Brief Report Folia Primatol 1998;69:318–324
Received: June 4, 1997 Accepted after revision: June 18, 1997
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Spontaneous Tool Use by a Tonkean Macaque (Macaca tonkeana) Yoshikazu Ueno a, Kazuo Fujita b a b
Center for Experimental Plants and Animals, Hokkaido University, Sapporo, and Department of Psychology, Faculty of Letters, Kyoto University, Kyoto, Japan
Key Words Tool use · Macaques · Hand preference · Distance recognition
Introduction Great apes, particularly chimpanzees, and capuchin monkeys are known to use a variety of tools, both in the laboratory and in the wild [1–14]. Among Old World monkeys, on the other hand, reports of tool use have been much scarcer. So far, there have been several reports showing that at least 3 macaque and 1 baboon species were able to use tools in situations where tool using was strongly encouraged to solve artificial problems given to the monkeys. Tokida et al. [15] reported a most elegant example performed by a female Japanese macaque. She invented a method of throwing stones into a transparent tube to obtain food from there. She chose stones of appropriate size and controlled the momentum of the stones. Finally she learned to send her infant into the tube to get the food. Lion-tailed macaques succeeded in using sticks to extract syrup from an apparatus [16]. Tonkean macaques also used a rod to obtain honey from a container [17]. Anubis baboons used soft materials to sponge sweet liquid [18]. In more natural situations, Jaqanese macaques were reported to use objects in playful contexts. Huffman and Quiatt [19] reported how stone-handling play spread among a provisioned troop. Machida [20] observed 3 juvenile females stand a pole to climb up to lick a wall. It is now evident that ability to use tools is shared not only by great apes and one unusually intelligent group of the New World monkeys, but also by some of the Old World monkeys. However, it is still unclear how flexible and adaptive Old World monkeys are in their use of tools. Natale et al. [21] compared the ability to use sticks to obtain food of a Japanese monkey and a gorilla. They noted that the Japanese macaque rotated the stick in a stereotyped movement to obtain food, getting only ran-
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© 1998 S. Karger AG, Basel 0015–5713/98/0695–0318 $15.00/0 Article accessible online at: http://BioMedNet.com/karger
Yoshikazu Ueno Center for Experimental Plants and Animals Hokkaido University, N10 W8 Kita-ku, Sapporo (Japan) Tel. +81 11 706 3580, Fax +81 11 726 3476 E-Mail [email protected]
dom successes. On the other hand, the gorilla, faced with the same situation, spontaneously started to use a blanket when the stick proved to be less useful. In this report, we show a case in which a Tonkean macaque spontaneously used sticks quite flexibly in a fashion adaptive to the situation.
Method Subject Our subject was a fully adult male Macaca tonkeana named Banga (fig. 1). We found this individual during our research on the senses of taste and smell in Sulawesi macaques in 1996. This subject had been kept as a pet for 5 years by a resident in Desa Kabonga Besar, in the suburbs of Palu city, Central Sulawesi, Indonesia. The subject was chained to a tree. Procedure Preliminary Observation. We happened to witness this subject use a withered soft stalk of a coconut leaf to obtain a piece of food on the ground out of his reach (fig. 2). The tool was about 90 cm long. It was folded in the middle, hence looked like a jointed stick. One half was strong, but the other half was weak. He picked up the tool with his left hand, grasped one end with his thumb on one side and the other 4 fingers on the other side, reached for the food, moved the stick inwards until the food came within his reach, dropped the stick, picked up the food and ate it. He performed all of this in just a few seconds with a perfectly smooth movement and no hesitation. We next placed a piece of Salak, a local palm fruit (fig. 3a), out of his reach. He picked up the same stick and tried to get the food, but he failed this time, apparently because the stick was too weak to get the food stuck in the grass. He dropped the stick, immediately went to the other side of the tree to which he was chained, picked up another bamboo stick, which was much stronger than the first one, and used it in exactly the same manner as noted in the first observation to get the food successfully in just 1 or 2 s. Experiment. Two sticks of different length were used (fig. 3b, bottom two sticks). One was from the second observation. The length was 61 cm and the diameter was 1.7 cm. The other was a stem of the tree. The length was 90 cm and the diameter was 1.9–2.8 cm. Pieces of Salak fruit were presented in a green plastic bowl 11.5 cm in diameter and 7 cm deep. In a first series (condition: far), the experimenter (K.F.) put the food bowl about 35 cm out of the subject’s reach. After the subject had come up and seen the food, the experimenter placed the two sticks on one side of the monkey separated by about 50 cm from each other. The side on which the sticks were put was switched in every trial. The sticks were placed at the same distance from the monkey. The observer (Y.U.) recorded the stick and the hand the subject used. Trials were repeated 10 times and were recorded by a video camera (Sony CCD-TR303). In a second series (condition: near), the experimenter put the bowl about 10 cm out of the subject’s reach. Other conditions were exactly the same as in the first series.
