Effects of early rearing conditions on problem-solving skill in captive male chimpanzees (Pan troglodytes).код для вставкиСкачать
American Journal of Primatology 72:626–633 (2010) RESEARCH ARTICLE Effects of Early Rearing Conditions on Problem-Solving Skill in Captive Male Chimpanzees (Pan troglodytes) NARUKI MORIMURA1,2 AND YUSUKE MORI2 1 Wildlife Research Center, Kyoto University, Uki, Kumamoto, Japan 2 Chimpanzee Sanctuary Uto, Kumamoto, Japan Early rearing conditions of captive chimpanzees characterize behavioral differences in tool use, response to novelty, and sexual and maternal competence later in life. Restricted rearing conditions during early life hinder the acquisition and execution of such behaviors, which characterize the daily life of animals. This study examined whether rearing conditions affect adult male chimpanzees’ behavior skills used for solving a problem with acquired locomotion behavior. Subjects were 13 male residents of the Chimpanzee Sanctuary Uto: 5 wild-born and 8 captive-born. A pretest assessed bed building and tool use abilities to verify behavioral differences between wild- and captive-born subjects, as earlier reports have described. Second, a banana-access test was conducted to investigate the problem-solving ability of climbing a bamboo pillar for accessing a banana, which might be the most efficient food access strategy for this setting. The test was repeated in a social setting. Results show that wild-born subjects were better able than captive-born subjects to use the provided materials for bed building and tool use. Results of the banana-access test show that wild-born subjects more frequently used a bamboo pillar for obtaining a banana with an efficient strategy than captive-born subjects did. Of the eight captive-born subjects, six avoided the bamboo pillars to get a banana and instead used, sometimes in a roundabout way, an iron pillar or fence. Results consistently underscored the adaptive and sophisticated skills of wild-born male chimpanzees in problem-solving tasks. The rearing conditions affected both the behavior acquisition and the execution of behaviors that had already been acquired. Am. J. Primatol. 72:626–633, 2010. r 2010 Wiley-Liss, Inc. Key words: rearing condition; problem-solving skill; cognitive task; chimpanzees INTRODUCTION Restrictive rearing conditions in captivity affect chimpanzee (Pan troglodytes) behavior, even years after restrictions were terminated [Brent, 2001; Turner et al., 1969]. Videan  reported that wild-born chimpanzees built and used beds significantly more than captive-born individuals. Bed building is a socially facilitated learned behavior acquired during the first years of life. Menzel et al.  pointed out that wild-born chimpanzees were better at performing a task requiring the use of tools than captive-born (restriction reared) individuals were. Brent et al.  demonstrated by using a large sample size of 45 chimpanzees that behavioral differences in tool-using ability between captive- and wild-born chimpanzees appeared even in less-restrictive rearing environments, indicating that rearing conditions engender differences in later tool-use abilities. Rearing conditions affect other behaviors related to sexual and maternal competence [Brent et al., 1996]. Nursery-reared chimpanzees engaged in sexual behavior less than mother-reared individuals did [Baker et al., 2000]. Consequently, restricted rearing conditions in early lifetime make it difficult r 2010 Wiley-Liss, Inc. to acquire some behavioral repertoires; the rearing conditions, thereby, strongly affect the daily life of captive chimpanzees. The acquisition of behavior and its expression characterize the overall performance of captive chimpanzees in daily life [Pruetz & McGrew, 2001]. Anecdotal records suggest that restricted rearing conditions in early life might affect the expression of behavior that an animal acquires. At the Chimpanzee Sanctuary Uto (CSU), Japan, a nursery-reared female moved around by jumping only on concrete areas of floors in an outdoor compound, using such Contract grant sponsor: Japan Society for the Promotion of Science (JSPS) and the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan Grants-in-Aid for Scientific Research; Contract grant numbers: 19650225; 9330159; Contract grant sponsor: 2008 IPS Captive Care Grant. Correspondence to: Naruki Morimura, Wildlife Research Center, Kyoto University, 990 Ohtao, Uki, Kumamoto, 8693201, Japan. E-mail: email@example.com Received 15 April 2009; revised 16 January 2010; revision accepted 2 February 2010 DOI 10.1002/ajp.20819 Published online 4 March 2010 in Wiley InterScience (www. interscience.wiley.com). Problem-Solving Skill in Chimpanzees / 627 areas as stepping stones. It took about 1 month for her to become accustomed to walking on the ground [CSU, unpublished observations]. Another nurseryreared female at CSU used to walk on a beam while gripping the bars of the ceiling in an outdoor compound, instead of brachiating. Even though the chimpanzees had acquired behavioral skills for walking and hanging, their behaviors differed markedly from those of wild chimpanzees. Moreover, systematic studies of macaques revealed that early rearing conditions affect problem-solving behavior and their underlying cognitive processes. Isolation-reared rhesus monkeys (Macaca mulatta) adjusted more slowly to reinforcement contingencies [Lichstein & Sackett, 1971] and performed poorly on complex tasks, such as an oddity learning set [Gluck et al., 1973]. Novak and Sackett  pointed out that behavioral and cognitive problems in these isolation-reared monkeys were not simply the result of sensory deprivation attributable to a lack of opportunity to experience manipulating objects or a lack of exposure to social stimuli. The findings described above imply that chimpanzees and some other primates develop a behavioral tendency in the exertion of acquired behavior that is characterized by the early rearing condition. Little attention has been devoted to the effects of early rearing conditions on acquired behavior in captive chimpanzees. This study specifically addressed the effect of early rearing conditions on task-solving behavior of captive chimpanzees. The performance of tasks by wild- and captive-born subjects in this study was compared directly. The groups raised in the wild vs. those raised in captivity differed in their first few years. In post-infancy, almost all chimpanzees experienced isolation and all experienced biomedical testing; all had resided in an old-fashioned captive condition for most of their post-infancy life. All chimpanzees were living successfully in a social group under a less restrictive condition during the experiment period. A more likely explanation could be that differences in their rearing experiences from birth to 2–3 years of age would be the cause if group differences were found. The experiment examined the behavioral skill of chimpanzees used for accessing food by presenting a banana placed on the top or bottom of a bamboo pillar. Climbing a tree or a pillar is a common behavior both in the wild and in captivity. Accessing the roof of an outdoor compound by climbing a pillar or fence was an acquired behavioral skill in daily life for all subjects. In addition, the subjects were presented with alternatives for their access: climbing an iron pillar or fence at another place or moving along the ceiling horizontally by brachiation. Furthermore, the experiment was conducted in a social situation. This setting enabled every member to learn repeatedly, through mutual observation, how to access a banana. Under those conditions, the strategies used in solving the tasks were assessed in groups of wild- and captive-born chimpanzees. Additionally, to verify the behavioral differences between wild- and captive-born chimpanzees, described in reports of earlier studies by Videan  and Brent et al. , their bed-making and toolusing abilities were tested using a one-trial simple task before the banana-access test. A correlation of behavioral tendencies between bed-building and tool-using abilities and behavioral skills for accessing a banana, if detected, would provide complementary evidence, supporting the effects of early rearing conditions on banana-access test results. However, the experimental design of this study makes it difficult to measure the effects of early rearing conditions directly with counterbalancing of other possible influential factors, especially because of the small sample size, comprising individuals of a single sex. Consequently, the conclusions obtained from this study are expected to be more suggestive than definitive. METHODS Study Subjects and Sites The chimpanzees examined in this study were housed at the CSU (a former laboratory facility). All subjects (n 5 13) were males, including 8 captiveborn adults (Group A) and 5 wild-born adults (Group B). Group A was an all-male