Effects of proximity and behavioral context on acoustic variation in the coo calls of Japanese macaques.код для вставкиСкачать
American Journal of Primatology 69:1412–1424 (2007) RESEARCH ARTICLE Effects of Proximity and Behavioral Context on Acoustic Variation in the Coo Calls of Japanese Macaques HIDEKI SUGIURA Primate Research Institute, Kyoto University, Japan Acoustic features of coo calls in Japanese macaques (Macaca fuscata) show large and graded variation. To explore the relevance of acoustic variation in coo calls, I examined whether acoustic features differed by the caller’s activity and proximity to group members. The subjects were five adult females from a wild, habituated group of Japanese macaques consisting of 23 individuals. Coo calls from the five females were recorded with their activity and proximity to group members. Acoustic features of 280 calls were measured with a sound spectrograph. Some of the acoustic variables differed by proximity but not by activity. The callers produced coo calls with larger frequency modulation and longer duration when they were far from group members compared to when they were near another member. The results suggest that Japanese macaques produce calls with more detectable and locatable features depending on the proximity to group members. Am. J. Primatol. 69:1412–1424, 2007. r 2007 Wiley-Liss, Inc. Key words: acoustic feature; behavioral context; detectability; locatability; proximity INTRODUCTION A basic question in vocal communication of animals is the relationship between the acoustic features of a vocalization and the situation in which it is given. This relationship provides clues to the function of the vocalization and to the control of vocal production depending on the situation [e.g., Gouzoules et al., 1984; Seyfarth et al., 1980]. Acoustic features of animal vocalizations are correlated with several variables, including the distance between the sender and the recipient and the behavioral context of the caller. The distance between the sender and the recipient affects the acoustic features of vocalizations because signals incur more attenuation, degradation, and distortion with increased distance [Morton, 1975]. Adapting to such environmental constraints, acoustic features of vocal signals are differentiated Correspondence to: Hideki Sugiura, Primate Research Institute, Kyoto University, Kanrin 41, Inuyama, Aichi 484-8506, Japan. E-mail: email@example.com Received 20 November 2006; revised 20 February 2007; revision accepted 12 April 2007 DOI 10.1002/ajp.20447 Published online 16 May 2007 in Wiley InterScience (www.interscience.wiley.com). r 2007 Wiley-Liss, Inc. Acoustic Variation in Japanese Macaques / 1413 depending on the distance to be transmitted [e.g., Mitani & Stuht, 1998; Wiley & Richards, 1978]. In group-living primates, intragroup vocal communication must cover a large range of distances because members of a group often remain close together (e.g., while they are resting) and they can spread over considerable distances (e.g., while traveling or foraging). Adjusting to such different situations, animals may need to use different types of vocalization or they may need to modify the acoustic features of a vocalization depending on the distance to other group members. Attempts to examine the effect of the distance on vocal behavior have been limited. Some observational studies have been conducted in natural settings. In pygmy marmosets, Cebuella pygmaea, different types of trills are uttered according to the distance between the caller and the respondent [Snowdon & Hodun, 1981]. Contact calls by free-ranging ring-tailed lemurs, Lemur catta, also differ according to the caller’s proximity to group members [Oda, 1996]. Under experimental conditions, acoustic features of ‘‘isolation calls’’ in common squirrel monkeys, Saimiri sciureus, differed according to the separation distance [Masataka & Symmes, 1986]. Under experimentally controlled noisy conditions, common marmosets, Callithrix jacchus, and cotton-top tamarins, Saguinus oedipus, modify the acoustic features of their calls [Brumm et al., 2004; Egnor & Hauser, 2006; Egnor et al., 2006]. The coo call of wild Japanese macaques, Macaca fuscata, is a suitable subject to examine the effect of distance on vocal behavior in nonhuman primates. Japanese macaques form a cohesive group with stable members, and the coo call is basically considered a within-group contact vocalization [Itani, 1963] to maintain group cohesion. It is often responded to vocally by group members, thereby forming a vocal exchange [Mitani, 1986; Sugiura, 1993]. The call is exchanged over distances ranging from 0 m to more than 30 m [Okayasu, 1987]. Moreover, its acoustic features are highly variable and graded both among and within individuals [Green, 1975b; Inoue, 1988; Mitani, 1986]. The first aim of this study was to examine the effect of distance