Results First Series – Condition Far The subject chose the longer stick 9 times out of 10 trials. This was statistically significant (p = 0.011, one-tailed). He always used his left hand to reach the food. When the longer stick was placed on his left, he always picked it up with his left hand and immediately reached for the food. When the longer stick was on his right, he flipped it to the left with his right hand, then picked it up with his left hand 4 times out of 5 trials. In all trials, he tried to pull the food bowl towards himself. He succeeded in getting the food in 9 trials. On the last trial the food bowl rolled away and he lost sight of the small piece of food.
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Fig. 1. The subject M. tonkeana. Fig. 2. An example of tool use. a The subject approaches the bowl with pieces of food in it, with a stick in his left hand. b He pulls the bowl toward him with the stick. c He gets the bowl and eats the food in it.
1
2b
2a
2c
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a
b Fig. 3. The food we used to test the monkey’s performance (a) and the tools the subject used (b).
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Folia Primatol 1998;69:318–324
321
Second Series – Condition Near The subject used each stick equally often. He chose the stick on the left with his left hand in all 10 trials, irrespective of the length of the stick. This was statistically significant (p = 0.001, one-tailed). During the course of this series, the experimenter mistakenly placed the food bowl too near the subject in 3 trials (these were not counted as test trials). In these cases, the subject extended his hand directly to get the bowl. In another trial he failed to pull the bowl with the shorter stick, because the bowl rolled away. The subject immediately changed the stick to the longer one and got the food. As a consequence, he succeeded in getting the food in all trials.
Discussion When the food was close to the macaque, he did not care about the length of the tool but picked up the one that was the most easily available to him, i.e. the one on his left. When the food was farther away, he carefully chose the longer stick. The results of the two simple experiments clearly demonstrate that this monkey ‘knew’ how he should solve the problem before he actually started to tackle it. He not only used sticks to get the food beyond his reach, but he also chose the correct stick to solve the problem. In addition, he did not insist on using the same stick once he started. He quickly changed the shorter stick to the longer one, once he recognized that the food had moved farther away. He showed similar flexibility in using the stick when he recognized that the quality of the stick was not good enough for the situation. In the second observation, he changed a weak stick for a stronger one to get the food stuck in the grass. It is clear that this monkey had the ability to use sticks appropriate to the situation. Another anecdotal observation showing the intelligence of this subject was that he pulled a part of the chain wound around the tree when he climbed up the tree, apparently because the chain often got stuck on the middle of the tree (fig. 4). He did this almost every time he climbed up. We tried to get the information as to how this subject acquired this tool-using skill by asking the owner if anybody had taught him to do so. The answer was no. According to the owner, nobody has ever taught him, nor has demonstrated in front of him, how to use the tool. Thus, this monkey appeared to have acquired this skill spontaneously. The fact that there were many sticks around him probably helped considerably. No matter how he learned this skill, it is now evident that flexible use of a tool, appropriate to the situation, is not only shared by apes and capuchins, but also by at least one macaque monkey.
Acknowledgments The first author of this report was determined by a coin toss. The authors are grateful to Dr. Bambang Suryobroto and Mr. Entang Iskandar of Bogor Agricultural Institute for their help in conducting the study.
