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Ethology RESEARCH PA PERS

Cross-Sectional and Longitudinal Studies of the Development of Group Differences in Acoustic Features of Coo Calls in Two Groups of Japanese Macaques Toshiaki Tanaka, Hideki Sugiura & Nobuo Masataka Primate Research Institute, Kyoto University, Inuyama, Aichi, Japan

Correspondence Hideki Sugiura, Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan. E-mail: [email protected]

Received: October 29, 2003 Initial acceptance: February 19, 2005 Final acceptance: March 12, 2005 (J. Lazarus)

Abstract Japanese macaques, Macaca fuscata, frequently utter coo calls to maintain vocal contact. Cross-sectional and longitudinal comparisons were conducted on the acoustic features of coo vocalizations of two groups of M. fuscata, Yakushima and Ohirayama groups, to explore the possibility of vocal plasticity. These two groups derive from the same local population but have been separated for more than 34 yr. The Yakushima group is non-provisioned, while the Ohirayama group is provisioned. Initially, coo calls in the two groups were compared cross-sectionally in females ranging from 0 to 18 yr. Mean values of the four variables studied (start, end, maximum, and minimum frequencies) were consistently lower in all age groups of the Ohirayama individuals compared with the Yakushima individuals. Secondly, longitudinal comparisons were conducted on individuals in the 1–4 yr after birth. Mean values of the five frequency variables studied (start, end, maximum, minimum and average frequencies) were again consistently lower in all age groups of Ohirayama compared with Yakushima individuals, although mean values of both groups gradually declined with an increase in age. Inter-group differences were significant at all ages in minimum frequency and at the first, second and third years in start frequency. Longitudinal comparisons of individuals aged 4–11 mo were also conducted. Regarding the four variables that differed between the two groups in the cross-sectional study, the mean values of minimum and start frequency did not differ significantly between the two groups at 4–5 mo, but were significantly lower in Ohirayama individuals aged 7–8 and 9–11 mo. Although provisioning may have had an effect on the weight difference between the groups, and consequently on vocalization frequency, these results suggest that the inter-group differences in coo call features form approximately 6–7 mo after birth as a result of vocal plasticity.

Introduction Learning and experience are known to be essential for the development of vocalization in human infants, birds (e.g. Kroodsma & Baylis 1982), cetaceans (e.g. Tyack & Sayigh 1997) and seals (e.g. Ralls et al. 1985), but few studies have suggested the importance of experience in modifying call strucEthology 112 (2006) 7–21 ª 2006 The Authors Journal compilation ª 2006 Blackwell Verlag

tures in non-human primates, especially during early development. Most studies on primates suggest the influence of heredity rather than plasticity on vocal production, on differences in vocalizations among subspecies (for example, squirrel monkeys, Saimiri sciureus, Winter 1969; and ruffed lemurs, Varecia variegata, Macedonia & Taylor 1985), on deafening or social isolation (for example, in chimpanzees, Pan 7

Development of Group Differences in Coo Calls of Japanese Macaques

troglodytes, Kellogg 1968; and squirrel monkeys, Talmage-Riggs et al. 1972; Winter et al. 1973; Hammerschmidt et al. 2001), and on studies of hybrid animals (for example, in gibbons, Hylobates lar and Hylobates pileatus, Brockelman & Schilling 1984). Various problems are associated with studies on non-human primate vocal production. For example, in contrast to birdsongs, acoustic modifications of vocalizations resulting from plasticity are very subtle and liable to be overlooked (Marler & Mitani 1988). Furthermore, many experimental methods for acoustic or social isolation that have been developed for studies on songbirds (Snowdon & Elowson 1992) are difficult to carry out on non-human primates because they are highly social animals and thus cannot be raised in isolation without behavioral abnormalities (Snowdon & Elowson 1992; Hauser 1996; Seyfarth & Cheney 1997). As a result, difficulties arise in separating the relative roles of genetic and experiential factors affecting vocal production. To overcome this problem, cross-fostering experimental studies have been conducted, but comparisons of cross-fostering experiment results in Japanese macaques and rhesus macaques (Macaca mulatta) have been controversial (Masataka & Fujita 1989; Owren et al. 1992). A third problem is that many of the calls that have been investigated developmentally in non-human primates are agonistic, for example, threat or alarm calls. These types of vocalization have a high survival value and might be expected to be highly conservative, and therefore less likely to be modified through development, unlike affiliative vocalizations such as contact calls (Snowdon & Elowson 1992; Snowdon et al. 1997). To examine vocal plasticity in non-human primates, selecting affiliative vocalizations that are not expected to be conservative is suitable, although a counterexample has been reported (Hammerschmidt et al. 2000). Recent studies using more refined acoustic analyses have revealed a greater flexibility in non-human primate vocal production than previously thought (for example, trills in pygmy marmosets, Cebuella pygmaea, Elowson & Snowdon 1994; Snowdon & Elowson 1999; pant hoots in chimpanzees, Mitani & Brandt 1994; Marshall et al. 1999; and coo calls in Japanese macaques, Sugiura 1998). Considering these recent findings and the aforementioned problems of studying non-human primate vocal production, it is clear that a re-examination of vocal development in non-human primates is necessary. One method would be to compare vocal production between groups or populations (Seyfarth 1987; Janik 8

