Traditions in monkeys

ARTICLES

Traditions in MonkeysSUSAN PERRY AND JOSEPH H. MANSON

Cultural primatology traces its ori-gins to 1952, when Imanishi1 encour-aged animal behaviorists to look for

within-species, between-group behav-ioral differences, working from the as-sumption that such behaviors were at-tributable to social learning (that is,culture, as he used the term) ratherthan instinct. Influenced by this land-mark work, Japanese primatologistsduring the following decades docu-mented numerous traditions in free-living, mostly provisioned, Japanesemacaques.2–4 With few exceptions(for example, Stephenson5), Westernprimatologists did not pursue this lineof research until the 1990s, when sys-tematic investigation of chimpanzeecultural differences was undertakenby researchers from several countrieswho eventually joined to produce asystematic description of this varia-tion.6 Though the study of culture wasformerly undertaken almost exclu-sively within social science and hu-manities departments in Western ac-ademic traditions, recent theoreticaldevelopments in gene-culture coevo-lution7,8 have aroused the interest ofevolutionary biologists as well.

As more researchers begin investi-gating social learning and culture innonhumans, the time is ripe to coor-dinate comparative studies of thesephenomena, both in the field and inthe lab. To understand the evolutionof culture in its human form, we needto understand what socioecologicalconditions favor social learning in na-ture,9 and to accomplish this, we needto expand the quest for data beyondthe apes to include not only monkeys,but also nonprimates such as ceta-ceans10 and birds.11 It is also useful tounderstand how the transmissionspeed and fidelity of socially learnedbehaviors are affected by the type ofsocial learning mechanism employed,though this is a particularly difficultmission to accomplish in the field.Psychologists have produced elabo-rate taxonomies of the ways in whichanimals’ acquisition of behavior pat-terns could be affected by conspecif-ics.9 In general, true imitation, inwhich an individual reproduces se-quences of actions after observing an-other perform these sequences, andemulation are regarded as the mostcomplex and the taxonomically rarestof these processes. Most researchersprefer to invoke simpler social learn-ing mechanisms, such as stimulus en-hancement, in the absence of convinc-ing evidence for imitation oremulation.

Cultural primatology is a fieldplagued by many definitional quan-dries. For the purposes of this article,we define a tradition as “a behavioralpractice that is relatively long-lasting(i.e. is performed repeatedly over aperiod of time) and that is sharedamong members of a group in partthrough social learning.”12 We do notrequire that a behavior persist for anyspecified length of time in order toqualify as a tradition, that all groupmembers share the trait in question,

Susan Perry is the head of the Cultural Phy-logeny Group at the Max Planck Institute forEvolutionary Anthropology and is AssistantProfessor of Anthropology at the Universityof California, Los Angeles. Her researchcurrently focuses on social learning, tradi-tions, and infant development in white-faced capuchin monkeys. She is co-editor(with Dorothy Fragaszy) of The Biology ofTraditions: Models and Evidence, which isforthcoming from Cambridge UniversityPress. Email: [email protected]

Joseph Manson is a staff scientist at theCultural Phylogeny Group at the MaxPlanck Institute for Evolutionary Anthropol-ogy and is Associate Professor of Anthro-pology at the University of California, LosAngeles. He has studied female matechoice in free-ranging rhesus macaques.Currently, he is interested in the compara-tive study of social learning primates.

Key words: culture, conventions, foraging tech-niques, food choice, interspecific interactions

Evolutionary Anthropology 12:71–81 (2003)DOI 10.1002/evan.10105Published online in Wiley InterScience(www.interscience.wiley.com).

Traditions, defined as relatively long-lasting behavioral practices shared amongmembers of a group partly via social learning, were studied in monkeys, specificallyJapanese macaques, before being studied in great apes. Although apes and humansmay share some social learning capacities that are absent in monkeys, a completeunderstanding of the roots of human culture requires attention to the socioecologicalconditions favoring traditions, however generated, in animals generally and in multiplebehavioral domains. Using the four criteria of intergroup variation, observation of theorigin and spread of a novel behavior, dissemination patterned according to age orkinship, or individuals’ close observation of others’ performance of the behavior beforeengaging in it, over twenty-five behaviors have been nominated as traditions infree-ranging monkey populations. Tolerant gregariousness has been proposed toincrease the likelihood of the emergence of traditions in any behavioral domain.Omnivory and extractive foraging should favor the emergence of foraging-relatedtraditions; strong cooperative relationships and flexible coalitionary structure shouldfavor the emergence of social conventions that function to test social bonds. Theseconditions are taxonomically widespread. Thus, the current restriction of most re-ported free-ranging monkey traditions to two taxa (Macaca fuscata and Cebus) is likelyto reflect variation in primatologists’ research goals, methods, and concepts ratherthan real interspecific variation in the propensity to generate traditions.

Evolutionary Anthropology 71

or that individuals acquire the trait byimitation or emulation as distinctfrom simpler forms of social learning.We recognize that many factors, in-cluding ecological and genetic factors,may bias an animal toward engagingin particular behaviors. We do not in-sist that the influences of such factorsbe completely eliminated as possibili-ties in order for a behavioral patternto be defined as a tradition, but we dorequire that some role of social influ-ence on the acquisition of the trait bedemonstrated. We generally avoid us-ing the word “culture” because muchof the debate over its definition hasshed more heat than light, but wherewe do use it we mean simply behav-ioral variation, the distribution ofwhich is determined at least in part bysocial learning.

