- Email: [email protected]
Effect of others’ attentional states on vocalizations in Japanese monkeys (Macaca fuscata)
Behavioural Processes 73 (2006) 285–289
Effect of others’ attentional states on vocalizations in Japanese monkeys (Macaca fuscata) Chieko Yamaguchi, Akihiro Izumi ∗ Department of Behavioral and Brain Sciences, Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan Received 9 July 2006; accepted 11 July 2006
Abstract We investigated the effects of other’s attentional states on vocalizations in monkeys. The subjects were 14 Japanese monkeys (Macaca fuscata), which vocalized spontaneously in the feeding context. In the initial experiment, an experimenter moved towards and away from the subject monkeys. The monkeys vocalized more frequently when the experimenter moved away rather than towards them. To examine the effects of the experimenter’s body orientations and moving directions separately, additional experiments were conducted. When the experimenter stood facing towards and facing away from the subject monkeys, the monkeys vocalized more frequently when the experimenter stood facing away rather than facing towards. When the experimenter moved towards and away from the subject monkeys while facing them, the monkeys vocalized more frequently when the experimenter moved away from them rather than towards them. These results suggested that the monkeys vocalized more frequently when the situation changed to that where the monkeys were not likely get food from the experimenter. It seems that monkeys recognize the attentional states of others by body orientation and modify their vocalizing behavior accordingly. © 2006 Elsevier B.V. All rights reserved. Keywords: Vocalization; Attentional state; Japanese monkey
1. Introduction Whether or not non-human primates understand the intentions and attentional states of others has received much interest (Premack and Woodruff, 1978; Maestripieri, 2003; Cheney and Seyfarth, 1990; Cheney et al., 1986; Povinelli et al., 1990; Theall and Povinelli, 1999). Some researchers have shown that nonhuman primates, especially chimpanzees, discriminate these states of others. For example, Hare et al. (2000, 2001) found that chimpanzees know what their conspecifics can and cannot see. They placed a dominant and subordinate chimpanzee in food competitive situations where one of two pieces of food was visible to both individuals and the other was visible only to the subordinate. The subordinate chimpanzee more frequently visited the piece of food hidden from the dominant chimpanzee’s view. Observational research has also shown that apes more frequently gesture to conspecifics who oriented ∗
Corresponding author at: 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. Tel.: +81 42 346 1754; fax: +81 42 346 1754. E-mail address: [email protected] (A. Izumi). 0376-6357/$ – see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.beproc.2006.07.002
towards them (siamang: Liebal et al., 2004, gorilla: Pika et al., 2003). Chimpanzees also change their behavior in response to the attentional states of humans; such abilities have been observed in food-begging situations. Povinelli et al. (2003) revealed that chimpanzees altered the location of their gestures depending on whether or not the human experimenter’s attention was focused on the food. When the experimenter focused on the food, the chimpanzees were inclined to gesture at the food; however, when the experimenter did not focus on the food, the chimpanzees gestured at the experimenter’s point of focus before gesturing at the food. Chimpanzees also use different modalities as a function of others’ visual attention (Hostetter et al., 2001; Leavens et al., 2004). In these studies, the chimpanzees gestured more frequently when a human experimenter oriented towards them; however, they emitted vocalizations when the experimenter oriented away. Several studies have been conducted with regard to monkeys’ understandings of attentional states of others. Monkeys could follow the gaze of their conspecifics (Emery et al., 1997; Tomasello et al., 1998). Ferrari et al. (2000) revealed that pigtailed macaques could follow human experimenters’ head direction and gaze. Anderson and Mitchell (1999) also examined
286
C. Yamaguchi, A. Izumi / Behavioural Processes 73 (2006) 285–289
whether stump-tailed macaques and black lemurs have the ability to engage in visual co-orientation (VOC), defined as turning to look in the same direction as another individual whose focus of attention changes. The macaques showed VOC whereas the lemurs showed no such response. Although macaques can follow the gaze of conspecifics and human experimenters, they seem to be unable to use a human experimenter’s gaze cues to pass object choice tasks. Anderson et al. (1995, 1996) examined whether capuchin and rhesus monkeys use pointing and gaze cues of a human experimenter to locate a food reward, and found that these monkeys used pointing and not gaze cues. Flombaum and Santos (2005) showed that rhesus monkeys adjust their behavior in response to the attentional states of humans. Two experimenters who stood near food changed their body orientations, face orientations, gaze, and with concealed or visible face and eye, and examined which experimenter’s food was stolen. The monkeys retrieved the food from the experimenter who was incapable of seeing the food rather than the experimenter who was visually aware. Although monkeys have been shown to understand others’ attentional states (i.e., gazing, pointing, head directions), there are few studies that examined whether monkeys modify their communicative behavior according to others’ attentional states. In the present study, we investigated whether Japanese monkeys (Macaca fuscata) modified their vocalizing behavior according to the attentional states of humans. Experimental sessions were conducted in a feeding context; subject monkeys spontaneously vocalized to the human experimenter who had monkey chow. If the monkeys vocalized differently according to whether the experimenter attended to the monkeys or not, it would suggest that they recognized the experimenter’s attentional states and modified their behavior accordingly. 2. Experiment 1 The experimenter moved towards and away from the monkeys, and the effects of the movement on the monkeys’ vocalizations were examined. 2.1. Method 2.1.1. Subjects The subjects were 14 Japanese monkeys (seven females and seven males; age: 3–26 years). All experiments adhered to the Guide for the Care and Use of Laboratory Primates (second edition, 2002) of the Primate Research Institute, Kyoto University. The monkeys were housed in individual cages with freely available water. They were fed once daily on a diet of monkey chow. Of these, thirteen monkeys were mother-reared and the other one was human-reared. All monkeys vocalized spontaneously in the feeding context without training. 2.1.2. Procedure Experiments took place in the rooms where the subject monkeys were housed (Fig. 1). In each room, there were two lines of six individual cages (91 cm wide × 76 cm deep × 82 cm high); 12 cages in total. The subject monkey was placed in the right
Fig. 1. Schematic representation of the cage room in which the monkeys were housed (top view). There were two lines of six cages; 12 cages in total. The subject’s cage is the right innermost. The cage opposite the subject’s cage was kept empty, and the other 10 cages were occupied by roommate monkeys. “Near,” “Far,” and “Out” were the names of three predetermined positions, and the experimenter moved between these positions.
