182

PRIMATES,26(2) : 182--194, April 1985

Comparison of Object Manipulation Among 74 Speciesof Non-human Primates
TAKASHI TORIGOE
Hiroshhna University

ABSTRACT. Seventy-four primates species (24 genera of six families) were presented with a nylonrope and a wooden cube, and their subsequent manipulations were recorded in detail. Five hundreds
and six manipulation patterns were distinguished on the basis of the actions performed, body-parts
used and relations to other objects. Inter-specific comparisons revealed three groups: (1) lemurs, marmosets, spider monkeys and leaf-eaters; (2) Old World monkeys except leaf-eaters; and (3) cebus monkeys and apes. The first group had the smallest repertoire of manipulations, in which only a few typesof actions and body-parts were involved. The second and third groups had more varied modes ofmanipulation. Actions such as Roll, Rub and Slide, and use of fingers characterized these groups.
Except for the lesser ape, their manipulations were frequently related with other objects. Moreover,actions such as Drape, Drop, Strike, Swing and Throw were typical of the third group. The factors
producing such inter-specific differences in manipulations and the relations to tool use are discussed.
Key Words: Object manipulation; Inter-specific comparison; Phylogency; Tool use.

INTRODUCTION
The variety, versatility and skillfulness of manipulation of non-edible environmental
objects by primates are the most characteristic features which sharply distinguish them from
non-primate mammals. Many researchers of primate behavior have investigated this subject
theoretically and empirically (CANDLA~D & JOHNSON, 1978; CONNOLLY & ELLIOTT, 1972;
DERIAOINA, 1982; JORDAN, 1982; MASON, HARLOW & RUEPING, 1959; MENZEL, 1966;
PARKER, 1973, 1974a, b, 1978; PARKER& GIBSON, 1977; VAUCLAIR& BARD, 1983). However,from the standpoint of making inter-specific comparisons, few empirical data were obtained
systematically under comparable conditions over a wide range of species (except by PARKER,
1974a, b). Comparative evidence is needed in order to elucidate the evolution of object manipulation in primates.
Generally speaking, the similarities observed among species reflect a common ancestor
or similar environmental pressures (WILSON, 1975). The detection of manipulation patterns
specific to a given species or to a given species group can thus serve to clarify factors contributing to the evolution of object manipulation. Comparative evidence o f manipulation is
also needed for placing our own species within the farmework o f primates: object manipulation has been assumed to be a precursor o f tool use, which was and is one of the most effective
strategies of adaptation to the environment especially among human beings. Intensive andextensive analyses of object manipulation in primates may thus help to elucidate the conditions and restrictions underlying the occurrence of tool use and may suggest factors whichhave made our own species the most eminent tool-user.
PA~KER (1974a, b) observed the object manipulation o f as many as 11 species of primates

Inter-specific Comparison of Object Manipulation

183

ranging from the lemur to chimpanzee under comparable conditions and analyzed qualitatively the various aspects of their modes of manipulation. Some of his data indicated speciesspecific modes o f manipulation. However, from these data, it is not possible to distinguisha species-specific pattern from a species group (e.g., genus)-specific one, since he employed
only one species in each group except for the great apes. For example, he reported that rollingthe manipulandum back and forth by the palmar hands was specific to capuchins, whereas
it may not be specific to capuchins but common to all cebus species. In addition, ITANt (1957)
has reported that rolling objects were frequently observed in Japanese monkeys.
The present study extends the work of PA~KE~. As many as 74 species (covering 24 generaof 6 families) were observed under conditions similar to PAP,KER'S, in an attempt to reveal
the characteristic nature of object manipulation in primates and to provide a comprehertsive
and exhaustive framework for further comparative studies on manipulation.
METHODSUBJECTSAND HOUSING CONDITIONSThis study was performed at the Japan Monkey Centre (JMC) and Primate ResearchInstitute of Kyoto University, lnuyama, Japan.
Table 1 provides a list of the species employed and the numbers of subjects observed inthis study. All subjects were housed in outdoor cages in groups of two to seven members,
includirtg at least one adult male and one adult female, of art identical species, except for

