天行长臂猿鸣唱的声谱特征与性别差异

郭亭妍; 马海港; 韩普; 王子荻; 祝常悦; 楚原梦冉; 张利祥; 李如雪; 戚嘉儒; 李家华; 范朋飞

doi:10.16829/j.slxb.150870

兽类学报 >

2024 , Vol. 44 >Issue 1: 14 - 25

DOI: https://doi.org/10.16829/j.slxb.150870

研究论文

天行长臂猿鸣唱的声谱特征与性别差异

郭亭妍 ,
马海港 ,
韩普 ,
王子荻 ,
祝常悦 ,
楚原梦冉 ,
张利祥 ,
李如雪 ,
戚嘉儒 ,
李家华 ,
范朋飞

展开

1 中山大学生态学院, 深圳 518000;
2 中山大学生命科学学院, 广州 510275;
3 云南高黎贡山国家级自然保护区保山管护局, 保山 678000;
4 云南铜壁关省级自然保护区管护局, 德宏 678400;
5 大理白族自治州云山生物多样性保护与研究中心, 大理 671000;
6 云南高黎贡山国家级自然保护区保山管护局隆阳分局, 保山 678000

郭亭妍(2002-)，女，本科生，主要从事长臂猿声音通讯研究.

收稿日期: 2023-10-20

修回日期: 2023-12-11

网络出版日期: 2024-01-25

基金资助

科技部重点研发项目:濒危旗舰动物的濒危过程与机制(#2022YFF1301500)

收起

Spectral characteristics and sex differences in the song of Skywalker hoolock gibbon (Hoolock tianxing)

GUO Tingyan ,
MA Haigang ,
HAN Pu ,
WANG Zidi ,
ZHU Changyue ,
CHU Yuanmengran ,
ZHANG Lixiang ,
LI Ruxue ,
QI Jiaru ,
LI Jiahua ,
FAN Pengfei

Expand

1 School of Ecology, Sun Yat-sen University, Shenzhen 518000, China;
2 School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China;
3 Baoshan Management and Protection Bureau of Gaoligongshan National Nature Reserve, Baoshan 678000, China;
4 Management and Protection Bureau of Tongbiguan Provincial Nature Reserve, Dehong 678400, China;
5 Cloud Mountain Conservation, Dali 671000, China;
6 Longyang Branch of Baoshan Management and Protection Bureau of Gaoligongshan National Nature Reserve, Baoshan 678000, China

Received date: 2023-10-20

Revised date: 2023-12-11

Online published: 2024-01-25

Fold

摘要

白眉长臂猿属(Hoolock)物种声音长期被认为不具有性二型，但是识别其声音的性别差异有助于该属物种的种群动态监测与行为学研究。本研究以天行长臂猿(Hoolock tianxing)作为研究对象，标注了11个个体的鸣声数据。我们通过k-中心点聚类(k-medoids聚类)识别音节类型，基于音节组成和音句长度划分音句类型，并且识别了音节特征和音句使用上的性别差异。本研究识别出wa、oo、whoop、ow和eek 5种音节类型以及7种音句类型。雌性的wa和ow音节频率变化的幅度与速率比雄性更大；oo音节的各项频率指标比雄性更低；whoop音节频率变化的幅度与速率相比于雄性更小。在音句的使用上，独猿个体鸣叫的音句与合唱时各自性别贡献的部分更为相似，雄性极少唱主要由whoop音节与ow音节组成的音句G，雌性极少唱音句B (wa-whoop)和C (wa-oo-wawhoop)。本研究表明天行长臂猿的声音中存在性二型，该性别差异不仅有助于对天行长臂猿的监测，而且有助于理解不同声音类型及性别差异的功能。

关键词： 白眉长臂猿; 声谱分析; 声音通讯; 鸣唱; 性二型

本文引用格式

郭亭妍 , 马海港 , 韩普 , 王子荻 , 祝常悦 , 楚原梦冉 , 张利祥 , 李如雪 , 戚嘉儒 , 李家华 , 范朋飞 . 天行长臂猿鸣唱的声谱特征与性别差异[J]. 兽类学报, 2024 , 44(1) : 14 -25 . DOI: 10.16829/j.slxb.150870