T. Tanaka, H. Sugiura & N. Masataka

& Slater 1997; Snowdon et al. 1997). Differences in vocal signals between populations of potentially interbreeding individuals have been extensively reported in songbirds (e.g. Kroodsma & Baylis 1982; Baker & Cunningham 1985) and in some non-song birds (for example, in black-capped chickadees, Parus atricapillus, Mammen & Nowicki 1981; Nowicki et al. 1989). On the contrary, there have been relatively few documentations of such differences between groups or populations of mammals (Snowdon et al. 1997). In non-human primates, group and population differences in vocal production have been reported in Japanese macaques (food calls, Green 1975a), red-chested tamarins (Saguinus l. labiatus) (long calls, Maeda & Masataka 1987), saddleback tamarins (Saguinus fuscicollis) (long calls, Hodun et al. 1981), chimpanzees (pant hoots, Mitani et al. 1992), and Barbary macaques (Macaca sylvanus) (shrill barks, Fischer et al. 1998). Although these studies suggest vocal plasticity, no data exists on whether breeding occurs between the compared populations or on whether the origin of the founder monkeys is the same. Additionally, little is known about the role of vocal development in population differences. Japanese macaques exchange coo calls in a variety of contexts, but not agonistically (Itani 1963; Green 1975b). In addition, mother Japanese macaques can recognize the coo calls of their offspring (Pereira 1986). The basic function of this coo call seems to be to locate group members and maintain vocal withingroup contact (Okayasu 1987; Sugiura 1998). In this study, we examine whether vocal structure changes when we compare the coo calls, affiliative vocalizations, of two Japanese macaques groups derived from the same initial population (the Ohirayama and the Yakushima groups). Also, if the vocal structure changes, we then examine the time at which it changes in the course of vocal development. First, coo calls of females ranging from 0 to 18 yr were compared cross-sectionally between the two groups (Section 1). Second, the vocal development of four infants from each group was studied longitudinally for 4 yr to augment the results of the cross-sectional comparisons (Section 2). These crosssectional and longitudinal studies indicated that significant inter-group differences in coo call structure emerged at approximately the first year after birth, therefore six infants from each group, at three developmental phases: 4–5, 7–8 and 9–11 mo, were followed for the first year after birth to explore when these inter-group differences emerge (Section 3). Factor analysis was conducted to investigate the Ethology 112 (2006) 7–21 ª 2006 The Authors Journal compilation ª 2006 Blackwell Verlag


relationship among the acoustic variables used in the analysis of Sections 1–3 (Section 4). The Yakushima group, with an evergreen forest habitat, is non-provisioned; while the Ohirayama group, with a habitat of dirt or gravelly ground with little vegetation, is provisioned. In the light of these differences, it is thought that there are five possible explanations for the mechanisms and functions of the inter-group differences in coo call structure; body size, genetic drift, vocal plasticity, and social or habitat factors. We discuss these five possible explanations in the Discussion section.


Table 1: Composition of the Yakushima and Ohirayama groups during vocal recordings Adults (‡5 yr) Troop

Male

Female

Yakushima P T H S Nina-A B Ohirayama

4 4 6 5 10 6 17

6 3 8 4 18 7 19

Juveniles (1–4 yr)

2 3 9 5 18 9 27

Infants

1 0 1 0 12 2 11

Total

13 10 24 14 58 24 74

Section 1: Cross-Sectional Study Methods Study site and subjects

Two groups of Japanese macaques were studied, the Yakushima group and the Ohirayama group. The Yakushima group is a wild population that inhabits a warm temperate forest in west Yakushima Island (30N, 130E), southern Japan. The Ohirayama group is a semi free-ranging group whose original members were captured in 1956 near the study site of the Yakushima group (J. Itani, pers. comm.) and immediately transported to Mount Ohirayama (35N, 136E), central Japan. They have been provisioned under semi free-ranging conditions since their capture (for further details of this group and its habitat, see Kawai 1960). The two groups are geographically separated by more than 700 km and have had no contact with each other since their separation in 1956. In the Ohirayama group, no animals have been newly introduced since translocation and no resident animals have been allowed to outbreed. In addition, population genetic studies of Japanese macaques have revealed that genetic variability on Yakushima Island is very small (Nozawa et al. 1991). Furthermore, morphological studies have revealed that the morphological traits of Yakushima and Ohirayama individuals do not differ (Kuroda 1992) and therefore, it can be assumed that the two groups have not differentiated genetically. Six free-ranging troops (H, P, T, S, Nina-A and B) distributed adjacently were sampled from the Yakushima group. The H, P and T troops have been habituated since 1973 (Maruhashi 1980), the S troop since 1992 (Sugiura & Masataka 1995), and the Nina-A and B troops since 1994 (the authors). These six troops were studied without provisioning. Table 1 shows the compositions of the Yakushima and Ohirayama groups during vocal recordings. All focal Ethology 112 (2006) 7–21 ª 2006 The Authors Journal compilation ª 2006 Blackwell Verlag

animals in each troop of the Yakushima group and all animals in the Ohirayama group were identified before vocal recordings commenced. Females were selected as subjects, because coo calls are mainly exchanged among these individuals (Mitani 1986). Twenty-three females were selected from the Yakushima group (three from B troop, one from the H, seven from P, three from T, one from S and eight from Nina-A) and 30 from the Ohirayama group. The subjects were selected reasonably evenly from all age groups; mean age was 4.3 yr (range: 0– 18) in the Yakushima group and 5.0 yr (range: 0– 18) in the Ohirayama group. The ages of subject females did not significantly differ between the two groups (Mann–Whitney U-test: U = 285, n1 = 23, n2 = 30, p = 0.28). Collection of acoustic data