In this paper, we first present theo-retical reasons for expecting tradi-tions in monkeys, and then summa-rize relevant empirical findings.Finally we discuss some implicationsof the details of the spread of tradi-tions in free-ranging animals andpresent suggestions for future re-search in this area.

TAXONOMIC DISTRIBUTION OFTRADITIONS: THEORETICAL

CONSIDERATIONS

Aside from the steady interest intraditions among Japanese research-ers focusing on macaques, primatolo-gists’ quest for data on cultural behav-iors has focused primarily on theapes. However, a deeper understand-ing of the evolution of cultural capac-ities requires a broader comparativedatabase. It is necessary to look at awide range of socioecological contextsin phylogenetically distant species todetermine the conditions under whichsocial learning is favored and tradi-tions become possible.

Generally speaking, those speciesthat are highly social, and in whichindividuals are tolerant of intense ob-servation by others, will be most ca-pable of social learning.13–15 Giventhat most monkey species are farmore gregarious than most ape spe-cies,16 it seems that they should bemore effective in learning socially un-less apes possess cognitive mecha-nisms that are absent in monkeys and

make them more effective at sociallearning. However, we know fromstudies of nonprimates such asrats17,18 that quite stable traditionscan emerge in species that employvery simple social learning mecha-nisms, such as acquiring food prefer-ences simply by smelling foods onconspecifics. Thus, it would be sur-prising if monkeys did not commonlyexhibit traditions. Of course the costsand benefits of engaging in sociallearning will vary according to behav-ioral domain, so any kind of sophisti-cated model attempting to predict theemergence of traditions will have toconsider which aspects of a species’

cognitive abilities, social structure,and ecology are relevant to the adap-tive problem it faces.

Van Schaik13 and van Schaik,Deaner, and Merrill14 have developeda model predicting the conditions un-der which tool-use culture will emergein primates. Only in species that en-gage in dexterous extractive foragingare individuals expected to devisefeeding tools. For such innovations tospread and thereby produce routine,population-wide tool use and inter-population variability, the speciesmust also have the ability to learn by

imitation and/or emulation, and indi-viduals must practice a high degree oftolerant gregariousness. Based on thismodel, van Schaik, Deaner, and Mer-rill14 predict that only great apes willshow routine tool use in the wild be-cause, unlike monkeys, great apes arecapable of imitation and emulation19

(but see Tomasello20 for a differentperspective). However, recent demon-strations of imitation in capuchins21

and marmosets22 have challenged thisphylogenetic distinction and may ne-cessitate a revision to the predictionsgenerated by van Schaik, Deaner, andMerrill’s14 model.

In any case, the complete model ap-plies only to material culture. Tradi-tions in other domains may be pre-dicted by different sets of independentvariables, although tolerant gregari-ousness is likely to facilitate the emer-gence of traditions in any domain.13

For example, social conventions(clique- or dyad-specific communica-tive innovations23) that function totest social bonds are expected inhighly social species that have long-lasting cooperative relationships, par-ticularly if they are embedded in acomplex coalitionary structure (seelater discussion of social conven-tions). Such conditions are commonin monkeys, but virtually no researcheffort has been expended to investi-gate this topic. Communicative sig-nals could spread by the process ofontogenetic ritualization or conven-tionalization,24 which may be moretaxonomically widespread than imita-tion or emulation.

Traditions regarding food choiceare expected to be particularly com-mon in omnivores, and are predictedtheoretically whenever social cues offood quality are more reliable thannonsocial cues.25 Quite simple cogni-tive processes and social learningmechanisms suffice to transmit suchtraditions.18 Hence, there is no reasonto expect food-choice traditions to bemore common in apes than in mon-keys.

Given the high degree of danger as-sociated with learning about preda-tors via individual experimentation, itis to be expected that social influencewill quite frequently be important inlearning about the proper way to in-teract with heterospecifics in gregari-

Cultural primatology is afield plagued by manydefinitional quandries.For the purpose of thisarticle, we define atradition as “abehavioral practice thatis relatively long-lasting(i.e. is performedrepeatedly over aperiod of time) and thatis shared amongmembers of a group inpart through sociallearning.”

72 Evolutionary Anthropology ARTICLES

ous species generally, as long as thereis frequent opportunity to observeconspecifics’ interactions with otherspecies.26

Finally, more heterogeneous obser-vation opportunity for the animals (asoccurs in orangutans and chimpan-zees, with their fission-fusion life-styles) is likely to be more effective formaintaining detectable behavioralvariation than are the larger, morestable groupings in which monkeysmore typically reside.27

EVIDENCE FOR TRADITIONS INMONKEYS

Table 1 lists traditions proposed toexist among free-ranging monkeys,along with several parameters re-garded as theoretically important. Be-cause, as discussed earlier, differentindependent variables are expected toinfluence the emergence of traditionsin different behavioral domains, wedivide our presentation along this di-mension. We have restricted Table 1to putative traditions meeting at leastone of the following criteria: the be-havior is customary in some socialgroups, yet absent or very rare in oth-ers where it is ecologically possible;the origin and spread of the behaviorwas observed, or at least the behaviorwas observed to spread from one age-sex class to another; the behaviorspread in accordance with links viamaternal kinship, observed proximity,and/or age structure; and individualswere seen to intently observe othersperforming the behavior prior to ex-hibiting it themselves or participate init unwillingly (as when mothers dunktheir infants in the water, in bathing).