Table 1. Species observed. The numbers of subjects are indicated in parentheses.
Lemur catra (5) L. macaco (2) L. variegatus (2)Callithrix penicillata (2) C. ]acchus (3) C. argentata (2)Saguinus weddelli (4) S. labiatus (3) S. mystax (2) S. midas (2)Atetes geoj)i'oyi (2) A. belzebuth (2) A. paniscus (1)Lagothrix lagotricha (2)Cebus nigrivittatus (5) C. capucinus (3) C. apella (7) C. albifrons (5)Saimiri schtreus (6)Callicebus moloch (3)Aotus trivirgatus (2)Macaca syh,anus (3) M. fi~scata fi~scata (3) M. f. yakui (4) M. arctoides (3) M. thibetana (2) A1. nemestrina (2) M. mulatta (3) 3I. assamensis (2) M. eyclopis (4) N/. shzica(2) M. radiata (4) 3I. fascicularis (4) M. silenus (2) ~1. maura (2)Cercopithecus hamO'ni (3) C. petaurista (3) C. aethiops (5) C. albogularis (2) C. ascanius (2) C. I'hoesti (3) C. talapoin (2) C. cephus (2) C. neglectus (2) C. mona (4)C. nigtvvirMis (2)Cercocebus torquatus (2) C. t. hmulatus (5) C. ao's (2) C. albigena (1) C. galeritus (2)C. g. chrysogaster (2)Er)'throcebtts patas (2)AIandrUhts leucophaeus (5) 3I. sphinx (2)Papio hamadryas (2) P. O'nocephahts (2) P. anubis (4)Theropithecus gelada (2)Colobus guereza (1)Presbytis fi'ancoisi (2) P. obscurus (2) P. pileatus (2) P. entellus (3) P. cristatus (5)Nasalis larvatus (5)Hylobates lar (2) H. agillis (2) H. moloch (1) H. klosii (2)Symphalangus syndactyhts (2)Pongo p)gmaeus (4)Pan troglodytes (5)Gorilla gorilla (2)184

T. TORIGOE

Ateles paniscus, Colobus guereza, and Hylobates moloch which were housed individually,
and Cercocebus albigena and C. galeritus which were housed in a cage. Some groups included
infants (less th~.n one year old), the data of which were excluded from analysis, since a pilot
study on Japanese monkeys had indicated that the manipulation patterns of infants werequalitatively different from those o f other members.
The standard home cage measured about 2 • 2 • 3 m, varying according to the group sizeand species concerned: it was larger for a great ape and smaller for a marmoset. The floor
and one of the walls of the cage were made of concrete and the ceiling and other three walls
were made of wire-mesh. All cages were equipped with a water vessel and some wooden
perches. The subjects were fed daily in the morning and late afternoon.
PROCEDURES

The observational procedures were similar to those o f PARKER (1974a, b), except for the
manipulanda and the observational setting. Two manipulanda were employed in the present
study. One of them consisted of a white three-strand nylon rope with two knots made at eachend to prevent loosening, measuring 120 cm in length and 10 m m in diameter for great apes,
60 cm in length and 4 m m in diameter for marmosets, and 90 cm in length and 7 m m indiameter for other species. The rope was not attached to the cage, in contrast to PARKER'S
studies, since a pilot study had indicated that an unattached rope elicited a greater variety ofmanipulation patterns than an attached one. The other manipulandum was a wooden cube
measuring 3 :~ 3 • 3 cm for great apes, 1 • 1 • 1 cm ~br marmosets and 2.5 • 2.5 • 2.5 cm forother species.
The experiments were performed in a social setting, which was also shown in the pilot
study to inhibit or eliminate neophobia towards novel objects placed in the cage. The experimenter placed the manipulandum in the group cage, and recorded the subject manipulating
it and the mode of manipulation in detail for 45 min. Ortly qualitative aspect of the manipulation were recorded: quarttitative aspects such as frequency or duration were not recorded.
When the manipulandum was left alone for more than 20 min, the observation was brought
to art end. Data were obtained from as many subjects of the species concerned as possible.
Therefore, second and, if necessary, third manipulanda of the same kind were placed in thecage and focused on, in cases where one subject held the manipulandum exclusively for morethan 20 min. Subjects were neither deprived of food before the experiment nor rewarded for
manipulations carried out. Each species received one session with each manipulandum.