Vocal recordings were conducted intermittently between 1990 and 1998. Vocal recordings for each subject were completed within 2 mo. The average of recording days per individual was 4.5 d in Yakushima and 7.8 d in Ohirayama. Acoustic and behavioral data was collected using a focal animal sampling method (Altmann 1974) in which by staying near the focal animal, its spontaneous vocalizations were recorded for a 60 min period using a hand-held microphone (Sony ECM-672 directional microphone, Tokyo, Japan) and a tape recorder (Sony WM-D6C) or an MD recorder (AIWA AM-F1, Tokyo, Japan). Whenever the focal animals emitted coo calls, behavioral activities were also recorded. If the focal animal was lost sight of, it was relocated as soon as possible to allow observations to resume. If the focal animal could not be located within 20 min, the recording session was terminated and the data were not used for analyses. Sessions were distributed almost equally throughout the day between 08.00 9


Acoustic analysis

Coo calls were defined according to the classification by Green (1975b). Such calls are tonal and their fundamental frequency elements are usually the most dominant. Moreover, the fundamental frequency of coo calls contributes most to the perception of vocal sounds (Kojima & Nagumo 1996). Macaques produce these calls in calm or relaxed situations, for example when feeding, moving, grooming or resting (Sugiura & Masataka 1995), and especially during feeding and moving under free-ranging situations (Itani 1963). It is possible that coo calls emitted during different types of behavior differ acoustically, and so to exclude this possibility only coo calls produced when feeding were analyzed. In the Ohirayama group, calls made just before artificial feeding were excluded from subsequent analysis, because there are no comparable calls in the Yakushima group that was studied without provisioning. From all recorded feeding vocalizations, 20 calls were randomly chosen from each subject for analysis; however, when several calls were emitted successively, only one call per bout was chosen. Calls were analyzed quantitatively using a Kay DPS Sonagraph 5500 or Sound Scope 16 Version 1.44 (GW Instruments, Somerville, MA, USA) on a Power Macintosh 7100; both operate with a narrow band filter (512 pts: 59 Hz) on a frequency scale of 0–8 kHz. Most coo call frequency components lie between 0.3 and 8 kHz. Seven acoustic variables of the fundamental frequencies of a chosen call were measured; namely duration, start frequency, end frequency, maximum frequency, minimum frequency, frequency range (maximum minus minimum frequency), and the location of the maximum 10

8

Frequency (kHz)

and 17.00 hours for the Yakushima group and between 09.30 and 16.30 hours for the Ohirayama group. As the frequency of vocal emissions varied considerably among individuals, the data collection method was designed to obtain a similar number of vocalizations from each individual per group. The habitat of the Yakushima group is evergreen forest and that of Ohirayama group is dirt or gravelly ground with little vegetation and very little snow; therefore, there is no reason that vocalizations might vary with the time of year because of climatic or other effects, and there was no seasonal differences in sound transmission in each habitat (H. Sugiura, T. Tanaka, N. Masataka, unpubl. data). A total of 112 and 270 sessions were conducted with the Yakushima and Ohirayama groups, respectively.


4 Maximum frequency Start frequency Minimum frequency

0

End frequency Time to maximum frequency Duration

0

Time (ms)

100

Fig. 1: A representative sound spectrogram of the coo calls of a Japanese macaque. The acoustic parameters measured for analysis are shown

frequency (time to maximum frequency/duration). A representative spectrogram is shown in Fig. 1. Statistical analysis

The five frequency variables (start frequency, end frequency, maximum frequency, minimum frequency and frequency range) were transformed to a logarithm and the location of the maximum frequency was transformed to an arcsine before statistical analysis. Because the frequency range values could be zero, 10 Hz were added to these values before logarithmic transformation. Logarithmic transformation was selected to remedy the situation wherein the mean value is positively correlated with variance (greater mean values are accompanied by greater variances). Arcsine transformation was selected to normalize data in proportions whose distributions fits a binomial distribution, because in a binomial distribution the variance become smaller when the mean value become farther from 0.5 and arcsine transformation stretches out both tails of a binominal distribution and compresses the middle. In addition, it was confirmed that the data satisfied normality and homogeneity of variance before anova or ancova was conducted. The mean values of each subject were used for comparisons between the two groups, and thus degrees of freedom were based on the total number of subjects, not the number of calls. There is evidence that age explained by variations in weight has an influence on the structure of calls (Inoue 1988; Fitch 1997; Hammerschmidt et al. 2000, 2001; Fischer 2002; Reby & McComb 2003); therefore, regression analysis of age was conducted. The pooled regression coefficients of the two groups were calculated by first calculating the variance and Ethology 112 (2006) 7–21 ª 2006 The Authors Journal compilation ª 2006 Blackwell Verlag



Table 2: Results of regression analysis of acoustic variables on age and the main effects of group difference by ANCOVA or ANOVA

Pooled regression

Effect of group

Parameter

Coefficient of regression

F (df)

F (df)

Duration Start frequency Minimum frequency Maximum frequency End frequency Frequency range Location of maximum frequency

)0.004 )0.023 )0.024 )0.016 )0.024 0.008 )0.008

8.3** 97.8*** 118.8*** 54*** 109.4*** 1.0 1.2

(1,50) (1,50) (1,50) (1,50) (1,50) (1,50) (1,50)

0.03 28.9*** 31.1*** 17.8*** 22.8*** 1.2 1.0

Test (1,50) (1,50) (1,50) (1,50) (1,50) (1,51) (1,51)