Food Processing and FoodChoice

The majority of traditions that havebeen documented in monkeys involvesome form of foraging skill or foodchoice. The most famous, best docu-mented, and most durable monkeyforaging traditions are the feedingtechniques invented during the 1950sby the young Japanese macaque Imoof the Koshima troop.28 She beganwashing provisioned sweet potatoes,and later wheat, in salt water, whichserved to clean the food of sand and

dirt, while simultaneously seasoningit. Both these behaviors spread first toother juveniles and to Imo’s mother,but eventually they were adopted by alarge fraction of the group, thoughmany adult males never engaged inthese behaviors. At other sites, sweet-potato washing has been occasionallyobserved but has not been widelypropagated.4 Washing apples in snowor hot springs spread to most of theShiga-A group within six months afterprovisioning began.29 Food-washingtraditions seem particularly likely toarise in macaques, even in captivity,30

though this propensity may be taxo-nomically widespread, because cap-tive brown capuchins also readilyadopted food-washing.31 The originand spread of several traditions of eat-

ing novel provisioned foods(wheat,32,33 corn,33 and candy34) havebeen documented at several Japanesemacaque sites. After provisioning wasdramatically reduced at Koshima fol-lowing a rapid increase in population,peripheral adult males began eatingdead fish, and this habit spread tomost of the social group during thefollowing six years.35

In a group of wild vervet monkeysduring a drought, the oldest femalebegan dipping dry Acacia tortilis podsinto the viscous exudate contained inthe well of an A. tortilis tree. Withintwenty-two days, seven of the group’sten members were using the sametechnique.36 The following year, whenrainfall levels were normal, pod-dip-ping was not observed. Experimen-tally induced food choice traditions

have been produced among wildvervets and chacma baboons.37

Nut-cracking with rocks is quitecommon in one semi-free-ranginggroup of brown capuchins,38 though ithas not been observed in other groupswith access to the same materials.White-faced capuchins at Lomas Bar-budal, Costa Rica, kill squirrels with asingle bite to the neck, whereas at thenearby site of Santa Rosa this tech-nique is not employed.39,40 This differ-ence may account for the greaterhunting efficiency of the Lomas Bar-budal capuchins compared to those atSanta Rosa. Finally, at Lomas Barbu-dal and the neighboring site of PaloVerde, several food-processing tech-niques, all involving pounding or rub-bing plant foods, vary within groups.Individuals that spend more time inproximity show a significant tendencyto use the same technique.41

Surprisingly, food-processing andfood-choice traditions have not beensystematically documented underfree-ranging conditions for other spe-cies of monkey, although predationon vertebrates by olive baboons,42

food-washing by provisioned free-ranging long-tailed macaques,43 anddietary differences between neighbor-ing white-faced capuchin groups44

have been proposed as traditional.However, it may be that foraging tra-ditions are more common in naturethan the literature suggests, and thatconceptual and methodological con-fusion prevents their discovery.12 Themost common method currently em-ployed by primatologists to identifytraditions in wild populations is toidentify an intergroup difference, andthen exclude ecological differencesand genetic differences as possible ex-planations (for example, Whiten andcoworkers6). Thus, “tradition” be-comes a residual concept, invoked toexplain intergroup differences afterall other explanations have been falsi-fied. This analytical procedure posesthe risk that many traditions, as wehave defined the term, will be over-looked.

Consider, for example, food choiceby wild mantled howler monkeys, Al-ouatta palliata.45 The leaves of only asmall minority of tree species in eachsocial group’s home range, and onlysome individual trees within these

. . . it may be thatforaging traditions aremore common in naturethan the literaturesuggests, and thatconceptual andmethodologicalconfusion prevents theirdiscovery.

ARTICLES Evolutionary Anthropology 73

species, contain a high enough ratioof protein to secondary compounds tomake them nutritionally suitable. In-

dividual trial-and-error learning byweaned infants could produce severepoisoning. Limited systematic obser-

vations indicate that infants feed onleaves only after older individualshave begun feeding in the same tree,

