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Japanese monkeys (Macaca fuscata) discriminate between pictures of conspecific males and females without specific training
Behavioural Processes 79 (2008) 70–73
Contents lists available at ScienceDirect
Behavioural Processes journal homepage: www.elsevier.com/locate/behavproc
Short report
Japanese monkeys (Macaca fuscata) discriminate between pictures of conspecific males and females without specific training Reiko Koba ∗ , Akihiro Izumi 1 Primate Research Institute, Kyoto University, Kanrin 41, Inuyama 484-8506, Japan
a r t i c l e
i n f o
Article history: Received 14 November 2007 Received in revised form 31 March 2008 Accepted 11 April 2008 Keywords: Japanese macaque Sex categorization Conspecific picture Visual paired comparison Novelty preference
a b s t r a c t We investigated whether Japanese monkeys can discriminate pictures of conspecific males and females using a visual paired comparison (VPC) task. Whole-body pictures of adult and nonadult monkeys were used as stimuli. The monkeys were first familiarized with pairs of pictures of different monkeys from one sex category (the familiarized sex). Pairs of novel pictures of a member of the familiarized sex and the opposite sex (novel) were then presented in test. The monkeys showed a preference for novel-sex pictures of both adult and nonadult individuals, indicating that they perceive the differences between familiarized- and novel-sex pictures. These results suggest that monkeys discriminate between pictures of males and females without specific training. © 2008 Elsevier B.V. All rights reserved.
1. Introduction Sex categorization seems to have a fundamental role in reproductive success in primates. We previously demonstrated that Japanese monkeys were able to discriminate between pictures of conspecific males and females after substantial training (Koba and Izumi, 2006). Many previous studies have also reported that primates possess the capacity for discrimination of others’ various attributes, such as species, individuality, and kinship using tasks such as discrimination tasks and matching-to-sample tasks (Yoshikubo, 1985; Parr and de Waal, 1999; Parr et al., 2000). Since these tasks needed substantial amount of training and repeated presentation of training stimuli, it is difficult to investigate spontaneous discrimination abilities. In these tasks, we could not know whether the training made it possible for primates to discriminate others’ various attributes or they were spontaneously able to discriminate. In the present study, we used a visual paired comparison (VPC) task to investigate whether monkeys discriminate the sex of conspecific individuals without specific training. In the VPC task, after the subjects were habituated with stimuli from famil-
∗ Corresponding author. Present address: Department of Animal Models for Human Disease, National Institute of Neuroscience, National Center of Neurology and Psychiatry, 4-1-1 Ogawa-Higashi, Kodaira, Tokyo 187-8502, Japan. E-mail address: [email protected] (R. Koba). 1 Akihiro Izumi is also now at the same institute. 0376-6357/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.beproc.2008.04.005
iarization category, a pair of stimuli of the familiarization and novel category appeared in the test. A preference for looking at novel category stimuli implied the subjects perceive the differences between stimuli of familiarization and novel category. As this procedure measures the subjects’ looking behavior and requires no specific training, it is suitable for investigating cognitive abilities in human infants and nonhumans. For example, Quinn et al. (2002) revealed the sex categorization of faces by human infants with the VPC task. Gunderson and Sackett (1984) made use of the task to examine the developmental changes of visual recognition in pigtail monkeys. Murai et al. (2004) examined whether infant Japanese macaques categorize objects (animals, furniture, and vehicles) without training. Because the VPC task is applicable both to humans and nonhumans, some studies have used this task to directly compare cognition in humans and nonhuman primates (Pascalis and Bachevalier, 1998; Deputte et al., 2001; Neiworth et al., 2007). In previous studies using the VPC task, monkeys’ movements were controlled during the presentation of stimuli. For example, monkeys were placed in a primate chair (Zola et al., 2000; Gothard et al., 2004) or placed in a small testing cage (Deputte et al., 2001), while infant monkeys were held by human caretakers (Gunderson and Sackett, 1984; Murai et al., 2004). To maintain monkeys’ attention to the monitor, monkeys were given juice when they looked at a monitor (Gothard et al., 2004; Dufour et al., 2006). In the present study, the experiments were conducted in our subject monkeys’ usual cage and the subjects were allowed to move away from the monitor. We measured the subjects’ voluntary looking behavior
R. Koba, A. Izumi / Behavioural Processes 79 (2008) 70–73
71
Fig. 1. (a) Schematic representation of the apparatus attached to an individual cage. (b) Example of video-captured image of a subject monkey looking rightward. (c) Example of a trial. After the subject monkey was familiarized with pairs of adult-female pictures (f1 to f8) in the four familiarization presentations, a pair of an adult-female (f9, familiarized sex) and an adult-male picture (m1, novel sex) appeared in the test presentation.