RESULTSCATEGORIES OF MANIPULATION PATTERNSIn this study, manipulation was defined as any physical contact with the manipulandum
placed in the cage, except for incidental contact. Therefore, visual exploration and sniffing
without making physical contact were not recorded as manipulations. Each manipulation
pattern consisted of three compov.ents: actions performed, body-parts used and the relation
to other objects or the substrate.
Five hundreds and six manipulation patterns were identified, of which 254 were observed
only for the rope, 157 only for the cube, and 95 for both.

Inter-specific C o m p a r i s o n o f Object M a n i p u l a t i o n

185

The third component involved two types of manipulation: primary manipulation andsecondary manipulation. The former was defined as object manipulation with no relation toanother object or in global relation to the substrate. The latter was defined as object manipulation in relation to some specific feature of the environment. For example, rolling the manipulandum on the floor was classified as primary, while roiling it in the water vessel wasclassified as secondary. Two body-parts pulling the rope in opposition to each other wasclassified as primary, while the same action by way of the wire-mesh was classified as secondary. Of the 506 manipulation patterns, 449 were primary and 57 were secondary manipulations.
Table 2 shows the kinds of actions and the numbers of kinds of primary manipulation
patterns in which each action was performed. Twenty-one actions were distinguished, of
which one was only for the wooden cube, six were only for the rope, and the others werefor both. Most of the secondary manipulations included the same actions as the primaryones, while some were specific to the secondary manipulations, as described elsewhere inthis paper.

Table 2. Categories of actions artd their definitions. T h e n u m b e r s of m a n i p u l a t i o n p a t t e r n s are indicated in parentheses.
Drape ([6):
placing the maniptdandum over a body-part
Drop (4):releasing the manipulandum, not including passive dropping
Flip (9):flipping the manipulandum sideways or upward with rapid finger action, little or
no arm movement
Mouth (13):touching orally, biting or licking the manipulandum
Passive hold (10):holding, resting on or sitting on the manipulandum without movement
Pick up (19):lifting the manipulandum up off the floor
Pull (19):
two or more body-parts pulling the manipulandum in opposition to each other
Push or Press (19): applying pressure on the manipulandum with a body-part without moving it
Roll (43):rolling the manipulandum against the floor, wall or a body-part
Rotate (3):turning the manipulandum in the hands or lips
Rub (60):
rubbing the manipulandum against the floor, wall or a body-part
Shift (29):moving the manipulandum on the floor without picking it up off the floor
Slide or Stroke (71): moving a body-part along the surface of the manipulandum or sliding the manipulandum across a body-part by pulling it
Strike (26):striking the manipulandum with a body-part or striking something with it
Swing (28):waving or shaking the manipulandum in an alternating or circular motion
Throw (14):throwing the manipulandum
Touch (18):touching the manipulandum without manipulating it further
Transfer (9) :changing the holding state, e.g., from oral holding to manual holding
Transport (24):locomotion while holding the manipulandum
Untwist (14):untwisting the rope strands, including actions attempting to untwist and actions
with a strands-untwisted rope
Wad (l):making a compact mass or wad

