Journal of Comparative Psychology Copyright 1997 by the American Psychological Association, Inc. 1997, Vol. 111, No. 2, 159-173 0735-7036/97/$3.00 Development of Stone Tool Use by Wild Chimpanzees (Pan troglodytes)

Noriko Inoue-Nakamura Tetsuro Matsuzawa Kwansei Gakuin University Kyoto University

At the age of 3.5 years, wild chimpanzees at Bossou, Guinea, begin to use hammer and anvil stones to crack oil-palm nuts to get the kernels. To clarify the developmental processes, the authors did a field experiment in which stones and oil-palm nuts were provided. Infant chimpanzees' stone-nut manipulation was observed and video recorded. Data were collected from 3 infants younger than 4 years old from 1992 to 1995. The authors analyzed 692 episodes of infants' stone-nut manipulation and 150 episodes of infants' observation of nut cracking performed by adults. Infants observed other chimpanzees' nut cracking and got the kernels from them. The stone-nut manipulation developed from a single action on a single object to multiple actions on multiple objects. Although infant chimpanzees at the age of 2.5 years already acquired basic actions necessary for nut cracking, they did not combine the actions in an appropriate sequence to perform actual nut cracking.

The acquisition of tool-use behavior is a sort of problem- tool-using skills indicated the cognitive capacity of the solving task and inevitably reflects cognitive development. children and the emergence of strategies to solve a pm-tic- Connolly and Dalgleish (1989) examined the developmental ular problem. Thus, it is important to investigate tool-using change of a spoon-using skill by human children younger skills for understanding the cognitive development of hu- than 2 years old. They suggested that the acquisition of man children. In an evolutionary context, it is also important to study tool-use behaviors in chimpanzees (Pan troglodytes), the Noriko Inoue-Nakamura, Department of Psychology, Kwansei species genetically closest to humans. So far there have Gakuin University, Nishinomiya, Japan; Tetsuro Matsuzawa, De- been a number of observations about the various kinds of partment of Behavioral and Brain Sciences, Primate Research Institute, Kyoto University, Inuyama, Japan. tool use by chimpanzees in the wild (e.g., Goodall, 1970, The present research was financed by Grant 01041058 from the 1986; McGrew, 1992; Nishida & Hiraiwa, 1982). However, International Research Program of the Ministry of Education, as far as we know, there have been few studies in the wild Science, Sports, and Culture, Japan. Preparation of the article was on the acquisition processes of tool-using skills (Boesch, supported by the Fellowship of the Japan Society for the Promo- 1991a; Matsuzawa, 1994). Although there were a couple of tion of Science for Japanese Junior Scientists (No. 0801). The field studies in groups of captive chimpanzees (Hannah & study was carried out with the collaboration of the Direction McGrew, 1987; Sumita, Kitahara-Frisch, & Norikoshi, Nationale de la Recherche Scientifique et Technique, R6publique 1985), no previous studies in the wild have reported the de Guin6e, and the villagers at Bossou. We wish to thank Yukimaru Sugiyama, who has conducted field quantitative analysis of behavioral change from an ontoge- research at Bossou since 1976 and who gave us the opportunity to netic perspective through direct observation and video do this research. Special thanks are due to the following colleagues recording. during the research periods: Rikako Tonooka, Gen Yamakoshi, Among the tool-use behaviors in the wild, nut-cracking Jeremy Koman, Guano Goumy, and Tino Camara. A part of the behavior is of special interest because it is the most "com- video-recorded data (February-March 1994) was collected by R. plicated" tool use chimpanzees perform. It basically con- Tonooka. We also express our thanks to members of the Japanese sists of the following actions: (a) picking up a nut, (b) Embassy in the R6publique de Guin6e and C6te d'Ivoire and the putting it on an anvil stone, (c) holding a hammer stone, (d) Japan International Cooperation Agency of C6te d'Ivoire. The preparation of the manuscript was done during the period when hitting the nut on the anvil stone with the hammer stone, and Noriko Inoue-Nakamura stayed at the Department of Ecology and (e) picking up the kernel in the cracked hard shell and eating Evolutionary Biology, Princeton University. We wish to express it. This behavior is characterized by the collaboration of our thanks for the helpful comments on an earlier draft made by bimanual and asymmetric manipulation. The chimpanzees Alison Jolly. Noriko Inoue-Nakamura is grateful to Hiroshi Imada at Bossou, Guinea, use a pair of stones as a hammer and an for his generous guidance throughout the present study and also anvil to crack open oil-palm nuts to get the kernels (Sug- thanks Katsuki Nakamura for invaluable suggestions on data anal- iyama & Koman, 1979b). This tool-use behavior has been yses and constant encouragement. Correspondence concerning this article should be addressed to reported only among chimpanzees of a limited area of West Noriko Inoue-Nakamura, who is now at the Department of Behav- Africa (Boesch, Marchesi, Fruth, & Joulian, 1994; Kort- ioral and Brain Sciences, Primate Research Institute, Kyoto Uni- landt, 1986; McGrew, 1992; Sugiyama, 1993). No chim- versity, Inuyama, Aichi, 484 Japan. Electronic mail may be sent panzees in East Africa have been observed to crack nuts via Internet to [email protected]. with stones although stones and nuts are available (Goodall, 159 160 1NOUE-NAKAMURA AND MATSUZAWA

