NORTH-WESTERN JOURNAL OF ZOOLOGY 13 (2): 347-351 ©NwjZ, Oradea, Romania, 2017 Article No.: e161705 http://biozoojournals.ro/nwjz/index.html

Sound spectrum characteristics of Eastern Black Crested Gibbons

Huaiqing DENG#, Huamei WEN# and Jiang ZHOU*

School of Life Sciences, Guizhou Normal University, Guiyang, Guizhou, 550001, China, E-mail: [email protected] # These authors contributed to the work equally and regarded as Co-first authors. * Corresponding author, J. Zhou, E-mail: [email protected], Tel.:13985463226

Received: 01. November 2016 / Accepted: 07. September 2016 / Available online: 19. September 2016 / Printed: December 2017

Abstract. Studies about the sound spectrum characteristics and the intergroup differences in eastern black crested gibbon (Nomascus nasutus) song are still rare. Here, we studied the singing behavior of eastern black crested gibbon based on song samples of three groups of gibbons collected from Trung Khanh, northern Vietnam. The results show that: 1) Song frequency of both adult male and adult female eastern black crested gibbon is low and both are below 2 KHz; 2) Songs of adult male eastern black gibbons are composed mainly of short syllables (aa notes) and frequency modulated syllables (FM notes), while adult female gibbons only produce a stable and stereotyped pattern of great calls; 3) There is significant differences among the three groups in highest and lowest frequency of FM syllable in males’ song; 4) The song chorus is dominated by adult males, while females add a great call; 5) The sound spectrum frequency is lower and complex, which is different from Hainan gibbon. The low frequency in the singing of the eastern black crested gibbon is related to the structure and low quality of the vegetation of its habitat.