ANCOVA ANCOVA ANCOVA ANCOVA ANCOVA ANOVA ANOVA

**p < 0.01; ***p < 0.001.

covariance for each group separately and then pooling these results (Sokal & Rohlf 1995). Duration and the four frequency variables (start, end, maximum, and minimum frequency) showed significant negative regression with age (Table 2). For these variables, a one-factorial analysis of covariance (ancova) was conducted with the age of the caller as a covariate and the group as the main effect, to examine the effect of the group. Prior to ancova, the homogeneity of the slopes with age were tested and it was confirmed that they did not differ between the two groups for all five of the variables (F1,49 = 0.8, p = 0.37 for duration; F1,49 = 0.7, p = 0.40 for start frequency; F1,49 = 0.7, p = 0.40 for end frequency; F1,49 = 2.9, p = 0.10 for maximum frequency; and F1,49 = 0.7, p = 0.42 for minimum frequency). The two other variables (frequency range and the location of the maximum frequency) were not significantly affected by age (Table 2) and were thus examined using a one-factorial analysis of variance (anova), using the group as the main effect. In these anova, subjects are entered as a nested effect within the group. Because the subject represents a subsampling unit within each group, a more accurate estimate of the variability within each group can be provided. Hence, the appropriate error term for testing the main effect of the group is the error of subject within the group, not the residual error. Detailed information on nested design is given in Sokal & Rohlf (1995). Results Inter-group differences were significant in the four frequency variables (Table 2); the mean values for the Ohirayama individuals being consistently lower than those of the Yakushima individuals at all ages (Fig. 2). Females of the Ohirayama group produced Ethology 112 (2006) 7–21 ª 2006 The Authors Journal compilation ª 2006 Blackwell Verlag

coo calls with a lower fundamental frequency than females of the Yakushima group. This tendency was especially clear in the start and minimum frequencies (Table 2). In contrast, no significant differences were detected in duration, frequency range, and location of maximum frequency between the two groups (Table 2; Fig. 2). Section 2: Longitudinal Study 1 The results of the cross-sectional study indicated that the mean values of the four variables (start, end, maximum, and minimum frequency) for Ohirayama individuals were consistently lower than those for Yakushima individuals at all ages, whereas mean values gradually declined with increased age in both groups. Next, the vocal development of four infants from each of the groups was followed annually for 4 yr to augment the results of the cross-sectional study, and to ascertain when in development, if at all, call structures began to diverge. Methods Study sites and subjects

The subject groups were mostly the same as in the cross-sectional study except only the Nina-A and B troops were selected to make up the Yakushima group. The composition of both groups during vocal recordings was similar to that in the cross-sectional study. Four infant females from the Yakushima group (three from the Nina-A troop and one from the B troop) and four infant females from the Ohirayama group were selected as subjects. All subjects in the Yakushima group were born in 1994 but the exact month of birth was not recorded; therefore, in accordance with Fooden & Aimi (2003), the birth date was assumed to be Apr. 30. In the Ohirayama 11

0.4 0.3 0.2 0.1

Minimum frequency (Hz)

Duration (s)

0.5

1500

Maximum frequency (Hz)


1500


1000

500

0

1000

500

1000

500

1000

1500

Frequency range (Hz)

End frequency (Hz)

Start frequency (Hz)

1500

1000

500

500

100 50 0

5

10

15

20

Location of max. freq. (%)

Age (yr) 100

50

0 0

5

10

15

20

Age (yr)

group, one subject was born in May 1990, another in May 1992, and the other two in May 1993. Collection of acoustic data

Acoustic and behavioral data during the four developmental phases was collected annually at the first year (9–10 mo for Ohirayama subjects and 7 mo for Yakushima subjects), the second year (22–23 mo for Ohirayama subjects and 19–20 mo for Yakushima subjects), the third year (33–36 mo for Ohirayama subjects and 31 mo for Yakushima subjects), and the fourth year after birth (44–48 mo for Ohirayama subjects and 46 mo for Yakushima subjects). Data collection times for each developmental phase were as follows: Feb. 1991, Feb. 1992, Jan. 1993, and Apr. 1994 for one subject in the Ohirayama group; Jan. 1993, Mar. 1994, Apr. 1995, and Apr. 1996 for 12

Fig. 2: Mean values and SDs of the acoustic parameters of coo calls given by 53 macaque individuals: 23 from Yakushima and 30 from Ohirayama. Closed symbols represent Yakushima individuals and open symbols represent Ohirayama individuals. The results of ANCOVA showed that inter-group differences were significant in start, maximum, minimum, and end frequency

another subject in the Ohirayama group; Mar. 1994, Mar. 1995, Apr. 1996, and Dec. 1996 for the other subjects in the Ohirayama group; Nov. 1994, Nov. 1995, Nov. 1996, and Feb. 1998 for all Yakushima subjects at the first, second, third, and fourth years, respectively, after birth. Data collection procedures were the same as those for the cross-sectional study except for the observation sessions for each subject, which were day-long sessions of following each subject and were conducted daily between 08.00 and 17.00 hours in the Yakushima group and between 09.30 and 16.30 hours in the Ohirayama group. The total number of observation sessions were 6, 14, 5, and 6 for the Yakushima group, and 24, 9, 19, and 9 for the Ohirayama group at the first, second, third and fourth years, respectively, after birth. Ethology 112 (2006) 7–21 ª 2006 The Authors Journal compilation ª 2006 Blackwell Verlag



Acoustic analysis

Acoustic analysis was conducted using the same methods applied in the cross-sectional study apart from the addition of a new variable, average frequency, defined as the arithmetic mean of the fundamental frequency measured by the peak-picking algorithm (Coughlam et al. 1993). Eight acoustic variables of fundamental frequency were measured for each call. Statistical analysis

To examine the effects of group (Yakushima and Ohirayama), age (first, second, third and fourth years), and group · age interactions, one between and one within factor analyses of variance (anova) were conducted for each variable. In these anova tests, the effect of the subject was nested within the effect of the group to control variations between individuals. When the effect of group · age interactions was significant, simple main effect tests were conducted to investigate the main effect of the group at each age. Results