1986; Nishida, 1990). Nut cracking with stones is a strong folding for drinking water (Tonooka, Inoue, & Matsuzawa, 1995), example of the diversity of material culture among and pestle pounding for extracting sap from oil-palm trees (Sug- chimpanzees. iyama, 1994b; Yamakoshi & Sugiyama, 1995). In the field, however, it is difficult to directly observe nut This study focused on 3 infant chimpanzees younger than 4 years old in January 1995: Yolo, Fotayu, and Vuavua. The subjects cracking of chimpanzees because the bush beneath the palm were observed for 4 years. The longitudinal data of the 3 infant trees is thick, and also because the chimpanzees are too chimpanzees were divided into four age groups: 0.5 (0-1 year timid to be observed when they are in the secondary forest old), 1.5 (1-2 years old), 2.5 (2-3 years old), and 3.5 (3-4 years near the village where palm trees are. Therefore, field old). Table 1 shows the information about each age"group. Chim- experiments have been carded out at Bossou since 1987 to panzees younger than 4 years old are usually classified as "in- study chimpanzees' tool-use behavior in detail. An outdoor fants." Weaning occurs around age 2.5 to 3 years. The interbirth laboratory was established in the central part of chimpan- interval is about 4 to 6 years. Length of life is estimated as 40 to zees' free-ranging area where stones and oil-palm nuts were 50 years (Goodall, 1986). provided by the experimenters (Fushimi, Sakura, Matsu- zawa, Ono, & Sugiyama, 1991; Matsuzawa, 1991, 1994; Procedure Sakura & Matsuzawa, 1991; Sugiyama, Fushimi, Sakura, & Matsuzawa, 1993). Observational periods. The present study reports the field The present study aims to investigate the developmental experiments and the behavioral observation done during four dry process of the tool-use skill from the point of ontogenetic seasons: (a) January 1992 (18 days), (b) December 1992 to January view. The field experiments have revealed that chimpanzees 1993 (20 days), (c) January 1994 (5 days) and February to March at Bossou younger than 3.5 years old cannot perform nut 1994 (30 days), and (d) January 1995 (21 days). Table 1 also provides general information about the records of observation: the cracking (Inoue, Tonooka, & Matsuzawa, 1996; Matsu- days we observed, the total time of observation, and the number of zawa, 1994). The purpose of the present study was to parties that visited the outdoor laboratory. answer the following questions by means of behavioral Setting. In general, about 50 stones and approximately 2-5 kg observations and an analysis of video-recorded data in the of oil-palm nuts (Elaeis guineensis) were provided at an outdoor outdoor laboratory: How do infant chimpanzees younger laboratory sized 10 m wide by 5 m deep. The observer hid behind than 3.5 years old acquire nut-cracking skill? What kind of a screen made of grass about 4 m long and 2 m high. The distance social influences are involved in the acquisition process? between the observer and the cracking site was about 20 m. The observer stayed there continuously from 7 a.m. till 6 p.m. All behaviors were directly observed and videotaped (Sony, CCD- Method TR3) for further analysis. Figure 1 shows a representative scene of nut cracking by chimpanzees in the outdoor laboratory. Subjects The subjects of this study were wild chimpanzees (Pan trogl- Data Analysis odytes) at Bossou, on the southeastern edge of the Republic of Guinea, West Africa. There was a group of 18-19 chimpanzees at Definition of behavioral episodes and observational episodes. Bossou during the present study of 1992-1995. Focal animal sampling was performed on all of the video-recorded The chimpanzees at Bossou have been investigated without data of the 4 years (4,674 min total). The target behaviors were (a) supplemental feeding since 1976 by Sugiyama and his colleagues manipulation of stones and/or nuts and (b) observation of the other (Sugiyama, 1984, 1988, 1994a; Sugiyama & Koman, 1979a, chimpanzees that performed nut cracking. 1987). Each member of this group has been identified. Chimpan- We defined a behavioral episode as infants' manipulating stones zees at Bossou show various tool-use behaviors, such as nut and/or nuts by themselves. As a definition, the episode started cracking, ant catching (Sugiyama, Koman, & Sow, 1988), leaf when the chimpanzee contacted stones and/or nuts and ended

Table 1 Composition of Age Group and Total Record of Observation Subject age (year:month) Records of observation Groups of Study Time age (years) period Yoloa Fotayu Vuavua Daysb (in min) Parties c 0.5 1992 0:2 0:7 0:7 17/18 1,441 44 (6.2) 1.5 1993 1:2 1:7 1:7 17/20 1,620 59 (5.5) 2.5 1994 2:2 2:7 2:7 19/35 518 40 (6.4) 3.5 1995 3:2 3:7 3:7 15/21 1,095 42 (6.3) a Male subject, bin the observational days, the first number represents the days in which the chimpanzees were actually observed, and the second number represents the days in which the observers waited for the chimpanzees in the outdoor laboratory, c One party means a group of chimpanzees that come to the outdoor laboratory. As a definition, a party lasted from the point when the first chimpanzee came in to the point when the last one left. Therefore, the size of one party could vary from 1 chimpanzee to all of the 18-19 chimpanzees. The number in parentheses represents the mean party size. STONE TOOL USE BY CHIMPANZEES 161

Figure 1. Nut cracking by chimpanzees in the outdoor laboratory. when the subject moved without contacting stones and/or nuts. In vided into two classes according to the total number of objects other words, each behavioral episode continued as long as each manipulated in a behavioral episode: a single object (Class A-I) subject did not change the sitting spot and also when the subject and multiple objects (Class A-2). The behavioral episodes belong- moved while contacting the same stones and/or nuts (e.g., trans- ing to Class A-1 were further divided into two classes according to porting stones and/or nuts or stepping on stones). the variety of actions: a single action (Class A-l-i) and multiple As to their observing the other chimpanzees that performed nut actions (Class A-l-ii). The behavioral episodes belonging to Class cracking, we recorded it as an observational episode. It did not B were subdivided into two classes according to the relation of matter whether there was physical contact between the performer objects manipulated simultaneously: no relation at all (Class B-l) and the infants or not. For the definition of the observational or any kind of relation among objects (Class B-2). Finally, the episode, it was required that the subject's face was oriented to the behavioral episodes in which a subject successfully hit a nut on a performer for 3 s or more from less than 1 m away. stone with another stone were classified into Class C. Each class of Definition of fundamental actions. We postulated that each A-l-i, A-l-ii, A-2, B-l, B-2, and C is described as "a single action behavioral episode could consist of single fundamental action or on a single object," "successive actions on a single object," "suc- various combination of fundamental actions. Fundamental actions cessive actions on multiple objects," "simultaneous actions on on stones and those on nuts were separately defined and listed in multiple objects while no relation among objects," "simultaneous Table 2. The number and sequence of fundamental actions in- actions on multiple objects while any relation among objects," and volved in a behavioral episode could vary. The duration of a "nut cracking," respectively. behavioral episode was also different among the episodes. Each behavioral episode was coded according to this hierarchi- A coding system of behavioral episodes. First, the behavioral cally organized, mutually exclusive and exhaustive system. The episodes were divided into two main categories: manipulation of highest code was recorded for each behavioral episode. stones and/or nuts while not in physical contact with the other Recorded data. We measured the start time and the end time chimpanzees (designated Category I) and manipulation of stones of an episode to get the duration of the episode. For each behav- and/or nuts while in physical contact with the other chimpanzees ioral episode, we also recorded the manipulated objects, the fun- (designated Category II). Then, the types of behavioral episode damental actions involved, and the code of behavioral episodes. were coded with a system designed to capture a range of behav- For observational episodes, we recorded the duration of an episode ioral episodes involving from a single action on a single object, and the performer of nut cracking that the infants observed. and multiple actions on multiple objects, to nut cracking in each category. Results Table 3 illustrates the coding system of behavioral episodes we adopted. The coding system was hierarchically organized accord- Table 4 shows the records of observation in each age ing to the number of manipulated objects, the relation of multiple objects manipulated, and the variety of actions involved in a group: the total time the 3 infants were actually observed, behavioral episode. All behavioral episodes were divided into two the mean duration of stay in the outdoor laboratory by an main classes according to the number of objects manipulated at a infant, and the number of stays for each infant. According to moment: a single object (Class A) and multiple objects (Class B). the definitions, we identified 692 behavioral episodes and The behavioral episodes belonging to Class A were then subdi- 150 observational episodes in total. 162 INOUE-NAKAMURA AND MATSUZAWA