Key words: Nomascus nasutus; song; sound spectrum analysis

Gibbons (Hylobatidae) are arboreal, territorial report about the sound frequency of eastern black small ape that are restricted to eastern Asia and crested gibbons is wrong. China's Yunnan Province, Guangxi Province and Gibbon song is considered as defining their Hainan Province (Haimoff et al. 1986). Singing is a taxonomic classification and explaining their evo- very typical feature of gibbons. Adult individuals lution (Geissmann 1993, Konrad & Geissmann are able to produce loud, continuous, complex and 2006) by being the song of each gibbon species stably structured songs (Geissmann 2002). Except remarkably similar in its organizational structure. for Kloss gibbon (Hylobates klossii) (Tenaza 1976) However, sound spectrum characteristics of east- and Moloch (H. moloch) (Dallmann et al. 2001), ern black crested gibbons remains poorly re- adult gibbon pairs participate in choruses and searched. Therefore, to find out song differences display sex differences in vocalizations (Geiss- between species of the Nomascus genus and their mann 2002). Studies on gibbon singing behavior, evolutionary and biological significance, we com- song characteristics, function and the influence pared sound spectrum characteristics of the factors of the genera Hylobates, Hoolock, Nomascus, Hainan gibbons (Deng et al. 2014) to new song re- and Symphalangus, are helpful for better classifica- cordings of wild eastern black crested gibbons col- tion of gibbons (Fan et al. 2013, Rawson 2010, lected from a population residing in Trung Khanh Cheyne 2007). district. Historically, eastern black crested gibbons (Nomascus nasutus) are distributed in the east of Study areas and animals. Our research was performed at the Red River of South China and northern Viet- Trung Khanh of northern Vietnam, which is a typical sub- tropical karst limestone stone cluster landform. It is 500- nam. Since the 1950s, they are believed to have 800 m above the sea level with a subtropical monsoon died out from China (Tan 1985), and since 1960s forest climate. The annual temperature averages 19.9 ℃ there is no news about their precise distribution in and annual rainfall reaches 1583 mm (Schilling 1984). The Vietnam (Geissmann et al. 2003). It was not until sampling site is located in Thieng lieng of Trung Khanh 2002 that investigators rediscovered this species in (22°52'27''N, 106°19'21''E). Three groups of eastern black a karst forest in Trung Khanh of northern Viet- crested gibbons were available for recording and identi- nam, a county bordering China (La et al. 2002). Up fied as G1, G2 and G3 group. G1 group included 4 gibbon individuals: one adult male, two adult females and one to now there were only two research papers pub- infant; G2 group included five gibbons: one adult male, lished on the song behavior of eastern black two adult females and two infants; G3 group includes six crested gibbons (Fei et al. 2010, Feng et al. 2013). gibbons: one adult male, two females, one juvenile, and As Feng et al. (2013) looked the echo frequency as two infants. The songs of individuals in the three groups the singing frequencies of the spectrograms, their have been all sampled. The study period was conducted 348 H. Deng et al. between September and November 2005. (Table 1). This is followed by FM syllable that con- Data collection. We followed gibbons every day after sists of 2-4 long syllable (Fig. 1), with the fre- sunrise and recorded their singing activity with a Sam- quency changes from highest 1.69 kHz to the low- sung YV–150 recorder. Factors being noted down in- est 1.00 kHz. cluded the starting time and ending time of their chirp; orientation and geographical coordinates (GPS); call types The frequency of each syllable between differ- (such as female excited singing, male solos, chorus, etc.). ent groups of male solo is different. The lowest We followed the gibbons all day and recorded time, song frequency of all short syllables shows significant type and location of each next chirps. To eliminate the in- differences among the three groups (F = 1.61, df = fluence of day length on gibbons, the starting time as rela- 45, P < 0.05), and the highest frequency of FM syl- tive to the dawn is calculated by deducting dawn length lables and their duration time also show signifi- from the time of start (Rawson 2010). cant differences (F = 12.66, df = 45, P < 0.05; F = Sound spectrum analysis. We included into the analysis all complete sound recordings from the three 0.05, df = 45, P < 0.05). groups. Audio files were first converted to wav format Chorus. The male usually initiates, ends and and later analyzed the sound spectrum using Batsound takes the lead of the chorus. In a full chorus, the (version 4.14) Analysis parameters are as follows: sam- male gibbon begins with a song consisting of some pling frequency 12 kHz, fast Fourier transforms (FFT) simple repetitive short syllables and FM syllables. value of 1024 for processing, hamming analysis window. As the number of repetitive short syllable in- All song analysis and description of terms are according creases, the female produce great calls to match to Geissmann’s (2002) standards. Data analysis. All data were normally distributed, the male in the climax (Fig. 2). There is around single factor variance and LSD multiple comparison tests 18.25s of interval after the climax, after which the were used to test the difference in song parameters be- male will end the duet by FM syllables. The great tween groups. We set the significance level to α = 0.05 calls of the female and conducted all analyses in SPSS 18.0. gibbon are stable and stereotyped. It starts with short, single syllable and then turns into loud call During the study period, we collected 30 songs which consists of 1-3 short syllables (introductory from three social groups of eastern black crested notes) and multiple repetitive rapidly rising vibra- gibbons. Nine male songs and four chorus out of tion of tremolo (wa notes), which lasts about 9.3s 30 samples, which were without background noise (Fig. 2). The highest frequency of female song is and recorded within 30 meters of distance, were 1.43±0.10 kHz, and the lowest is 0.83±0.03 kHz analyzed for sound spectrum characteristics. (Table 2). Male song. Male song is composed of two syl- When the females produce excited call, the lables: simple repetitive short syllables (aa notes) number of simple repetitive syllable by males in- and frequency modulated syllables (FM notes). creases; FM syllables in chorus are obviously of Simple repetition of short syllables consists of 6-14 greater number than in solos, with starting fre- short and similar syllables with little fluctuation in quency and highest frequency both on increase, frequency. Among the simple repetition of short but frequency decreases in ending syllables pro- syllables, the first to five short syllables have duced by males. In a full chorus the frequency higher frequency than the latter short syllables variation is: adult male FM syllables starts at 1.11

Table 1. Sound spectrum of eastern black crested gibbons G1-3.