The anova results revealed that there are no significant effects of group, age or group · age interaction in duration (Table 3; Fig. 3). There were significant main effects of age and group in start, end, maximum, minimum, and average frequencies (Table 3). As individuals in both groups grew older, the mean values of the five frequency variables gradually declined (Fig. 3) with the mean values of the Ohirayama individuals being

Table 3: Results of ANOVA tests on the Yakushima and Ohirayama groups during longitudinal comparisons of individuals 1–4 yr after birth Parameter

Group (F1,6)

Age (F3,18)

Group · age (F3,18)

Duration Average frequency Start frequency Minimum frequency Maximum frequency End frequency Frequency range Location of maximum frequency

0.4 129.7*** 42.5*** 68.8*** 76.7*** 71.7*** 17.6** 0.1

0.9 318.6*** 614.3*** 826.2*** 169.8*** 288.3*** 2.7 0.7

2.3 2.1 7.0** 6.1** 1.1 1.1 1.7 3.4*

Sample sizes were as follows: n = 4 females from each of the Yakushima and Ohirayama groups, with a mean of 20 coo calls analyzed for each female. All p-values are two tailed: *p < 0.05; **p < 0.01; ***p < 0.001.

Ethology 112 (2006) 7–21 ª 2006 The Authors Journal compilation ª 2006 Blackwell Verlag

lower than those of the Yakushima individuals (Fig. 3). For start and minimum frequencies, the effect of group · age interactions was significant and therefore simple main effect tests were performed to examine the effect of group at each age. The main effects of group on minimum frequency were significant at all ages and those on start frequency were significant at the first, second and third years but not at fourth year (Table 4; Fig. 3). Overall, the frequency variables were lower in the Ohirayama group than in the Yakushima at each age. There was a significant effect of group, but not of age or group · age interactions in frequency range (Table 3). Inter-group differences existed until the third year, but became unclear at the fourth year; individuals for each group did not show consistent developmental change (Fig. 3). There were no significant main effects of group or age, but there was a significant group · age interaction effect in the location of the maximum frequency (Table 3). Simple main effect tests were therefore performed to examine the main effects of the group at each age. However, the mean values of the location of the maximum frequency did not differ significantly between the two groups at any age (Table 4). Section 3: Longitudinal Study 2 The results of the cross-sectional study and the longitudinal study 1 showed significant differences between the Ohirayama and Yakushima groups in some coo call frequency variables. These results suggested that group difference may emerge before 1 yr; therefore, more detailed longitudinal comparisons of vocalizations in the Ohirayama and Yakushima groups were conducted during the first year after birth. Methods Study sites and subjects

The Yakushima Nina-A and B troops, and the Ohirayama group were selected as the subject groups. Constituent members of the Yakushima (Nina-A and B troops) and Ohirayama groups during vocal recordings were similar to those studied in the crosssectional study. Five infant females and one infant male from the Yakushima group (five from the Nina-A troop and one from the B), and five infant females and one infant male from the Ohirayama group were chosen as subjects. As coo calls are mainly exchanged 13


Average frequency (Hz)

1500

0.3

0.2

1000

0.1

500

1500

1500

Minimum frequency (Hz)


Duration (s)

0.4


1000

1000

500

500

1500


1000

1000

500

500

500

100



End frequency (Hz)

1500

100

50

50

0 0

1

2

3

4

0

1

Table 4: Results of simple main effect tests of group difference at each age

Parameter Start frequency Minimum frequency Location of maximum frequency

First year (F1,6)

Second year (F1,6)

Third year (F1,6)

Fourth year (F1,6)

20.8** 23.3** 2.4

9.1* 15.8** 0.0

10.0* 22.9** 0.3

5.27 8.94* 0.28

All p-values are two tailed: *p < 0.05; **p < 0.01.

between females it was hoped that only females would be the subjects (Mitani 1986), but as only five infants were identified as females in the Yakushima 14

2

Age (yr)

Age (yr)

3

4

Fig. 3: Annual mean values of acoustic variables in coo calls from observations of eight individuals, four each from the Yakushima and Ohirayama groups over the 4 yr following birth. Closed symbols represent Yakushima individuals and open symbols represent Ohirayama individuals. The results of ANOVA showed that inter-group differences were significant in average, start, minimum, maximum, end frequency, and frequency range. The results of simple main effect tests showed that inter-group differences were significant at all ages in minimum frequency and at the first, second and third years in start frequency. The ellipses and error bars represent the mean values and SDs of each age category of data of four subjects in each of the Yakushima (black ellipse) and Ohirayama (white ellipse) groups, at each age category

group, one male infant was added to each of the groups. The exact date of birth of the subjects in the Yakushima group was not recorded, but it could be confirmed that all subjects were born before Jul. 6. The age in days of the subjects from the Yakushima group were counted assuming that they were born on Apr. 30, 1996; as at Jul. 6, when all subjects were assessed, it appeared from their body sizes and fur coloration that all were at least 2 mo or more. Because infants of Macaca fuscata yakui were born with black hair and their body coloration gradually turns brown by around 3 mo, the age in days of the infants can be reasonably estimated using fur coloration. Therefore, it is very likely that the age in days Ethology 112 (2006) 7–21 ª 2006 The Authors Journal compilation ª 2006 Blackwell Verlag


of subjects were not estimated as being younger than they really were. As for the Ohirayama group, all subjects were born between the Apr. 8 and 30, 1996. Collection of acoustic data and analysis