Table 2 List of Fundamental Actions on Objects Object Action Definition Stones Touch Touch a stone by hands and/or feet. Kiss Bring a stone into contact with lips (kiss), tongue (licking), and nose (sniffing). Step Step on a stone by feet; distinguished from Touch by the bipedal upright posture. Lay Lay on a stone on the back. Roll Roll a stone on the ground by hands. Pull Pull a stone by hands and/or feet. The distinguishing feature is a horizontal movement on the ground. Hold Hold a stone in a hand, including transporting it. The stone has to be rifted up. Press Press a stone against the ground or another stone by hands and/or feet; distinguished from Touch by the jerky movement of the stone. Lift Lift a stone with both hands, including transporting the stone in the hands. Kick Kick a stone with a foot. Hit Hit a stone on the ground or another stone with the hands, whether or not the subject held a stone or a nut. Push Push a stone by hands and/or feet. The opposite movement of Pull. Put Put a stone on another stone with hands. Hug Hold a stone in arms in contact with the subject's breast. Sit Sit on a stone in contact with the subject's hip. Fling Fling up a stone by hands. Turn Turn over a stone by bands and/0r feet. Point Point to a stone with an index finger. Brush Pretend to brush pieces of nuts on a stone by the back of a hand, although there are no nuts on the stone. Support Support a stone by hands and/or feet to fix it. Drop Drop the stone that is put on another stone by hands.

Nuts Take Take a nut, a kernel, or a piece of kernel stuck inside a broken shell in a hand. Pick Pick up a nut, a kernel, or a piece of kernel stuck inside a broken shell with fingers. Mouth Place a nut in the mouth; distinguished from Bite or Eat by the lack of use of the teeth. Touch Touch nuts by hands or feet. Bite Bite a nut by using the teeth. Simultaneous contact by a hand was required. Point Point to a nut with an index finger. Rake Rake together nuts on the ground with hands. Scrounge Scrounge the kernel cracked open by an adult. Eat Eat a kernel by using the teeth. Simultaneous contact by a hand was not required. Press Press a nut against the ground, stone, or subject's own body by hands or feet. Peel Peel off the shell of a nut, including intending to pick out the stuck kernel. Roll Roll a nut on the ground by a hand. Put Put a nut on a stone with a hand. Kiss Bring a nut into contact with lips and nose. Hit Hit a nut on the ground or on a stone with the hands, whether or not the subject held a stone or a nut. Grasp Grasp plural nuts in a hand. Brush Brush pieces of nuts on a stone by the back of a hand. Support Support a nut on the stone by a hand not to roll over. Replace Replace a nut on the stone by a hand. Note. The actions are listed according to the order of appearance through the development.

Total Duration of Behavioral and time that the infants stayed at the outdoor laboratory for Observational Episodes each age group. At the age of 0.5 years, the infants spent little of their time (7%) in behavioral and observational Figure 2 shows proportions of the amount of time of episodes. At the age of 1.5 years, the infants spent 13% of behavioral episodes and observational episodes to the total their total stay time in either behavioral episodes or obser- STONE TOOL USE BY CHIMPANZEES 163

Table 3 Hierarchical Classification of Behavioral Episodes Class Definition A-l-i: A single action Subjects manipulated only one object, a stone or a nut, by means of a single action in a on a single object behavioral episode. The repetition of the single action is involved in this category. (Example: kissing a stone; taking a nut.) A-l-ii: Successive Subjects manipulated only one object by means of two or more kinds of actions successively actions on a single in a behavioral episode. (Example: pulling a stone with one hand, stepping on the stone, object and then flinging it with both hands; picking up a nut with one hand and then mouthing it.) A-2: Successive Subjects manipulated several objects successively, but only one object at a moment, by actions on multiple means of two or more kinds of actions in a behavioral episode. (Example: rolling a stone objects with one hand, pulling up another stone with the other hand, and then pressing the stone with both hands; raking together nuts on the ground with one hand, and then touching a stone with the same hand.) B-l: Simultaneous Subjects manipulated several objects simultaneously by means of two or more kinds of actions on multiple actions while no physical contact among objects in a behavioral episode. (Example: rolling objects while no a stone on the ground with one hand while touching another stone with the other hand; relation among biting a nut held in one hand while pushing a stone on the ground with one foot.) objects B-2: Simultaneous Subjects manipulated several objects simultaneously by means of two or more kinds of actions on multiple actions while any physical contact among objects in a behavioral episode. (Example: objects while any picking up a nut and putting it on a stone with one hand while touching the stone by the relation among other hand.) objects C: Nut cracking Subjects performed nut cracking; picking up a nut, putting it on a stone, and then hitting it with another stone. It did not matter whether they succeeded to crack open a nut and ate the kernel in it or not.

vational episodes. At the age of 2.5 and 3.5 years, they spent tively. Duration also tended to increase between the ages of 37% and 44% of their total stay time, respectively. Duration 2.5 and 3.5 years, although the difference was slightly less increased significantly across age groups in Kruskal-Wallis than significant, U(N = 15, 32) = 159, p = .065. The test, H(3, N = 842) = 48.3, p < .001. relative time of Category II (Figure 2, hatched columns) Duration was examined separately for Category I and also changed across age groups, H(3, N = 282) = 10.64, Category II of behavioral episodes and observational epi- .01

.05; 2.5-3.5 years, U = 292.5, p > The relative amount of time in Category I (Figure 2, filled .05). columns) changed significantly as a function of age, H(3, By contrast, the relative amount of time of observational N = 410) = 65.5, p < .001. Duration increased signifi- episodes (open columns) did not change across age groups, cantly between the age of 0.5 and 1.5 years and between 1.5 H(3, N = 150) = 4.4, p > .05. At the age of 3.5 years, 2 and 2.5 years in Mann-Whitney U test, U(N = 29, 38) = chimpanzees, Fotayu and Vuavua, succeeded in performing 232, p < .001; U(N = 38, 15) = 102, p < .001, respec- nut cracking. However, they still observed adults' per-