TABLE 1. Putative Traditions in Free-Ranging Monkeys

Species TraditionCriteria forDesignationa Domainb

No. ofSocialGroupsc

MaximumPercentagePractitionersd

PropagationPatternse

Durationf

(max) References

Macacafuscata

Sweet-potato washing C/A, Orgn,Mat, Age,

Obs

FP 1 84 I/I, I/A, M/O 49� years 4, 28

Wheat placer mining C/A, Orgn,Mat, Age,

Obs

FP 1 39 I/I, I/A, M/O 46� years 4, 28

Apple washing Orgn FP 1 58 A/A, A/I,?M/O

? 29

Fish-eating C/A, Orgn FC 1 75 A/A, ?M/I,?A/I

4 years 35

Wheat eating Orgn, Prox,Obs

FC � 100 I/I, I/A, A/A,M/O

? 2, 32, 33

Corn eating Orgn, Prox,Obs

FC � 100 I/I, I/A, AA,M/O

? 33

Caramel unwrapping& eating

Orgn FP, FC � 60 I/I, I/A, A/A N/A 34

Four courtship gestures C/A SC 3 100 ? ? 5Four distinct louse-handling techniques ingrooming

Orgn, Mat SC? Studiedwithin-group

variation

Studiedwithin-group,

between-matrilinevariation

M/O, ?I/I,?A/I

At least 3years

50, 51

Stone handling C/A, Orgn,Age, ?Obs

Other 2 �100? I/I, M/O 23� years 47, 56, 57

Bathing (seawater &hot spring)

?C/A, Orgn,Obs

Other 2 63 I/I, I/A, M/O 43� years 28, 29

“Give-me-some”gesture

C/A Other 1 79 ? 42� years 4, 28

Cercopithecusaethiops

Acacia pod dipping Orgn, Mat FP 1 70 M/O, A/A,A/I

�1 year 36

Use of artificial baitclues to find food

Orgn FC � 100 ? ? 37

Cebuscapucinus

Pounding or scrubbingof 16 different foodspecies

C/A, prox insome cases

FP 10 highlyvariable

? ? 41

Neck bite to killsquirrels

C/A IS, FP 1 observed inall kills in 1

group

? 1 year 39, 40

Hand sniffing C/A, Orgn SC 5 43 A/A 7 years 23Appendage sucking C/A SC 3 45 ? 6 months 23Finger-in-mouth game C/A, Incr SC 1 22 A/I, A/A 10 years 23Hair game C/A, Incr SC 1 35 A/I, A/A 10 years 23Toy game C/A, Incr SC 2 46 A/I, A/A 9 years 23Grooming of spidermonkeys

C/A IS 2 �25 ? at least 4years

39, 40

Tolerance of indigosnakes

C/A IS 1 ? ? at least 1year

39, 40

Army ant following C/A IS 2 ? ? ? 39, 41Cebus apella Nut cracking with

stonesC/A, Obs FP 1 83 (100% of

adults)? ? 38

Papio ursinus Use of artificial baitclues to find food

Orgn, Age FC � 100 I/A? ? 37

a C/A � customary in some social group(s), yet absent or very rare in other(s) where it is ecologically possible. Orgn � origin of thetrait observed; an initially absent trait spreads through a social group. Incr � increase in the number of animals engaging inbehavior, though the origin is not observed. Mat � spread of the trait occurs approximately in accordance with maternal kinshiplines (a proxy for observation opportunity). Prox � spread of the trait occurs in accordance with documented proximity patterns(that is, opportunity for social learning). Age � spread of the trait occurs in accordance with age-structure—that is, from juvenilesto similar-aged playmates (assumed to approximate social learning opportunity). Obs � monkeys intently observe one anotherperforming the behavior prior to exhibiting it themselves, or participate in it by force (as when mothers dunk their infants in thewater, in bathing).

b FP � food processing; FC � food choice; SC � social convention; IS � interspecific interactions.c Presumed independent inventions of the tradition. � Experimentally induced tradition with artificial stimulus.d In one social group.e I/I � among immatures. I/A � from immatures to adult kin. A/A � among adults. M/O � mother to offspring. A/I � nonmaternal

adult to offspring.f � � Tradition continues to the present.


and that they watch their mothersfeed just before ingesting leaves, sug-gesting that leaf choice is learned so-cially. If this is true, then each A. pal-liata group’s set of leaf preferencesqualifies as a tradition in our sense.Yet, using primatologists’ typical cri-teria for identifying traditions, an an-alyst would find no intragroup varia-tion in leaf choice, and would ascribeany observed intergroup variation toecological factors (each group has thenutritionally optimal set of leaf pref-erences for its home range) ratherthan to group-specific traditions. Onthe other hand, merely showing thatneighboring groups use a particularfood species at different frequencies,even though its density does not differbetween their home ranges, does notby itself demonstrate a traditional dif-ference.44 According to optimal forag-ing theory, to predict whether a foodtype will enter the diet, one needs toknow its profitability relative to that ofall other available food types. Thus, inthe absence of extremely detailedknowledge of local geographical vari-ation in food availability, it is impos-sible to distinguish socially learnedgroup-specific food preference tradi-tions from individually learned foodpreferences developed under the guid-ance of a reinforcement systemevolved to produce optimal foraging.(See Dewar25 for further discussion ofthis issue and some possible method-ological solutions.)