The body-parts were classified imo 18 categories. Table 3 shows the numbers of kinds ofmanipulation patterns in which each body-part was engaged. The sum of the manipulation
patterns exceeds 506 because most of the manipulation patterns were related with two or
more bodyparts.
COMPARISON OF MANIPULATION PATTERNSIn the following analysis, an inter-species group comparison was performed for each

186

T. TORIGOE

Table 3. Categories of body-parts used and the numbers of kinds of manipulation patterns in which
each body-part was engaged.
Head and Neck
20
Face, excluding mouth
4
Body trunk
17
Feet and Legs
73
Mouth and Lips
75
Arms
19
Hands and/or fingers not moving independently or used non-opposably
Palmar side
393
Radial side
4
Ulnar side
6
Dorsal side
16
Fingers moving independently or used opposably
Finger I
12
Finger I[
21
Finger III
1
Fingers I-I[
12
Fingers II-III
7
Fingers III-IV
2
Finger V
1
Fingers I-V
4componertt as well as an inter-specific one. For the former analysis, 11 groups of species wereselected mainly on the basis of genus: (1) lemurs (Lemur), (2) marmosets, including Callithrix
and Saguinus; (3) spider monkeys, including Ateles and Lagothrix; (4) cebus monkeys (Cebus); (5) macaques (Macaca); (6) guenons (Cercopithecus); (7) mangabeys (Cercocebus);(8) baboons, including Papio, Mandrillus and Theropithecus; (8) leaf-eaters including Colobus,
Presbytis and Nasalis; (10) the lesser apes, including Hylobates and Symphalangus; and (11)the great apes including Pongo, Pan and Gorilla. Saimiri sciureus, Callicebus moloch, Aotus
trivirgatus and Erythrocebus patas did not belong to any of these species groups. The species
groups corresponded partially to the ten species observed by PAR~ER (1974a, b).
Figure 1 shows the numbers o f kinds of manipulation patterns observed in each species.
0
I

I

lemur
marmoset

I

i

I

50
I

I

I

I

I

100

~,
~

spider ~
9

cebus

9

~

macaqueguenonmangabey

~-w

w
~

9

9

baboonleaf-eaters
lesser apessrea~ apes

Fig. 1. Numbers of kinds of manipulation patterns observed in each species. Each dot represents asingle species.

Inter-specific Comparison of Object Manipulation

187

The score for each species was counted from the pooled data for the subjects of the species
concerned. (Similarly, the scores for each species described below were calculated from thepooled data for subjects of that species.) The results indicate that the great apes and cebusmonkey have the most varied repertoire of manipulations. The lesser apes, macaque, guenon,
mangabey and baboon form the next group having various modes of manipulation, akhough
there is great variety within each species group. The lemur, marmoset, spider monkey andleaf-eaters have the fewest modes of manipulation. The rank order of the species groups
resembles that of the diversity measures reported by PARKER (1974a, b), except that thecebus monkey and guenon occupy a higher rank and the lemur a lower rank.
Actions
Figure 2 shows the median numbers of kinds, for each species group, of manipulation
patterns, in which each action was performed. Pick up, Mouth and Transport were observedin all of the species groups, suggesting that these actions are primate-common ways of manipulation. Rotate, Transfer, Pull and Passive hold are also considered to be primate-common,since these actions were observed in 9 or 10 out of the 11 species groups. The lemur, marmoset, spider monkey and leaf-eaters performed exclusively these primate-common actions andvery rarely other actions.
Roll, Slide and Rub are dominant actions in Old World monkeys (except for leaf-eaters),
the cebus monkey and great apes (apart from Roll). In addition, some details of manipulation differed among these groups. For example, rolling the manipulandum on the floor,back and forth, with one hand or with both hands in coordination formed commort manipulation patterns in these groups, while rolling in an alternate motion of both hands was typicalof the macaque and guenon. Rubbing the manipulandum against the substrate with a palmar
hand pressing the substrate was commonly observed in four species groups of Old World
monkeys and the cebus monkey, but rarely in the great apes, in which rubbing against the
subject's own body parts was typical.