Table 4 Records of Observation in Each Age Group Observation of infants No. of episodes Groups of Total time" M durationb age (years) (rain) (rain) No. of staysc Behaviorald Observational 0.5 1,033 35.6 13/12/4 0/33 65 1.5 1,047 27.6 20/8/10 107/131 45 2.5 262 17.5 7/4/4 83/58 12 3.5 834 26.1 11/12/9 220/60 28 Total 3,176 27.9 51/36/27 410/282 150 "The total time the 3 infants were actually observed, b The mean duration of one stay when an infant appeared in the outdoor laboratory, c The number of stays for each infant (Yolo/Fotayu/ Vuavua). d The first number represents the number of behavioral episodes in Category I, and the second number represents the number of behavioral episodes in Category II. 164 INOUE-NAKAMURA AND MATSUZAWA

50 ~ Behavioral episodes: Category I

40 ~;~ Behavioral episodes: Category II

x.J D Observational episodes 30

20

10 0t 0.5 1.5 2.5 3.5

Groups of age Figure 2. Percentage amount of time of behavioral and observational episodes in each age group.

formances (Fotayu, eight instances; Vuavua, seven quency of scrounging the kernel cracked open by an adult to instances). the total frequency of the manipulation of only nuts were These data indicate that the older infants spent more time 0% (0/24), 50% (37/74), 76% (28/37), and 86% (25/29) for in behavioral episodes in which the subjects manipulated the 0.5-, 1.5-, 2.5-, and 3.5-year age groups, respectively. At objects while not in physical contact with the other chim- the age of 3.5 years, 2 chimpanzees that succeeded in panzees and that they still observed adults' performances performing nut cracking still scrounged adults' kernels even after succeeding in performing nut cracking. (60%, 15/25 in frequency). These results indicate that the manipulation of both stones and nuts in an episode in- Manipulated Objects Involved in Each creased as the age progressed and that the infants stole Behavioral Episode kernels from their mothers continuously even after succeed- ing in performing nut cracking. We analyzed developmental processes of objects manip- ulation by classifying all behavioral episodes into three Fundamental Actions Involved in Each different types according to the objects manipulated in each Behavioral Episode behavioral episode: (a) manipulation of only stones, (b) manipulation of only nuts, and (c) manipulation of both A variety of fundamental actions on stones and nuts were stones and nuts, in a behavioral episode. Relative frequency performed in behavioral episodes. The number of behav- of behavioral episodes involved in each type was compared ioral episodes in which each fundamental action occurred among four age groups in each category (see Figure 3). for each age group is presented in Table 5. In both cases of Category I (Figure 3a) and Category II At the age of 0.5 years, the variety of the fundamental (Figure 3b), the manipulation of the objects significantly actions were only two on stones and seven on nuts. The changed as a function of age in chi-square test, X2(4, N = variety of actions on both stones and nuts dramatically 410) = l13,p < .001 and X2(6, N = 282) = 42.6,p < .001, increased at the age of 1.5 years. Five basic actions are respectively. In both cases of Category I and II, the manip- needed to perform nut cracking: (Action A) taking (or ulation of both stones and nuts in a behavioral episode picking up) a nut, (Action B) putting a nut, (Action C) increased significantly, X2(2, N = 410) = 90.1, p < .001 holding a stone, (Action D) hitting a nut, and (Action E) and X2(3, N = 282) = 31.7, p < .001, respectively, while it eating a nut (in bold in Table 5). All of them already was not observed at the age of 0.5 years. In both cases of occurred at this age. The fundamental actions, such as Category I and II, the manipulation of only stones decreased Brush, Support, and Replace, occurred at the age of 2.5 and significantly, X2(2, N = 410) = 15.9, p < .001 and 9(2(3, 3.5 years. These actions were accompanied in some cases N = 282) = 19.5, p < .001, respectively. In the case of with nut cracking. The four fundamental actions--laying on Category I, the manipulation of only nuts decreased signif- a stone, pointing a stone, raking nuts, and rolling a nut-- icantly, XZ(2, N = 410) = 72.6, p < .001. However, it did disappeared at the age of 3.5 years. None of these actions not change in the case of Category II, X2(3, N = 282) = 6.6, are essential for performing nut cracking. p > .05. In the case of Category II, the proportional fre- The frequency of fundamental actions also changed STONE TOOL USE BY CHIMPANZEES 165

(a) Category I 0 107 83 220 100- I oth stones and nuts

Only nuts 80 D Only stones io o 40

20

0 0.5 1.5 2.5 3.5

Groups of age

(b) Category II 33 131 58 60 100 -- -!//. f///, 80 N "!!!1 60 711i ¢////

o 40 a,

2o

0 0.5 1.5 2.5 3.5

Groups of age Figure 3. Developmental processes of the objects manipulated in each behavioral episode in (a) Category I and (b) Category II. The number above each column represents the total number of observed episodes. across age groups. Especially, the proportional frequency of Frequency of Behavioral Episodes in Each the five basic actions for nut cracking--(Action C) Hold Hierarchical Class on stones, and (Action A) Take (or Pick), (Action E) Eat, (Action B) Put, and (Action D) Hit on nuts--increased Figures 4a and 4b present relative frequency of the be- significantly as a function of age: )(2(3, N = 2,084) = 73.3, havioral episodes in each hierarchical class compared p < .001; X2(3, N = 2,084) = 11.2, p < .02; X2(3, among four age groups in Category I and Category II, N = 2,084) = 10.1, p < .02; X2(3, N = 2,084) = 71.2, respectively. p < .001; and X2(3, N = 2,084) = 77.9, p < .001, In Category I, the infants at the age of 0.5 years did not respectively. manipulate any object while not in physical contact with the 166 INOUE-NAKAMURA AND MATSUZAWA

