Species Discrimination of Male Song in Gibbons JOHN C

American Journal of Primatology 13:413-423 (1987)

Species Discrimination of Male Song in Gibbons JOHN C. MITANI The Rockefeller Uniuersity Field Research Center, Tyrrel Road, Millbrook, New York 12545

Acoustic analyses and field playback experiments were conducted to inves- tigate interspecific song differences and discrimination in male gibbons. Songs were recorded and analyzed from males of three populations: agile gibbons (Hylobates agilis) in West Kalimantan and South Sumatra and Miiller’s gibbons (Hylobates muelleri) in East Kalimantan. Male songs from each of the three populations were played back to West Kalimantan agile gibbons. Acoustic analyses indicated that the songs of the two species differed in spectral features and in the temporal patterning of syllables. Agile gibbon songs from the West Kalimantan and South Sumatran populations varied in song durations and in the maximum frequencies of one song element. Field playbacks showed that West Kalimantan agile gibbons respond in a similar manner to local songs and to conspecific songs from South Sumatra. In contrast, the animals responded differentially to conspecific and heterospecific Muller’s gibbon songs. These results indicate that gibbons discriminate specific differences in songs, and support the division of agile and Muller’s gibbons into distinct species.

Key words: songs, gibbon taxonomy INTRODUCTION Distinctive loud vocalizations, used to mediate spacing between conspecifics, are characteristic elements of the vocal repertoires of many nonhuman primates [Mitani & Marler, in press]. To serve a spacing function, loud vocalizations must retain species-specific features while transmitted over long distances. Acoustic analyses routinely reveal variation in loud calls both within and between species [eg, Struh- saker, 1970; Hodun et al, 1981; Waser, 1982; Oates & Trocco, 1983; Macedonia & Taylor, 1985; Snowdon et al, 19861, but few field studies have investigated whether animals recognize this variability. Do primates discriminate between the vocalizations of conspecifics and those of closely related heterospecifics? Gibbons (Hylobatidae) are ideal animals in which to examine species differences in vocal behavior. These territorial monogamous apes are distributed widely throughout the remaining rain forests of Southeast Asia. Adult males and mated pairs defend their territories through the use of songs [Mitani, 1985a,b;Raemaekers & Raemaekers, 19851, which vary markedly between species [Marshall & Marshall,

Received March 30,1987; revision accepted June 24, 1987. Address reprint requests to Dr. John C. Mitani, The Rockefeller University Field Research Center, BOX 38B, RR2, Tyrrel Road, Millbrook, NY 12545.