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a
b
c d Fig. 4. a–d The subject pulling the chain when he climbs up the tree.
References 1 2 3 4 5 6 7 8
9 10 11
12
Sugiyama Y, Koman J: Tool using and making behavior in wild chimpanzees at Bossou, Guinea. Primates 1979;20:513–524. Goodall J: The Chimpanzees of Gombe: Patterns of Behavior. Cambridge, Harvard University Press, 1986. Chevalier-Skolnikoff S: Spontaneous tool use and sensorimotor intelligence in Cebus compared with other monkeys and apes. Behav Brain Sci 1989;12:561–627. Chevalier-Skolnikoff S: Tool use by wild Cebus monkeys at Santa Rosa National Park, Costa Rica. Primates 1990;31:375–383. Nishida T, Nakamura M: Chimpanzee tool use to clear a blocked nasal passage. Folia Primatol 1993;61: 218–220. Russon AE, Galdikas BMF: Imitation in free-ranging rehabilitant orangutans (Pongo pygmaeus). J Comp Psychol 1993;107:147–161. Russon AE, Galdikas BMF: Constraints on great apes’ imitation: Model and action selectivity in rehabilitant orangutan (Pongo pygmaeus) imitation. J Comp Psychol 1995;109:5–17. Matsuzawa T: Field experiments on use of stone tools by chimpanzees in the wild; in Wrangham RW, McGrew WC, de Waal FBM, Heltne PG (eds): Chimpanzee Cultures. Cambridge, Harvard University Press, 1994, pp 351–370. Savage-Rumbaugh ES, Roger L: Kanzi: The Ape at the Brink of the Human Mind. New York, Wiley & Sons, 1994. Visalberghi E, Limongelli L: Lack of comprehension of cause-effect relations in tool-using capuchin monkeys (Cebus apella). J Comp Psychol 1994;108:15–22. Matsuzawa T, Yamakoshi G: Comparison of chimpanzee material culture between Bossou and Nimba, West Africa; in Russon AE, Bard KA, Parker ST (eds): Reaching into Thought: The Minds of the Great Apes. Cambridge, Cambridge University Press, 1996, pp 211–232. Visalberghi E, Fragaszy DM, Savage-Rumbaugh ES: Performance in a tool-using task by common chimpanzees (Pan troglodytes), bonobos (Pan paniscus), an orangutan (Pongo pygmaeus) and capuchin monkeys (Cebus apella). J Comp Psychol 1995;109:52–60.
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Yamakoshi G, Sugiyama Y: Pestle-pounding behavior of wild chimpanzees at Bossou, Guinea. Primates 1995;36:489–500. Ingmanson EJ: Tool-using behavior in wild Pan paniscus: Social and ecological considerations; in Russon AE, Bard KA, Parker ST (eds): Reaching into Thought: The Minds of the Great Apes. Cambridge, Cambridge University Press, 1996, pp 190–210. Tokida E, Tanaka I, Takefushi H, Hagiwara T: Tool-using in Japanese macaques: Use of stones to obtain fruit from a pipe. Anim Behav 1994;47:1023–1030. Westergaard GC: Lion-tailed macaques (Macaca silenus) manufacture and use tools. J Comp Psychol 1988;102:152–159. Anderson JR: Development of tool-use to obtain food in a captive group of Macaca tonkeana. J Hum Evol 1985;14:637–645. Westergaard GC: Object manipulation and the use of tools by infant baboons (Papio cynocephalus anubis). J Comp Psychol 1992;106:398–403. Huffman MA, Quiatt D: Stone handling by Japanese macaques (Macaca fuscata): Implications for tool use of stone. Primates 1986;27:413–423. Machida S: Standing and climbing a pole by members of a captive group of Japanese monkeys. Primates 1990;31:291–298. Natale F, Poti P, Spinozzi G: Development of tool use in a macaque and a gorilla. Primates 1988;29:413–416.