group of nine individuals. The remaining wild-born chimpanzees in Group A had participated in the experiment, although the records were eliminated from the data analysis of the study. Captive-born subjects included both mother- and nursery-reared individuals (Table I). Mother-reared subjects (n 5 5) were reared for more than 1 year after their birth (mean7SEM 5 14707497.9 days) by wild-born mothers in a social group. Nursery-reared subjects (n 5 3) were separated from their mothers for the first year (mean7SEM 5 103759.2 days) and reared in a nursery group. The housing types were classified as traditional. The outdoor compounds of Groups A and B were, respectively, 128 m2 (W:D:H 5 10.0:12.8:3.8 m) and 117 m2 (W:D:H 5 8.5:12.8:3.8 m). Both compounds were covered with iron mesh fences. Some grass and shrub vegetation was present on the ground. Climbing structures of logs, used fire hoses for moving, hammocks made of burlap sacks, and several feeding devices were present in the compound for environmental enrichment. Indoor rooms were old-fashioned small cells of 4 m2 (W:D:H 5 2.0:2.0:2.7 m). The subjects were isolated in indoor rooms from evening until the next morning, but they were able to communicate through the iron bars with neighboring individuals by visual and physical contact. Food and water were not controlled for the study. The care and use of the Am. J. Primatol. Am. J. Primatol. August, 2004 June, 2003 A B Group Time of group formation 16 18 20 21 21 24 Mikota Kanao Takashi Norihei Kazuya Kenji 26 26 27 27 30 16 Minato Shiro Goro Norio Naoya Takabo 15 James Name CSU, Japan CSU, Japan CSU, Japan CSU, Japan CSU, Japan CSU, Japan CSU, Japan CSU, Japan Africa Africa Africa Africa Africa Age at the study Birthplace 1983 1983 1983 1983 1980 – – – – – – – – Arrival year in Japan 2000 2000 2000 2000 2000 – – – – – – – – Arrival year at CSU (Yes) (Yes) (Yes) (Yes) (Yes) 0 390 205 388 106 1,460 2,920 2,190 Mother rearing (days) TABLE I. The Rearing Experience of 13 Male Chimpanzees in the Study n.a. n.a. n.a. n.a. n.a. Yes Yes Yes Yes Yes No No No Nursery rearing Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Isolation for biomedical experiments Rearing experience Yes Yes Yes Yes Yes Yes No Yes Yes Yes Yes Yes Yes Experience of biomedical experiments No No No No No Yes Yes Yes Yes Yes Yes Yes Yes Social living before the present group 628 / Morimura and Mori Problem-Solving Skill in Chimpanzees / 629 chimpanzees conformed to the Guide for the Care and Use of Great Apes of the Chimpanzee Sanctuary Uto, Kumamoto, Japan. This experiment was performed with CSU approval. The guide is compiled to include the ethical policy of the Primate Research Institute, Kyoto University, and domestic laws related to welfare and management of animals. Data Collection Pretest: The test consisted of two one-trial tasks––a bed-building task and a tool-using task. Each task was conducted for each subject in an indoor room at 5 pm. In the bed-building task, two natural plants (bamboo branches and straw) and two artificial objects (burlap sack and cotton sheet) were provided as bed material because material preferences might affect bed-building performance. Those objects were selected in the contrast of unfamiliar vs. familiar and natural vs. artificial. Straws and towels of cotton sheets were not provided except for the pretest. Bamboo was provided occasionally as environmental enrichment. A burlap sack was sometimes provided, especially for the nursery group, as a blanket during the night. The sizes of the bamboo stalk, fascicle of straw, burlap sack, and towel were, respectively, approximately 1.5 0.5 m, 1.0 0.2 m diameter, 0.8 1.0 m, and 1.0 2.0 m. Each of the four materials was provided only once, and on a different day. Providing objects without food provisioning in an indoor room was an unusual event for the subjects, during the study period. The task performance was recorded within 5 min after providing the material. During the period, the subjects who had made a bed or a bed-like circle structure using the material and/or those who used it as a bed were judged as successful. The tool-using task was such that a subject drank orange juice from a bottle by dipping a wooden stick during the routine food provision period in the evening. Before starting the task, an experimenter passed a wooden stick (approximately 30 cm length and 0.5 cm diameter) to a subject in an indoor room. The stick-like object of wood was