innermost cage; subject monkeys were taken to the cage at least one day before the experimental period then housed there until completion. The cage opposite the subject’s cage was kept empty and the other 10 cages were occupied by other monkeys. These roommate monkeys were of various ages and either sex. It was possible that the roommate monkeys’ vocalizations may affect the subject monkey’s vocalizations. To control the roommates’ vocalizations, a human experimenter fed the roommates 1 h before each experimental session. The subject monkey was fed after each session, i.e., only the subject monkey was hungry in each experimental session. During each session, the experimenter held a transparent plastic bowl (19 cm in diameter) with both hands. The bowl contained monkey chow and it was always in front of the experimenter’s body. Although the monkeys could see the monkey chow, they were not allowed to eat. The experimenter moved between three predetermined positions as follows: • Near: In front of the subject’s cage. The subject monkey could see the experimenter who oriented towards the subject monkey. • Far: Five meters away from the subject’s cage. The subject monkey could see the experimenter who oriented in the direction of movement. • Out: Out of the cage room. The subject monkey could not see the experimenter. The experimenter’s face orientation was in accordance with the body orientation. The order of movements was Out–Far–Near–Far–Out, and each session consisted of three cycles. Each condition was 15 s in which the experimenter
C. Yamaguchi, A. Izumi / Behavioural Processes 73 (2006) 285–289
Fig. 2. The number of vocalizations made by subject monkeys during the five sessions under each condition in Experiment 1 (median ± quartile deviations).
moved from one position to the next and stayed in the latter position. Each monkey performed five sessions in total, one per day. One hour before each experimental session, a human experimenter placed a video camera in the room, and all experimental sessions were recorded. From these recordings, the number of vocalizations by each subject monkey was determined. In addition, the total number of vocalizations made by the roommate monkeys was also recorded to examine its influence on the subject monkeys’ vocalizing behavior. When two successive vocalizations were separated by an interval longer than 1 s they were counted as two distinct vocalizations. 2.2. Results and discussion Fig. 2 shows the median number of vocalizations made by the subject monkeys over the five sessions under each condition. The number of vocalizations was affected by the conditions (Friedman test, P < 0.001). The subject monkeys vocalized more frequently when the experimenter moved away (i.e., under Near-to-Far and Far-to-Out conditions). Pairwise comparisons between conditions (binomial test, Ryan’s procedure) revealed that the subject monkeys vocalized more frequently in Near-to-Far and Far-to-Out conditions than in Far-to-Near and Out-to-Far conditions (P < 0.05). These results indicated that the monkeys vocalized more frequently when the experimenter did not attend to them. It seems that the monkeys recognize a human’s attentional state and modify their behavior accordingly. To investigate the effects of roommate monkeys’ vocalizations on the subject monkeys’ vocalizations, the total number of vocalizations by the 10 roommates was also measured. Fig. 3 shows the median number of vocalizations made by the roommates over the five sessions under each condition. Total number of vocalizations by the 10 roommates was comparable to the number of vocalizations by a subject monkey. This suggests that a subject monkey vocalized about 10 times as frequently as a roommate monkey. The frequency of roommate monkeys’ vocalizations was also affected by the conditions (Friedman test: P < 0.001). Pairwise comparisons between the conditions (binomial test, Ryan’s procedure) confirmed that the roommates vocalized more frequently
287
Fig. 3. Total number of vocalizations made by the 10 roommate monkeys during the five sessions under each condition in Experiment 1 (median ± quartile deviations).