Folia Primatol 1998;69:318–324
Ueno/Fujita
Received: June 4, 1997 Accepted after revision: June 18, 1997
oooooooooooooooooooooooooooooooo
Spontaneous Tool Use by a Tonkean Macaque (Macaca tonkeana) Yoshikazu Ueno a, Kazuo Fujita b a b
Center for Experimental Plants and Animals, Hokkaido University, Sapporo, and Department of Psychology, Faculty of Letters, Kyoto University, Kyoto, Japan
Key Words Tool use · Macaques · Hand preference · Distance recognition
Introduction Great apes, particularly chimpanzees, and capuchin monkeys are known to use a variety of tools, both in the laboratory and in the wild [1–14]. Among Old World monkeys, on the other hand, reports of tool use have been much scarcer. So far, there have been several reports showing that at least 3 macaque and 1 baboon species were able to use tools in situations where tool using was strongly encouraged to solve artificial problems given to the monkeys. Tokida et al. [15] reported a most elegant example performed by a female Japanese macaque. She invented a method of throwing stones into a transparent tube to obtain food from there. She chose stones of appropriate size and controlled the momentum of the stones. Finally she learned to send her infant into the tube to get the food. Lion-tailed macaques succeeded in using sticks to extract syrup from an apparatus [16]. Tonkean macaques also used a rod to obtain honey from a container [17]. Anubis baboons used soft materials to sponge sweet liquid [18]. In more natural situations, Jaqanese macaques were reported to use objects in playful contexts. Huffman and Quiatt [19] reported how stone-handling play spread among a provisioned troop. Machida [20] observed 3 juvenile females stand a pole to climb up to lick a wall. It is now evident that ability to use tools is shared not only by great apes and one unusually intelligent group of the New World monkeys, but also by some of the Old World monkeys. However, it is still unclear how flexible and adaptive Old World monkeys are in their use of tools. Natale et al. [21] compared the ability to use sticks to obtain food of a Japanese monkey and a gorilla. They noted that the Japanese macaque rotated the stick in a stereotyped movement to obtain food, getting only ran-
Fax + 41 61 306 12 34 E-Mail [email protected] www.karger.com
© 1998 S. Karger AG, Basel 0015–5713/98/0695–0318 $15.00/0 Article accessible online at: http://BioMedNet.com/karger
Yoshikazu Ueno Center for Experimental Plants and Animals Hokkaido University, N10 W8 Kita-ku, Sapporo (Japan) Tel. +81 11 706 3580, Fax +81 11 726 3476 E-Mail [email protected]
dom successes. On the other hand, the gorilla, faced with the same situation, spontaneously started to use a blanket when the stick proved to be less useful. In this report, we show a case in which a Tonkean macaque spontaneously used sticks quite flexibly in a fashion adaptive to the situation.
Method Subject Our subject was a fully adult male Macaca tonkeana named Banga (fig. 1). We found this individual during our research on the senses of taste and smell in Sulawesi macaques in 1996. This subject had been kept as a pet for 5 years by a resident in Desa Kabonga Besar, in the suburbs of Palu city, Central Sulawesi, Indonesia. The subject was chained to a tree. Procedure Preliminary Observation. We happened to witness this subject use a withered soft stalk of a coconut leaf to obtain a piece of food on the ground out of his reach (fig. 2). The tool was about 90 cm long. It was folded in the middle, hence looked like a jointed stick. One half was strong, but the other half was weak. He picked up the tool with his left hand, grasped one end with his thumb on one side and the other 4 fingers on the other side, reached for the food, moved the stick inwards until the food came within his reach, dropped the stick, picked up the food and ate it. He performed all of this in just a few seconds with a perfectly smooth movement and no hesitation. We next placed a piece of Salak, a local palm fruit (fig. 3a), out of his reach. He picked up the same stick and tried to get the food, but he failed this time, apparently because the stick was too weak to get the food stuck in the grass. He dropped the stick, immediately went to the other side of the tree to which he was chained, picked up another bamboo stick, which was much stronger than the first one, and used it in exactly the same manner as noted in the first observation to get the food successfully in just 1 or 2 s. Experiment. Two sticks of different length were used (fig. 3b, bottom two sticks). One was from the second observation. The length was 61 cm and the diameter was 1.7 cm. The other was a stem of the tree. The length was 90 cm and the diameter was 1.9–2.8 cm. Pieces of Salak fruit were presented in a green plastic bowl 11.5 cm in diameter and 7 cm deep. In a first series (condition: far), the experimenter (K.F.) put the food bowl about 35 cm out of the subject’s reach. After the subject had come up and seen the food, the experimenter placed the two sticks on one side of the monkey separated by about 50 cm from each other. The side on which the sticks were put was switched in every trial. The sticks were placed at the same distance from the monkey. The observer (Y.U.) recorded the stick and the hand the subject used. Trials were repeated 10 times and were recorded by a video camera (Sony CCD-TR303). In a second series (condition: near), the experimenter put the bowl about 10 cm out of the subject’s reach. Other conditions were exactly the same as in the first series.