Table 5 In Category II, at the age of 0.5 years, Class A-1 was Variation and Frequency of Fundamental Actions dominant (97%, 32/33). At the age of 1.5 years, behavioral Groups of age (years) episodes in Class A-1 were still dominant (73%, 95/131), but those in Class A-2 increased (19%, 25/131) and Class B Object Action 0.5 1.5 2.5 3.5 started to appear (8%, 11/131). At the age of 2.5 years, Stones Touch 9 78 32 85 Class B increased (29%, 17/58) whereas Class A-l-i de- Kiss 1 6 4 1 creased (17%, 10/58). At the age of 3.5 years, as in Cate- Step 44 22 41 gory I, nut cracking started to be observed. Of behavioral Lay 1 2 Roll 10 29 25 episodes, 52% (31/60) belonged to Class B and Class C. Pull 10 12 26 The relative frequency of behavioral episodes changed sig- Hold 8 13 138 nificantly as a function of age, )(2(15, N = 282) = 97.8, Press 5 4 20 p < .001. Lift 3 9 9 In both Category I and Category II, relative frequency of Kick 3 2 4 Hit 3 8 14 behavioral episodes in hierarchically higher classes in- Push 2 3 1 creased whereas that of behavioral episodes in lower classes Put 2 2 2 decreased as a function of age. Hug 1 2 10 Sit 1 4 9 Fling 9 11 Duration of Behavioral Episodes in Each Turn 8 7 Point 1 Hierarchical Class Brush 1 1 Support 20 Durations of all behavioral episodes in each hierarchical Drop 12 class were compared in four age groups in Category I and Category II. The values of duration are presented in Table 6. Nuts Take 15 94 52 167 Pick 1 7 6 27 Figure 5 shows statistical results among durations in each Mouth 14 57 21 16 hierarchical class, using Mann-Whitney U test. At the age of Touch 9 20 13 5 0.5 years, in Category II, durations of behavioral episodes in Bite 2 28 41 35 Class A-l-i were significantly shorter than those in Class Point 1 3 3 2 A-l-ii. At the age of 1.5 years, in both Category I and Rake 1 7 5 Scroungea 48 (1) 41 (2) 48 (3) Category II, durations of behavioral episodes in Class A-l-i Eat 31 22 99 were significantly shorter than those in Classes A-1-ii, A-2, Press 6 2 2 and B. Class A-l-ii were significantly shorter than Class Peel 6 2 3 A-2. At the age of 2.5 years, in both Category I and Roll 4 2 Put 3 13 122 Category II, durations of behavioral episodes in Class A-l-i Kiss 2 1 1 were significantly shorter than those in Classes A-l-ii, A-2, Hit 2 4 107 B-I, and B-2. In Category I, durations of behavioral epi- Grasp 2 2 5 sodes in Class B-1 were shorter than those in Class B-2. In Brush 1 6 Category II, durations of behavioral episodes in Class A-l-ii Support 1 9 Replace 45 were shorter than those in Class B-1. At the age of 3.5 years, Note. Basic actions for nut cracking are represented in boldface. in Category I, durations of behavioral episodes in Classes a The first number represents the number that infants scrounged A-l-i and A-l-ii were significantly shorter than those in kernels from their own mothers. The number in parentheses rep- Classes A-2, B-l, and B-2, which were shorter than Class C. resents the number that infants scrounged kernels from chimpan- In Category II, durations of behavioral episodes in Classes zees other than their own mothers. A-l-i and A-l-ii were significantly shorter than those in Classes B-1, B-2, and C. In both Category I and Category II other chimpanzees (n = 0)because they were always at- in each age group, duration of each behavioral episode tached to their mothers. At the age of 1.5 years, behavioral lengthened as a function of hierarchy defmed by the coding episodes in Class A-1 were dominant (77%, 82/107). The system of the present study. infants at the age of 1.5 years also showed behavioral episodes in Class A-2 (10%, 11/107) and Class B (13%, Interaction With the Other Chimpanzees 14/107). At the age of 2.5 years, behavioral episodes in Class A-l-i decreased (7%, 6/83) whereas those in Class In Category II of behavioral episodes, the other chimpan- A-2 (19%, 16/83) and Class B (31%, 26/83) increased. At zees with whom the infants were in physical contact were the age of 3.5 years, 2 chimpanzees, Fotayu and Vuavua, mostly their own mothers: at the age of 0.5 years, 33 out of started nut cracking (Class C; 39%, 86/220). At this stage, 33 behavioral episodes (100%); at the age of 1.5 years, 128 75% of behavioral episodes observed (166/220) belonged to out of 131 (98%); at the age of 2.5 years, 51 out of 58 Class B or C. The relative frequency of behavioral episodes (88%); and at the age of 3.5 years, 54 out of 60 (90%). except the 0.5-age group changed as a function of age, There were 16 instances in total in which the infants were in )(2(10, N = 410) = 185.9, p < .001. physical contact with other chimpanzees than their own STONE TOOL USE BY CHIMPANZEES 167

(a) Category I

Groups of age

(b) Category II

Groups of age

Figure 4. Developmental processes of the behavioral episodes for each hierarchical class in (a) Category I and (b) Category II (see Table 3 for class description). The number above each column represents the total number of behavioral episodes. 168 INOUE-NAKAMURA AND MATSUZAWA

Table 6 Duration of Behavioral Episodes (in Seconds) in Each Hierarchical Class in Four Age Groups Category I Category II Groups of age (years) Class M Min Max Mdn No. M Min Max Mdn No. 0.5 A-l-i 16 3 45 11 16 A-l-ii 110 23 390 75 16 A-2 77 77 1

1.5 A-l-i 6 2 25 5 39 13 2 60 10 45 A-l-ii 19 3 118 11 43 38 4 200 25 50 A-2 52 14 146 31 11 64 9 122 65 25 B-1 48 2 183 16 13 65 5 275 32 8 B-2 27 27 1 213 10 540 90 3

2.5 A-l-i 5 2 13 4 6 11 3 24 9 10 A-l-ii 20 2 80 15 35 29 5 102 18 27 A-2 46 6 165 21 16 31 13 50 31 4 B-1 28 4 71 22 13 111 13 556 60 14 B-2 48 11 76 58 13 92 20 137 119 3

3.5 A-l-i 10 2 35 8 16 25 2 95 12 8 A-l-ii 15 2 101 10 27 16 2 75 7 13 A-2 48 11 265 22 11 28 17 40 25 8 B-1 44 2 205 22 35 76 13 161 50 11 B-2 70 4 451 28 45 112 8 333 110 12 C 93 6 526 52 86 175 15 550 113 8 Note. See Table 3 for class description. Min = minimum, Max = maximum.

