexity in De
Brazza’s monkey (Cercopithecus neglectus). Laterality 10, 7–27.
Vallortigara, G., Rogers, L.J., 2005. Survival with an asymmetrical brain: advantages
and disadvantages of cerebral lateralization. Behav. Brain. Sci. 28, 575–633.
Vauclair, J., Meguerditchian, A., Hopkins, W.D., 2005. Hand preferences forunimanual and coordinated bimanual tasks in baboons (Papio anubis). Cogn.
Brain Res. 25, 210–216.
Ward, J.P., Hopkins, W.D., 1993. Primate Laterality. Current Behavioral Evidence ofPrimate Asymmetries. Springer, New York.
Warren, J.M., 1980. Handedness and laterality in humans and other animals. Physiol.
Psychol. 8, 351–359.
Watanabe, K., Kawai, M., 1993. Lateralized hand use in the precultural behavior of
the Koshima monkeys (Macaca fuscata). In: Ward, J.P., Hopkins, W.D. (Eds.),
Primate Laterality. Springer, New York, pp. 183–192.
Westergaard, G.C., Suomi, S.J., 1993a. Hand preference in the use of nut-cracking
tools by tufted capuchin monkeys (Cebus apella). Folia. Primatol. 61, 38–42.
Westergaard, G.C., Suomi, S.J., 1993b. Hand preference in capuchin monkeys varies
with age. Primates 34, 295–299.
Westergaard, G.C., Suomi, S.J., 1996. Hand preference for stone artefact production
and tool-use by monkeys: possible implications for the evolution of righthandedness in hominids. J. Hum. Evol. 30, 291–298.
Westergaard, G.C., Suomi, S.J., 1997. Lateral bias in capuchin monkeys (Cebus apella):concordance between parents and offspring. Dev. Psychobiol. 31, 143–147.
Westergaard, G.C., Kuhn, H.E., Suomi, S.J., 1998a. Laterality of hand function in
tufted capuchin monkeys (Cebus apella): comparison between tool use actions
and sponataneous non-tool actions. Ethology 104, 119–125.
Westergaard, G.C., Kuhn, H.E., Suomi, S.J., 1998b. Bipedal posture and hand preference in humans and other primates. J. Comp. Psychol. 112, 56–63.

Please cite this article in press as: Leca, J.-B., et al., Principles and levels of laterality in unimanual and bimanual stone handling patterns by
Japanese macaques, J Hum Evol (2009), doi:10.1016/j.jhevol.2009.09.005

Glance-6476 and her infant (Arashiyama)

Glance-6476 in January 1987

Momo-5978 and her infant in 1989 (Arashiyama)

Stone handling juveniles at Takasakiyama (Nov. 1989)

Photos by M.A. Huffman

Stones left on flat stone
surface by free-ranging
stone handlers) at
Takasakiyama

Cuddling (young)1

Scattering2

Cuddling (adult)1

Grasp with hand1

Move and push2

Gathering1

Rub with hand2

Examples of stone handling patterns by Japanese macaques(1: photos by J.-B. Leca, 2: photos by N. Gunst)

Rub together2

Social influence of the mother in stone handling acquisition by infants1

Handling stones while involved in a social play interaction…1… or in a grooming interaction1

Stone handling in long-tailed macaques1

Fish eating by Japanese macaques at Koshima1

Dental flossing (Arashiyama)1