Results First Series – Condition Far The subject chose the longer stick 9 times out of 10 trials. This was statistically significant (p = 0.011, one-tailed). He always used his left hand to reach the food. When the longer stick was placed on his left, he always picked it up with his left hand and immediately reached for the food. When the longer stick was on his right, he flipped it to the left with his right hand, then picked it up with his left hand 4 times out of 5 trials. In all trials, he tried to pull the food bowl towards himself. He succeeded in getting the food in 9 trials. On the last trial the food bowl rolled away and he lost sight of the small piece of food.
Tool Use by a Macaque
Folia Primatol 1998;69:318–324
319
Fig. 1. The subject M. tonkeana. Fig. 2. An example of tool use. a The subject approaches the bowl with pieces of food in it, with a stick in his left hand. b He pulls the bowl toward him with the stick. c He gets the bowl and eats the food in it.
1
2b
2a
2c
320
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a
b Fig. 3. The food we used to test the monkey’s performance (a) and the tools the subject used (b).
Tool Use by a Macaque
Folia Primatol 1998;69:318–324
321
Second Series – Condition Near The subject used each stick equally often. He chose the stick on the left with his left hand in all 10 trials, irrespective of the length of the stick. This was statistically significant (p = 0.001, one-tailed). During the course of this series, the experimenter mistakenly placed the food bowl too near the subject in 3 trials (these were not counted as test trials). In these cases, the subject extended his hand directly to get the bowl. In another trial he failed to pull the bowl with the shorter stick, because the bowl rolled away. The subject immediately changed the stick to the longer one and got the food. As a consequence, he succeeded in getting the food in all trials.
Discussion When the food was close to the macaque, he did not care about the length of the tool but picked up the one that was the most easily available to him, i.e. the one on his left. When the food was farther away, he carefully chose the longer stick. The results of the two simple experiments clearly demonstrate that this monkey ‘knew’ how he should solve the problem before he actually started to tackle it. He not only used sticks to get the food beyond his reach, but he also chose the correct stick to solve the problem. In addition, he did not insist on using the same stick once he started. He quickly changed the shorter stick to the longer one, once he recognized that the food had moved farther away. He showed similar flexibility in using the stick when he recognized that the quality of the stick was not good enough for the situation. In the second observation, he changed a weak stick for a stronger one to get the food stuck in the grass. It is clear that this monkey had the ability to use sticks appropriate to the situation. Another anecdotal observation showing the intelligence of this subject was that he pulled a part of the chain wound around the tree when he climbed up the tree, apparently because the chain often got stuck on the middle of the tree (fig. 4). He did this almost every time he climbed up. We tried to get the information as to how this subject acquired this tool-using skill by asking the owner if anybody had taught him to do so. The answer was no. According to the owner, nobody has ever taught him, nor has demonstrated in front of him, how to use the tool. Thus, this monkey appeared to have acquired this skill spontaneously. The fact that there were many sticks around him probably helped considerably. No matter how he learned this skill, it is now evident that flexible use of a tool, appropriate to the situation, is not only shared by apes and capuchins, but also by at least one macaque monkey.
Acknowledgments The first author of this report was determined by a coin toss. The authors are grateful to Dr. Bambang Suryobroto and Mr. Entang Iskandar of Bogor Agricultural Institute for their help in conducting the study.