mothers: 2 instances in Yolo, 13 instances in Fotayu, and 1 five basic actions were involved, two behavioral episodes instance in Vuavua, respectively. Except their own mothers, were performed by Fotayu, which was already able to do nut the other adult females (75%) and the sibling (25%) were cracking, and the others were performed by Yolo, which the chimpanzees that were in physical contact with the was not yet able. infants manipulating stones and/or nuts. Figure 6 shows the conditional probabilities of occurrence We also investigated the proportion of subjects that the of each basic action in each age group except those in the infants observed in observational episodes (i.e., whether the 0.5-year age group. At the age of 1.5 years, the sequence infants observed their own mothers or not). The proportion from Action A (Take or Pick) to Action E (Eat) was most of observation of their mothers were 100%, 71%, 42%, and dominant, and it decreased as a function of age. In contrast, 14% for the 0.5-, 1.5-, 2.5-, and 3.5-year age groups, re- the probability of the sequence from Action A (Take or spectively. The proportion decreased significantly as a func- Pick) to Action B (Put) increased as a function of age. At the tion of age, X2(3, N = 150) = 74.8, p < .001. These data age of 2.5 and 3.5 years, the probabilities of the sequence indicate that older infants observed more often the other from Action A (Take or Pick) to Action B (Put), from B to chimpanzees than their own mothers. Other than their own D (Hit), and from D to A were getting higher. The proba- mothers, the infants observed the other adult females (64%), bility of the sequence from Action C (Hold) to Action D juveniles (21%), an alpha male (9%), and the siblings (7%). (Hit) was almost zero for all age groups. It indicates that the infants seldom hold a stone to hit. It has to be noted that a Five Basic Actions for Nut Cracking lot of "reverse" and "short-cut" sequences were observed for all age groups. Table 7 shows the frequency of behavioral episodes in Table 8 provides a more detailed analysis of the types of which at least one of the five basic actions necessary for nut Hit action excluding the behavioral episodes in which actual cracking were involved. The behavioral episodes of actual nut cracking was involved. Among the various possible nut cracking were omitted from this analyses. At the age of combinations, the infants did not show the action of "hitting 0.5 years, 15 out of 33 behavioral episodes (45%) involved a nut on the ground by a stone." a basic action, but the remaining 18 behavioral episodes did Another analysis of Hit actions revealed that Hit actions not involve any basic action. The basic action observed at did not appear in the class of a single action on a single this age was limited to Take or Pick. At the ages of 1.5 and object (Class A-I-i). In contrast, more than 97% of simul- 2.5 years, three basic actions at maximum were involved in taneous actions on multiple objects (Class B-1 and B-2) a behavioral episode. At the age of 3.5 years, four or even involved Hit actions. It was also revealed that Hit actions all of the five basic actions were involved in a behavioral frequently appeared when the infants manipulated both episode. Out of six behavioral episodes in which all of the stones and nuts in a behavioral episode (81%). STONE TOOL USE BY CHIMPANZEES 169

Category I Category H 0.5 3 @

1.5 @

2.5 j -i -i

3.5

1)

Figure 5. Statistical results among durations in each hierarchical class (see Table 3 for class description) using Mann-Whimey U test. The results are schematically drawn in each age group and in Category I and Category II. The single and double lines represent statistically significant differences at the level ofp < .05 and p < .01, respectively. Each arrow is drawn from the shorter to the longer duration. 170 INOUE-NAKAMURA AND MATSUZAWA

Table 7 Frequencies of Behavioral Episodes Involving Basic Actions Groups of No. of basic actions involved in a behavioral episode age (years) 1 2 3 4 5 0.5 15 (A; 15) 0 0 0 0 1.5 104 (A; 79) 15 (A,E; 13) 2 (A,B,C; 2) 0 0 (E; 17) (A,D; 2) (C; 6) (B; 1) (D; 1) 2.5 54 (A; 33) 15 (A,E; 7) 7 (A,B,D; 3) 0 0 (E; 11) (A,B; 5) (A,B,C; 1) (C; 9) (A,C; 3) (A,C,E; 1) (B; 1) (B,E; 1) (B,C,E; 1) (B,D,E; 1) 3.5 55 (A; 22) 36 (A,B; 18) 21 (A,B,C; 13) 5 (A,B,D,E; 3) 6 (A,B,C,D,E; 6) (E; 17) (A,E; 12) (A,B,E; 4) (A,B,C,D; 2) (C; 16) (A,C; 4) (A,B,D; 2) (C,E; 2) (A,C,E; 2) Note. A = Take or Pick; B = Put; C = Hold; D = Hit; and E = Eat.

Discussion of a hand, and then picked up a piece of kernel stuck inside of a broken shell from the ground and ate it. In another case, The present study has focused on the acquisition of nut- the infants once put a nut on a stone and then turned to the cracking skill by wild infant chimpanzees younger than 4 mothers to scrounge a kernel in the nut that was cracked years old in the outdoor laboratory. The quantitative anal- open by their mothers. ysis of stone-nut manipulation shown in the results has Similar observation was also reported in human infants illuminated the developmental changes leading to the actual (Connolly & Dalgleish, 1989). Human infants younger than nut cracking. The following two major points are discussed: 2 years old sometimes put their spoon with one hand into the ontogeny of chimpanzees' stone-nut manipulation and and out of the dish repeatedly while taking food from the the social influence on the acquisition of nut cracking. dish with the other hand. Both infant chimpanzees of the age group of 2.5 years old Ontogeny of Stone-Nut Manipulation and human infants younger than 2 years old have already acquired each basic action. However, neither of them can As shown in the process of acquisition of nut cracking, combine together each action in an appropriate manner. The the infants manipulated a single object in a single action in lack of adequate composition of each action is a common the early stage of development. As a function of age, a characteristic of the chimpanzees and humans just before single action on a single object (only stone or only nut) acquiring the tool-use skills. developed into multiple actions on multiple objects (some On the other hand, we found an interesting difference stones, some nuts, or both stones and nuts). The older infants had a tendency to manipulate both stones and nuts between the two species in an action involved in the stone- successively or simultaneously and to physically contact nut manipulation. Infant chimpanzees in the present study nuts with stones in a behavioral episode. As the age that were not able to perform nut cracking never hit a nut progressed, the infants showed the more complex and the with a hammer stone. On the contrary, human infants more hierarchically organized pattern of action-object showed "hitting a nut on the ground with a stone held by a relationship. hand" in the developmental process to acquire the nut- To accomplish the nut cracking, the infant chimpanzee cracking skill (Matsuzawa, 1994). The infant chimpanzees must put together the five basic actions: Take (Pick), Put, had a tendency to easily relate a nut with an anvil in an early Hold, Hit, and Eat. At the age of 1.5 years, all of these basic stage like 1.5 years old; that is, they could put a nut on a actions had already been performed, and the frequency of stone. However, it may be difficult for chimpanzees to hold these basic actions increased as a function of age. However, a stone and hit a nut with the stone. A juvenile female, infants did not combine with each basic action in an appro- Yunro (7 years old in 1992), was not able to use stones as priate way. It took 3.5 years for infant chimpanzees to a tool to crack open a nut. In her case, she put a nut on a succeed in combining these actions in an adequate sequence stone and hit the nut with her left knuckle or her right foot, and performing actual nut cracking. whereas she never held a hammer stone. This behavior was For instance, the infant chimpanzees of the age of 2.5 exactly the same as those shown in the 2.5-year-old chim- years often put a nut on a stone but hit the nut with the back panzees just before starting actual nut cracking. STONE TOOL USE BY CHIMPANZEES 171