familiar because some vegetation in the outdoor compound was freely accessible for the subjects. The task was started when the experimenter placed a bottle (approximately 20 cm height and 7 cm diameter) filled with orange juice in front of the cage door. Whether a subject drank juice from the bottle using the stick was observed. Successful subjects used the stick as a tool within 5 min from the beginning of the test period. The task was done only once for each subject. Banana-access test: Three bamboo pillars with no branches (approximately 6 m height and 8 cm diameter at breast height) were fixed in each outdoor compound of Groups A and B. The 3 pillars were more than 3 m distant from each other. Although some structures and fixtures for climbing up to the ceiling of the outdoor compound were present, no object that could aid climbing was placed within 1 m from a bamboo pillar. The pillars were driven straight into the ground. The top was secured to an iron bar on the ceiling using a nylon rope. Two bananas were tied with a nylon rope at the top and bottom of the pillar. To prevent subjects from finding the upper banana of each pillar from an entrance gate when they were introduced into a compound by opening the gate, the upper banana of each pillar was fixed at the opposite side of the pillar from the entrance. Bananas at the pillar bottoms were fixed at about 1 m height from the ground facing the entrance, enabling subjects to find them easily. The test was conducted in a reunited situation of a group in the morning, when they were brought together in the outdoor compound by moving them one by one from each indoor room. The test began when a first individual entered the compound and lasted until subjects had consumed all six bananas. Individuals in the first half of the order possibly obtained bananas more easily than those in the last half. Consequently, the test was repeated until all subjects had consumed more than 10 bananas by controlling the introduction order. The subjects’ behavior was observed and recorded throughout the series of tests using a digital video recording device (DCR-SR3000; Sony Corp., Tokyo, Japan). Statistical Analysis To evaluate group differences, we compared the number of each measured variable for all individuals from Groups A and B. For the pretest, a success score (0–1) was calculated for each subject for comparison between the two groups using a non-parametric Fisher’s exact test with statistical analysis software R [R Development Core Team, 2007]. Data of the banana-access tests were analyzed in terms of physical skill, experience in social setting, age, and the early rearing condition (origin). A group comparison was done fundamentally using a non-parametric Mann–Whitney U-test, because the subjects in a group to be tested were fewer than five individuals in some analyses. A comparison of ages of the two groups was tested using Student’s t-test. The significance level was set to 0.05. RESULTS In the bed-building task of the pretest, two subjects of Group A and four of Group B showed bed building or related behavior within the first 5 min. Bamboo, a familiar and natural object, was used as bedding material by four individuals in Group B (Fisher’s exact test, P 5 0.007). A burlap sack, a familiar artificial object, was used by each of two individuals in Groups A and B (Fisher’s exact test, P 5 0.510). Straw, an unfamiliar and natural object, was used by three individuals in Group B (Fisher’s exact test, P 5 0.035). No subject used the towel, an Am. J. Primatol. 630 / Morimura and Mori Number of bananas consumed unfamiliar and artificial object. They showed bedbuilding behavior, such as holding, stepping on, and shaping in a circle on the floor around them. The remaining subjects responded by dropping it on the stairs leading down to the entrance of the room, displaying it, and chewing it. Subjects of Group B used three of four materials for bed building. Each of the four subjects of Group B used more than two types of material for bed building among three materials. In contrast, two individuals of Group A who had succeeded at the task used only the burlap sack as bedding material. In the tool-using task, three of eight subjects of Group A and all five subjects of Group B drank juice using a wooden stick that had been provided as a tool. Subjects of Group B were better at the task of using tools than subjects of Group A were (Fisher’s exact test, P 5 0.044). The banana-access