To illustrate further the difficulty ofidentifying foraging traditions in na-ture, consider the following hypothet-ical example: Suppose that membersof all populations of a particular mon-key species having access to a partic-ular kind of nutritious nut learnedhow to crack it. If the trait was inde-pendently invented in each socialgroup, yet there was one clearly supe-rior nut-cracking technique, allgroups might converge on the samesolution eventually, even if sociallearning was crucial for transmittingthe trait within each social group.Given the difficulty of documentingthe precise role of social learning inthe ontogeny of any particular traitwithout employing experimental con-trols, it is perhaps inevitable that so-cially learned food-processing traitsare infrequently reported in the wild.

Some primatologists feel comfortableascribing a role of social learning to atrait only if they can show, minimally,that the trait covaries with spatialproximity—that is, individuals thatassociate frequently will tend to pro-cess the same foods using the sametechniques.46 This method requiresnatural intragroup variation: Eithersome animals must process the foodwhile others do not or multiple tech-niques must be used to process a food.

The former condition is highly un-likely if the food is part of the group’soptimal diet. It is likely to be seenchiefly when new foods have been in-troduced to the animals (Japanesemacaque sweet-potato washing andwheat washing) or during food short-ages (vervet pod-dipping, Japanesemacaque fish-eating) in which ani-mals must resort to new food sources

because preferred ones have been de-pleted. By observing the transmissionphase of a tradition,47 it is possible todocument a role for social learningbecause close associates of the inno-vator will be most likely to acquire thetrait first. Once the trait has spread toall group members, as is expected if itis a particularly useful trait, the role ofsocial influence will be difficult, if notimpossible, to detect.

If, however, there are multiple waysto process the same food that do notvary substantially in their effective-ness, so that individual experimenta-tion will be less likely to eliminatesome possibilities in favor of others,then behavioral variation should bemaintained in the group. Under suchcircumstances, it is much easier totest for a role of social learning in theacquisition of traits because the trans-mission phase does not have to be ob-served. This reasoning led us to exam-ine whether dyadic similarity in foodprocessing techniques co-varied withspatial proximity41 in white-faced ca-puchins.

In general, behavioral variation ismost likely to exist for foraging tasksin which multiple steps must be em-ployed to process the food. Therefore,food processing traditions are mostlikely to be found in monkey taxa suchas Cebus that engage in extractive for-aging and must deal with problemssuch as mechanical defense of plantfoods. Hunting also presents a com-plex foraging challenge. It seems plau-sible that those few monkey speciesthat hunt may use different sociallylearned techniques for capturing, kill-ing, and processing prey. Besideswhite-faced capuchin squirrel-killingtechniques, relay chasing of prey byolive baboons may be sociallylearned.42

Social Conventions

Very little research on traditions innonhumans has focused on the behav-ioral domain of social conventions—that is, dyadic social behaviors orcommunicative behaviors that areunique to particular groups or cliques.Social conventions are particularlyrelevant to debates about the learningmechanisms that produce traditionsbecause, in contrast to asocial behav-iors such as food processing, it is dif-

. . . to predict whether afood type will enter thediet, one needs to knowits profitability relative tothat of all otheravailable food types.Thus, in the absence ofextremely detailedknowledge of localgeographical variationin food availability, it isimpossible to distinguishsocially learned group-specific food preferencetraditions fromindividually learnedfood preferencesdeveloped under theguidance of areinforcement systemevolved to produceoptimal foraging.


ficult to conceive of how the numberof practitioners could increase with-out the involvement of some form ofsocial learning. Although some socialconventions such as hand-claspgrooming48 and leaf clipping,49 havebeen reported for chimpanzees, suchreports are rare in monkeys. One ex-ample is Stephenson’s5 report, basedon analysis of extensive film footage,that four Japanese macaque courtshipbehaviors (for example, “FemaleMounts Male”) were observed at onlyone or two of three study sites. Alter-native louse handling techniques in al-logrooming have been reported inJapanese macaques,50,51 though thesevariants seem to be more analogous totechnological differences rather thanhaving different social signalingvalue.

Another group-specific form of ges-tural communication in Japanese ma-caques is the “give-me-some” gesturedirected by the monkeys of Koshimatoward humans providing food.4,28

One hand is held out toward the hu-man, palm up, after which the mon-key usually takes the food with theother hand. This gesture is not part ofthe natural Japanese macaque behav-ioral repertoire, and may have arisenin interaction with humans via (possi-bly inadvertent) operant conditioning,in which humans preferentially gavefood to monkeys that happened toproduce ever closer approximationsto the human-like begging gesture. IfJapanese macaques can learn gesturesfrom allospecifics via conditioning,perhaps they can learn them fromconspecifics as well, just as femalecowbirds shape male song structureby producing wing strokes in responseto favored songs.52

Social Conventions in White-Faced Capuchins

The clearest examples of social con-ventions in a monkey come from thewhite-faced capuchin monkey, inwhich five such behaviors, all ofwhich occur variably both amonggroups and over time, have been doc-umented in a data set consisting of19,000 hours of observation on thir-teen social groups at four study sitesin northwestern Costa Rica.23 Forthree of these behavior patterns, inter-individual transmission chains were

documented. All five social conven-tions involve an element of risk or dis-comfort, and all require quiet focus bythe participants. We describe each ofthem in turn.