toward stimuli. Such an experimental setting was chosen so that we could effectively collect data from many experimentally na¨ıve monkeys.
stimulus monkeys because they had been reared in one of the colonies in past times. 2.3. Procedure
2. Materials and methods 2.1. Subjects The subjects were 45 Japanese macaques (Macaca fuscata, 24 males and 21 females) aged between 3 and 20 years. They were housed in 80 cm wide × 80 cm deep × 180 cm high individual cages with water freely available. They were fed with about 100 g of monkey pellets twice a day. The use of the monkeys adhered to the “Guide for the Care and Use of Laboratory Primates (Second Edition, 2002)” of the Primate Research Institute, Kyoto University. 2.2. Stimuli A total of 120 colored still pictures of 30 male and 30 female Japanese macaques were used as stimuli. Two different pictures were prepared for each stimulus monkey. For each sex, stimuli were classified into two age groups (adult stimuli: 7–26 years old; nonadult stimuli: 3–6 years old). The resolution of the stimuli was 500 × 500 pixels, and the picture size was approximately 13.5 cm wide × 13.5 cm high on the display. Each picture depicted clearly a frontal view of the monkey’s whole body. Nipples and underbelly were easily seen in each picture. The stimulus monkeys were shown as sitting down with neutral faces. For each stimulus picture, the background was made black. The pictures were taken in seven open-air colonies or six group cages of the Primate Research Institute, Kyoto University, from April to July, 2004. Most stimulus monkeys were unfamiliar with the subject monkeys. However, there was possibility that some subject monkeys had met a few
The experiments were carried out in the cage rooms where the subject monkeys had been housed for about a week before the test. We used one of the individual cages as the testing cage. The subjects were moved into the testing cage from their home cage for daily trials. A large acrylic panel with a 21.3-in. TFT color computer monitor faced the testing cage (Fig. 1a). The monitor was approximately 20 cm away from the front side of the testing cage. The stimuli were presented on the monitor using a customized program. The subjects’ behaviors, such as head and eye movements, were monitored and recorded for later analysis using a camera located at the center of the monitor (Fig. 1b). A trial consisted of four familiarization presentations and one test presentation (Fig. 1c). Each familiarization and test presentation lasted 5 s. Each interval between two presentations was longer than 3 s. Each presentation was initiated when an experimenter, who sat behind the apparatus, judged that the subjects’ eyes were oriented toward the monitor. In a familiarization presentation, subjects were presented a pair of pictures from different monkeys of one sex category (i.e., familiarized sex). After the four familiarization presentations, one test presentation then appeared. The stimuli for the test presentation were a pair of a novel picture of the familiarized sex and a picture of the opposite sex (i.e., novel sex). The left–right positions of the stimuli were counterbalanced across trials. There were four-test conditions (two familiarized sex (male or female) × two age groups of stimuli (adult or nonadult)). For example, when adult-female pictures appeared in the familiarization presentations, an adult-female and adult-male picture pair appeared in the test presentation (i.e., adult, female-
72
R. Koba, A. Izumi / Behavioural Processes 79 (2008) 70–73
familiarization; Fig. 1c). Each monkey had 6 trials per day and completed 24 trials, including 12 male-familiarization (4 adult trials and 8 nonadult trials) and 12 female-familiarization (4 adult trials and 8 nonadult trials). 2.4. Analysis We assessed subjects’ looking behavior from video recordings frame by frame. Because the camera was placed in the middle of the monitor, subjects’ looking direction (direction of head and eyes, left or right) could be easily assessed. In case when subjects’ looking direction was difficult to determine or subjects faced away from the monitor, these durations were excluded from the analysis. If a subject attended to less than 30% of the total duration of four familiarization presentations, the trial was excluded from the analysis. A score of novel-sex preference was calculated for each test presentation: percentage of novel-sex preference = looking time at novel-sex stimuli/(looking time at familiar sex stimuli + looking time at novel-sex stimuli) × 100. To avoid biases in assessment, the experimenter did not know the positions of the familiarized- and novel-sex pictures. If the monkeys discriminated the pictures based on the sex of the depicted individuals, then the looking times at novel-sex stimuli would be longer than those at familiarized-sex stimuli (i.e. novel-sex preference would be above 50%). Stimulusdirected behavior such as lip smacking, touching and hindquarter presentation were observed, but these behaviors were not analyzed as occurrences because they were infrequent and highly variable among subjects. 