test was repeated for 27 and 23 sessions in Group A and B, respectively; each subject received more than 10 bananas. In all, 285 cases of accessing a banana by 13 subjects were analyzed. The average quantities of bananas consumed by subjects of Groups A and B were 18.4 and 27.6, respectively, (Mann–Whitney U-test, U 5 17.5, P 5 0.713), although the total number of bananas that each subject consumed differed greatly among subjects, presenting a range of 10–51. All subjects climbed to access a banana at the top of the bamboo pillar, ranging from 25–85% in the total consumption for each subject. The banana-accessing behaviors were categorized as climbing the bamboo, an iron pillar, or fence, and moving horizontally by walking or brachiation. These three behavioral types were used to determine the strategies for food access that were examined in the study. Group differences in each strategy for accessing a banana appeared in the bamboo use among three strategies (Mann–Whitney U-test, U 5 3.5, P 5 0.011; Fig. 1). Two subjects in Group A and five in Group B used a bamboo pillar for accessing a banana. Subjects of Group B were better at the bamboo use in solving the task than subjects of Group A (Fisher’s exact test, P 5 0.016). The remaining two strategies were not different between the two groups (Fisher’s exact test, iron pillar/fence, P 5 0.385; walking/brachiation, P 5 1.000). To determine the physical skill necessary for accessing the banana, the respective values of consumption of bananas at the bottom of bamboo pillars by walking were compared between the two groups. The average quantities of bananas at the bottom consumed by subjects of Groups A and B were 9.0 and 13.8, respectively (Mann–Whitney U-test, U 5 13.5, P 5 0.338). In addition, among seven subjects that used bamboo, the banana consumption by climbing up a bamboo pillar was not different between the two groups (Table II). The remaining two strategies showed a similar tendency. The experience of the test, namely the number of bananas consumed before taking each of three strategies for the first time, was not different among subjects of the two groups (Table III). The strategy of moving horizontally (walking/brachiation) required the least experience. Of the 13 subjects, 10 adopted the strategy for the very first access to a banana with no experience. Of the 7 subjects that used bamboo, 4 TABLE II. Comparision of Group A and B: Banana Consumption by Strategy for Accessing a Banana in the Banana-Access Test Group A Strategy n Bamboo pillar 2 Iron pillar/fence 8 Walk/brachiation 8 Group B Median (Range) n 7 (4–10) 3 (1–7) 10 (3–34) 5 4 5 Median (Range) 10 (3–19) 1.5 (1–3) 10 (5–39) U P value 3.5 0.558 7.5 0.136 19.5 0.942 GroupA(n=8) GroupB(n=5) ** TABLE III. Comparison of Group A and B Individuals: Banana Consumption as an Experience Before Using Each of Three Strategies for the First Time in the Banana-Access Test Group A bamboo iron pillar/fence walking/brachiation Banana access strategies Fig. 1. Comparison of three strategies for getting a banana between Group A (n 5 8) and B (n 5 5) subjects in the bananaaccess test. Group B banana consumption per individual using a bamboo pillar differed significantly from that of Group A. The error bars represent the standard error of the mean of banana consumption. Am. J. Primatol. Strategy n Bamboo pillar 2 Iron pillar/fence 8 Walk/brachiation 8 Group B Median (Range) n 4 (2–6) 2 (0–9) 0 (0–5) 5 4 5 Median (Range) 1 (0–20) 4 (0–22) 0 (0–2) U P value 3.0 0.434 13.5 0.668 15.5 0.373 Problem-Solving Skill in Chimpanzees / 631 used the strategy with the earlier experience of getting fewer than 3 bananas, as did 8 of 12 subjects that used the iron pillar or fence. Consequently, repetition of the test in a social setting did not aid subjects’ experience of climbing a bamboo pillar. In the test, subjects showed a strategy by which a subject got two bananas at both the top and bottom of a bamboo pillar in a sequential movement. For example, a subject climbed up to access a banana at the top of a bamboo pillar after getting a banana at the bottom of the pillar. The sequential gathering of two bananas at a bamboo pillar can be recognized in the situation in which a subject was highly motivated to get them. In the sequential gathering, climbing up and down a bamboo pillar for accessing food was the most efficient strategy. In contrast, moving to an iron pillar or fence for the remaining banana at a bamboo