Infants under 3 mo did not often utter coo calls. Sufficient samples of coo calls from infants under 3 mo could not be collected, and so vocalizations were collected from infants over 3 mo. Acoustic and behavioral data during three developmental phases over the first year after birth for each group were recorded: at 4–5 mo (124–139 and 160–165 d for the Ohirayama and Yakushima subjects, respectively), at 7– 8 mo (223–237 and 256–265 d for the Ohirayama and Yakushima subjects, respectively) and at 9– 11 mo (282–299 and 339–347 d for the Ohirayama and Yakushima subjects, respectively). Data collection times for each developmental phase were in Aug. to Sep. 1996, Dec. 1996, and Feb. 1997 for the Ohirayama group, and in Oct. 1996, Jan. 1997, and Apr. 1997 for the Yakushima group at 4–5, 7–8 and 9–11 mo, respectively, after birth. Considering that individuals in the Ohirayama group were provisioned and were in better growth condition than individuals in the Yakushima group, acoustic and behavioral data from the Ohirayama group were collected first followed by the Yakushima group at each developmental phase. Procedures of data collection were the same as those conducted for the first longitudinal study. The total number of observation sessions were 6, 10 and 9 for the Yakushima group, and 7, 10 and 7 for the Ohirayama group at the 4–5, the 7–8 and the 9–11 mo, respectively, after birth. Acoustic and statistical analyses were the same as those used in the first longitudinal study. In the anova, group (Yakushima and Ohirayama) and age (4–5, 7–8 and 9–11 mo) were entered as factors. Results

The anova tests revealed no significant effects of group, age or group · age interactions in duration (Table 5; Fig. 4). There were significant main effects of group in average, start, and minimum frequencies, and significant main effects of age in start, end, maximum, minimum, and average frequencies (Table 5). The effects of group · age interactions were also significant in the five frequency variables (Table 5), and so simple main effect tests were performed to examine the main effects of group at each age. For average, Ethology 112 (2006) 7–21 ª 2006 The Authors Journal compilation ª 2006 Blackwell Verlag


Table 5: Results of ANOVA tests on the Yakushima and Ohirayama groups during longitudinal comparisons of individuals aged 4–11 mo Parameter

Group (F1,10)

Age (F2,20)

Group · age (F2,20)

Duration Average frequency Starting frequency Minimum frequency Maximum frequency End frequency Frequency range Location of maximum frequency

0.9 12.2** 36.2*** 19.1** 2.1 2.7 3.9 40.7**

1.7 180.8*** 179.1*** 146.5*** 88.4** 132.6** 0.5 1.9

1.2 38.5*** 49.5*** 33.3*** 13.9** 22.0** 0.3 3.8*

Sample sizes were as follows: n = 6 (five females and one male) from the Yakushima and Ohirayama groups, with mean values of 20 coo calls analyzed for each female. All p-values are two tailed: *p < 0.05; **p < 0.01; ***p < 0.001.

start and minimum frequencies, there were no significant inter-group differences at 4–5 mo; however, differences did emerge at 7–8 and 9–11 mo (Table 6). The mean values for the end and maximum frequencies did not differ significantly between the two groups at any age (Table 6). The mean values showed a decline with increasing age in both groups, although the slopes of decline were steeper in the Ohirayama group compared with the Yakushima group at 7–8 and 9–11 mo (Fig. 4). This tendency was particularly clear in the average, start and minimum frequencies. There were no significant effects of group, age and group · age interaction in frequency range (Table 5; Fig. 4). In location of the maximum frequency, the mean values of individuals in the Ohirayama group were higher than those of individuals in the Yakushima group at all ages (Fig. 4). There was a significant main effect of group, a significant interactive effect of group · age, but no significant main effect of age (Table 5). The results of simple main effect tests revealed that the mean values of the Ohirayama and Yakushima groups did not differ significantly at 4– 5 mo (Table 6). This might have been affected by the mean of one subject in the Yakushima group whose results are considerably higher than the other subjects of the group (Fig. 4). On the contrary, the mean values of the Ohirayama and the Yakushima group differed significantly at 7–8 and 9–11 mo (Fig. 4; Table 6). Section 4: Factor Analysis of Acoustic Variables To investigate the relationship among the acoustic variables used in the analysis of Sections 1–3, all of the data sets in Sections 1–3 were pooled and factor 15


Average frequency (Hz)

1500

0.3

0.2

1500

1500 Minimum frequency (Hz)

700

1000

1000

700

700

1500

1500

1000

700 500

1000

700 100



1000

0.1


End frequency (Hz)


Duration (s)

0.4

100

50

50

0 3

4

5

6

7 8 9 10 11 12 Age (mo)

3

4

5

6

7 8 9 10 11 12 Age (mo)

Table 6: Results of simple main effect tests of group difference at each developmental phase Parameter

4–5 mo (F1,10) 7–8 mo (F1,10) 9–11 mo (F1,10)

Average frequency Starting frequency Minimum frequency Maximum frequency End frequency Location of maximum frequency

0.2 0.1 0.0 0.7 0.5 4.8

9.0* 21.9** 12.0** 2.1 2.4 15.6**

12.4** 31.0*** 17.0** 3.6 4.2 24.1**

All p-values are two tailed: *p < 0.05; **p < 0.01; ***p < 0.001.

analysis was conducted. Seven acoustic variables were chosen, namely, duration, start frequency, end frequency, maximum frequency, minimum frequency, 16