to other group members on the acoustic features of coo calls in Japanese macaques. The behavioral context of the caller is also a major source of acoustic variation in primates. In general, behavioral contexts have been viewed as correlates of the internal state of a sender and as correlates of external phenomena. The internal state of the sender, such as its emotional state or motivation, involuntarily modifies the acoustic features of a vocalization [Morton, 1977; Scherer, 2003; Scherer & Kappas, 1988]. The relationship between external phenomena and acoustic features provides clues to explore the possibility that a vocalization refers to external objects or events, i.e., that it is semantic [Zuberbühler et al., 1999]. Note that it is usually difficult to distinguish between these two underlying mechanisms, and they are not necessarily mutually exclusive. Acoustic variation has been studied in several behavioral contexts. Alarm vocalizations differ acoustically according to the type of predator [Oda, 1998; Seyfarth et al., 1980; Zuberbühler et al., 1997]. Screams in an agonistic situation also differ according to the severity of the situation [Gouzoules & Gouzoules, 1995; Gouzoules et al., 1984]. Acoustic features of within-group contact vocalizations differ by behavioral context. In cotton-top tamarins, some types of ‘‘chirp’’ vocalizations are restricted to a foraging context [Elowson et al., 1991]. In common squirrel monkeys, the peak frequency of chuck vocalizations is lower Am. J. Primatol. DOI 10.1002/ajp 1414 / Sugiura in a foraging context than in a non-foraging context [Boinski & Mitchell, 1997]. In chimpanzees, Pan troglodytes, acoustic features of rough grunts are associated with food preference [Slocombe & Zuberbühler, 2006]. In Japanese macaques, coo calls are uttered in a broad range of contexts, and their acoustic features have been suggested to vary with context. Green [1975b] divided this call into seven subtypes based on acoustic features and showed that the seven types were associated with social context in provisioned groups, mostly in cases where the sender and the recipient were obvious; thus, the social relationship between the sender and recipient was apparent. He suggested that the acoustic features of coo calls are influenced by the sender’s motivation for contact with group members. He also emphasized that the peak location (position of the maximum frequency relative to the entire duration) was a key acoustic feature that varied with context. However, the generality of Green’s claims has never been fully examined, especially in the wild. A gap between his study and natural conditions involves the range of contexts in which coo calls are given. Under natural conditions, the call is given both when the group members stay close and when they spread out, and it is usually unclear to whom the call is addressed. In addition, ‘‘food calls’’ have been reported in study animals that were artificially provisioned [Green, 1975a]. Food calls are acoustically similar to coo calls and are therefore likely to be variants of coo calls. If this is the case, then the acoustic features of coo calls may be modified according to the feeding context. The second aim of this study was to explore the possibility that the behavioral context influences the acoustic features of coo calls. As a behavioral context, I chose the caller’s ongoing activities, i.e., foraging, moving, resting, and grooming, for the following reasons. First, these activities are obvious and cover the range of contexts in which coo calls are given under natural conditions; thus, recording calls during these activities is reliable and feasible to examine the effects of behavioral context. Second, acoustic features of coo calls may differ in the context of feeding, which has been inferred from the existence of food calls. In this study, I analyzed the effects of proximity to other group members and ongoing activity of a caller as two independent factors affecting within-individual acoustic variability of coo calls under natural conditions. In addition, I compared the acoustic variables modified in this study to a previous study by Green [1975b] and discuss the possible function of this vocalization, and the control of vocal production depending on the behavioral context of the caller. METHODS This study complied with the Research Guidelines of the Primate Research Institute, Kyoto University, and adhered to the legal requirements of Japan. Subjects I investigated a group of wild Japanese macaques on Yakushima Island, located south of Kyushu, Japan. The study group (B-group) was habituated to observers, and members have been individually identified since 1994 with no provisioning. The group’s home range covered approximately 50 ha of the warm–temperate forest on the western slope of Mt. Kuniwari-dake, Yakushima Island (30.41N, 130.41E; elevation 100–300 m a.s.l.). The