in Far-to-Out condition than in the other conditions (P < 0.05). This suggested that the roommates vocalized more frequently when the experimenter left the room, just as with the subject monkeys. Although the subject monkeys vocalized more frequently in Near-to-Far condition than in Far-to-Near condition, such a difference was not seen in the roommates. This may be due to various locations of the roommates’ cages: the apparent moving directions of the experimenter were various for the roommates in these conditions. Together with the subject monkeys’ high rate of vocalizations, the difference between the subject and the roommate monkeys’ vocalizations suggested that the subject’s vocal behavior was to some extent independent of that of the roommates. 3. Experiment 2 In Experiment 1, with the experimenter’s body oriented in the direction of movement, it was not possible to distinguish between the effects of the experimenter’s body orientations and the moving directions. In Experiment 2, we examined the effect of the experimenter’s body orientations with the experimenter standing in front of the monkeys. The body orientation was varied while maintaining a constant distance between the monkeys and the experimenter. If the monkeys vocalized differently according to the experimenter’s body orientations, it would suggest that they recognized the experimenter’s attentional state by the body orientation and modified their vocalizing behavior accordingly. 3.1. Method 3.1.1. Subjects The subjects were the same 14 monkeys as used in Experiment 1. 3.1.2. Procedure The procedure was generally identical to that of Experiment 1 except for the experimenter’s conditions. The experimenter stayed in front of the subject’s cage (the same place as Near in Experiment 1), and employed one of the following two conditions:
288
C. Yamaguchi, A. Izumi / Behavioural Processes 73 (2006) 285–289
Fig. 4. The number of vocalizations made by subject monkeys during the five sessions under each condition in Experiment 2 (median ± quartile deviations).
• Front: The experimenter stood facing the subject monkey. • Back: The experimenter stood facing away from the subject monkey. The experimenter held the food bowl with the right hand beside the body. The food was visible to the monkeys, and the distances between the food and the monkeys did not differ in both of the two conditions. The initial condition was selected randomly, and the experimenter alternately presented one of the two conditions nine times in each session. Each condition lasted for 15 s. Each monkey performed five sessions in total, one per day.
Fig. 5. The number of vocalizations made by subject monkeys during the five sessions under each condition in Experiment 3 (median ± quartile deviations).
4.1.2. Procedure The procedure was generally identical to that of Experiment 1 except for the experimenter’s conditions. The experimenter moved in the cage room as in Experiment 1, but the experimenter’s body and face always oriented towards the subject monkeys. The initial position was Far (Fig. 1), and the experimenter alternately moved between Far and Near four cycles in one session. In the Far-to-Near condition, the experimenter walked forwards. However, the experimenter had to walk backwards in the Near-to-Far condition. 4.2. Results and discussion
3.2. Results and discussion Fig. 4 shows the median number of vocalizations made by the subject monkeys over the five sessions under each condition. The monkeys vocalized more frequently when the experimenter stood facing away than facing towards the monkeys (signed-rank test: T = 12.5, P = 0.019). Although the distance between the monkey and the experimenter were the same during both the conditions, the monkeys vocalized more frequently when the experimenter stood facing away from them. Together with the results from Experiment 1, the monkeys seemed to recognize the experimenter’s attentional state by body orientation and modified their vocal behavior accordingly. 4. Experiment 3 In this experiment, we examined the effect of moving direction of the experimenter who always oriented towards the monkeys. 4.1. Method 4.1.1. Subjects The subjects were 8 (6 females and 2 males; age: 6–22 years) of the subject monkeys from Experiments 1 and 2.
Fig. 5 shows the median number of vocalizations made by the subject monkeys over the five sessions under each condition. The monkeys’ vocal behavior was affected by the distance of the experimenter: they vocalized more frequently in the Nearto-Far condition than in the Far-to-Near condition (signed-rank test: T = 0, P = 0.006). In addition to the experimenter’s attentional states, the moving directions are suggested to affect the monkeys’ vocalizations. 5. General discussion In Experiment 1, we examined the effects of the experimenter’s movement on the monkeys’ vocalizations. The monkeys vocalized more frequently when the experimenter moved away from the monkeys. In Experiments 2 and 3, we examined the effects of the experimenter’s body orientations and moving directions separately. The monkeys vocalized more frequently when the experimenter stood facing away or moved away from the monkeys. These results indicated that the monkeys vocalized more frequently when the situation changed to that where the monkeys were not likely to get food from the experimenter. When caregivers give food to a monkey, they generally stand in front of the monkey and attend to it. The monkeys may anticipate food when the experimenter was in such a state, and
C. Yamaguchi, A. Izumi / Behavioural Processes 73 (2006) 285–289
they seemed to vocalize more frequently when the experimenter’s states changed to that where they could not anticipate food. In Experiment 2, the monkeys vocalized more frequently when the experimenter stood facing away rather than facing towards them. The monkeys were suggested to recognize the experimenter’s attentional state by the body orientation and modified their vocal behavior accordingly. The pattern of the monkeys’ vocal regulations seemed to get the attention of the experimenter: they vocalized more frequently when the experimenter did not attend to them. Such rational behavior has been shown in chimpanzees (Hostetter et al., 2001; Leavens et al., 2004). Recent studies have shown that some animal species, other than primates, can also discriminate the attentional states of humans. McKinley and Sambrook (2000) showed that despite individual differences, domestic dogs and horses were able to find hidden food with human-given cues. Hare et al. (2002) revealed that dogs have such ability, but wolves – a closely related species – do not. They suggested that dogs’ ability were acquired during domestication. It is likely that monkeys did not evolve flexible vocal behaviors to communicate with humans, but rather with their conspecifics. The monkeys in the present study might apply their vocalizations to communicate with the human experimenter. In the present study, we did not analyze the acoustic structures of monkeys’ vocalizations. Koda (2004) found that wild Japanese monkeys modify the acoustic properties of vocalizations during vocal exchange. When a monkey emitted a call but others did not respond, the monkey tended to emit another call which was acoustically different from the initial call. Koda discussed that the repeated call appears better able to attract the attention of others. It would be interesting to examine whether monkeys also modify acoustic structures according to others’ attentional states. Povinelli and Eddy (1996) showed that chimpanzees were sensitive to the orientation of the body and not to the orientation of face or eyes. Kaminski et al. (2004) revealed that apes were sensitive to an experimenter’s body and face orientation separately. Only in the case when the experimenter’s body oriented towards, the apes were sensitive to the face orientation. It is necessary to examine which part of the body is important for monkeys to perceive others’ attentional states. Acknowledgments This study 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, Japan. The authors are grateful to Prof. Nobuo Masataka and Mr. Sumiharu Nagumo for their support throughout the research. We also thank Ms. Akemi Kato and Satomi Araya for assistance and daily care of the monkeys. The present study complied with the current laws of Japan.