Fig. 4: Mean values of acoustic variables in coo calls from observations of 12 individuals, six from each of the Yakushima and Ohirayama groups at three developmental phases over 1 yr following birth. Closed symbols represent Yakushima individuals and open symbols represent Ohirayama individuals. The results of ANOVA showed that inter-group differences were significant in average, start, and minimum frequency. The results of simple main effect tests showed that inter-group differences were significant at 7–8 mo and, 9– 11 mo in average frequency, minimum frequency, start frequency, and location of maximum frequency. Ellipses and error bars represent the mean values and SDs of each age category of data from six subjects in the Yakushima (black ellipse) and Ohirayama (white ellipse) groups, respectively, at each age category

frequency range, and the location of maximum frequency. Average frequency was excluded from factor analysis because this variable was not used in the analysis in Section 1. Principal factor analysis was chosen to extract factors from the correlation structure. All factors with eigenvalues ‡1 were extracted, and varimax rotation used to transform the factors. Table 7 shows the results of factor analysis. Three factors were extracted; start, minimum, maximum and end frequencies strongly and positively associated with the first factor. Duration and frequency range strongly and positively associated with the second factor. Location of maximum frequency strongly and positively associated with the third factor. Ethology 112 (2006) 7–21 ª 2006 The Authors Journal compilation ª 2006 Blackwell Verlag



Table 7: Results of factor analysis of the acoustic variables in Sections 1–3 Variables

Factor 1

Factor 2

Factor 3

Start frequency Minimum frequency Maximum frequency End frequency Duration Frequency range Location of maximum frequency

0.98 0.92 0.97 0.99 0.17 )0.12 0.06

)0.05 0.29 0.01 )0.09 0.69 0.82 0.01

)0.10 0.08 0.11 )0.04 )0.30 0.29 0.93

Discussion Cross-sectional comparisons of the coo calls of the Ohirayama and Yakushima groups revealed subtle but significant inter-group differences in the four frequency variables (minimum, start, maximum, and end frequencies). These variables were consistently lower in the Ohirayama group than in the Yakushima individuals at all ages, although the mean values gradually declined with age in the both groups. In addition, inter-group differences were still significant in these four frequency variables even when the two individuals with high frequency values, Hatu and Masu, in the Yakushima group (Fig. 2) were excluded from the data set. The results for the frequency variables in longitudinal study 1 approximately replicated those in the cross-sectional study. The effect of the group was significant in regard to frequency range but the effects of age were not in longitudinal study 1. In addition, inter-group differences of frequency range did not emerge in the cross-sectional comparisons. Duration and location of maximum frequency did not show significant inter-group differences or consistent changes with age in longitudinal study 1. The results of longitudinal study 2 showed that the mean values of start, minimum and average frequencies of Ohirayama individuals did not differ from those of the Yakushima individuals at 4–5 mo, but became lower at 7–8 and 9–11 mo. The location of the maximum frequency of the Ohirayama individuals did not differ from those of the Yakushima individuals at 4–5 mo, but became higher at 7–8 and 9–11 mo. However, this latter inter-group difference disappeared by 1 yr of age. Duration and frequency range did not show significant inter-group differences or consistent differences with age. From the results of factor analysis of the acoustic variables, the first, second, and third factors represent ‘frequency’, ‘duration and frequency range’, and ‘location of maximum frequency’, respectively. Ethology 112 (2006) 7–21 ª 2006 The Authors Journal compilation ª 2006 Blackwell Verlag

The frequency variables that were significant in the analyses of the cross-sectional study and the two longitudinal studies can be summarized as ‘frequency’. The frequency of coo calls in the Ohirayama group was thus consistently lower than in Yakushima individuals. In addition, this inter-group difference in frequency formed approximately 6–7 mo after birth. It is thought that there are five possible explanations for the mechanisms and functions of the intergroup differences in the frequency variables: body size, genetic drift, vocal plasticity, and social or habitat factors. We discuss these five different explanations below. Body Size

There is evidence that body size influences the acoustic features of vocalization (Inoue 1988; Fitch 1997; Hammerschmidt et al. 2000, 2001; Bee 2002; Fischer 2002; Reby & McComb 2003). There is a possibility that the individuals of the Ohirayama group utter lower frequency calls than the Yakushima group at the same age because they have larger body sizes caused by the effects of provisioning. We discuss this possibility from three viewpoints. First, although there are no data to directly compare body sizes between the Yakushima and the Ohirayama groups, the only available data suggest that the bone size of females is not so different between the two groups (Kuroda 1992). Second, Masataka (1994) reported that body weight does not correlate significantly with either minimum or maximum frequency values in coo calls in Japanese macaques at 16 mo after birth. Body weight in that study ranged from 2.4 to 2.8 kg, and the results suggest that, at least to this extent of difference in body weight, it does not affect the frequency values of coo calls. We judged from the appearances of the two groups at the same age, that their weights did not appear to differ as much as the body weight range in Masataka’s study. Third, the rate of body weight increase in Japanese macaques is generally constant from birth to the fourth year (Inoue 1988; Kurita et al. 2002). Additionally, there is no difference in the rate of body weight change around 6–7 mo of age, when group differences in vocalization emerged and when weaning begins (Kurita et al. 2002). The rate of the decrease in frequency of calls in each group, however, does not seem to be constant (Figs 3 and 4 and interaction terms in Tables 3 and 5). In the Ohirayama group, the values of the frequency variables rapidly declined from 4 to 5 mo to the second year, 17


and from then on the rate of decline became moderate. As for the Yakushima group, the rate of decline was relatively moderate between 4–5 and 9–11 mo, subsequently marked by a rapid decline until the second year, and then became moderate again from the third year or later. Thus, the rate of frequency decrease does not parallel that of body weight increase in each group. Consequently, the difference in body size alone might be insufficient to explain the observed inter-group differences in the frequency variables. To take this discussion further, it would be necessary to investigate in more detail the relationship between body weight and the development of vocalization in the two groups. Genetic Drift