forest had a closed canopy, and the shaded conditions kept the undergrowth thin on the forest floor. Detailed descriptions of the study site and subjects can be found in reports by Agetsuma and Nakagawa  and Sugiura et al. . Am. J. Primatol. DOI 10.1002/ajp Acoustic Variation in Japanese Macaques / 1415 I collected data during the non-mating season between 24 May 1997 and 11 August 1997. During the study period, the group consisted of 23 individuals, including six adult females (Z5 years old), seven adult males (Z5 years), three juvenile females (1–4 years), six juvenile males (1–4 years), and one infant (o1 year). Data Collection I focused on the vocal behavior of adult females, because adult males give coo calls infrequently [Mitani, 1986], and because vocal behaviors of juveniles or infants can differ from those of adults [e.g., Masataka and Fujita, 1989]. I chose five of the six adult females as subjects; one adult female was excluded because her call rate was extremely low. I collected data using the focal animal sampling method [Altmann, 1974]. During a focal animal sampling session, I recorded most calls from the focal subject (88%). I supplemented those samples with some vocalizations emitted by one of the five subject females who was not the focal female during that session (12%). Data were collected from subject females other than the focal animal only when the calling female stayed within my visible and audible range (i.e., the calling female was close to the focal female) and her activity and proximity to group members were observable. Since the frequency of vocalization varied individually, I spent a variable amount of time with each female to obtain a sufficient number of calls for each subject. The total observation time was 67 h 10 min, and the average observation time per subject was 13 h 26 min (range, 7 h 29 min–21 h 28 min). Each subject was observed 2 h at most on a given day. I recorded vocalizations using a digital audiotape recorder (Sony TCD-D8). I aimed a directional microphone (Sony ECM-672) at the focal female to record her vocalizations and held a nondirectional microphone (Sony ECM-261) to record vocalizations of non-focal animals in the background as well as my oral comments. When coo calls occurred, I recorded the activity and proximity of the focal female in relation to the nearest group member. Activity was divided into four categories: foraging, grooming, moving, and resting. Foraging included searching for, handling, and processing food, and moving within a food patch. Grooming comprised social grooming, selfgrooming, and other grooming activities before grooming, such as approaching a grooming partner or soliciting grooming. Thus, moving includes movement between food patches and resting sites but excludes movement within a food patch and that before grooming. Resting was defined as the time when animals neither moved nor performed any particular activity such as feeding or grooming. Proximity was defined mainly by whether adult females stayed close to the focal female because coo calls are usually exchanged between adult female group members [Mitani, 1986]. I defined ‘‘near a group member’’ as cases in which at least one adult female stayed within 10 m of the calling female, and ‘‘far from a group member’’ as cases in which neither adult females nor adult males were within 10 m of the calling female. Few calls (N 5 6) occurred when, in the absence of another female, one or more adult males stayed within 10 m of the focal female. I excluded these calls from the analysis, because the effect of proximity by adult males was unknown and the data were too few to examine the effect. The criterion of 10 m was chosen because I was usually able to see the monkeys reliably within this radius in the forest. When my visibility did not cover a 10-m radius around the subject, the data were excluded from the analysis. Am. J. Primatol. DOI 10.1002/ajp 1416 / Sugiura For the acoustic analysis, recorded calls were chosen randomly by subject, activity, and proximity. Acoustic Analysis I defined a coo call as one that was completely or predominantly tonal. Most coo calls were completely tonal (86%) but some contained a harsh component to the call (14%; Fig. 1). I basically treated these two call types as a single category for the following reasons. Acoustically, the harsh components usually occurred around the highest pitch in calls whose fundamental frequency reached a very high frequency. Also, the distribution of acoustic measures of the two types extensively overlapped with each other. Behaviorally, both types were intermingled in vocal exchanges and elicited identical vocal responses. Thus, the harsh component is likely a variant of tonal coo calls that may occur accompanied by the utterance of high-pitched vocalizations. However, the precise position of the maximum frequency is difficult to determine in