3. Results and discussion For the analysis, we included 33 of the 45 monkeys that completed all four-test conditions. Table 1 shows the mean looking times and percentages of novel-sex preferences for each stimulus condition during the test presentations. For both male and female subjects, a t-test showed that the percentage of novel-sex preference was significantly above the chance level of 50% in each of the four stimulus conditions. These results suggested that the monkeys discriminated familiarized- and novel-sex pictures. As in our previous study (Koba and Izumi, 2006), the present results revealed that Japanese monkeys have the ability to discriminate between whole-body pictures of males and females. The present results are neither monkeys have similar concept of sex that humans have nor they use the same cues to those of humans in sex categorization. The discrimination has probably been based on visual differences in the whole-body pictures associated with sex. In the previous study (Koba and Izumi, 2006), it was unknown whether the training was necessary for the monkeys to perform sex discrimination because the monkeys were tested after substantial training. In that study, two male Japanese monkeys were trained
to perform a two-choice sex categorization task in which each of two choice keys was assigned to male and female, respectively. The monkeys showed successful transfer of discrimination in the test with novel monkey pictures. The monkeys in the present study were not trained to perform such a discrimination task, so we conclude the monkeys performed sex discrimination spontaneously. However we do not know whether some sort of experience is necessary for the monkeys to acquire the ability. Social interaction with other individuals in childhood might be important. To examine the effect of familiarized sex (male or female) and stimulus age (adult or nonadult), a two-way repeated measure ANOVA was conducted for each of the male and female subjects. Both male and female subjects looked longer at the novelsex stimuli when the stimuli were adult monkeys than when they were nonadults (male: F(1, 17) = 5.43, p = 0.032; female: F(1, 14) = 4.87, p = 0.045). The reason why the subject monkeys showed less novel-sex preference for nonadult pictures might be that they had difficulty in discriminating nonadult males and females. Male scrotums and female nipples in nonadult monkeys are less conspicuous than in adults. Nipples and testis mature fully at about 10 and 7 years old, respectively (Hamada et al., 2005). Our present results are consistent with those of Koba and Izumi (2006), in which monkeys discriminated between the pictures of adult males and females, but discrimination of nonadult (3–6 years old) pictures was difficult. Male subjects looked significantly longer at the novel-sex pictures when the familiarized sex was female than when it was male (F(1, 17) = 6.47, p = 0.021). The data from the female subjects did not show such an effect of familiarized sex (F(1, 14) = 0.01, p = 0.911). There was no interaction between the two factors (male: F(1, 17) = 0.75, p = 0.400; female: F(1, 14) = 0.03, p = 0.865). These results have suggested that the male subjects attended more to the pictures of males than to those of females in the test presentations. Female subjects did not show such a sex preference, implying that there were sex differences of attention toward other monkeys. Another possible explanation of this sex difference is that the reproductive states of the female subjects affected their preferences toward conspecifics. Cycling female rhesus monkeys looked longer at the faces of male conspecifics than at female faces when estradiol levels were high (Lacreuse et al., 2007). Further studies should examine the interaction between preference for the sex of conspecifics and the reproductive states of subject monkeys. Preferences for the opposite sex of conspecifics are affected by different visual attributes of stimuli (Waitt et al., 2003), and it is likely that visual attributes contribute to mate choice in monkeys. The ability to discriminate between other individuals may serves as a basis for mate choice in primate. Table 2 summarizes the number of subjects included and excluded from the analysis. The proportion of excluded subjects in adults was higher than that in nonadults, but there was no signif-
Table 1 Mean looking times and percentages of novelty preferences for each stimulus condition during the test presentations Subject
Male
Stimulus
Novel-sex preference (%)
t
p
Familiarized sex
Age group
Novel sex
Male
Adult Nonadult Adult Nonadult
2.3 2.2 3.0 2.4
± ± ± ±
1.5 1.7 1.6 1.6
1.5 1.4 1.1 1.3
± ± ± ±
1.4 1.4 1.1 1.2
60.8 57.8 73.2 64.0
± ± ± ±
18.5 11.9 13.4 12.5
2.48 2.77 7.36 4.74
0.024 0.013 <0.001 <0.001
Adult Nonadult Adult Nonadult
2.6 1.8 2.8 2.2
± ± ± ±
1.6 1.5 1.4 1.6
1.1 1.3 1.4 1.2
± ± ± ±
1.3 1.5 1.3 1.2
70.0 62.0 68.7 62.1
± ± ± ±
17.7 16.5 16.8 17.0
4.40 2.82 4.31 2.75
<0.001 0.014 <0.001 0.016
Female Female
Looking time (s)
Male Female
Familiar sex
Looking times and percentages of novelty preferences are shown as mean ± S.D. Percentages of novelty preferences were compared to the chance level (50%) with t tests.