.......

~.o. / / / / / / / / / / / / ~ / / / / / d / /o~,,'~///VH~/.V/.V~VP///VV//.... , , o - / / / r 1 6 2//<. . . . . / / / V / / / / V / V / ( / / / / / V / /o~<:~o,,///(VVV/V/V/V////VV//~-o~"11 ~ ( l i d / V / P / V / / / ~ I V / /,~ o.~_,]-/iiillV I I11 I11 / I I V / i /~~/ _ / W / I V i / V l l i l l , / l r<,;]{ .,],~V / IVVVVl IIVCVVVr
Fill, 2, Median numbers of kinds of manipulation patterns in each action,

188

T. TORIGOE

Drop, Drape, Swing and Throw are typical o f the cebus monkey, the lesser and the great
apes (apart from Drop). In these actions, some differences were observed among the species
groups. Swing can be divided into rapid movement or shake (l 7 kinds o f manipulation patterns) and slow movement or wave (11 kinds). Shake was rather dominant in the lesser apes
(the median number o f kinds o f manipulation patterns in the species o f that group was 11)
and in the great apes (median number, six kinds), as opposed to the cebus monkey (threekinds). On the other hand, wave was dominant in the cebus monkey (five kinds) as opposedto the lesser and the great apes (one and two kinds, respectively). Another difference wasthat the cebus monkey threw the manipulaxtdum mainly upwards with the elbow stretched;
the lesser apes with the wrist dorsiflexed or adducted; and the great apes with a swinging arm.
Strike is another characteristic action observed in the cebus monkey and the great apes.
This action can be further divided into two categories: striking the manipulandum with thebody-parts (7 kinds of manipulation patterns) and striking the substrate with the manipulandum grasped (19 kinds). In the cebus monkey, the latter category showed a greater variety o fmanipulation patterns (17 kinds) than the former (2 kinds), in contrast to the great apes
(6 and 3 kinds, respectively).
The next step in the analysis examined the relations among the species groups on the basisof the occurrence of each action. A 74 (species) • 21 (actions) one-zero matrix was subjected
to HAYASHI'S quantification model lII analysis I~ (HAYASHI, 1952), which is a useful tool for
rearranging similar items nearer and different items farther away in a multi-dimensional
space. Two axes were extracted, whose eigenvalues were 0.1514 and 0.1002 (the correlation
coefficients between species and actions were 0.389 artd 0.316, respectively). Figure 3 shows
the distribution o f actions in the two-dimensional space. The primate-common actions
described above were distributed around Jaegative values o f axis I and positive values ofaxis II. Drape, Drop, Strike, Swing, Throw and Untwist were distributed around positive
values of both axes. The other actions were distributed around negative values of axis II.
Each species was also plotted in this two-dimeasionM space. For information reduction,
the mean normalized score in each species group is plotted in Figure 4. The 11 species groups
can be classified further into three groups: first, the lemur, marmoset, spider monkey andleaf-eaters; second, macaque, guenon, mangabey and baboon; and third, cebus monkey,
and lesser and great apes. Axis I is similar to the rank order of diversity measures reported
by PARKER (1974a, b). This axis was therefore assumed to reflect the diversity of manipulation. Axis II was unique in the present study. Most of the actions distributed around negativevalues of axis II were actions in relation to the substrate, such as Shift, Rub, Flip, Roll andPush. On the other hand, most of the actions distributed around positive values of axis II
did not necessitate the substrate. This axis can therefore be said to reflect substrate-related or
substrate-non-related actions.

Body-parts
Figure 5 shows the percentages o f body-parts used in relation to the total kinds o f manipulation patterns observed in each species. The palmar side o f the hand was involved mostdominantly; roughly 9 0 ~ of the manipulation patterns were performed by this body-part.
1) This analysis was performed with HITAC M-180 at the Information Processing Center of Hiroshirrm University, using the Program Package for Social Science II (PPSS II).