harsh coo calls, and two acoustic variables were not measured. Therefore, to be cautious, I analyzed the acoustic features in two ways: tonal coos alone and pooled tonal and harsh coo calls. I did not analyze harsh coo calls alone because the sample size was too small. I measured the fundamental frequency components of recorded coo calls using a sound spectrograph (Kay DSP Sonagraph model 4,300). Time measures were determined on the spectrogram display with a frequency scale of 0–8,000 Hz and a timescale of 0–2 s, using a wideband filter (274 Hz) with a resolution of 0.003 s. Frequency measures were determined on the power spectrum display with a narrowband filter (94 Hz) with a resolution of 20 Hz connected with the time cursor of the spectrogram display. Five acoustic measures (start frequency, maximum frequency, end frequency, duration to maximum frequency, and total duration) are shown in Fig. 1. On the basis of these measures, I calculated three additional measures: maximum minus start frequency, maximum minus end frequency, and peak location (duration to maximum peak/total duration). As the harsh component usually occurred around the highest pitch, I measured the highest tonal component as the maximum frequency for harsh coo calls. Because the precise position of frequency peaks was difficult to determine in harsh coo calls, the duration to maximum frequency and peak location were not measured for this type. Thus, the data for Fig. 1. Representative sound spectrogram of a Japanese macaque coo call. Left, completely tonal calls; right, coo calls with a harsh component. The acoustic variables measured for the analysis are indicated. Am. J. Primatol. DOI 10.1002/ajp Acoustic Variation in Japanese Macaques / 1417 these two variables were derived only from tonal coos. In addition, peak location was determined from the calls with a distinct peak, of which either maximum minus start frequency or maximum minus end frequency was 40 Hz or more (93.4% of the tonal coo calls) because the minimum discriminative frequency difference is approximately 20–30 Hz [Sinnott et al., 1987]. I measured inter-call intervals between the end of the first call and the start of the next one to define spontaneous calls. A previous study on the vocal exchange of coo calls indicated that Japanese macaques respond to coo calls given by another group member within approximately 1.5 s and that such calls are acoustically similar to the preceding coo calls [Sugiura, 1998]. Therefore, I analyzed spontaneous calls only and excluded response calls to avoid any influence of previous calls. I defined spontaneous calls as those that were not preceded by other calls within 2.5 s. The criterion of 2.5 s was determined by adding a 1-s margin to the result that a response occurs within approximately 1.5 s. When more than one spontaneous call was recorded from the same female within 1 min, one call was chosen randomly to avoid sampling twice or more from a series of consecutive calls. To approximate normal distributions for the statistical analysis, duration to maximum frequency, total duration, start frequency, maximum frequency, and end frequency were logarithmically transformed. Maximum minus start frequency and maximum minus end frequency were square-root transformed, and peak location was arcsine transformed. For the statistical analysis, I used mixed-model analyses of variance (ANOVAs) with a general linear model procedure with type III error [SAS Institute Inc., 1988]. The mean squares of the error and the interaction with a random effect were pooled as the denominator according to Satterthwaithe’s approximation [Sokal & Rohlf, 1995]. For the post hoc multiple comparisons, I used the GT-2 method at a significance level of Po0.05. Each of the eight acoustic variables was analyzed by a three-way ANOVA, with ‘‘activity’’ (resting, foraging, and moving) and ‘‘proximity’’ (near or far from a group member) as the fixed effects and ‘‘caller’’ (N 5 5) as the random effect. Grooming was excluded from this analysis because situations in which a female groomed more than 10 m away from her group members were rare, and I obtained few coo calls in this context. To evaluate the effect of activity including grooming, I conducted a two-way ANOVA, with ‘‘activity’’ (grooming, resting, foraging, and moving) as the fixed effect and ‘‘caller’’ (N 5 3) as the random effect, but only when callers were near a group member. Because two of the five females rarely called while they were grooming, data from these two subjects were eliminated from the analysis. RESULTS I examined whether the acoustic features of spontaneous coo calls differed depending on activity and proximity. Table I shows the number of coo calls analyzed by context and by individual. Of the 280 spontaneous calls, 86.7% (243/ 280) were tonal coo calls and 13.2% (37/280) were harsh coo calls. Tonal coo calls were given more