R. Koba, A. Izumi / Behavioural Processes 79 (2008) 70–73 Table 2 Number of included and excluded subjects in the analysis Excluded
References
Age group
Sex
Adult
Male Female
9 8
5 4
35.7 33.3
Nonadult
Male Female
9 7
1 2
10.0 12.5
33
12
26.7
Total
Included
73
Excluded (%)
icant difference (p = 0.15, Fisher’s exact test), possibly because the number of subjects was not sufficiently high. Older monkeys might have been less interested in the stimuli than younger monkeys, and they also might have been affected more by the environment of the cage room where other monkeys were kept. To collect data more efficiently, therefore, it might be better to only use young monkeys. In the present study, the monkeys were allowed to move away from the monitor, and they looked at the stimulus voluntarily. Although it was true that many monkeys failed to complete the experiment, we were able to collect data from many untrained monkeys while they remained in their usual cages. The present method is thus suggested as a convenient way to assess cognitive abilities in large numbers of monkeys without training. Acknowledgments We thank Nobuo Masataka, Sumiharu Nagumo for support throughout the research. Thanks are also extended to Akemi Kato and Satomi Araya for assistance and the daily care of the monkeys. This work was supported by a Grant for Biodiversity Research of the 21st Century COE (A14, Kyoto University) from the Ministry of Education, Culture, Sports, Science and Technology of Japan. The present study complies with the laws of Japan.
Deputte, B.L., Pelletier, S., Barbe, S., 2001. Visual categorization of natural and abstract items in forest monkeys and humans. Behav. Process. 55, 51–64. Dufour, V., Pascalis, O., Petit, O., 2006. Face processing limitation to own species in primates: a comparative study in brown capuchins, Tonkean macaques and humans. Behav. Process. 73, 107–113. Gothard, K.M., Erickson, C.A., Amaral, D.G., 2004. How do rhesus monkeys (Macaca mulatta) scan faces in a visual paired comparison task? Anim. Cogn. 7, 25–36. Gunderson, V.M., Sackett, G.P., 1984. Development of pattern recognition in infant pigtailed macaques (Macaca nemestrina). Dev. Psychol. 20, 418–426. Hamada, Y., Suzuki, J., Ohkura, S., Hayakawa, S., 2005. Changes in testicular and nipple volume related to age and seasonality in Japanese macaques (Macaca fuscata), especially in the pre- and post-pubertal periods. Primates 46, 33–45. Koba, R., Izumi, A., 2006. Sex categorization of conspecific pictures in Japanese monkeys (Macaca fuscata). Anim. Cogn. 9, 183–191. Lacreuse, A., Martin-Malivel, J., Lange, H.S., Herndon, J.G., 2007. Effects of the menstrual cycle on looking preferences for faces in female rhesus monkeys. Anim. Cogn. 10, 105–111. Murai, C., Tomonaga, M., Kamegai, K., Terazawa, N., Yamaguchi, M.K., 2004. Do infant Japanese macaques (Macaca fuscata) categorize objects without specific training? Primates 45, 1–6. Neiworth, J.J., Hassett, J.M., Sylvester, C.J., 2007. Face processing in humans and new world monkeys: the influence of experiential and ecological factors. Anim. Cogn. 10, 125–134. Pascalis, O., Bachevalier, J., 1998. Face recognition in primates: a cross-species study. Behav. Process. 