0 1987 Alan R. Liss, Inc. 414 I Mitani 19761. Playbacks of tape-recorded vocalizations have been employed successfully to elicit responses from gibbons under natural social and environmental settings [Mi- tani 1984, 1985a,b,c; 1987; Raemaekers & Raemaekers, 19851, thus providing an objective method to assess an animal’s ability to discriminate between the songs of different species. Research on song variation is of particular interest given its critical role in discussions of gibbon systematics. Controversy exists regarding the number of species composing the Hylobatidae [reviews in Preuschoft et al, 1984; Marshall & Sugardjito, 19861. While comparative anatomists recognize as few as five species of gibbons [eg, Creel & Preuschoft, 19841, ethologists maintain the existence of nine species, largely on the basis of population differences in female singing behavior [eg, Marler & Tenaza, 1977; Haimoff et al, 1984; Marshall & Sugardjito, 19861. Resolu- tion of this debate has been precluded, in part, by two factors. First, despite agree- ment over the use of vocal signals to determine taxonomic relationships among gibbons [Creel et al, 19841, there is a paucity of data regarding male gibbon singing behavior. Second, scant attention has been paid to the critical issue regarding the biological significance of population differences in gibbon singing behavior; this problem requires data on the singing patterns of different populations, the responses of gibbons to songs from different populations, and the function of singing behavior. In this paper, male song variation and discrimination are examined among gibbons from three Indonesian populations: Miiller’s gibbons (Hylobates muelleri) in East Kalimantan, and agile gibbons (Hylobates agilis) in South Sumatra and West Kalimantan. First, the acoustic basis of species differences in song is investigated through an analysis of male songs selected from the three populations. Second, a series of experimental field playbacks is used to test whether gibbons discriminate species differences in song. Results of this study confirm the role song plays in species identification in gibbons and clarify current problems in gibbon taxonomy. METHODS Observations of Singing Behavior Male singing behavior was studied at three locations in Indonesia from 1980 to 1986. Observations of male Muller’s gibbon singing behavior were conducted in East Kalimantan during September 1980-October 1982 and March-May 1984 at the Kutai Game Reserve. Observations of male agile gibbon singing were made in Lampung, South Sumatra, during June 1984 at the Waykambas National Park and in West Kalimantan during July-October 1985 and July-October 1986 at the Gun- ung Palung Nature Reserve. Male singing performances were recorded at Kutai and Waykambas with a Uher 4400 Report Stereo IC tape recorder; recordings at Gunung Palung were made with Sony TCD-5M and TCD-5PRO cassette decks. A Sennheiser ME 20 omnidirectional microphone attached to a 13-cm parabolic reflector was used to make all recordings analyzed here. The frequency response of these recording systems was flat over the range of interest (& 3 dB from 150-2500 Hi,cf. Fig. 1). Analysis of Singing Behavior Tape recordings of male singing performances were made opportunistically. From the available set of clear recordings, a singing performance was selected randomly from four males in each population. A sample of 12 consecutive songs was then drawn from each of these individuals for acoustic analysis. Male gibbon singing performances can last up to 2 hours and typically begin with a series of short songs consisting of a few simple syllable types. As performances continue, the songs become increasingly longer and complex in syllable type number and morphology. Songs were sampled from the end of performances, after males had been singing for Species Song Discrimination in Gibbons I 415 30 minutes. Interspecific variation in syllable morphology complicates the compari- son of song syllables among populations. One syllable type, a simple frequency upsweep, is found in the songs of all three populations, however. To compare song syllables among populations, frequency upsweeps were sampled and analyzed 12 samples consisting of 12 syllables were drawn by selecting one syllable from the 12 songs of each male. Songs were digitized at a sampling rate of 5 kHz and 128 point Fourier trans- forms were performed using a DEC PDP 11/23 microcomputer and a digital signal processing program developed by Dr. Christopher Clark and Kim Beeman at The Rockefeller University Field Research Center [Clark et al, in press]. The resulting frequency domain representations of songs spanned 0-2,000 Hz with a frequency resolution of 39 Hz at sampled intervals of 26 ms. Four variables-song duration, the number of syllables in each song, the maximum frequency of the song, and the minimum frequency of the song-were measured from each song. The durations, maximum frequencies, and minimum frequencies of frequency upsweep song syllables were also measured. The songs of male agile and Muller’s gibbons vary markedly in their temporal patterning to the human ear. The temporal patterning of song syllables within songs were examined by dividing each song into two halves and counting the number of syllables that were delivered per second in each half of the song. Variation in songs and song syllables within and among populations was evalu- ated by performing nested analyses of variance on the values of each measured variable. If significant variation existed among populations, the T method was used to examine whether means differed between populations. Descriptions of