Inter-specific Comparison of Object Manipulation

189

II
9

l~outhTransfer
Fick upTransport
Rotate9
Touch

9

9

9

Untwist9
9

Passive

~ft
Pull
Elide
9

Flip9

FGIi
9 9 Push

Fig. 3. Distribution of actions m two dimensions extracted by HAYASHI'Squantification model III
analysis.

IIl'lesser apes

spider~]zrea~ a p e ~ +I leaf-earers

guenonIK~

busmangabey
macaque,~
I baboonFig. 4. Distribution of species groups in two dimensions extracted by HAYASHI'S quantification model
III analysis. The horizontal and vertical lines across each dot represent 2 SDs of the normalized
scores.

Little difference among species group was noted. The mouth was also used dominantly by all
species, hi particular, the marmoset and lemur tended to manipulate orally more dominantly than the other groups. The feet were markedly used by the lesser apes. They grasped,
picked up, mouthed, transported, transferred, etc., by feet frequently, in contrast to otherspecies performing the same actions c o m m o n l y by hand.
Use o f the fingers moving opposably to or independently o f each other was frequently

190

T. TORIGOE

observed in the macaque, guenon, mangabey, baboon, lesser ape and great ape species. The
most popular mode o f finger use was that involving the thumb and index finger or thumb andother fingers opposably. Of 48 species in which finger use was recorded, 35 species utilized
this mode most dominarttly. As for the other firtger uses, that involving the irtdex finger alone
was characteristic of the gelada baboon (14 700)and chimpanzee (11.9 ~o), as opposed to otherspecies (less than 7 ~). For example, fixing the manipulandum with the index finger followedby mountirtg was observed in the chimpanzee; picking the manipulandum up with the irtdex
finger was observed in the chimpanzee; pressing it with the index finger in the gelada baboon
and chimpanzee; pressing the edge o f the cube against the floor with one index finger or both,and making it roll in the gelada baboon; and touching and shifting it with the index finger
irt the chimpartzee.
As for the other body-parts, use o f the head and neck was typical in the cebus monkey,
the lesser and the great apes (3.3, 5.3 and 4.8 ~o, respectively; 0 ~o for others); arm use wastypical in the cebus mortkey, the lesser and the great apes (3.9, 2.3 artd 5.6 ~ , respectively;
100

50
HAND

T t

MOUTH

"~
FINGERS

w

0

~

~

~

~

o~

~

o~

~

~

Fig. 5. Percentages of occurrence of body-parts to the total numbers of kinds of manipulation patterns. Each dot represents a single species.

Inter-specific Comparison of Object Manipulation

191

0 ~ for others); use of the body trunk in the cebus monkey and the great apes (0.8 and 3.6 ~,respectively; 0 ~ for others); face use in the great apes (2.4 ~o; 0 ~ for others); use of theulnar side of the hand in the cebus monkey (1.4 ~ ; 0 ~/ofor others); and use of the back of thehand in the cebus monkey and the great apes (0.7 and 5.6 ~, respectively; 0 ~ for others).
Thus, the great apes and cebus monkey manipulated the manipulandum with the most varied
parts of the body; and the lesser apes with more varied parts than other species groups except
the great apes and cebus monkey.