289
References Anderson, J.R., Mitchell, R.M., 1999. Macaques but not lemurs co-orient visually with humans. Folia Primatol. 70, 17–22. Anderson, J.R., Montant, M., Schmitt, D., 1996. Rhesus monkeys fail to use gaze direction as an experimenter-given cue in an object-choice task. Behav. Proc. 37, 47–55. Anderson, J.R., Sallaberry, P., Barbier, H., 1995. Use of experimenter-given cues during object-choice tasks by capuchin monkeys. Anim. Behav. 49, 201–208. Cheney, D., Seyfarth, R., 1990. How Monkeys See the World: Inside the Mind of Another Species. Chicago University of Chicago Press, Chicago. Cheney, D., Seyfarth, R., Smuts, B., 1986. Social relationships and social cognition in nonhuman primates. Science 234, 1361–1366. Emery, N.J., Lorincz, E.N., Perrett, D.I., Oram, M.W., Baker, C.I., 1997. Gaze following and joint attention in rhesus monkeys (Macaca mulatta). J. Comp. Psychol. 111, 286–293. Ferrari, P.F., Kohler, E., Fogassi, L., Gallese, V., 2000. The ability to follow eye gaze and its emergence during development in macaque monkeys. Proc. Natl. Acad. Sci. USA 97, 13997–14002. Flombaum, J.I., Santos, L.R., 2005. Rhesus monkeys attribute perceptions to others. Curr. Biol. 15, 447–452. Hare, B., Brown, M., Williamson, C., Tomasello, M., 2002. The domestication of social cognition in dogs. Science 298, 1634–1636. Hare, B., Call, J., Agnetta, B., Tomasello, M., 2000. Chimpanzees know what conspecifics do and do not see. Anim. Behav. 59, 771–785. Hare, B., Call, J., Tomasello, M., 2001. Do chimpanzees know what conspecifics know? Anim. Behav. 61, 139–151. Hostetter, A.B., Cantero, M., Hopkins, W.D., 2001. Differential use of vocal and gestural communication by chimpanzees (Pan troglodytes) in response to the attentional status of a human (Homo sapiens). J. Comp. Psychol. 115, 337–343. Kaminski, J., Call, J., Tomasello, M., 2004. Body orientation and face orientation: two factors controlling apes’ begging behavior from humans. Anim. Cogn. 7, 216–223. Koda, H., 2004. Flexibility and context-sensitivity during the vocal exchange of coo calls in wild Japanese macaques (Macaca fuscata yakui). Behaviour 141, 1279–1296. Leavens, D.A., Hostetter, A.B., Wesley, M.J., Hopkins, W.D., 2004. Tactical use of unimodal and bimodal communication by chimpanzees. Pan troglodytes. Anim. Behav. 67, 467–476. Liebal, K., Pika, S., Tomasello, M., 2004. Social communication in siamangs (Symphalangus syndactylus): use of gestures and facial expressions. Primates 45, 41–57. Maestripieri, D., 2003. Primate Psychology. Harvard University Press, Cambridge. McKinley, J., Sambrook, T.D., 2000. Use of human-given cues by domestic dogs (Canis familiaris) and horses (Equus caballus). Anim. Cogn. 3, 13–22. Pika, S., Liebal, K., Tomasello, M., 2003. Gestural communication in young gorillas (Gorilla gorilla): Gestural repertoire, learning, and use. Am. J. Primatol. 60, 95–111. Povinelli, D.J., Eddy, T.J., 1996. What young chimpanzees know about seeing. Monogr. Soc. Res. Child Dev. 61 (3, Serial No. 247), 1–152. Povinelli, D.J., Nelson, K.E., Boysen, S.T., 1990. Inferences about guessing and knowing by chimpanzees (Pan troglodytes). J. Comp. Psychol. 104, 203–210. Povinelli, D.J., Theall, L.A., Reaux, J.E., Dunphy-Lelii, S., 2003. Chimpanzees spontaneously alter the location of their gestures to match the attentional orientation of others. Anim. Behav. 66, 71–79. Premack, D., Woodruff, G., 1978. Does the chimpanzee have a theory of mind? Behav. Brain Sci. 4, 515–526. Theall, L.A., Povinelli, D.J., 1999. Do chimpanzees tailor their gestural signals to fit the attentional states of others? Anim. Cogn. 2, 207–214. Tomasello, M., Call, J., Hare, B., 1998. Five primate species follow the visual gaze of conspecifics. Anim. Behav. 55, 1063–1069.