frequently when the callers were near than when they were far from a group member. When macaques were near group members, 95% (168/178) of coo calls were tonal and 5% (8/178) were harsh. When macaques were far from group members, 72% (75/104) were tonal and 28% (29/104) were harsh. First, I analyzed tonal coo calls alone using a three-way ANOVA (proximity activity caller, Table IIA). The effect of proximity was significant Am. J. Primatol. DOI 10.1002/ajp 1418 / Sugiura TABLE I. Number of coo calls used for analyses by call type, proximity, activity, and caller Caller Call type Tonal coo call Proximity Activity Near Far Harsh coo call Near Far BI KS ST TH TR Total Rest Forage Move Groom Total Rest Forage Move Groom Total 8 5 3 7 23 1 2 4 (0) 7 7 15 4 (1) 26 5 13 11 (0) 29 18 6 9 19 52 6 5 5 (1) 16 8 6 4 (1) 18 5 3 3 (0) 11 18 13 10 6 47 6 2 3 (0) 11 59 45 30 32 166 23 25 26 0 74 Rest Forage Move Groom Total Rest Forage Move Groom Total 0 0 0 0 0 2 3 7 (0) 12 0 0 0 (0) 0 0 2 1 (0) 3 1 0 0 0 1 1 0 3 (0) 4 2 1 2 (0) 5 4 0 5 (0) 9 0 0 1 1 2 0 0 1 (0) 1 3 1 3 1 8 7 5 17 (0) 29 Cells with parentheses indicate the number of calls that were acoustically measured but not used for statistical analyses. for two variables (start frequency and maximum frequency). For each of these variables, the mean was larger when the caller was far from a group member than when she was near a group member. The other six variables had high statistical values (0.05oPo0.08), and the means tended to be higher when the caller was far from a group member than when she was near. In contrast, the effect with activity was not significant in any variable, and the interaction between proximity and activity was not significant in any variable. Second, I analyzed pooled tonal and harsh coo calls using a three-way ANOVA (Table IIB). The effect of proximity was significant for five variables (start frequency, maximum frequency, end frequency, maximum minus start frequency, and total duration). Again, the mean was larger when the caller was far from a group member than when she was near a group member for each of these variables (Fig. 2). The effect of activity was significant only for start frequency. Post hoc multiple comparisons revealed that the mean start frequency was significantly higher when animals were moving than when they were foraging or resting. Means when foraging and resting did not differ significantly. The interaction between proximity and activity was not significant for any variable. When harsh coo calls were added to the tonal calls, the tendency remained that acoustic variables differed according to proximity rather than activity, and in addition, the difference became more prominent. Finally, to evaluate the effect of activity including grooming, I conducted a two-way ANOVA (activity caller) only when callers were near a group member. Again, I first analyzed tonal coo calls alone and then pooled with harsh coo calls. Am. J. Primatol. DOI 10.1002/ajp Acoustic Variation in Japanese Macaques / 1419 TABLE II. Results of a three-way ANOVA of acoustic variables of tonal coo calls (A) and pooled tonal and harsh coo calls (B), with ‘‘proximity’’ and ‘‘activity’’ as the fixed effects and ‘‘individuality of callers’’ (N 5 5) as the random effect Proximity Variables A. Tonal coo calls Start freq. Maximum freq. End frequency Maximum—start freq. Maximum—end freq. Duration to max. freq. Total duration Peak location B. Tonal and harsh coo calls Start freq. Maximum freq. End frequency Maximum—start freq. Maximum—end freq. Duration to max. freq. Total duration Peak location F 19.1 7.7 6.3 6.2 5.0 5.3 6.0 6.2 pooled 38.7 12.0 11.6 8.2 4.5 — 18.5 — (df) Activity F Proximity activity (df) F (df) (1, 5.4) (1, 4.3) (1, 4.2) (1, 4.3) (1, 5.0) (1, 4.2) (1, 4.3) (1, 4.8) 1.8 2.4 3.8 2.4 2.6 0.4 0.5 3.3 (2, (2, (2, (2, (2, (2, (2, (2, 12.1) 11.2) 12.4) 11.0) 13.4) 10.1) 11.5) 19.0) 1.7 2.9 1.7 3.1 1.2 0.9 0.5 0.2 (2, 12.9) (2, 11.8) (2, 11.4) (2, 11.2) (2, 9.7) (2, 10.2) (2, 13.5) (2, 10.3) (1, 4.4) (1, 4.1) (1, 4.1) (1, 4.0) (1, 4.1) 8.5 2.2 2.4 2.0 0.2 — 0.5 — (2, (2, (2, (2, (2, 9.2) 8.9) 8.9) 9.0) 8.7) 2.8 0.4 0.3 0.9 0.1 — 1.3 — (2, 10.1) (2, 8.9) (2, 8.7) (2, 8.7) (2, 8.6) (1, 4.1) (2, 8.9) (2, 8.9) The two fixed effects and their interaction are shown. *Po0.05; **Po0.01. Duration to maximum frequency and peak location were not analyzed in B because these two variables were not measured for harsh coo calls. No significant effect of activity was evident for any variables in tonal coo calls or in pooled tonal and harsh coo calls. DISCUSSION Effects of Proximity and Activity on Acoustic Variation The results indicate that Japanese macaques alter the acoustic variation of coo calls depending on the distance to group members but not depending on their ongoing activity. When the distance to another member increased, they produced calls with longer duration and a larger frequency