Mean±SE The lowest The highest Number of Syllable duration(s) frequency(KHz) frequency(KHz) recordings(n) The first short 0.18±0.15 1.05±0.03 1.28±0.12 9 The second short 1.18±0.02 1.06±0.03 1.23±0.05 9 The third short 0.21±0.02 1.05±0.15 1.21±0.01 9 The fourth short 0.24±0.05 1.06±0.02 1.23±0.04 9 The fifth short 0.25±0.04 1.07±0.01 1.23±0.01 9 The sixth short 0.38±0.01 1.07±0.04 1.25±0.01 9 The seventh short 0.35±0.03 1.11±0.03 1.26±0.03 7 The first long 1.42±0.16 1.04±0.01 1.42±0.07 9 The second long 0.66±0.10 1.02±0.01 1.53±0.06 9 The third long 0.37±0.05 1.01±0.02 1.51±0.09 6

(Due to the large home range of G3 group, it is difficult to monitor their group singing, so only one com- plete male solo of this group is tested) Song behavior and Spectrum Characteristics of Nomascus nasutus 349

Figure 1. Song spectra of the male eastern black crested gibbons in group G2. (Note: aa notes: short syllables; FM notes: frequency- modulated notes)

Figure 2. Song spectra of chorus of eastern black crested gibbons in group G1 and G2.

Table 2. Sound spectrum characteristics of female eastern low compared to Hainan gibbons and other gib- black crested gibbons. bon species (Table 3). Our result is different with

Mean±SE Lowest Highest Feng et al. (2013) research for they looked the echo

Duration frequency frequency frequency as the singing frequencies of the spec- Group (s) (KHz) (KHz) trograms, so they think as eastern black crested G1 8.55±0.08 0.84±0.03 1.36±0.10 gibbon song highest frequency over 5 KHz. This G2 9.26±0.05 0.83±0.03 1.43±0.10 study shows eastern black crested gibbons have Note: Due to the large home range of G3 group, no chorus is re- developed a low song frequency which may corded for this group. spread more easily and farther across long dis- tance with low vegetation, which is consistent ± 0.13 kHz with a duration of 0.76±0.13s, then ris- with Waser (1977) and Haimoff (1984) research ing to 1.57 ± 0.05 kHz which lasts for 1.08 ± 0.22s; conclusions. Eastern black crested gibbons inhabit FM syllable in middle of chorus starts at 1.33± 0.05 in the tropical monsoon forest among karsts stone kHz, then rising to 2.09±0.09 kHz with a duration mountains, where trees (arbor) averages 9 m with of 0.36± 0.09 s; FM syllables in chorus ends at a 4m high of trunks, 17.4 cm of cross-section tree frequency of 1.23± 0.04 kHz, and then rose to 1.59 trunk diameter and 5 m of crown breadth (Zhang ± 0.07 kHz, with a duration of 0.96± 0.23s (Fig. 2). 2010), and the terrain and vegetation environment In eastern black crested gibbon chorus, adult is relatively simple. This study shows eastern female highest syllable frequency is 1.81 kHz, each black crested gibbons have developed a low song syllable average lasts for 0.25±0.02s, and males’ frequency through evolution which spreads more highest frequency is 2.09 kHz, which is significant easily and farther across long distance with low higher than solo 1.69 kHz. vegetation, which is consistent with Haimoff (1984) and Whitten (1982) research conclusions. Gibbons have species-specific songs with fre- Our research results suggest male eastern quency varying from 0.2 to 5 kHz (Geissmann black crested gibbon song consists of simple re- 1993). In this research, we found song frequencies petitive short and FM syllables, while females only of both sexes of eastern black crested gibbon are produce great calls, which is an obvious difference

350 H. Deng et al.

Table 3. Comparison to male and female singing the highest frequency in Nomascus.

Male Female Species Highest frequency Highest frequency Highest frequency Source of short syllables (KHz) of FM syllables (KHz) of great call (KHz) N. nasutus 1.22 1.51 1.43 This study N. concolor 1.23 5.82 5.83 Fan et al., 2010 N. hainanus 1.43 2.40 1.88 Deng et al., 2014 N. leucogenys 1.42 4.10 4.6 Geissmann, 2002 N. gabriellae 1.50 2.42 3.7 Rawson, 2010

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