1. Handsniffing: In this behavior,one monkey places its foot or handover another’s face, in the latter casesometimes inserting its fingers up thepartner’s nostrils, and the two mon-keys inhale repeatedly for over aminute, often swaying slowly as theydo so. In some groups, this behavior ismutual, with each monkey having itsfingers up the partner’s nose. Somevariant of handsniffing was com-monly observed in five different social

groups at three different study sites.In four of these cases researcherswere present for either the beginningor the end of this tradition, and in theone case in which both the onset andextinction of the behavior were ob-served, the tradition lasted sevenyears.

2. Sucking of body parts: In this be-havior, one animal sucks on the fin-gers, tail, or ears of the partner for upto an hour or more; this behavior isoften mutual, with each partner suck-ing on some part of the partner.

3. Various games: In the “finger-in-mouth” game, one participant insertsits finger into the other’s mouth. Thepartner bites down hard enough thatthe finger cannot be easily removed,and the owner of the finger strugglesto pry the partner’s mouth open inorder to retrieve the finger. When thefinger is finally retrieved, the game isgenerally repeated, often with theroles reversed. In the “hair” game, onepartner bites a large tuft of hair out ofthe partner’s face or shoulder, and thehair-donor tries to pry the mouthopen to retrieve its hair. The hair ispassed forcibly from mouth to mouthuntil it has all been lost, and then thegame is repeated, sometimes with theroles reversed. In the “toy” game, onemonkey puts an inedible object (astick, green fruit, or piece of bark) inits mouth and the partner attempts toretrieve it. As in the other games, theobject is passed with gentle force frommouth to mouth, and monkeys usetheir hands, feet and mouths to pryopen the partner’s mouth and retrievethe object.

Perry and coworkers23 hypothesizethat these social conventions functionto test social bonds by imposing on apartner, a phenomenon hypothesizedby Zahavi53 and argued to be manifestin olive baboon greetings.54 Several ofthe design features of white-faced ca-puchins’ flexible signals make themparticularly well-suited for testingcommitment to social alliances.23 Ifthe logic of this argument is correct,then it is to be expected that similarsocial conventions might emerge inother species that have complex socialstructures and intense cooperative re-lationships as well, such as some ba-boon and macaque species, and dol-phins.

Interspecific Interactions

It seems plausible that social learn-ing might guide individuals’ attitudestoward allospecifics. However, asidefrom a few studies of predator recog-nition, very little research has ad-dressed this topic. An elegant series ofexperiments by Mineka and Cook26

has demonstrated that social learningis involved in the acquisition of fear ofsnakes in rhesus monkeys. Captive-born monkeys that had no prior expe-rience with or fear of snakes, instantly

The clearest examplesof social conventions ina monkey come fromthe white-facedcapuchin monkey, inwhich five suchbehaviors, all of whichoccur variably bothamong groups and overtime, have beendocumented in a dataset consisting of 19,000hours of observation onthirteen social groups atfour study sites . . .


developed a fear of snakes after ob-serving snake-experienced models ex-hibit fearful responses to snakes.Monkeys who watched models behavenonfearfully in the presence of snakesfor six trials did not show significantenhancement of snake fear after sub-sequent exposure to a fearful model.Although social learning plays an im-portant role in the establishment ofsnake phobias in these monkeys, so-cial learning is less effective in condi-tioning fearful responses to less dan-gerous objects such as flowers.Stimuli that have been associatedwith dangerous situations over evolu-tionary time seem to be more salientto the animals, so that it was possibleto condition monkeys (by havingthem observe a videotaped model) toexhibit fear to toy snakes or croco-diles, but not to flowers or toy rab-bits.55

Because of the high costs of mis-identifying a predator, it makes sensethat social learning rather than trial-and-error learning would be involvedin shaping responses toward potentialpredators, and that identical tradi-tions in response pattern toward pred-ators would emerge across study sites.However, it might be expected thatmore variable group-specific tradi-

tions would emerge regarding interac-tions with less dangerous allospecif-ics, and particularly with species thatare ecologically neutral to the studyspecies. However, a systematic studyof this issue in white-faced capu-chins39,40 revealed surprisingly few in-tersite differences. One allospecific,indigo snakes, which apparently arenot dangerous to capuchins, receivedanti-predator responses from all mon-keys at one site, anti-predator re-sponses from only juveniles at anothersite, and completely tolerant re-sponses at a third site (with one ob-servation of an adult female actuallydrinking in contact with the snake!).Another striking difference was in ca-puchins’ attitudes to howler monkeys.At one site, the capuchins were farmore aggressive to howlers than at theother site. These differences appearednot to be related to greater feedingcompetition at the first site, thoughthe estimate of feeding competitionused was crude. Responses to unfa-miliar humans vary strikingly acrossstudy sites, though it is not clear towhat extent social learning is involvedin shaping these responses. The capu-chins of one site groomed and affili-ated with spider monkeys; this trait isnot observed elsewhere.