Effect of others’ attentional states on vocalizations in Japanese monkeys (Macaca fuscata) Chieko Yamaguchi, Akihiro Izumi ∗ Department of Behavioral and Brain Sciences, Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan Received 9 July 2006; accepted 11 July 2006
Abstract We investigated the effects of other’s attentional states on vocalizations in monkeys. The subjects were 14 Japanese monkeys (Macaca fuscata), which vocalized spontaneously in the feeding context. In the initial experiment, an experimenter moved towards and away from the subject monkeys. The monkeys vocalized more frequently when the experimenter moved away rather than towards them. To examine the effects of the experimenter’s body orientations and moving directions separately, additional experiments were conducted. When the experimenter stood facing towards and facing away from the subject monkeys, the monkeys vocalized more frequently when the experimenter stood facing away rather than facing towards. When the experimenter moved towards and away from the subject monkeys while facing them, the monkeys vocalized more frequently when the experimenter moved away from them rather than towards them. These results suggested that the monkeys vocalized more frequently when the situation changed to that where the monkeys were not likely get food from the experimenter. It seems that monkeys recognize the attentional states of others by body orientation and modify their vocalizing behavior accordingly. © 2006 Elsevier B.V. All rights reserved. Keywords: Vocalization; Attentional state; Japanese monkey
1. Introduction Whether or not non-human primates understand the intentions and attentional states of others has received much interest (Premack and Woodruff, 1978; Maestripieri, 2003; Cheney and Seyfarth, 1990; Cheney et al., 1986; Povinelli et al., 1990; Theall and Povinelli, 1999). Some researchers have shown that nonhuman primates, especially chimpanzees, discriminate these states of others. For example, Hare et al. (2000, 2001) found that chimpanzees know what their conspecifics can and cannot see. They placed a dominant and subordinate chimpanzee in food competitive situations where one of two pieces of food was visible to both individuals and the other was visible only to the subordinate. The subordinate chimpanzee more frequently visited the piece of food hidden from the dominant chimpanzee’s view. Observational research has also shown that apes more frequently gesture to conspecifics who oriented ∗
Corresponding author at: 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. Tel.: +81 42 346 1754; fax: +81 42 346 1754. E-mail address: [email protected] (A. Izumi). 0376-6357/$ – see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.beproc.2006.07.002
towards them (siamang: Liebal et al., 2004, gorilla: Pika et al., 2003). Chimpanzees also change their behavior in response to the attentional states of humans; such abilities have been observed in food-begging situations. Povinelli et al. (2003) revealed that chimpanzees altered the location of their gestures depending on whether or not the human experimenter’s attention was focused on the food. When the experimenter focused on the food, the chimpanzees were inclined to gesture at the food; however, when the experimenter did not focus on the food, the chimpanzees gestured at the experimenter’s point of focus before gesturing at the food. Chimpanzees also use different modalities as a function of others’ visual attention (Hostetter et al., 2001; Leavens et al., 2004). In these studies, the chimpanzees gestured more frequently when a human experimenter oriented towards them; however, they emitted vocalizations when the experimenter oriented away. Several studies have been conducted with regard to monkeys’ understandings of attentional states of others. Monkeys could follow the gaze of their conspecifics (Emery et al., 1997; Tomasello et al., 1998). Ferrari et al. (2000) revealed that pigtailed macaques could follow human experimenters’ head direction and gaze. Anderson and Mitchell (1999) also examined
286
C. Yamaguchi, A. Izumi / Behavioural Processes 73 (2006) 285–289
whether stump-tailed macaques and black lemurs have the ability to engage in visual co-orientation (VOC), defined as turning to look in the same direction as another individual whose focus of attention changes. The macaques showed VOC whereas the lemurs showed no such response. Although macaques can follow the gaze of conspecifics and human experimenters, they seem to be unable to use a human experimenter’s gaze cues to pass object choice tasks. Anderson et al. (1995, 1996) examined whether capuchin and rhesus monkeys use pointing and gaze cues of a human experimenter to locate a food reward, and found that these monkeys used pointing and not gaze cues. Flombaum and Santos (2005) showed that rhesus monkeys adjust their behavior in response to the attentional states of humans. Two experimenters who stood near food changed their body orientations, face orientations, gaze, and with concealed or visible face and eye, and examined which experimenter’s food was stolen. The monkeys retrieved the food from the experimenter who was incapable of seeing the food rather than the experimenter who was visually aware. Although monkeys have been shown to understand others’ attentional states (i.e., gazing, pointing, head directions), there are few studies that examined whether monkeys modify their communicative behavior according to others’ attentional states. In the present study, we investigated whether Japanese monkeys (Macaca fuscata) modified their vocalizing behavior according to the attentional states of humans. Experimental sessions were conducted in a feeding context; subject monkeys spontaneously vocalized to the human experimenter who had monkey chow. If the monkeys vocalized differently according to whether the experimenter attended to the monkeys or not, it would suggest that they recognized the experimenter’s attentional states and modified their behavior accordingly. 2. Experiment 1 The experimenter moved towards and away from the monkeys, and the effects of the movement on the monkeys’ vocalizations were examined. 2.1. Method 2.1.1. Subjects The subjects were 14 Japanese monkeys (seven females and seven males; age: 3–26 years). All experiments adhered to the Guide for the Care and Use of Laboratory Primates (second edition, 2002) of the Primate Research Institute, Kyoto University. The monkeys were housed in individual cages with freely available water. They were fed once daily on a diet of monkey chow. Of these, thirteen monkeys were mother-reared and the other one was human-reared. All monkeys vocalized spontaneously in the feeding context without training. 2.1.2. Procedure Experiments took place in the rooms where the subject monkeys were housed (Fig. 1). In each room, there were two lines of six individual cages (91 cm wide × 76 cm deep × 82 cm high); 12 cages in total. The subject monkey was placed in the right
Fig. 1. Schematic representation of the cage room in which the monkeys were housed (top view). There were two lines of six cages; 12 cages in total. The subject’s cage is the right innermost. The cage opposite the subject’s cage was kept empty, and the other 10 cages were occupied by roommate monkeys. “Near,” “Far,” and “Out” were the names of three predetermined positions, and the experimenter moved between these positions.