these statistical tests can be found in Sokal and Rohlf [1981]. Playback Site and Subjects Playback experiments were conducted during July-October 1986 at the Cabang Panti Research Station in the Gunung Palung Nature Reserve, West Kalimantan, Indonesia. The 15-km2study area comprises a mixture of lowland dipterocarp, peat swamp, and hill dipterocarp forests. Nine groups of agile gibbons found in lowland forest served as test subjects. These groups, ranging from three to seven individuals, consisted of mated pairs and their offspring. Playback Procedure The nine test groups were exposed once to three playback treatments: male agile gibbon songs from West Kalimantan and South Sumatra, and male Muller’s gibbon songs from East Kalimantan. Playback types were assigned numeric codes, and their order of presentation to the test subjects was determined with the use of a random numbers table. Playback experiments followed a design established in an earlier study [Mitani, 19871. In each experiment, the test group was located prior to playback and was followed for at least 10 minutes. Following this period, a field assistant played back a 10-minute segment of a male singing performance using a Sony TC-D5M or TC-D5PRO cassette tape recorder and a Nagra DH amplifier- speaker. Songs used in playback presentations were selected from the end of performances, following 30 minutes of male singing. All playbacks were administered approximately 125 m away from the gibbons. Test tapes were edited, and back- ground noise was attenuated with a Krohn-Hite 3700 bandpass filter. Territorial intrusions were simulated by presenting all songs to the subjects from positions within their territories. Male songs from the Cabang Panti site used in playback experiments were recorded from mated individuals living in areas beyond the audible range of the territories of the test subjects. Since gibbon groups possess 416 I Mitani stable territories that do not change over periods lasting several years [Chivers & Raemakers, 19801, it is unlikely that the test subjects were familiar with any of the songs used in playbacks. A minimum set of standard conditions had to be met before experiments were initiated. Songs were presented on dry mornings between 0630 and 1000 hours and at least 15 minutes after any singing by the test group. Songs were played back while the test group was either feeding or resting, and thus stationary. The gibbons were not permitted to identify the source of the playback. If any member of the test group began to approach within visual range of the playback apparatus during the 10-minuteplayback period, my field assistant was alerted, and he hid both himself and the recording equipment. To prevent habituation to the playbacks, test subjects were not exposed to playbacks more than once every 2 days. Response Variables and Statistical Analysis During the 10-minute playback period and for 10 minutes afterwards, the following responses were recorded from adult males and females: 1) approaches toward the speaker, 2) alarm calls, 3) male songs, 4) female songs, and 5) song duets. Cochran’s Q test was employed to evaluate heterogeneity in response among the three playback treatments [Sokal & Rohlf, 19811. Based on the results of the acoustic analyses, it was hypothesized that the gibbons would respond differentially to population variations in songs, and one-tailed McNemar’s tests for significance of changes were used to assess response differences between playbacks [Sokal & Rohlf, 19811. RESULTS Acoustic Analysis of Songs Figure 1 shows representative spectrograms of songs from the three populations of gibbons. The sampled male Muller’s gibbon songs consisted of a few introductory syllables containing little or no frequency modulation followed by a trill of simple frequency upsweeps. Male agile gibbon songs comprise a greater variety of syllable types and also differ from Muller’s gibbon songs by lacking a trill component. Table I shows means and standard deviations of each of the measured song variables. Significant interindividual variation within populations existed in all of the measures. Similarly, all of the variables, with the exception of the duration of frequency upsweep song syllables, showed significant heterogeneity among populations. Table I1 shows a distinctive features matrix of the population differences. Interspecific differences were evident in several measures. First, the maximum and minimum frequencies of songs differed between species. Agile gibbon songs from West Kalimantan and South Sumatra covered a greater frequency range than those of East Kalimantan Muller’s gibbons. Second, the minimum frequencies of frequency upsweep song syllables were significantly lower in agile gibbon songs than those in Muller’s gibbon songs. Finally, the temporal pattern of delivery of song syllables varied interspecifically. Agile gibbon songs comprised more syllables at their beginnings than at their endings, while Muller’s gibbon songs showed the opposite pattern. Population variations in agile gibbon songs were apparent in other temporal and spectral measures (Tables I and ID. Songs from West Kalimantan agile gibbons were shorter and thus comprised fewer syllables than those of their South Sumatran conspecifics. In addition, the maximum frequencies of frequency upsweep syllables were significantly higher in West Kalimantan songs than in South Sumatran songs. In summary, results of these analyses show that the songs of male Muller’s and agile gibbons differ substantially, but that the songs of agile gibbons from different Species Song Discrimination in Gibbons I 417 West Kalirnontan, tj. oqilis