Other Traditions

Among the best-documented andmost enigmatic traditions in a mon-key is stone-handling by Japanese ma-caques.47,56,57 While chewing provi-sioned wheat and corn, the monkeysmanipulate stones in various ways in-cluding picking them up, scatteringthem, and sometimes rubbing, carry-ing, clacking, or cuddling them. Thisbehavior is indulged in solitarily, andin fact the post-feeding time period inwhich it occurs is typically used forplaying or grooming when food otherthan hard grains has been consumed.At Arashiyama, the behavior was firstobserved in 1979 and by 1982, after athree-year gap in observation, had be-come very common. The adaptive sig-nificance, if any, of stone handling re-mains unclear; it may be thenonadaptive byproduct of a desire todo something with the hands whilechewing novel food that requires verylittle processing outside of the mouthbut does require lengthy chewing.56

A bathing tradition has arisen atleast twice in free-ranging provisionedJapanese macaques: Juveniles at Ko-shima began bathing in the sea afterhumans threw peanuts into the wa-

Box 1. Transmission Patterns and Learning Mechanisms

What, if anything, can we learnabout learning mechanisms by study-ing transmission patterns of traditionsin the wild? Lefebvre59 argued thatsocial learning could be distinguishedfrom individual learning using data onthe rates at which novel behavioralpatterns spread through socialgroups. Social learning was predictedto produce an accelerating function,as the increase in the number of prac-titioners of the new behavior in-creased the likelihood of naı̈ve indi-viduals being exposed to it,60

whereas individual learning was pre-dicted to produce a nonacceleratingfunction. Based on this line of reason-ing, Lefebvre concluded from avail-able data that 16 of 21 analyzablecases of primate traditions were con-sistent with social learning, and that

all five cases that fit the predictedindividual learning pattern were inJapanese macaques. However, La-land and Kendal61 have recently ar-gued that normally distributed indi-vidual learning abilities in apopulation could produce an acceler-ating pattern even in the absence ofsocial learning (Fig. 1) and, con-versely, that variation in learning abil-ity could cause social learning to pro-duce a nonaccelerating function.Laland and Kendal61 do proposesome alternative methods for detect-ing social transmission (as opposedto asocial learning), but these requirethat the precise timing of the spreadof the trait be documented and thatassociation patterns and/or kinshipnetworks be documented.

Given the lack of experimental con-trols normally available to field re-searchers, it is unlikely that research-ers will be able to distinguish betweendifferent kinds of social learning in thewild unless the animals can be per-suaded to participate in field experi-ments involving methods such astwo-action tests.62 However, oncethe range of learning mechanismspossible for a particular species hasbeen documented by researchersworking in captivity, field researcherscan determine the speed and fidelitywith which behaviors can be trans-mitted via various learning mecha-nisms under varying naturally occur-ring demographic conditions andecological circumstances.


ter,28 and juveniles at Shiga-A beganbathing in hot springs in cold weatherafter becoming habituated to humanpresence.29

Looking beyond the Anthropoideato the Prosimians, use of the sameterritory and scent-marking locationsover a 23-year period by a troop ofring-tailed lemurs has been claimed asa tradition,58 though this case meets

none of the criteria used to constructTable 1.

PROPAGATION SPEED ANDPATTERN

The transmission patterns of tradi-tions in wild populations may shedlight on the learning mechanisms in-volved, though such inferences are

likely to be indirect and contentious(see Box 1). Field researchers can alsodocument how the behavioral domainof a given trait affects its route oftransmission. Different activities suchas foraging and playing and differentlife-history stages27 are characterizedby access to different models. Suchsocial organizational constraints, inaddition to the cognitive constraintsafforded by different social learningcapabilities, must be taken into ac-count when attempting to model so-cial transmission patterns for particu-lar types of traits. During thetransmission phase56,63 of the spreadof nonhuman primate traditions, theorder of acquisition of the behavior isoften affected by age, sex, dominancerank, and kinship or other socialbonds.2,4,56,63,64 In Japanese ma-caques, food processing techniques(potato washing and wheat washing)spread mostly from juveniles to theirmothers and siblings,28 whereas con-sumption of new foods such as fish35

spread mostly from older to youngerindividuals, while stone handlingspread only among juveniles.57

Currently we lack high-quality datasets on the interrelationship betweenassociation patterns, activity, life his-tory stage, and reliability of modelsfor all species except orangutans.27

Such data, once available, will shedlight on the differences in transmis-sion patterns across behavioral do-mains. It is important to distinguishfactors affecting innovation from fac-tors promoting social transmission.For example, as Laland and Hoppit68

point out, subordinate animals areboth more likely to innovate, due totheir lesser access to resources, andless likely to transmit innovations toothers, due to their tendency to oc-cupy peripheral spatial positions ingroups, which makes them ineffectualmodels. The initial acquisition of fish-eating by peripheral adult male Japa-nese macaques may be attributable totheir lack of access to more preferredfoods;35 the slow spread of the behav-ior may be attributable to more cen-tral animals’ lack of opportunity toobserve the initial practitioners of thebehavior. On the other hand, juvenilesare likely to be the most common in-ventors of new food-processing tech-niques because adults have typically