innermost cage; subject monkeys were taken to the cage at least one day before the experimental period then housed there until completion. The cage opposite the subject’s cage was kept empty and the other 10 cages were occupied by other monkeys. These roommate monkeys were of various ages and either sex. It was possible that the roommate monkeys’ vocalizations may affect the subject monkey’s vocalizations. To control the roommates’ vocalizations, a human experimenter fed the roommates 1 h before each experimental session. The subject monkey was fed after each session, i.e., only the subject monkey was hungry in each experimental session. During each session, the experimenter held a transparent plastic bowl (19 cm in diameter) with both hands. The bowl contained monkey chow and it was always in front of the experimenter’s body. Although the monkeys could see the monkey chow, they were not allowed to eat. The experimenter moved between three predetermined positions as follows: • Near: In front of the subject’s cage. The subject monkey could see the experimenter who oriented towards the subject monkey. • Far: Five meters away from the subject’s cage. The subject monkey could see the experimenter who oriented in the direction of movement. • Out: Out of the cage room. The subject monkey could not see the experimenter. The experimenter’s face orientation was in accordance with the body orientation. The order of movements was Out–Far–Near–Far–Out, and each session consisted of three cycles. Each condition was 15 s in which the experimenter
C. Yamaguchi, A. Izumi / Behavioural Processes 73 (2006) 285–289
Fig. 2. The number of vocalizations made by subject monkeys during the five sessions under each condition in Experiment 1 (median ± quartile deviations).
moved from one position to the next and stayed in the latter position. Each monkey performed five sessions in total, one per day. One hour before each experimental session, a human experimenter placed a video camera in the room, and all experimental sessions were recorded. From these recordings, the number of vocalizations by each subject monkey was determined. In addition, the total number of vocalizations made by the roommate monkeys was also recorded to examine its influence on the subject monkeys’ vocalizing behavior. When two successive vocalizations were separated by an interval longer than 1 s they were counted as two distinct vocalizations. 2.2. Results and discussion Fig. 2 shows the median number of vocalizations made by the subject monkeys over the five sessions under each condition. The number of vocalizations was affected by the conditions (Friedman test, P < 0.001). The subject monkeys vocalized more frequently when the experimenter moved away (i.e., under Near-to-Far and Far-to-Out conditions). Pairwise comparisons between conditions (binomial test, Ryan’s procedure) revealed that the subject monkeys vocalized more frequently in Near-to-Far and Far-to-Out conditions than in Far-to-Near and Out-to-Far conditions (P < 0.05). These results indicated that the monkeys vocalized more frequently when the experimenter did not attend to them. It seems that the monkeys recognize a human’s attentional state and modify their behavior accordingly. To investigate the effects of roommate monkeys’ vocalizations on the subject monkeys’ vocalizations, the total number of vocalizations by the 10 roommates was also measured. Fig. 3 shows the median number of vocalizations made by the roommates over the five sessions under each condition. Total number of vocalizations by the 10 roommates was comparable to the number of vocalizations by a subject monkey. This suggests that a subject monkey vocalized about 10 times as frequently as a roommate monkey. The frequency of roommate monkeys’ vocalizations was also affected by the conditions (Friedman test: P < 0.001). Pairwise comparisons between the conditions (binomial test, Ryan’s procedure) confirmed that the roommates vocalized more frequently
287
Fig. 3. Total number of vocalizations made by the 10 roommate monkeys during the five sessions under each condition in Experiment 1 (median ± quartile deviations).