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a
b
c d Fig. 4. a–d The subject pulling the chain when he climbs up the tree.
References 1 2 3 4 5 6 7 8
9 10 11
12
Sugiyama Y, Koman J: Tool using and making behavior in wild chimpanzees at Bossou, Guinea. Primates 1979;20:513–524. Goodall J: The Chimpanzees of Gombe: Patterns of Behavior. Cambridge, Harvard University Press, 1986. Chevalier-Skolnikoff S: Spontaneous tool use and sensorimotor intelligence in Cebus compared with other monkeys and apes. Behav Brain Sci 1989;12:561–627. Chevalier-Skolnikoff S: Tool use by wild Cebus monkeys at Santa Rosa National Park, Costa Rica. Primates 1990;31:375–383. Nishida T, Nakamura M: Chimpanzee tool use to clear a blocked nasal passage. Folia Primatol 1993;61: 218–220. Russon AE, Galdikas BMF: Imitation in free-ranging rehabilitant orangutans (Pongo pygmaeus). J Comp Psychol 1993;107:147–161. Russon AE, Galdikas BMF: Constraints on great apes’ imitation: Model and action selectivity in rehabilitant orangutan (Pongo pygmaeus) imitation. J Comp Psychol 1995;109:5–17. Matsuzawa T: Field experiments on use of stone tools by chimpanzees in the wild; in Wrangham RW, McGrew WC, de Waal FBM, Heltne PG (eds): Chimpanzee Cultures. Cambridge, Harvard University Press, 1994, pp 351–370. Savage-Rumbaugh ES, Roger L: Kanzi: The Ape at the Brink of the Human Mind. New York, Wiley & Sons, 1994. Visalberghi E, Limongelli L: Lack of comprehension of cause-effect relations in tool-using capuchin monkeys (Cebus apella). J Comp Psychol 1994;108:15–22. Matsuzawa T, Yamakoshi G: Comparison of chimpanzee material culture between Bossou and Nimba, West Africa; in Russon AE, Bard KA, Parker ST (eds): Reaching into Thought: The Minds of the Great Apes. Cambridge, Cambridge University Press, 1996, pp 211–232. Visalberghi E, Fragaszy DM, Savage-Rumbaugh ES: Performance in a tool-using task by common chimpanzees (Pan troglodytes), bonobos (Pan paniscus), an orangutan (Pongo pygmaeus) and capuchin monkeys (Cebus apella). J Comp Psychol 1995;109:52–60.
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15 16 17 18 19 20 21
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Yamakoshi G, Sugiyama Y: Pestle-pounding behavior of wild chimpanzees at Bossou, Guinea. Primates 1995;36:489–500. Ingmanson EJ: Tool-using behavior in wild Pan paniscus: Social and ecological considerations; in Russon AE, Bard KA, Parker ST (eds): Reaching into Thought: The Minds of the Great Apes. Cambridge, Cambridge University Press, 1996, pp 190–210. Tokida E, Tanaka I, Takefushi H, Hagiwara T: Tool-using in Japanese macaques: Use of stones to obtain fruit from a pipe. Anim Behav 1994;47:1023–1030. Westergaard GC: Lion-tailed macaques (Macaca silenus) manufacture and use tools. J Comp Psychol 1988;102:152–159. Anderson JR: Development of tool-use to obtain food in a captive group of Macaca tonkeana. J Hum Evol 1985;14:637–645. Westergaard GC: Object manipulation and the use of tools by infant baboons (Papio cynocephalus anubis). J Comp Psychol 1992;106:398–403. Huffman MA, Quiatt D: Stone handling by Japanese macaques (Macaca fuscata): Implications for tool use of stone. Primates 1986;27:413–423. Machida S: Standing and climbing a pole by members of a captive group of Japanese monkeys. Primates 1990;31:291–298. Natale F, Poti P, Spinozzi G: Development of tool use in a macaque and a gorilla. Primates 1988;29:413–416.
Folia Primatol 1998;69:318–324
Ueno/Fujita