Figure 1. How normally distributed learning abilities could produce an accelerating learningfunction. If a behavior is socially transmitted, an accelerating function such as the logisticfunction (a) is expected to characterize its spread, because as the number of practitioners ofthe behavior increase each naive individual has a higher probability of encountering a prac-titioner.60 However, an accelerating rate of learning could also characterize a behavior ac-quired entirely via individual (asocial) learning, if learning ability and hence, latency to acquirethe new behavior, were normally distributed in the population (b).61 As the behavior wasacquired by the subset of the population indicated by the thickened portion of the line in (b),accelerated spread would occur as indicated by the thickened portion of the line in (a).


already settled on particular tech-niques from which they rarely deviate(Perry, unpublished data). Sociallearning of food-processing tech-niques probably requires closer prox-imity to models than does food choicebecause fine details of motor behaviormust be observed. Hence, it seemslikely that the transmission of food-processing techniques will conformmore closely to the observed associa-tion patterns for that activity thanwould be the case for food choice, an-tipredator behavior, or display tech-niques, all of which are more conspic-uous from a distance. Thus, it is notsurprising that techniques such as po-tato and wheat washing were inventedby juveniles and then spread to theirkin and other close associates.

FUTURE RESEARCH DIRECTIONS

Many monkey species exhibit thesocioecological conditions that arepredicted13,14 to promote social learn-ing and the spread and maintenanceof traditions. In particular, we expectthat traditions are common in capu-chins and the more tolerant macaquespecies,13 that food-choice innova-tions and traditions will be particu-larly detectable in omnivorous spe-cies, and that food-processingtraditions will characterize those spe-cies that engage in extractive foraging.

So why have so few traditions beenreported for free-ranging monkeysother than Japanese macaques? Ei-ther this species is distinctive amongmonkeys in its capacity for generatingtraditions, which seems highly un-likely, or else researchers of othermonkey species have seldom askedthe right questions or collected theright kinds of data to discover tradi-tions, partly because of differences incultural background (see Box 2). Thedetection of traditions in wild primatepopulations is vastly more probable ifseveral (regrettably rare) researchconditions are present. All the follow-ing factors contributed to the discov-ery of traditional social conventions inwild white-faced capuchins12 as wellas the various Japanese macaque tra-ditions.

1. The availability of multiple long-term study sites for the same species.

2. Collection of high-quality ad libi-tum data on innovative behaviors andtheir spread throughout populationsrather than documentation of onlythose parts of the species’ behavioralrepertoire that are directly relevant toresearchers’ current study questions.

3. Regular visiting between sites. Ifresearchers who study the same spe-cies visit one another’s study sites tosee first-hand how their study popula-tions’ behavioral repertoires differ,they will not make the mistake of as-

suming that well-established tradi-tions at their own study sites are partof the species-typical behavioral rep-ertoire.

In cases in which it is logisticallyand ethically feasible, research on so-cial transmission can be enhanced byusing field experiments.68 Althoughethical considerations usually pre-clude translocation experiments inwild primates, it should sometimes bepossible to introduce novel behaviorsinto a population and observe thetransmission dynamics. Judicious useof field experiments can introducesome more experimental control—forexample, the researchers can makethe necessary materials for the taskavailable only to certain individualsunder certain audience conditions,thus producing more complete knowl-edge of the animals’ observation op-portunities.

Since very few experimental studiesof social transmission in the field havebeen performed to date,68 compara-tive studies of the socioecology of tra-ditions will have to rely for the timebeing on less convincing data sets,such as the ones in Table 1, in whichthe source of behavioral variation isnot known precisely, but there is goodreason to suspect that social learningis responsible for the distribution ofvariation.

Box 2. Cultural Primatology and the Cultures of Primatologists

In the long term, the scientific pro-cess transcends the cultural biases ofits practitioners and produces evermore accurate accounts of naturalphenomena.65 But in the short term,particularly in the infancy of scientificdisciplines and subdisciplines, scien-tists’ culturally acquired world viewsmay strongly influence researchquestions and methods and maythereby facilitate or inhibit discoveriesand their dissemination. Such effectsare detectable in the history of thefield now called cultural primatology.Imanishi’s1 call to look for intergroupbehavioral differences initially fell ondeaf ears in the West, as did the core

of the Japanese primatologists’methodological canon, long-term ob-servation of recognized individuals,which is necessary for the discoveryof traditions. This reaction was onlypartly attributable to the fact that al-most all the early Japanese work waspublished exclusively in Japanese.Publication by Japanese primatolo-gists in Western journals, and theconverse, had begun by 1960.66

Western biologists, even thosesteeped in the Darwinian world view,may have been reluctant to attributeto nonhuman animals such quintes-sentially human qualities as individu-ality, thought, and culture, an attitude

traceable to Descartes and beyondinto antiquity.67 In contrast, JapaneseBuddhist tradition, recognizing thecontinuity between human and non-human animal life, facilitated prima-tologists’ contemplation of their sub-jects’ individuality and their capacityfor innovation and tradition. It is per-haps no coincidence that the twononhuman primate species in whichtraditions have been studied exten-sively for many years (Macaca fuscataand Pan troglodytes) also happen tobe two of the species on which Jap-anese researchers have concentratedtheir long-term observations.


ACKNOWLEDGMENTS

We thank Pam Asquith and CharlieJanson for comments on this manu-script, and the Max Planck Institutefor Evolutionary Anthropology for itssupport.

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