43, 87–96. Parr, L.A., de Waal, F.B.M., 1999. Visual kin recognition in chimpanzees. Nature 399, 647–648. Parr, L.A., Winslow, J.T., Hopkins, W.D., de Waal, F.B.M., 2000. Recognizing facial cues: individual discrimination by chimpanzees (Pan troglodytes) and rhesus monkeys (Macaca mulatta). J. Comp. Psychol. 114, 47–60. Quinn, P.C., Yahr, J., Kuhn, A., Slater, A.M., Pascalis, O., 2002. Representation of the gender of human faces by infants: a preference for female. Perception 31, 1109–1121. Waitt, C., Little, A.C., Wolfensohn, S., Honess, P., Brown, A.P., Buchanan-Smith, H.M., Perrett, D.I., 2003. Evidence from rhesus macaques suggests that male coloration plays a role in female primate mate choice. Proc. R. Soc. Lond. B Biol. Sci. Suppl. 270, 144–146. Yoshikubo, S., 1985. Species discrimination and concept formation by rhesus monkeys (Macaca mulatta). Primates 26, 285–299. Zola, S.M., Squire, L.R., Teng, E., Stefanacci, L., Buffalo, E.A., Clark, R.E., 2000. Impaired recognition memory in monkeys after damage limited to the hippocampal region. J. Neurosci. 20, 451–463.
Contents lists available at ScienceDirect
Behavioural Processes journal homepage: www.elsevier.com/locate/behavproc
Short report
Japanese monkeys (Macaca fuscata) discriminate between pictures of conspecific males and females without specific training Reiko Koba ∗ , Akihiro Izumi 1 Primate Research Institute, Kyoto University, Kanrin 41, Inuyama 484-8506, Japan
a r t i c l e
i n f o
Article history: Received 14 November 2007 Received in revised form 31 March 2008 Accepted 11 April 2008 Keywords: Japanese macaque Sex categorization Conspecific picture Visual paired comparison Novelty preference
a b s t r a c t We investigated whether Japanese monkeys can discriminate pictures of conspecific males and females using a visual paired comparison (VPC) task. Whole-body pictures of adult and nonadult monkeys were used as stimuli. The monkeys were first familiarized with pairs of pictures of different monkeys from one sex category (the familiarized sex). Pairs of novel pictures of a member of the familiarized sex and the opposite sex (novel) were then presented in test. The monkeys showed a preference for novel-sex pictures of both adult and nonadult individuals, indicating that they perceive the differences between familiarized- and novel-sex pictures. These results suggest that monkeys discriminate between pictures of males and females without specific training. © 2008 Elsevier B.V. All rights reserved.