2- kHz A, - 1- /J 9 1

South Sumatra, H. aailis

123456 sec.

Eost Kolimantan, H_. muelleri

123456 sec. Fig. 1. Sound spectrograms of male gibbon songs from three populations. populations are qualitatively similar. The songs of species can be differentiated on the basis of spectral parameters and the temporal patterning of syllables. Agile gibbon songs span a broader frequency range than Miiller’s gibbon songs, and the presence of a trill component in Miiller’s gibbon songs gives them a distinctively different temporal patterning than agile gibbon songs. Intraspecific population differences in agile gibbon songs exist in measures of song duration and in the maximum frequencies of frequency upsweep syllables. 418 I Mitani

TABLE I. Means f Standard Deviations of Song Variables Measured From Three Populations of Gibbons* PoDulation East Kalimantan West Kalimatan South Sumatra (H. ugilis) Variable (H. ugilis) (H. agilis) (H. rnuelleri) Song Duration (s) 3.69 f 0.87a 5.54 f 1.12b 4.62 f 0.89 Number of 8.22 & 1.84a 12.94 f 2.60b 10.39 f 2.30" syllables Syllables/ s. 1st 2.44 f 0.46' 2.45 f 0.29" 1.83 f 0.45b half Syllables/ s. 2nd 1.93 f 0.71a 2.33 f 0.54" 3.19 & 0.77b half Maximum 1474 & 87a 1418 f 71" 1300 f 3gb frequency (Hz) Minimum 547 & 38" 519 30a 679 f 43b frequency Wz) Song syllable Duration (ms) 154 f 38 146 f 18 147 f 48 Maximum 1042 f 81a 915 & 106b 1179 f 87' frequency (Hz) Minimum 508 f 42' 503 f 43' 645 f 6gb frequency (Hz) *All song variables showed significant interindividual variability within populations at P < 0.05. Superscripts indicate population means that differed significantly at P < 0.05. n = 12 songs and song syllables from four males in each population. See text for further explanation.

TABLE 11. Male Song Variables That Showed Significant Differences Between Populations Population West Kalimatan South Sumatra East Kalimantan Variable (H. ugilis) (H. ugilis) (H. muelleri) Song Duration Short Long Intermediate Number of syllables Few Several Few Syllables is. 1st half Several Several Few Syllables/ s. 2nd half Few Few Several Maximum frequency High High Low Minimum frequency Low Low High Song syllable Maximum frequency Intermediate Low High Minimum frequency Low Low High

Responses to Playbacks Table I11 presents the responses of agile gibbons to male songs from local individuals in West Kalimantan, conspecifics in South Sumatra, and Muller's gibbons in East Kalimantan. The tendency for males to approach showed significant heterogeneity among the three playback treatments. Male agile gibbons approached conspecific songs from West Kalimantan and South Sumatra on all trials but only Species Song Discrimination in Gibbons I 419 TABLE 111. Approach and Vocal Responses of Agile Gibbons in West Kalimantan to Male Gibbon Songs From Different Populations* PoDulation West Kalimantan South Sumatra East Kalimantan Response (H. agilis) (H. ugilis) (H. muelleri) Male approach** 9 9 5*** Female approach 2 2 1 Female alarm call** 3*** 2**** 7 Male alarm call 6 3 3 Male song 1 0 0 Female song 1 1 0 Duet** 1 O**** 5 * ”he table shows the number of playbacks that elicited a response; n = 9 playbacks per treatment. See text for further explanation. ** P < 0.05, Cochran test for heterogeneity of response among the three playback treatments. *** P < 0.06, one-tailed McNemar test for changes in response between West Kalimantan and East Kalimantan song playbacks. **** P < 0.03, one-tailed McNemar test for changes in response between South Sumatran and East Kalimantan song playbacks.