Secondary manipulations
Figure 6 shows the numbers of kinds of secondary manipulations observed in each species.
The rank order is similar to that of the other manipulation parameters described above: thegreat apes show the highest rank; the next ranking group consists of the cebus monkey and
Old World monkeys except leaf-eaters; and the lemur, marmoset, spider monkey and leafeaters show the lowest ranks. It should also be noted that the lesser apes did not perform thistype of manipulation.
The main features of the environment, in relation to which subjects acted on the manipulandum, were wire-mesh (20 kinds of manipulation pattern) and water (28 kinds). Mostof the secondary manipulations in relation to wire-mesh or water involved the same actions
as the primary manipulations. However, some actions were unique to the secondary manipulations: chimpanzees floated the cube on the water and poked it with their finger tips; atoque monkey pushed the end of the rope out of the wire-mesh and pulled it through at
another place in the wire-mesh, repeating these actions as if sewing the wire-mesh with therope; and an orang-utah held both ends of the rope with each hand through the wire-meshand twisted the rope, making another rope.
The remainder of the secondary manipulations were related to rather accidental objects
which were not aw.ilable to all of the species: one orang-utah placed the cube repeatedly
into and out of a suspended tire; the same subject put the food on the cube; one chimpanzee

9 ....

,5,,,,lo

+s

,,

,r

lemur
marmoset ~|spider 9|
cebus
macaque IAwv

guenon 9
mangabey ~baboon 9 r

9leaf-eaTers i|lesser apes i|great apes

99Fig. 6. Numbers of kinds of secondary manipulations observed in each species. Each dot represents

a single species.

192

T. TORIGOE

pressed feces with the cube held manually; and a juvenile Cercopithecushamlyniwrapped the
cube with a cabbage leaf which had been placed in the cage for food.
DISCUSSION
CHARACTERISTIC NATURE OF MANIPULATIONS

The object manipulation of 74 primate species was observed under comparable conditions,and 506 manipulation patterns were distinguished on the basis of the actions performed,
body-parts used, and relations to other objects.
The results of art inter-species group comparison showed that the 11 groups of species
could be further classified into three groups:first, the lemur, marmoset, spider monkey andleaf-eaters; second, the Old World monkeys except leaf-eaters; and third, the cebus monkey,
the lesser and the great apes. The first group had the smallest repertoire of manipulations.
The primate-common actions, such as Pick up, Mouth and Transport, artd the body-partscommonly used by all the species, such as the/land and mouth, were mainly involved in the
manipulation modes displayed by this group. In addition, such manipulation patterns weredirected only towards the manipulandum presented, and in no relation to other environmental objects. In this group, differences among species groups and within each species groupwere not eminent.
The second group had more varied modes of manipulation than the first. The actions
characterizing this group were Roll, Slide and Rub, although some details of the manipulation patterns produced by these actions differed among the species groups. Use of the fingers
moving opposably to or independently of each other was also typical of this group.
The third group displayed the most varied repertoire of manipulations. Almost all theactions and body-parts were involved in their manipulations. In particular, Drape, Drop,
Strike, Swing and Throw characterized this group. In addition, their manipulations were
frequently related to other environmental objects, although the lesser apes were an exception.
Some species-specific features of the manipulations were also indicated. For example, useof the index finger was typical of the gelada baboon and chimpanzee; use of the ulnar sideof the hand was typical of some species o fcebus monkeys: and most of the secondary manipulations were species-specific as reported by PAt',KER (1974b). In addition, a species-specificmanipulation pattern could be distinguished from a pattern specific to a species group.
PA~KER (1974b) reported that rolling a rope on the floor, back and forth, with palm was
specific to capuchins; however, the results of the present study showed that this manipulation
pattern is observed not only in other species of cebus monkeys, but also in most of the oldworld monkeys.
EVOLUTION OF MANIPULATIONSThe next step is to attempt to specify those factors responsible for the differences andsimilarities in manipulations among the species revealed in the present study. Anatomicaldifferences among species can be considered to account for some of the differences in manipulation. For example, the lemur and marmoset cannot move each finger independently because of their anatomical restrictions. The leaf-eaters and spider monkey have shortened
thumbs or no thumb at all, which are disadvantageous for complex manipulations (CONNOLLY & ELLIOTT, 1972; NAPIER, 1961). However, anatomical restrictions cannot account forInter-specific Comparison of Object Manipulation193