1. Introduction Sex categorization seems to have a fundamental role in reproductive success in primates. We previously demonstrated that Japanese monkeys were able to discriminate between pictures of conspecific males and females after substantial training (Koba and Izumi, 2006). Many previous studies have also reported that primates possess the capacity for discrimination of others’ various attributes, such as species, individuality, and kinship using tasks such as discrimination tasks and matching-to-sample tasks (Yoshikubo, 1985; Parr and de Waal, 1999; Parr et al., 2000). Since these tasks needed substantial amount of training and repeated presentation of training stimuli, it is difficult to investigate spontaneous discrimination abilities. In these tasks, we could not know whether the training made it possible for primates to discriminate others’ various attributes or they were spontaneously able to discriminate. In the present study, we used a visual paired comparison (VPC) task to investigate whether monkeys discriminate the sex of conspecific individuals without specific training. In the VPC task, after the subjects were habituated with stimuli from famil-
∗ Corresponding author. Present address: Department of Animal Models for Human Disease, National Institute of Neuroscience, National Center of Neurology and Psychiatry, 4-1-1 Ogawa-Higashi, Kodaira, Tokyo 187-8502, Japan. E-mail address: [email protected] (R. Koba). 1 Akihiro Izumi is also now at the same institute. 0376-6357/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.beproc.2008.04.005
iarization category, a pair of stimuli of the familiarization and novel category appeared in the test. A preference for looking at novel category stimuli implied the subjects perceive the differences between stimuli of familiarization and novel category. As this procedure measures the subjects’ looking behavior and requires no specific training, it is suitable for investigating cognitive abilities in human infants and nonhumans. For example, Quinn et al. (2002) revealed the sex categorization of faces by human infants with the VPC task. Gunderson and Sackett (1984) made use of the task to examine the developmental changes of visual recognition in pigtail monkeys. Murai et al. (2004) examined whether infant Japanese macaques categorize objects (animals, furniture, and vehicles) without training. Because the VPC task is applicable both to humans and nonhumans, some studies have used this task to directly compare cognition in humans and nonhuman primates (Pascalis and Bachevalier, 1998; Deputte et al., 2001; Neiworth et al., 2007). In previous studies using the VPC task, monkeys’ movements were controlled during the presentation of stimuli. For example, monkeys were placed in a primate chair (Zola et al., 2000; Gothard et al., 2004) or placed in a small testing cage (Deputte et al., 2001), while infant monkeys were held by human caretakers (Gunderson and Sackett, 1984; Murai et al., 2004). To maintain monkeys’ attention to the monitor, monkeys were given juice when they looked at a monitor (Gothard et al., 2004; Dufour et al., 2006). In the present study, the experiments were conducted in our subject monkeys’ usual cage and the subjects were allowed to move away from the monitor. We measured the subjects’ voluntary looking behavior
R. Koba, A. Izumi / Behavioural Processes 79 (2008) 70–73
71
Fig. 1. (a) Schematic representation of the apparatus attached to an individual cage. (b) Example of video-captured image of a subject monkey looking rightward. (c) Example of a trial. After the subject monkey was familiarized with pairs of adult-female pictures (f1 to f8) in the four familiarization presentations, a pair of an adult-female (f9, familiarized sex) and an adult-male picture (m1, novel sex) appeared in the test presentation.
toward stimuli. Such an experimental setting was chosen so that we could effectively collect data from many experimentally na¨ıve monkeys.
stimulus monkeys because they had been reared in one of the colonies in past times. 2.3. Procedure
2. Materials and methods 2.1. Subjects The subjects were 45 Japanese macaques (Macaca fuscata, 24 males and 21 females) aged between 3 and 20 years. They were housed in 80 cm wide × 80 cm deep × 180 cm high individual cages with water freely available. They were fed with about 100 g of monkey pellets twice a day. The use of the monkeys adhered to the “Guide for the Care and Use of Laboratory Primates (Second Edition, 2002)” of the Primate Research Institute, Kyoto University. 2.2. Stimuli A total of 120 colored still pictures of 30 male and 30 female Japanese macaques were used as stimuli. Two different pictures were prepared for each stimulus monkey. For each sex, stimuli were classified into two age groups (adult stimuli: 7–26 years old; nonadult stimuli: 3–6 years old). The resolution of the stimuli was 500 × 500 pixels, and the picture size was approximately 13.5 cm wide × 13.5 cm high on the display. Each picture depicted clearly a frontal view of the monkey’s whole body. Nipples and underbelly were easily seen in each picture. The stimulus monkeys were shown as sitting down with neutral faces. For each stimulus picture, the background was made black. The pictures were taken in seven open-air colonies or six group cages of the Primate Research Institute, Kyoto University, from April to July, 2004. Most stimulus monkeys were unfamiliar with the subject monkeys. However, there was possibility that some subject monkeys had met a few