approached on approximately one-half of all playbacks of Muller’s gibbon songs from East Kalimantan (P < 0.06 for both comparisons). Female gibbons approached male songs rarely (Table III). Vocal responses also differed among the three playback treatments (Table 111). Females and pairs did not vocalize with equal frequency in response to West Kali- mantan, South Sumatran, and East Kalimantan songs. Pairwise comparisons re- vealed that Muller’s gibbon songs elicited more alarm calls from females than agile gibbons songs from West Kalimantan 8 < 0.06) and South Sumatra (P < 0.03). In addition, Muller’s gibbon playbacks elicited more song duets than Sumatran agile gibbon playbacks (P < 0.06); mated females initiated all song duets. Other vocal responses-male alarm calls, male songs, and female songs-did not show significant heterogeneity among the three playback treatments (P > 0.10). DISCUSSION Song Discrimination Acoustic analyses reveal species differences in the vocal behavior of a variety of animals, including amphibians [Littlejohn, 19771, birds [Becker, 19821, cetaceans [Steiner, 19811, and primates [Struhsaker, 1970; Waser, 1982; Snowdon et al, 19861. By responding differentially to vocalizations, animals exhibit abilities to discriminate between conspecific and heterospecific vocalizations [eg, Becker, 1982; Masa- taka, 1986; Payne, 19861. Although it is generally assumed that primates discriminate interspecific vocal differences, experimental field demonstrations are generally lacking for monkeys and apes. Elsewhere it has been shown that male gibbon song functions in the defense of space between conspecific groups [Mitani, 1985133. Given a territorial spacing function, natural selection has presumably favored the evolution of species differences in male songs to facilitate their rapid and unambiguous recognition by conspecifics [cf Marler, 19571. The acoustic analyses presented above indicate that male songs from West Kalimantan agile gibbons bear a close resemblance to the songs of agile gibbons from South Sumatra but differ from those of Muller’s gibbons in East Kalimantan. The results of playback experiments indicate that gibbons discriminate 420 I Mitani these specific differences in vocal behavior and suggest that song discrimination plays a role in species identification under natural circumstances. West Kalimantan agile gibbons respond in a similar fashion to local songs and to conspecific songs from South Sumatra; responses to agile gibbon songs differ from those given to the acoustically distinct Muller’s songs from East Kalimantan. Although the gibbons discriminate between the songs of different species, little is known regarding the precise acoustic cues that they employ in species recognition. Differences in the frequency range of songs, song syllable morphology, and the temporal patterning of songs identify these acoustic features as potential parameters used by gibbons in species recognition, but testing these possibilities will require additional field experiments in which each feature is varied systematically [eg, Emlen, 19721. The songs of agile gibbons also showed intraspecific population differences, but the results of playback experiments suggest that this variability is not biologically significant; the gibbons did not respond differentially to conspecific songs from two populations. Intraspecific variation in songs was found in measures of song duration, but additional playback experiments have shown that agile gibbons do not discriminate between short and long songs witani, unpublished data). Nevertheless, the populations differed in one measured spectral feature (Table ID, and males gave more alarm responses to local conspecific song than to those of South Sumatran agile gibbons (Table III). The possibility remains that a more sensitive response assay, coupled with a larger playback sample, may reveal that the gibbons perceive population differences in songs. Gibbon Taxonomy Primate biologists universally agree on the validity of five species of gibbons: the siamang, hoolock, concolor, K~OSS’S,and lar gibbons. There is considerable debate, however, regarding the number of species forming the lar group [reviews in Preuschoft et al, 1984; Marshall & Sugardjito, 19861. This group ranges from Thai- land in the north to the island of Java in the south and comprises five taxa: lar, pileated, moloch, agile, and Muller’s gibbons. Biochemical [Cronin et al, 19841 and morphological [Creel & Preuschoft, 1984; Groves, 19841 