1.5 while manipulating stones and nuts on their own in the process of acquiring the nut-cracking skill. As the age progressed, infant chimpanzees spent more time in observ- ing the other chimpanzees other than their own mothers throughout a period of learning skills of nut-cracking be- havior. Moreover, they even scrounged kernels from chim- panzees other than their own mothers. It suggests that moth- J ers are not the only resource to provide the model of the tool-use skill. The other chimpanzees in the same commu- nity seems to play very important roles in acquiring nut- cracking behaviors. For example, at Bossou there are two adult females, Nina and Pama, who cannot perform nut ® cracking. Their offspring, Na (6.5 years old in 1992) and Pili (5 years old in 1992), showed no retardation in acquir- ing nut-cracking skill (Matsuzawa, 1994). They were likely to acquire the skill under the influence of members in the 2.5 community and through practicing on their own. Social learning is likely to play an important role in the acquisition of tool-use behaviors for those chimpanzees living in a group in which such behaviors are relatively common (Beck, 1980; Thorpe, 1956). According to Thorpe (1956), there are three social learning processes. The first is social facilitation. The demonstrator may simply act as a releasing stimulus to the observer. The second is stimulus/ local enhancement. The demonstrator may influence learn- ing by making a particular stimulus or location more salient and thus more likely to draw the observer's attention. Stim- © ® ulus/local enhancement increases the likelihood that the observer will learn the behavior on its own by trial and error. The third is true imitation. The demonstrator may model the behavior, which the observer then copies in its 3.5 entirety. To qualify as true imitation, the observer must produce a topographical duplication of a novel behavior without trial and error. Tomasello, Davis-Dasilva, Camak, and Bard (1987) con- ducted an experimental study of social learning of a tool-use behavior by captive juvenile chimpanzees. They suggested that chimpanzees learned the skill of tool-use not through true imitation learning but through emulation learning. Em- ulation is a process similar tO stimulus enhancement but is a bit more sophisticated. Chimpanzees did not copy the demonstrator's actual methods of tool use by true imitation. However, they did not simply pay attention to the tool

Table 8 Figure 6. Conditional probabilities of occurrence of each basic Frequencies of Each Type of Hit Action on action. The thickness of arrows represents conditional probabili- Stones and Nuts ties. Only the five basic actions were taken into account in the present analysis. Because the other fundamental actions were Groups of age (years) omittr..d, A ---*B, for example, does not always represent "taking a Object On By 0.5 1.5 2.5 3.5 nut and then putting it on a stone." There is the probability of existence of some fundamental actions between the two basic Nuts Stone Hand 0 1 4 11 actions, "taking a nut" and "putting a nut on a stone." Ground Hand 0 1 0 0 Stone Nut 0 0 0 2 Ground Stone 0 0 0 0 Social Influence and Practice Stones Stone Hand 0 0 0 1 Ground Hand 0 3 6 6 Infant chimpanzees observed nut-cracking behaviors per- Ground Nut 0 0 2 0 formed by their own mothers or the other chimpanzees Ground Stone 0 0 0 7 172 INOUE-NAKAMURA AND MATSUZAWA

(stimulus enhancement) but also learned something about cracking in wild chimpanzees a cultural behavior? Journal of the general functioning of the task and the results obtained Human Evolution, 26, 325-338. by the demonstrator (emulation). Cormolly, K., & Dalgleish, M. (1989). The emergence of a tool- What type of social learning process is involved in the using skill in infancy. Developmental Psychology, 25, 894-912. acquisition of nut-cracking skill? True imitation cannot Fragaszy, D. M., & Visalberghi, E. (1989). Social influences on explain the results of the present study. The infants showed the acquisition of tool-using behaviors in tufted capuchin mon- keys ( Cebus apella). Journal of Comparative Psychology, 103, various combinations of stones and nuts. They also showed 159-170. a variety of fundamental actions. Not all of them were Fushimi, T., Sakura, O., Matsuzawa, T., Ono, H., & Sugiyama, Y. adequate actions for actual nut cracking. They gradually (1991). Nut-cracking behavior of wild chimpanzees (PantrogI- increased the relative frequency of adequate sequence of the odytes) in Bossou, Guinea (West Africa). In A. Ehara, T. basic actions through each stage of development. They did Kimura, O. Takenaka, & M. Iwamoto (Eds.), Primatology today not copy the motor patterns or the way to relate nuts with (pp. 695-696). Amsterdam: Elsevier. stones, which were shown in the tool use by mothers and the Goodall, J. (1970). Tool using in primate and other vertebrates. In other members of the community. As the present results D. S. Lehrman, R. A. Hinde, & E. Shaw (Eds.), Advances in the suggest, they learned the general functional relations of study of behavior (pp. 195-249). New York: Academic Press. stones and nuts and also learned the goals obtained by the Goodall, J. (1986). The chimpanzees of Gombe: Patterns of be- demonstrator. This learning process might be called havior. Cambridge, MA: Harvard University Press. emulation. Hannah, A., & McGrew, W. (1987). Chimpanzees using stones to Active teaching seems to be a clear distinction in the crack open oil palm nuts in Liberia. Primates, 28, 31-46. acquisition process between humans and chimpanzees. Ac- Inoue, N., Tonooka, R., & Matsuzawa, T. (1996). Developmental processes of nut-cracking skill among infant chimpanzees in the tive teaching is rare in chimpanzees in the wild although it wild. The Japanese Journal of Developmental Psychology, 7, is popular in humans. So far, there have been no instances 148-158. (in Japanese with English summary) of active teaching or guidance except two reported episodes Kortlandt, A. (1986). The use of stone tools by wild-living chim- in which mothers influenced their infants' attempt to crack panzees and earliest hominids. Journal of Human Evolution, 15, nuts (Boesch, 1991b). Human mothers usually give their 77-132. infants verbal instructions about how to grasp a spoon. They McGrew, W. C. (1992). Chimpanzee material culture. Cambridge, even mold the hands of infants to show the correct way of MA: Harvard University Press. grasping. In human societies, they also give their infants Matsuzawa, T. (1991). Nesting cups and metatools in chimpan- social reinforcement, such as social praise. On the contrary, zees. Behavioral and Brain Sciences, 14, 570-571. in the case of chimpanzees of the present study, they did not Matsuzawa, T. (1994). Field experiments on use of stone tools by show any kind of active teaching to the infants. They also chimpanzees in the wild. In R. Wrangham, W. McGrew, F. de did not give them any social reinforcement. The chimpanzee Waal, & P. Heltne (Eds.), Chimpanzee cultures (pp. 351-370). mothers' attitude toward their infants was characterized by Cambridge, MA: Harvard University Press. Nishida, T. (1990). The chimpanzees of the Mahale mountains: the lack of any feedback to infant chimpanzees' attempts at Sexual and life history strategies. Tokyo: Tokyo University nut-cracking behaviors. Press. In chimpanzee societies, adults are extremely tolerant of Nishida, T., & Hiraiwa, M. (1982). Natural history of a tool-using infants, which are common in some primate species includ- behavior by wild chimpanzees in feeding upon wood-boring ing humans (e.g., Fragaszy & Visalberghi, 1989; Visal- ants. Journal of Human Evolution, 11, 73-99. berghi & Fragaszy, 1990). In the case of juveniles, however, Sakura, O., & Matsuzawa, T. (1991). Flexibility of wild chimpan- the tolerance is weaker. For example, juvenile chimpanzees zee nut-cracking behavior using stone hammers and anvils: An were often observed not to be able to take the stones and/or experimental analysis. Ethology, 87, 237-248. nuts beside dominant adults. They were often chased out Sugiyama, Y. (1984). Population dynamics of wild chimpanzees at when they were trying to get stones and/or nuts at the side Bossou, Guinea, between 1976 and 1983. Primates, 25, of the adults. In summary, the members in the community 391-400. provided only the infants with the opportunities to freely Sugiyama, Y. (1988). Grooming interactions among adult chim- access stones and nuts. These opportunities could facilitate panzees at Bossou, Guinea, with special reference to social structure. International Journal of Primatology, 9, 393-407. the individual experience of stone-nut manipulation and Sugiyama, Y. (1993). Local variation of tools and tool use among result in the apparent social transmission of the tool-use wild chimpanzee populations. In A. Berthelet & J. Chavaillon behavior among the wild chimpanzees. (Eds.), The use of tools by human and non-human primates (pp. 175-187). Oxford, England: Clarendon Press. Sugiyama, Y. (1994a). Age-specific birth rate and life time repro- References ductive success of chimpanzees at Bossou, Guinea. American Journal of Primatology, 32, 311-318. Beck, B. B. (1980). Animal tool behavior. New York: Garland. Sugiyama, Y. (1994b). Tool use by wild chimpanzees. Nature, Boesch, C. (1991a). Handedness in wild chimpanzees. Interna- 367, 327. tional Journal of Primatology, 12, 541-558. Sugiyama, Y., Fushimi, T., Sakura, O., & Matsuzawa, T. (1993). Boesch, C. (1991b). Teaching among wild chimpanzees. Animal Hand preference and tool use in wild chimpanzees. Primates, 34, Behaviour, 41, 530-532. 151-159. Boesch, C., Marchesi, P., Fruth, B., & Joulian, F. (1994). Is nut Sugiyama, Y., & Koman, J. (1979a). Social structure and dynam- STONE TOOL USE BY CHIMPANZEES 173