The experiments were carried out in the cage rooms where the subject monkeys had been housed for about a week before the test. We used one of the individual cages as the testing cage. The subjects were moved into the testing cage from their home cage for daily trials. A large acrylic panel with a 21.3-in. TFT color computer monitor faced the testing cage (Fig. 1a). The monitor was approximately 20 cm away from the front side of the testing cage. The stimuli were presented on the monitor using a customized program. The subjects’ behaviors, such as head and eye movements, were monitored and recorded for later analysis using a camera located at the center of the monitor (Fig. 1b). A trial consisted of four familiarization presentations and one test presentation (Fig. 1c). Each familiarization and test presentation lasted 5 s. Each interval between two presentations was longer than 3 s. Each presentation was initiated when an experimenter, who sat behind the apparatus, judged that the subjects’ eyes were oriented toward the monitor. In a familiarization presentation, subjects were presented a pair of pictures from different monkeys of one sex category (i.e., familiarized sex). After the four familiarization presentations, one test presentation then appeared. The stimuli for the test presentation were a pair of a novel picture of the familiarized sex and a picture of the opposite sex (i.e., novel sex). The left–right positions of the stimuli were counterbalanced across trials. There were four-test conditions (two familiarized sex (male or female) × two age groups of stimuli (adult or nonadult)). For example, when adult-female pictures appeared in the familiarization presentations, an adult-female and adult-male picture pair appeared in the test presentation (i.e., adult, female-
72
R. Koba, A. Izumi / Behavioural Processes 79 (2008) 70–73
familiarization; Fig. 1c). Each monkey had 6 trials per day and completed 24 trials, including 12 male-familiarization (4 adult trials and 8 nonadult trials) and 12 female-familiarization (4 adult trials and 8 nonadult trials). 2.4. Analysis We assessed subjects’ looking behavior from video recordings frame by frame. Because the camera was placed in the middle of the monitor, subjects’ looking direction (direction of head and eyes, left or right) could be easily assessed. In case when subjects’ looking direction was difficult to determine or subjects faced away from the monitor, these durations were excluded from the analysis. If a subject attended to less than 30% of the total duration of four familiarization presentations, the trial was excluded from the analysis. A score of novel-sex preference was calculated for each test presentation: percentage of novel-sex preference = looking time at novel-sex stimuli/(looking time at familiar sex stimuli + looking time at novel-sex stimuli) × 100. To avoid biases in assessment, the experimenter did not know the positions of the familiarized- and novel-sex pictures. If the monkeys discriminated the pictures based on the sex of the depicted individuals, then the looking times at novel-sex stimuli would be longer than those at familiarized-sex stimuli (i.e. novel-sex preference would be above 50%). Stimulusdirected behavior such as lip smacking, touching and hindquarter presentation were observed, but these behaviors were not analyzed as occurrences because they were infrequent and highly variable among subjects. 3. Results and discussion For the analysis, we included 33 of the 45 monkeys that completed all four-test conditions. Table 1 shows the mean looking times and percentages of novel-sex preferences for each stimulus condition during the test presentations. For both male and female subjects, a t-test showed that the percentage of novel-sex preference was significantly above the chance level of 50% in each of the four stimulus conditions. These results suggested that the monkeys discriminated familiarized- and novel-sex pictures. As in our previous study (Koba and Izumi, 2006), the present results revealed that Japanese monkeys have the ability to discriminate between whole-body pictures of males and females. The present results are neither monkeys have similar concept of sex that humans have nor they use the same cues to those of humans in sex categorization. The discrimination has probably been based on visual differences in the whole-body pictures associated with sex. In the previous study (Koba and Izumi, 2006), it was unknown whether the training was necessary for the monkeys to perform sex discrimination because the monkeys were tested after substantial training. In that study, two male Japanese monkeys were trained