data show limited variability among these five taxa, leading some researchers to recognize only one species. In contrast, field biologists, noting variation in singing patterns, maintain that each taxon represents a separate species [Haimoff et al, 1984; Marshall & Sugardjito, 19861. The population of gibbons inhabiting West Kalimantan between the Kapuas and Barito rivers on the island of Borneo is central to this debate. Marshall and Marshall [1976], citing song evidence, were the first to contend that agile gibbons occupy this area. Others dispute this claim, given apparent morphological affinities of the West Kalimantan population of gibbons with other members of the lar species group [Creel & Preuschoft, 1984; Groves, 19841. The results of this study are consistent with the Marshalls’ observation and support the validity of classifying the lar gibbon group into five species. Playback experiments indicate that agile gibbons in West Kalimantan respond differentially to conspecific and Muller’s gibbon songs. Approach responses suggest that male agile gibbons do not recognize male Muller’s gibbons as territorial competitors. Similarly, vocal responses indicate that female agile gibbons discriminate conspecific from heterospecific males. These data are in accord with the results of an earlier study of the responses of lar gibbons to heterospecific songs. Playbacks of pileated gibbon female songs to lar gibbons elicited different responses than did the songs of female conspecifics [Raemaekers & Rae- maekers, 19851. Species Song Discrimination in Gibbons I 421 When considered in light of what is known regarding the function of gibbon singing behavior, these results suggest that neighboring gibbons with different singing patterns would not compete for territories and would not interbreed. The responses of female agile gibbons to heterospecific male song are consistent with this hypothesis. Alarm call and duetting responses indicate that heterospecific males, mimicked through song playback, disturb females and suggest that females might avoid such males if they came together in secondary contact. Behavioral differences frequently play important roles as premating species- isolating mechanisms under natural environmental and social settings [Mayr, 19631. Differences in acoustic behavior, in particular, have been shown to prevent inter- breeding between groups of morphologically indistinguishable insects and birds [eg, Henry, 1985; Payne, 19861. Agile and Miiller’s gibbons are allopatric throughout their geographic ranges except at the headwaters of the Barito river in Central Kalimantan, where there is limited hybridization [Brockelman & Gittins, 1984; Marshall & Sugardjito, 19861. Additional research at this area of sympatry is necessary to test critically whether song recognition hinders significant hybridization between these species. CONCLUSIONS 1. Acoustic analyses reveal that male songs of agile and Muller’s gibbons differ in spectral features and in the temporal patterning of song syllables. 2. The songs of male agile gibbons from different populations are qualitatively similar but vary quantitatively in song durations and in the maximum frequencies of one song syllable. 3. Responses to experimental playbacks show that agile gibbons respond similarly to local songs and to songs of conspecifics from another population; responses to conspecific songs differ from those to heterospecific Muller’s gibbon songs. 4. The results of acoustic analyses and playback experiments indicate that gibbons discriminate specific differences in male song and support the validity of classifying agile and Muller’s gibbons as distinct species. ACKNOWLEDGMENTS Field work was sponsored by the Indonesian Institute of Sciences, the Indone- sian Association of Zoological Parks, the Indonesian National Biological Institute, and the Indonesian Directorate General of Forest Protection and Nature Conserva- tion. Research was supported by grants from the NSF BNS-8022764, the L.S.B. Leakey Foundation, the Wenner-Gren Foundation, the National Academy of Sci- ences, the National Geographic Society, the NIH RR00169 and RR00166, and by fellowships from the Regents of the University of California and the U.S.P.H.S. NRSA 1 F32 NS07670. I am especially grateful to Sdr. Bastar, Yum, Supriadi, Tarmiji, and Saparudin for field assistance and to Chuck Darsono, Peter Rodman, Widodo Ramono, and Mark Leighton for logistic aid in the field. 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