ics of wild chimpanzees at Bossou, Guinea. Primates, 20, Tonooka, R., Inoue, N., & Mastuzawa, T. (1995). Leaf-folding 323-339. behavior for drinking water by wild chimpanzees at Bossou, Sugiyama, Y., & Koman, J. (1979b). Tool-using and making Guinea: A field experiment and leaf selectivity. Primate Re- behavior in wild chimpanzees at Bosson, Guinea. Primates, 20, search, 10, 307-313. (in Japanese with English summary) 513-524. Visalberghi, E., & Fragaszy, D. (1990). Do monkeys ape? In S. Sugiyama, Y., & Koman, J., (1987). A preliminary list of chim- Parker & K. Gibson (Eds.), "Language" and intelligence in panzees' alimentafion at Bossou, Guinea. Primates, 28, 133-147. primates: Comparative developmental perspectives (pp. 247- Sugiyama, Y., Koman, J., & Sow, M. B. (1988). Ant-catching 273). Cambridge, England: Cambridge University Press. wands of wild chimpanzees at Bossou, Guinea. Folia Primato- Yamakoshi, G., & Sugiyama, Y. (1995). Pestle-pounding behavior logica, 51, 56-60. of wild chimpanzees at Bossou, Guinea: A newly observed Sumita, K., Kitahara-Frisch, J., & Norikoshi, K. (1985). The tool-using behavior. Primates, 36, 489-500. acquisition of stone tool use in captive chimpanzees. Primates, 26, 168-181. Thorpe, W. H. (1956). Learning and instinct in animals. London: Methuen. Tomasello, M., Davis-Dasilva, M., Camak, L., & Bard, K. (1987). Received January 2, 1996 Observational learning of tool-use by young chimpanzees. Hu- Revision received October 3, 1996 man Evolution, 2, 175-183. Accepted October 22, 1996

Articles to Be Published in the Journal of Comparative Psychology

September 1997, Vol. 111, No.

Classical Conditioning Provides Paternity Advantage for Territorial Male Blue Gouramis (Trichogaster trichopterus) Karen L. Hollis, Victoria L. Pharr, Michelle J. Dumas, Gabrielle B. Britton, and Janet Field Vocal Development in Budgerigars (Melopsittacus undulatus): Contact Calls Elizabeth F. Brittan-PowelL Robert J. Dooling, and Susan M. Farabaugh Social Enhancement and Interference of Food Finding in Zebra Finches (Taeniopygia guttata) Scott L Coleman and Roger L Mellgren The Role of Nasal Chemical Senses in Garter Snake Response to Airborne Odor Cues From Prey Mimi Halpern, Jeffrey Halpern, Evelyn Erichsen, and Saihan Borghjid Perceptual Salience of Acoustic Features of Japanese Monkey Coo Calls Colleen Garbe Le Prell and David B. Moody Role of Reinforcement in Spaced-Trial Operant Learning in Pigeons (Columba livia) Mauricio R. Papini Gaze Following and Joint Attention in Rhesus Monkeys (Macaca mulatta) Nathan J. Emery, Erika N. Lorincz, David I. Perrett, Michael W. Oram, and Christopher I. Baker Pitch Discrimination in Field and Isolation Reared Black-Capped Chickadees (Parus atricapiUus) Milan Njegovan and Ron Weisman The Sublingual Plicae (Anterior Processes) Are Not Necessary for Garter Snake Vomeronasal Function Mimi Halpern and Saihan Borghjid