modulation range. These results suggest that Japanese macaques can modify the acoustic features of coo calls according to the distance to the recipient. Calls with a longer duration and larger frequency modulation are very likely to be detected over longer distances in noisy environments [Brumm et al., 2004]. In addition, such acoustic features are also likely to increase the locatability of the caller by the distant recipient. When the recipient is far from the caller, the locatability of vocal signals decreases [Waser, 1977], and larger frequency modulation increases the locatability [Brown et al., 1979]. The results are similar to those reported for some primate species, suggesting that acoustic features are modified to become more locatable when the caller is far from the recipient [Masataka & Symmes, 1986; Oda, 1996; Snowdon & Hodun, 1981]. Am. J. Primatol. DOI 10.1002/ajp 1420 / Sugiura Fig. 2. Means of eight acoustic variables of coo calls by callers measured under two independent contexts in which the calls were given; proximity (near or far from a member; left part of each graph) and activity (resting, foraging, and moving; right part of each graph). Results of tonal and harsh coo calls pooled are shown except for duration to maximum frequency and peak location. For these two variables, results of tonal coo calls are shown because they were not measured for harsh coo calls. Am. J. Primatol. DOI 10.1002/ajp Acoustic Variation in Japanese Macaques / 1421 In contrast, the ongoing activities of the caller did not influence the acoustic variation of coo calls. Of eight acoustic variables, only one differed according to the caller’s activities, and this may have occurred by chance. Thus, overall, the results suggest that acoustic features of coo calls are not associated with the ongoing activity of the caller. It has been suggested that some avian and primate species emit ‘‘food calls’’ when they find preferred or abundant food [Clark & Wrangham, 1994; Hauser et al., 1993; Marler et al., 1986], including Japanese macaques [Green, 1975a,b] and other macaque species [Dittus, 1984; Hauser, 1993]. Japanese macaques emit ‘‘food calls,’’ especially when they are artificially provisioned [Green, 1975a]. This vocalization appears to be a variation of the coo call in terms of its acoustic structure. If Japanese macaques in the wild emit acoustically distinctive calls related to food resources, then the acoustic features of coo calls while feeding should be different from those emitted during other activities. However, I failed to find a unique variation in calls related to a foraging context. In Japanese macaques, ‘‘food calls’’ may not directly refer to food resources. Alternatively, they may produce coo calls with an extended duration and large frequency-modulation to address group members over a wide range of situations in which most group members can come together, e.g., at abundant food patches. Comparison with Previous Studies The basic concept by Green [1975b] that Japanese macaques modify the acoustic variation of coo calls depending on context was confirmed by the present study. Some detailed points, however, are not necessarily supported by the present and other studies. Green [1975b] argued that acoustic variation, especially peak location, of coo calls is associated with fine social contexts. In my results, however, peak location was not associated with any context. However, it has been pointed out that frequency modulation is important for tonal vocalization in macaques [Hauser, 1996; Moody & Stebbins, 1989; Sugiura, 1993, 1998]. My results support the communicative importance of frequency modulation. The inconsistency between the results of Green [1975b] and this study can be explained in two ways. First, the behavioral contexts differed between the two studies. Green [1975b] focused on a narrower range of situations with a finer classification of social contexts, mostly when macaques stayed close to group members. In contrast, this study considered a broader range of situations with regard to the proximity of group members, with a relatively coarse classification of contexts. The second explanation is that the variation in peak position can be due mainly to interindividual differences, because Green [1975b] did not control for individual differences. In fact, this study showed that in some acoustic variables, including peak location, the effect of contextual differences was not significantly larger than that of individual differences. Owren and Casale  also showed in Japanese macaques that variation in peak location of coo calls occurred primarily because of individual differences rather than the behavioral contexts of callers. Similar results were obtained in rhesus macaques [Hauser, 1991]. To resolve these complex questions, further studies on acoustic variability are needed. The association between acoustic variation and