all the differences among species. It is unlikely, for example, that macaques do not strike theobject against the floor as cebus monkeys do because of some anatomical constraint.
PA~,KER artd GmSON (1977) reported that the apes and cebus monkeys were superior in
object manipulation and tool use to other primate species and discussed their evolution fromthe standpoint of feeding adaptation. PARKER (1978) assumed that the great diversity ofmanipulation in great apes had evolved through feeding adaptation as generalists. The findings of the present study support this assumption in part because many of the manipulation
patterns described here occur really in the feeding context: Pick up, Mouth, Transport,
Transfer and Rotate are commonly observed when animals treat their food and eat; somecebus monkeys strike hard-shelled nuts against wood trunks and open them before eating thecontents in their natural habitat (IZAWA & MIZUNO, 1977); and Japanese monkeys mayroll or rub their food frequently before eating it (ITANI, 1957; KAWAI, 1965). Nevertheless,
it is unlikely that other manipulation patterns such as Throw, Drape and Drop are related
to feeding. In chimpanzee, throwing or dropping an object was not observed in the context
of hunting prey animals or cracking objects, but was in the agonistic context (PARKEP, &GIBSON, 1979; SU6IYAMA & KOMAN, 1979). Orang-utans were found to swing on some
artificial objects or branches for locomotion (CHEVALIER-SKOLNIKOFF,GALDIKAS& SKOLNIKOEF, 1982; LETHMATE, 1979). It is clearly more appropriate to regard species-specific or
species group-specific features of object manipulation as having evolved not only throughfeeding adaptation, but also in other behavioral contexts. Thus, multiple factors must be
considered when examining the evolution of manipulation. Observations of manipulationin various behavioral contexts within the natural habitat are needed in order to specify theprecise factors corttributing to the evolution of species-specific modes of manipulation.
PRECURSORS OF TOOL USE: SECONDARYMANIPULATIONSObject manipulation is assumed to be a precursor of tool use (PARKER, 1974b). In orderthat art object caa serve as a tool, the animal must relate the object with another unfixed
object (BECK, 1980). In this respect, the secondary manipulations occupy the nearest place
to tool use.
One of the priacipal findings concerning secondary manipulation was that lesser apes did
not perform this type of manipulation. ABOROO (1976) noted the rarity of tool use in lesser
apes and concluded that this was due to their limited manipulative dexterity. However, thepresent study and the work of PARKER (1973, 1974a, b) have demonstrated a great variety
of manipulation in them comparable to that of the great apes and the Old World monkeys
except leaf-eaters. It may be more appropriate therefore to consider that tool use does notarise from the variety of manipulatious but from the extent to which the animal relates theobject with other objects. There were only a few unfixed objects available to be related to the
manipulandum in the observational setting of the present study. Data should therefore be
obtained systematically under a more complex setting concerning how the animal relates
the manipulartdum to environmental features, later-species comparisons based on such data
would contribute to clarifying the new aspects of tool use and tool manufacture.

Acknowledgements. This study was supportd financially by the Primate Research Institute of Kyoto
University as a Cooperation Research Program. I wish to express my gratitude to Mr. T. MATSUZAWA, Instructor at the Primate Research Institute of Kyoto University, Mr. S. KODERA,Director of
the Zoological Garden of JMC, Mr. J. YAMAOIWAand Mr. Y. HAMADA,Research Fellows at JMC,

194

T. TORIGOE

for their invaluable help and support during this study. I also wish to express my gratitude to Mr. T.
MATSUZAWAand Mr. Y. HABU, Professor of Hiroshima University, for their helpful comments inthe preparation of this manuscript.
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- - R e c e i v e d September 7, 1984; Accepted Jamtary 28, 1985
Author's Name and Address: TAI<:AS~TORIGOE. Department of Psychology, Faculty of Education, Hiroshima
University, 1-1-89 Higashisenda-machi, Naka-ku, Hiroshhna, 730 Japan.