in Far-to-Out condition than in the other conditions (P < 0.05). This suggested that the roommates vocalized more frequently when the experimenter left the room, just as with the subject monkeys. Although the subject monkeys vocalized more frequently in Near-to-Far condition than in Far-to-Near condition, such a difference was not seen in the roommates. This may be due to various locations of the roommates’ cages: the apparent moving directions of the experimenter were various for the roommates in these conditions. Together with the subject monkeys’ high rate of vocalizations, the difference between the subject and the roommate monkeys’ vocalizations suggested that the subject’s vocal behavior was to some extent independent of that of the roommates. 3. Experiment 2 In Experiment 1, with the experimenter’s body oriented in the direction of movement, it was not possible to distinguish between the effects of the experimenter’s body orientations and the moving directions. In Experiment 2, we examined the effect of the experimenter’s body orientations with the experimenter standing in front of the monkeys. The body orientation was varied while maintaining a constant distance between the monkeys and the experimenter. If the monkeys vocalized differently according to the experimenter’s body orientations, it would suggest that they recognized the experimenter’s attentional state by the body orientation and modified their vocalizing behavior accordingly. 3.1. Method 3.1.1. Subjects The subjects were the same 14 monkeys as used in Experiment 1. 3.1.2. Procedure The procedure was generally identical to that of Experiment 1 except for the experimenter’s conditions. The experimenter stayed in front of the subject’s cage (the same place as Near in Experiment 1), and employed one of the following two conditions:
288
C. Yamaguchi, A. Izumi / Behavioural Processes 73 (2006) 285–289
Fig. 4. The number of vocalizations made by subject monkeys during the five sessions under each condition in Experiment 2 (median ± quartile deviations).
• Front: The experimenter stood facing the subject monkey. • Back: The experimenter stood facing away from the subject monkey. The experimenter held the food bowl with the right hand beside the body. The food was visible to the monkeys, and the distances between the food and the monkeys did not differ in both of the two conditions. The initial condition was selected randomly, and the experimenter alternately presented one of the two conditions nine times in each session. Each condition lasted for 15 s. Each monkey performed five sessions in total, one per day.
Fig. 5. The number of vocalizations made by subject monkeys during the five sessions under each condition in Experiment 3 (median ± quartile deviations).
4.1.2. Procedure The procedure was generally identical to that of Experiment 1 except for the experimenter’s conditions. The experimenter moved in the cage room as in Experiment 1, but the experimenter’s body and face always oriented towards the subject monkeys. The initial position was Far (Fig. 1), and the experimenter alternately moved between Far and Near four cycles in one session. In the Far-to-Near condition, the experimenter walked forwards. However, the experimenter had to walk backwards in the Near-to-Far condition. 4.2. Results and discussion
3.2. Results and discussion Fig. 4 shows the median number of vocalizations made by the subject monkeys over the five sessions under each condition. The monkeys vocalized more frequently when the experimenter stood facing away than facing towards the monkeys (signed-rank test: T = 12.5, P = 0.019). Although the distance between the monkey and the experimenter were the same during both the conditions, the monkeys vocalized more frequently when the experimenter stood facing away from them. Together with the results from Experiment 1, the monkeys seemed to recognize the experimenter’s attentional state by body orientation and modified their vocal behavior accordingly. 4. Experiment 3 In this experiment, we examined the effect of moving direction of the experimenter who always oriented towards the monkeys. 4.1. Method 4.1.1. Subjects The subjects were 8 (6 females and 2 males; age: 6–22 years) of the subject monkeys from Experiments 1 and 2.
Fig. 5 shows the median number of vocalizations made by the subject monkeys over the five sessions under each condition. The monkeys’ vocal behavior was affected by the distance of the experimenter: they vocalized more frequently in the Nearto-Far condition than in the Far-to-Near condition (signed-rank test: T = 0, P = 0.006). In addition to the experimenter’s attentional states, the moving directions are suggested to affect the monkeys’ vocalizations. 5. General discussion In Experiment 1, we examined the effects of the experimenter’s movement on the monkeys’ vocalizations. The monkeys vocalized more frequently when the experimenter moved away from the monkeys. In Experiments 2 and 3, we examined the effects of the experimenter’s body orientations and moving directions separately. The monkeys vocalized more frequently when the experimenter stood facing away or moved away from the monkeys. These results indicated that the monkeys vocalized more frequently when the situation changed to that where the monkeys were not likely to get food from the experimenter. When caregivers give food to a monkey, they generally stand in front of the monkey and attend to it. The monkeys may anticipate food when the experimenter was in such a state, and
C. Yamaguchi, A. Izumi / Behavioural Processes 73 (2006) 285–289
they seemed to vocalize more frequently when the experimenter’s states changed to that where they could not anticipate food. In Experiment 2, the monkeys vocalized more frequently when the experimenter stood facing away rather than facing towards them. The monkeys were suggested to recognize the experimenter’s attentional state by the body orientation and modified their vocal behavior accordingly. The pattern of the monkeys’ vocal regulations seemed to get the attention of the experimenter: they vocalized more frequently when the experimenter did not attend to them. Such rational behavior has been shown in chimpanzees (Hostetter et al., 2001; Leavens et al., 2004). Recent studies have shown that some animal species, other than primates, can also discriminate the attentional states of humans. McKinley and Sambrook (2000) showed that despite individual differences, domestic dogs and horses were able to find hidden food with human-given cues. Hare et al. (2002) revealed that dogs have such ability, but wolves – a closely related species – do not. They suggested that dogs’ ability were acquired during domestication. It is likely that monkeys did not evolve flexible vocal behaviors to communicate with humans, but rather with their conspecifics. The monkeys in the present study might apply their vocalizations to communicate with the human experimenter. In the present study, we did not analyze the acoustic structures of monkeys’ vocalizations. Koda (2004) found that wild Japanese monkeys modify the acoustic properties of vocalizations during vocal exchange. When a monkey emitted a call but others did not respond, the monkey tended to emit another call which was acoustically different from the initial call. Koda discussed that the repeated call appears better able to attract the attention of others. It would be interesting to examine whether monkeys also modify acoustic structures according to others’ attentional states. Povinelli and Eddy (1996) showed that chimpanzees were sensitive to the orientation of the body and not to the orientation of face or eyes. Kaminski et al. (2004) revealed that apes were sensitive to an experimenter’s body and face orientation separately. Only in the case when the experimenter’s body oriented towards, the apes were sensitive to the face orientation. It is necessary to examine which part of the body is important for monkeys to perceive others’ attentional states. Acknowledgments This study 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, Japan. The authors are grateful to Prof. Nobuo Masataka and Mr. Sumiharu Nagumo for their support throughout the research. We also thank Ms. Akemi Kato and Satomi Araya for assistance and daily care of the monkeys. The present study complied with the current laws of Japan.