pillar after getting a banana at the bamboo pillar is a roundabout way. In all, 52 cases of sequential gathering were observed in the test. All subjects but one (Group A) showed sequential gathering. Sequential gathering was more frequent in Group B than in Group A (Table IV). In 33 of 52 sequential gatherings, the subject used a bamboo pillar for climbing up and down. Bamboo use in the sequential gathering was also more frequent in Group B than in Group A. All 7 subjects using bamboo in the sequential gathering showed a sophisticated strategy after a few experiences of getting bananas in a roundabout way 0–2 times. Consequently, the physical skill and the experience before adopting the strategy did not differ among the seven subjects that used bamboo in the sequential gathering. Table V presents results for each subject in the pretest and the banana-access test. Subjects of Group B were consistently better at solving tasks than subjects of Group A. The average ages of subjects of Group A and B were 18.9 and 27.2, respectively (t-test, t13 5 –5.4, Po0.001). DISCUSSION The series of tests used for this study demanded each participant’s decision-making for solving tasks. Results of the pretest and the banana-access test TABLE IV. Frequencies of Vertical Climbing (Up/Down) with Experience of a Sequential Gathering between Group A and B in the Banana-Access Test Group A Group B Behavior in a sequential gathering of bananas n Median (Range) n Median (Range) U P value All vertical climbing 7 5 0.017 2 6 (3–14) 1 (0–2) 4 (3–11) 3.0 Vertical climbing experience before using a bamboo pillar for the first time Bamboo pillar climbing 2 (1–5) 1.5 (1–2) 1 (1) 3.5 0.539 0.0 0.049 2 5 5 TABLE V. Summary of Results for the Pretest and Banana-Access Test Subjects Pretest Bed-building Group Subjects Origin A James Minato Mikota Kanao Takashi Norihei Kazuya Kenji Shiro Gorou Norio Naoya Takabo Captive-born Captive-born Captive-born Captive-born Captive-born Captive-born Captive-born Captive-born Wild-born Wild-born Wild-born Wild-born Wild-born B Bamboo Burlap sack Straw Towel Tool-using Banana-access test Bamboo climbing Am. J. Primatol. 632 / Morimura and Mori consistently revealed an identical tendency: the skills of Group B subjects were better than those of Group A subjects. The results of the two one-trial tasks were consistent with the earlier findings that the skill of wild-born subjects (Group B) is better than those of captive-born subjects (Group A). Meanwhile, novelty possibly affects material use by captive chimpanzees [Bloomsmith et al., 2006]. No subject used a towel as bedding material. The subjects’ experience with various objects had been limited through most of their lives. In addition, the one-trial task under unusual situations diminished the task-solving ability in subjects of Group A. However, subjects of Group B used unfamiliar objects as bedding material and showed better performance in the two tasks than Group A subjects under the unusual situation. Subjects of Group B were more adaptive than subjects of Group A, irrespective of the familiarity of material and experimental situations. The same group difference in solving a task emerged in the banana-access test. The behavioral difference between two groups in employing the strategy of bamboo climbing was not explainable simply by their physical ability and their experience in practicing the task. The physical abilities of subjects of the two groups were similar, indicating similarity in the banana consumption overall and similarity in walking. Among the seven subjects that used bamboo, banana consumption by climbing a bamboo pillar was not different between the two groups. Furthermore, no evidence suggested that the experience with the repetition of the test in the social setting facilitated climbing the bamboo pillar. Consequently, the results show that the pillar-climbing ability had already been acquired among subjects. The same behavioral tendencies of the two groups were reconfirmed in the sophisticated strategy of sequential gathering in the task. Age and differences of origin of the two groups are possible factors influencing the group difference. The effect of origin (early rearing condition) on the group difference was not examined independently of age, because captive-born individuals are generally the offspring of wild-born individuals. The studies of infant and juvenile chimpanzees (2–4 years old) revealed that tool use and