to perform a two-choice sex categorization task in which each of two choice keys was assigned to male and female, respectively. The monkeys showed successful transfer of discrimination in the test with novel monkey pictures. The monkeys in the present study were not trained to perform such a discrimination task, so we conclude the monkeys performed sex discrimination spontaneously. However we do not know whether some sort of experience is necessary for the monkeys to acquire the ability. Social interaction with other individuals in childhood might be important. To examine the effect of familiarized sex (male or female) and stimulus age (adult or nonadult), a two-way repeated measure ANOVA was conducted for each of the male and female subjects. Both male and female subjects looked longer at the novelsex stimuli when the stimuli were adult monkeys than when they were nonadults (male: F(1, 17) = 5.43, p = 0.032; female: F(1, 14) = 4.87, p = 0.045). The reason why the subject monkeys showed less novel-sex preference for nonadult pictures might be that they had difficulty in discriminating nonadult males and females. Male scrotums and female nipples in nonadult monkeys are less conspicuous than in adults. Nipples and testis mature fully at about 10 and 7 years old, respectively (Hamada et al., 2005). Our present results are consistent with those of Koba and Izumi (2006), in which monkeys discriminated between the pictures of adult males and females, but discrimination of nonadult (3–6 years old) pictures was difficult. Male subjects looked significantly longer at the novel-sex pictures when the familiarized sex was female than when it was male (F(1, 17) = 6.47, p = 0.021). The data from the female subjects did not show such an effect of familiarized sex (F(1, 14) = 0.01, p = 0.911). There was no interaction between the two factors (male: F(1, 17) = 0.75, p = 0.400; female: F(1, 14) = 0.03, p = 0.865). These results have suggested that the male subjects attended more to the pictures of males than to those of females in the test presentations. Female subjects did not show such a sex preference, implying that there were sex differences of attention toward other monkeys. Another possible explanation of this sex difference is that the reproductive states of the female subjects affected their preferences toward conspecifics. Cycling female rhesus monkeys looked longer at the faces of male conspecifics than at female faces when estradiol levels were high (Lacreuse et al., 2007). Further studies should examine the interaction between preference for the sex of conspecifics and the reproductive states of subject monkeys. Preferences for the opposite sex of conspecifics are affected by different visual attributes of stimuli (Waitt et al., 2003), and it is likely that visual attributes contribute to mate choice in monkeys. The ability to discriminate between other individuals may serves as a basis for mate choice in primate. Table 2 summarizes the number of subjects included and excluded from the analysis. The proportion of excluded subjects in adults was higher than that in nonadults, but there was no signif-
Table 1 Mean looking times and percentages of novelty preferences for each stimulus condition during the test presentations Subject
Male
Stimulus
Novel-sex preference (%)
t
p
Familiarized sex
Age group
Novel sex
Male
Adult Nonadult Adult Nonadult
2.3 2.2 3.0 2.4
± ± ± ±
1.5 1.7 1.6 1.6
1.5 1.4 1.1 1.3
± ± ± ±
1.4 1.4 1.1 1.2
60.8 57.8 73.2 64.0
± ± ± ±
18.5 11.9 13.4 12.5
2.48 2.77 7.36 4.74
0.024 0.013 <0.001 <0.001
Adult Nonadult Adult Nonadult
2.6 1.8 2.8 2.2
± ± ± ±
1.6 1.5 1.4 1.6
1.1 1.3 1.4 1.2
± ± ± ±
1.3 1.5 1.3 1.2
70.0 62.0 68.7 62.1
± ± ± ±
17.7 16.5 16.8 17.0
4.40 2.82 4.31 2.75
<0.001 0.014 <0.001 0.016
Female Female
Looking time (s)
Male Female
Familiar sex
Looking times and percentages of novelty preferences are shown as mean ± S.D. Percentages of novelty preferences were compared to the chance level (50%) with t tests.
R. Koba, A. Izumi / Behavioural Processes 79 (2008) 70–73 Table 2 Number of included and excluded subjects in the analysis Excluded
References
Age group
Sex
Adult
Male Female
9 8
5 4
35.7 33.3
Nonadult
Male Female
9 7
1 2
10.0 12.5
33
12
26.7
Total
Included
73
Excluded (%)
icant difference (p = 0.15, Fisher’s exact test), possibly because the number of subjects was not sufficiently high. Older monkeys might have been less interested in the stimuli than younger monkeys, and they also might have been affected more by the environment of the cage room where other monkeys were kept. To collect data more efficiently, therefore, it might be better to only use young monkeys. In the present study, the monkeys were allowed to move away from the monitor, and they looked at the stimulus voluntarily. Although it was true that many monkeys failed to complete the experiment, we were able to collect data from many untrained monkeys while they remained in their usual cages. The present method is thus suggested as a convenient way to assess cognitive abilities in large numbers of monkeys without training. Acknowledgments We thank Nobuo Masataka, Sumiharu Nagumo for support throughout the research. Thanks are also extended to Akemi Kato and Satomi Araya for assistance and the daily care of the monkeys. This work was supported by a Grant for Biodiversity Research of the 21st Century COE (A14, Kyoto University) from the Ministry of Education, Culture, Sports, Science and Technology of Japan. The present study complies with the laws of Japan.
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