context should be investigated considering several factors: individual differences, proximity to group members, and scale (fineness) of the context classification. Am. J. Primatol. DOI 10.1002/ajp 1422 / Sugiura Possible Function and Mechanism of Acoustic Modification of Coo Calls The current results suggest that a coo call does not provide information about the caller’s activity. The acoustic features of this call appear to increase detectability and locatability when the sender and potential recipient are distant. Thus, the basic function of this call is apparently to locate the caller. This view is consistent with previous studies. Wild Japanese macaques emit coo calls more frequently when they are moving and foraging compared to when they are resting and grooming [Itani, 1963; Okayasu, 1987]. When moving, they are dispersed and their location is likely to change. Two explanations are possible regarding the mechanism of acoustic modification of coo calls, although they are not necessarily mutually exclusive. One is the caller’s internal emotional or motivational state [Morton, 1977; Scherer, 2003] that is likely to be associated with proximity. Higher motivation for contacting group members when a macaque is distant from group members may cause higher pitched calls. The other is that the caller controls the acoustic features of the calls. Control of the acoustic features of the calls has been suggested in previous studies [Koda, 2004; Sugiura, 1998, 2007; Tanaka et al., 2006]. Assuming that calls with detectable features are more likely to elicit a vocal response when the potential recipients are some distance away, callers should be more likely to produce such calls during these situations. ACKNOWLEDGMENTS I thank the Field Research Center of the Primate Research Institute, Kyoto University, for providing full use of the Yakushima Field Station; the Yakushima Forest Environment Conservation Center for permission to perform field research; and Dr. Yasuyuki Muroyama for valuable comments on an earlier version of this manuscript. This work was supported by a Research Fellowship of the Japan Society for the Promotion of Science for Young Scientists and a Grant for Biodiversity Research of the 21st Century COE (A14) to Kyoto University. This study complied with the Research Guidelines for the Study of Wild Primates of the Primate Research Institute, Kyoto University, and adhered to the Wildlife Protection and Hunting Laws of Japan. REFERENCES Agetsuma N, Nakagawa N. 1998. Effects of habitat differences on feeding behaviors of Japanese monkeys: comparison between Yakushima and Kinkazan. Primates 39: 275–289. Altmann J. 1974. Observational study of behavior: Sampling methods. Behaviour 49: 227–267. Boinski S, Mitchell CL. 1997. Chuck vocalizations of wild female squirrel monkeys (Saimiri sciureus) contain information on caller identity and foraging activity. Int J Primatol 18:975–993. Brown CH, Beecher MD, Moody DB, Stebbins WC. 1979. Locatability of vocal signals in Old World monkeys: design features for the communication of position. J Comp Physiol Psychol 93:806–819. Am. J. Primatol. DOI 10.1002/ajp Brumm H, Voss K, Kollmer I, Todt D. 2004. Acoustic communication in noise: regulation of call characteristics in a New World monkey. J Exp Biol 207:443–448. Clark AP, Wrangham RW. 1994. Chimpanzee arrival pant-hoots: do they signify food or status? Int J Primatol 15:185–205. Dittus WP. 1984. Toque macaque food calls: semantic communication concerning food distribution in the environment. Anim Behav 32:470–477. Egnor SER, Hauser MD. 2006. Noise-induced vocal modulation in cotton-top tamarins (Saguinus oedipus). Am J Primatol 68: 1183. Egnor SER, Iguina CG, Hauser MD. 2006. Perturbation of auditory feedback causes systematic perturbation in vocal structure Acoustic Variation in Japanese Macaques / 1423 in adult cotton-top tamarins. J Exp Biol 209: 3652–3663. Elowson AM, Tannenbaum PL, Snowdon CT. 1991. Food-associated calls correlate with food preferences in cotton-top tamarins. Anim Behav 42:931–937. Gouzoules H, Gouzoules S. 1995. Recruitment screams of pigtail monkeys (Macaca nemestrina): ontogenetic perspectives. Behaviour 132:431–450. Gouzoules S, Gouzoules H, Marler P. 1984. Rhesus monkey (Macaca mulatta) screams: representational signaling in the recruitment of agonistic aid. Anim Behav 32: 182–193. Green S. 1975a. Dialects in Japanese monkeys: vocal learning and cultural transmission of locale-specific vocal behavior? Z Tierpsychol 38:304–314. Green S. 1975b. Variation of vocal pattern with social situation in the Japanese monkey (Macaca fuscata): a field study. In: Rosenblum LA, editor. Primate behavior. New York: Academic Press. p 1–102. Hauser MD. 1991. Sources of acoustic variation in rhesus macaque (Macaca mulatta) vocalizations. Ethology 89:29–46. Hauser MD. 1993. Food-associated calls in rhesus macaques (Macaca mulatta): I. Socioecological