communication skills became more flexible and sophisticated with age [Bard & Russell, 1999; Tomasello et al., 1994]. In contrast, old chimpanzees (30–40 years old) showed less aggressive behavior and object manipulation than younger chimpanzees (11–20 years old) [Baker, 2000]. Adult chimpanzees become less capable of daily life behaviors with age. Results of this study show that behavioral differences with age arising from behavioral development were insufficient to explain the group difference: the older subjects (Group B) of 27.2 years, on average, showed better skills in solving the tasks than younger subjects (Group A) of 18.9 years. Am. J. Primatol. Therefore, their experiences, specifically their different early rearing conditions––mother rearing in the wild and mother and human rearing in captivity––might provide a simpler explanation for the group differences that were observed consistently. Results of this study underscored the adaptive and sophisticated skills of wild-born chimpanzees in problem-solving tasks. Wild-born chimpanzees (Group B) used various objects with several alternatives for solving tasks efficiently, but captive-born chimpanzees (Group A) had fewer options for solving the tasks, and performed inefficiently. The results suggest that behavioral differences, according to the different rearing condition in the subjects’ first few years of life, were manifested not only in the behavioral repertoire of skills that they experienced and acquired, but also in the exertion of acquired behaviors in problem-solving, which is associated with underlying cognitive processes. The result implies that wild-born chimpanzees understand and utilize living spaces differently from captive-born chimpanzees. That cognitive difference [de Waal & Aureli, 1996] might affect bed building, tool use, maternal competence, and social communication skills throughout the life of captiveborn chimpanzees. Some physical and social deficits of captive-born adult chimpanzees might arise from the execution of behavioral repertoires that are acquired early in a chimpanzee’s life. Meanwhile, the higher-order intelligence of chimpanzees is apparently sufficient to compensate for the negative effects of early rearing conditions to some degree. The adaptive skills of two captive-born chimpanzees in the banana-access test suggest the flexibility of chimpanzee intelligence and the importance of environmental enrichment for the care of captive chimpanzees, as described by Bloomsmith et al. . Environmental enrichment programs should take rearing conditions into consideration, especially for restrictively reared chimpanzees, so that less skilled chimpanzees have plenty of time to become accustomed to the program in a better way through the experience of problem-solving. Further study is necessary to examine the effects of early rearing conditions on captive chimpanzee behavior in a large sample, including both sexes: this study investigated only 13 males at the CSU. Mother-reared and nursery-reared individuals of captive-born chimpanzees might differ in their execution of acquired behavior [e.g. Baker et al., 2000; Brent et al., 1995]. Better understanding of the effects of early rearing conditions on captive chimpanzees’ behavior in later life is necessary for alleviating the effects of rearing conditions and for improving the quality of life of captive-born, especially human-reared and nursery-reared chimpanzees. These efforts and results are expected to contribute greatly to establishing sustainable captive populations of chimpanzees. Problem-Solving Skill in Chimpanzees / 633 ACKNOWLEDGMENTS This research was financially supported by the 2008 IPS Captive Care Grant to Naruki Morimura. Thanks to Masaki Tomonaga, Susana Carvalho, and anonymous reviewers for their insightful comments related to an earlier version of the article. We also thank the staff members of the Department of Welfare and Longevity in the Wildlife Research Center, Kyoto University, and the Chimpanzee Sanctuary Uto for caring for the chimpanzees. All animal care and handling conformed to the Guide for the Care and Use of Great Apes of CSU. The experiments were performed with CSU approval. The guide is compiled with the ethical policy of Primate Research Institute, Kyoto University, ASP Principles for the Ethical Treatment of nonhuman Primates, and domestic laws on welfare and management of captive animals. 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