289
References Anderson, J.R., Mitchell, R.M., 1999. Macaques but not lemurs co-orient visually with humans. Folia Primatol. 70, 17–22. Anderson, J.R., Montant, M., Schmitt, D., 1996. Rhesus monkeys fail to use gaze direction as an experimenter-given cue in an object-choice task. Behav. Proc. 37, 47–55. Anderson, J.R., Sallaberry, P., Barbier, H., 1995. Use of experimenter-given cues during object-choice tasks by capuchin monkeys. Anim. Behav. 49, 201–208. Cheney, D., Seyfarth, R., 1990. How Monkeys See the World: Inside the Mind of Another Species. Chicago University of Chicago Press, Chicago. Cheney, D., Seyfarth, R., Smuts, B., 1986. Social relationships and social cognition in nonhuman primates. Science 234, 1361–1366. Emery, N.J., Lorincz, E.N., Perrett, D.I., Oram, M.W., Baker, C.I., 1997. Gaze following and joint attention in rhesus monkeys (Macaca mulatta). J. Comp. Psychol. 111, 286–293. Ferrari, P.F., Kohler, E., Fogassi, L., Gallese, V., 2000. The ability to follow eye gaze and its emergence during development in macaque monkeys. Proc. Natl. Acad. Sci. USA 97, 13997–14002. Flombaum, J.I., Santos, L.R., 2005. Rhesus monkeys attribute perceptions to others. Curr. Biol. 15, 447–452. Hare, B., Brown, M., Williamson, C., Tomasello, M., 2002. The domestication of social cognition in dogs. Science 298, 1634–1636. Hare, B., Call, J., Agnetta, B., Tomasello, M., 2000. Chimpanzees know what conspecifics do and do not see. Anim. Behav. 59, 771–785. Hare, B., Call, J., Tomasello, M., 2001. Do chimpanzees know what conspecifics know? Anim. Behav. 61, 139–151. Hostetter, A.B., Cantero, M., Hopkins, W.D., 2001. Differential use of vocal and gestural communication by chimpanzees (Pan troglodytes) in response to the attentional status of a human (Homo sapiens). J. Comp. Psychol. 115, 337–343. Kaminski, J., Call, J., Tomasello, M., 2004. Body orientation and face orientation: two factors controlling apes’ begging behavior from humans. Anim. Cogn. 7, 216–223. Koda, H., 2004. Flexibility and context-sensitivity during the vocal exchange of coo calls in wild Japanese macaques (Macaca fuscata yakui). Behaviour 141, 1279–1296. Leavens, D.A., Hostetter, A.B., Wesley, M.J., Hopkins, W.D., 2004. Tactical use of unimodal and bimodal communication by chimpanzees. Pan troglodytes. Anim. Behav. 67, 467–476. Liebal, K., Pika, S., Tomasello, M., 2004. Social communication in siamangs (Symphalangus syndactylus): use of gestures and facial expressions. Primates 45, 41–57. Maestripieri, D., 2003. Primate Psychology. Harvard University Press, Cambridge. McKinley, J., Sambrook, T.D., 2000. Use of human-given cues by domestic dogs (Canis familiaris) and horses (Equus caballus). Anim. Cogn. 3, 13–22. Pika, S., Liebal, K., Tomasello, M., 2003. Gestural communication in young gorillas (Gorilla gorilla): Gestural repertoire, learning, and use. Am. J. Primatol. 60, 95–111. Povinelli, D.J., Eddy, T.J., 1996. What young chimpanzees know about seeing. Monogr. Soc. Res. Child Dev. 61 (3, Serial No. 247), 1–152. Povinelli, D.J., Nelson, K.E., Boysen, S.T., 1990. Inferences about guessing and knowing by chimpanzees (Pan troglodytes). J. Comp. Psychol. 104, 203–210. Povinelli, D.J., Theall, L.A., Reaux, J.E., Dunphy-Lelii, S., 2003. Chimpanzees spontaneously alter the location of their gestures to match the attentional orientation of others. Anim. Behav. 66, 71–79. Premack, D., Woodruff, G., 1978. Does the chimpanzee have a theory of mind? Behav. Brain Sci. 4, 515–526. Theall, L.A., Povinelli, D.J., 1999. Do chimpanzees tailor their gestural signals to fit the attentional states of others? Anim. Cogn. 2, 207–214. Tomasello, M., Call, J., Hare, B., 1998. Five primate species follow the visual gaze of conspecifics. Anim. Behav. 55, 1063–1069.