factors. Behav Ecol Sociobiol 4: 194–205. Hauser MD. 1996. The evolution of communication. Cambridge: MIT Press. xii, 760 p. Hauser MD, Teixidor P, Field L, Flaherty R. 1993. Food-elicited cells in chimpanzees: effects of food quantity and divisibility. Anim Behav 45:817–819. Inoue M. 1988. Age gradation in vocalization and body weight in Japanese monkeys (Macaca fuscata). Folia Primatol 51:76–86. Itani J. 1963. Vocal communication of the wild Japanese monkey. Primates 4:11–66. Koda H. 2004. Flexibility and contextsensitivity during the vocal exchange of coo calls in wild Japanese macaques (Macaca fuscata yakui). Behaviour 141: 1279–1296. Marler P, Dufty A, Pickert R. 1986. Vocal communication in the domestic chicken: I. Does a sender communicate information about the quality of a food referent to a receiver? Anim Behav 34:188–193. Masataka N, Fujita K. 1989. Vocal learning of Japanese and rhesus monkeys. Behaviour 109:191–199. Masataka N, Symmes D. 1986. Effect of separation distance on isolation call structure in squirrel monkeys (Saimiri sciureus). Am J Primatol 10:271–278. Mitani JC, Stuht J. 1998. The evolution of nonhuman primate loud calls: Acoustic adaptation for long-distance transmission. Primates 39:171–182. Mitani M. 1986. Voiceprint identification and its application to sociological studies of wild Japanese monkeys (Macaca fuscata yakui). Primates 27:397–412. Moody DB, Stebbins WC. 1989. Salience of frequency modulation in primate communication. In: Dooling RJ, Hulse SH, editors. The comparative psychology of audition: perceiving complex sounds. Hillsdale: Lawrence Erlbaum Associates, Inc. p 353–376. Morton ES. 1975. Ecological sources of selection on avian sounds. Am Nat 109: 17–34. Morton ES. 1977. On the occurrence and significance of motivation-structural rules in some bird and mammal sounds. Am Nat 111: 855–869. Oda R. 1996. Effects of contextual and social variables on contact call production in freeranging ringtailed lemurs (Lemur catta). Int J Primatol 17:191–205. Oda R. 1998. The responses of Verreaux’s sifakas to anti-predator alarm calls given by sympatric ring-tailed lemurs. Folia Primatol 69:357–360. Okayasu N. 1987. Coo sound communication (in Japanese). Quaternary Anthropology 19:12–30. Owren MJ, Casale TM. 1994. Variations in fundamental frequency peak position in Japanese macaque (Macaca fuscata) coo calls. J Comp Psychol 108:291–297. SAS Institute Inc. 1988. SAS/STAT User’s Guide. Cary, NC.: SAS Institute Inc. Japanese translation, Tokyo: SAS Institute Japan. Scherer KR. 2003. Vocal communication of emotion: a review of research paradigms. Speech Commun 40:227–256. Scherer KR, Kappas A. 1988. Primate vocal expression of affective state. In: Todt D, Goedeking P, Symmes D, editors. Primate vocal communication. Berlin, Tokyo: Springer-Verlag. p 171–194. Seyfarth RM, Cheney DL, Marler P. 1980. Vervet monkey alarm calls: Semantic communication in a free-ranging primate. Anim Behav 28:1070–1094. Sinnott JM, Owren MJ, Petersen MR. 1987. Auditory frequency discrimination in primates: species differences (Cercopithecus, Macaca, Homo). J Comp Psychol 101: 126–131. Slocombe KE, Zuberbühler K. 2006. Foodassociated calls in chimpanzees: responses to food types or food preferences? Anim Behav 72:989–999. Snowdon CT, Hodun A. 1981. Acoustic adaptations in pygmy marmoset contact calls: locational cues vary with distance between conspecifics. Behav Ecol Sociobiol 9:295–300. Am. J. Primatol. DOI 10.1002/ajp 1424 / Sugiura Sokal RR, Rohlf JF. 1995. Biometry. New York: W.H. Freeman. 887p. Sugiura H. 1993. Temporal and acoustic correlates in vocal exchange of coo calls in Japanese macaques. Behaviour 124:207–225. Sugiura H. 1998. Matching of acoustic features during the vocal exchange of coo calls by Japanese macaques. Anim Behav 55: 673–687. Sugiura H. 2007. Adjustment of temporal call usage during vocal exchange of coo calls in Japanese macaques. Ethology in press. Sugiura H, Tanaka T, Masataka N. 2006. Sound transmission in the habitats of Japanese macaques and its possible effect on population differences in coo calls. Behaviour 143:993–1012. Tanaka T, Sugiura H, Masataka N. 2006. Cross-sectional and longitudinal studies of Am. J. Primatol. DOI 10.1002/ajp the development of group differences in acoustic features of coo calls in two groups of Japanese macaques. Ethology 112: 7–21. Waser PM. 1977. Sound localization by monkeys: A field experiment. Behav Ecol Sociobiol 2:427–431. Wiley RH, Richards DG. 1978. Physical constraints on acoustic communication in the atomosphere: Implications for the evolution of animal vocalizations. Behav Ecol Sociobiol 3:69–94. Zuberbühler K, Cheney DL, Seyfarth RM. 1999. Conceptual Semantics in a Nonhuman Primate. J Comp Psychol 113:33–42. Zuberbühler K, Noee R, Seyfarth RM. 1997. Diana monkey long-distance calls: messages for conspecifics and predators. Anim Behav 53:589–604.