The Yakushima and the Ohirayama groups are derived from the same initial population through translocation of the Ohirayama group 34 yr prior to this study (for further details see Methods in Section 1). Since the translocation, the size of the Ohirayama group has been maintained at approximately 90 individuals. Although no genetic data on the two groups are presented here, genetic drift is unlikely to be involved in producing the observed inter-group difference. Vocal Plasticity

There have been few studies suggesting that plasticity in early vocal development of non-human primates is contrary to that of birds or humans (for reviews of vocal development in primates; Snowdon & Elowson 1992; Seyfarth & Cheney 1997; Egnor & Hauser 2004). Some recent studies have reported negative results on plasticity in early vocal development in non-human primates (Hammerschmidt et al. 2000, 2001; Fischer 2002). However, our results indicate that the acoustic features of the two groups diverge from a very early age, which may suggest that the development of difference in call structure is rapid. Further examination of group difference, such as experimental translocation of additional monkeys, may contribute to clarifying the extent of vocal plasticity in non-human primates, although there are problems with this methodology, as noted in the introduction. Social Factor

Some group-living birds and mammals show vocal plasticity of calls in response to changes in social 18


environment (for example, black-capped chickadees, Nowicki et al. 1989; pygmy marmosets, Snowdon & Elowson 1999, and greater spear-nosed bats, Phyllostomus hastatus, Boughman 1998). Once the specific acoustic features take root in the groups, other individuals might affect infants in the acquisition of the specific acoustic features. However, from our data, this possibility cannot be confirmed or denied. Habitat Factor

One other possible explanation of the inter-group differences in coo calls of Japanese macaques is habitat matching (Janik & Slater 1997). Habitat matching resulting from learning has been reported in a few species of songbirds (the great tit, Parus major, Hunter & Krebs 1979; and the Rufous-Collared sparrow, Zonotrichia capensis, Nottebohm 1975; Handford 1981). A study of non-human primates has shown that some Old World monkeys have calls with acoustic features suited for transmission in their habitat (Brown et al. 1995). However, little is known about their vocal development. Six to seven months after birth, when group differences emerge, is also the beginning of the weaning period (Hasegawa 1983) and the time when the mother-infant distance increases drastically (Itoigawa 1973). Especially, coo calls are uttered frequently in moving, feeding, and poor visibility situations (Itani 1963; Okayasu 1987) and are exchanged frequently at distances between 3 and 30 m (Okayasu 1987). This means that coo calls are used at close or intermediate ranges. The habitat of the Yakushima group is evergreen forest, whereas the habitat of the Ohirayama group is dirt or gravelly ground with little vegetation. By measurement of the transmission of pure tones of various frequencies (range: 250– 8000 Hz) and of the recorded coo calls of Yakushima and Ohirayama groups in the two habitats, we found that lower frequency coo calls were more efficiently transmitted in the Ohirayama habitat. On the contrary, there was no effect of coo call frequency on transmission efficiency in the Yakushima habitat (H. Sugiura, T. Tanaka, N. Masataka, unpubl. data). It is therefore less likely that the present acoustic feature of coo calls in the Yakushima group is attributed to environmental influence. Moreover, the Ohirayama habitat has a louder ambient noise than the Yakushima habitat (H. Sugiura, T. Tanaka, N. Masataka, unpubl. data). These two habitats are very different, and thus it is quite possible that the observed intergroup difference in coo call could have been caused by habitat matching. When vocal contact is needed, Ethology 112 (2006) 7–21 ª 2006 The Authors Journal compilation ª 2006 Blackwell Verlag


the Ohirayama infants might modify the frequency features of their coo calls to match the acoustic environment of their habitat as a result of vocal plasticity. Acknowledgements We would like to thank Dr Tadasu Oyama for his advice and comments throughout this study; Dr Yasuyuki Muroyama for his comments on the early versions of this manuscript; Dr Sigetaka Kodera for permission to study in the Japan Monkey Center; Mr Kanji Sakurai, Mr Yasuaki Ishida, Mr Masaru Otake, Mr Masao Takai, Ms Miya Hamai and other members of staff of the Japan Monkey Center for their assistance with research; Dr Shozo Kojima and other members of the Primate Research Institute for their help during research at Ohirayama; the Forest Environment Conservation Center for permission to perform field research; the staff of the Field Research Center of PRI for affording us the full use of their facilities; and to many researchers and residents of Yakushima Island for their help during the field research. This study was supported by a grantin-aid for JSPS Research Fellowships for Young Scientists awarded to T. Tanaka and H. Sugiura, a Cooperative Research Fund of the Primate Research Institute, Kyoto University, awarded to T. Tanaka, a grant-in-aid from the Ministry of Education, Science and Culture, Japan entitled ‘Emergence of human cognition and language (05206104)’ awarded to N. Masataka and a Grant for Biodiversity Research of the 21st Century COE (A14) awarded to Kyoto University. Literature Cited Altmann, J. 1974: Observational study of behavior: sampling methods. Behaviour 49, 227—267. Baker, M. C. & Cunningham, M. A. 1985: The biology of bird-song dialects. Behav. Brain Sci. 8, 85—133. Bee, M. A. 2002: Territorial male bullfrogs (Rana catesbeiana) do not assess fighting ability based on size-related variation in acoustic signals. Behav. Ecol. 13, 109—124. Boughman, J. W. 1998: Vocal learning by greater spearnosed bats. Proc. R. Soc. Lond. B Biol. Sci. 265, 227—233. Brockelman, W. Y. & Schilling, D. 1984: Inheritance of stereotyped gibbon calls. Nature 312, 634—636. Brown, C. H., Gomez, R. & Waser, P. M. 1995: Old World monkey vocalizations: adaptation to the local habitat? Anim. Behav. 50, 945—961.



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