Abstract

Species of the genus Hoolock were previously thought to lack sexual dimorphism. Identifying sexual dimorphism in vocalizations is helpful for their population dynamics monitoring and behavioral research. In this study, we annotate the song bouts of 11 Hoolock tianxing individuals. We employed k-medoids clustering to divide note types, and we classified phrase types based on the length and note composition of phrases. We also compared sexual dimorphism in notes and phrases. We identified 5 note types: wa, oo, whoop, ow and eek. The range and rate of frequency modulation of wa and ow notes of females were higher than those of males, the frequency features of oo notes were lower than those of males, the range and rate of frequency modulation of whoop notes were lower than those of males. For the phrases use, solitary apes were more similar to the parts contributed by their respective genders during a chorus. Males seldom sing phrase G mainly composed of the whoop note and the ow note, females seldom sing phrase B (wa-whoop) and phrase C (wa-oo-wa-whoop). Our study demonstrated sexual dimorphism in the vocalizations of Hoolock tianxing, which is not only helpful for the monitoring of Hoolock tianxing, but also important for understanding the function of different note types and sex differences.

Key words： Hoolock gibbon; Spectrogram analysis; Vocal communication; Loud call; Sexual dimorphism

参考文献

Aung T, Hill A K, Pfefferle D, McLester E, Fuller J, Lawrence J M, Garcia-Nisa I, Kendal R L, Petersdorf M, Higham J P, Galat G, Lameira A R, Apicella C L, Barelli C, Glenn M E, Ramos-Fernandez G, Puts D A. 2023. Group size and mating system predict sex differences in vocal fundamental frequency in anthropoid primates. Nature Communications, 14 (1):4069.
Bernstein S K, Sheeran L K, Wagner R S, Li J H, Koda H. 2016. The vocal repertoire of Tibetan macaques (Macaca thibetana):A quantitative classification. American Journal of Primatology, 78 (9):937-949.
Brock G, Pihur V, Datta S, Datta S. 2008. clValid:An R Package for Cluster Validation. Journal of Statistical Software, 25 (4):1-22.
Chan B P L, Mak C F, Yang J H, Huang X Y. 2017. Population, distribution, vocalization and conservation of Gaoligong hoolock gibbon (Hoolock tianxing) in the Tengchong section of the Gaoligongshan National Nature Reserve, China. Primate Conservation, (31):107-113.
Charlton B D, Zhihe Z, Snyder R J. 2009. The information content of giant panda, Ailuropoda melanoleuca, bleats:acoustic cues to sex, age and size. Animal Behaviour, 78 (4):893-898.
Choudhury A. 1991. Ecology of the hoolock gibbon (Hylobates hoolock), a lesser ape in the tropical forests of north-eastern India.Journal of Tropical Ecology, 7:147-153.
Clarke E, Reichard U H, Zuberbuhler K. 2006. The syntax and meaning of wild gibbon songs. PLoS ONE, 1 (1):e73
Clink D J. 2008. Well-Separated clusters and optimal fuzzy partitions. Journal of Cybernetics, 4 (1):95-104.
Dooley H M, Judge D S, Schmitt L H. 2012. Singing by male and female Kloss gibbons (Hylobates klossii) in the Peleonan Forest, Siberut Island, Indonesia. Primates, 54 (1):39-48.
Fan P F, He K, Chen X, Ortiz A, Zhang B, Zhao C, Li Y Q, Zhang H B, Kimock C, Wang W Z, Groves C, Turvey S T, Roos C, Helgen K M, Jiang X L. 2017. Description of a new species of hoolock gibbon (Primates:Hylobatidae) based on integrative taxonomy.American Journal of Primatology, 79 (5):e22631
Fan P F, Turvey S T, Bryant J V. 2020. Hoolock tianxing (amended version of 2019 assessment). The IUCN Red List of Threatened Species 2020:e. T118355648A166597159.
Fan P F, Xiao W, Huo S, Ai H S, Wang T C, Lin R T. 2011. Distribution and conservation status of the vulnerable eastern hoolock gibbon Hoolock leuconedys in China. Oryx, 45 (1):129-134.
Fan P F, Xiao W, Huo S, Jiang X L. 2009. Singing behavior and singing functions of black-crested gibbons (Nomascus concolor jingdongensis) at Mt. Wuliang, central Yunnan, China. American Journal of Primatology, 71 (7):539-547.
Fan P L, Li J X, Yang L T, Sun T, Wu S J, Grueter C C, Huang C M, Zhou Q H, Li M. 2022. Vocal repertoire of the critically endangered white-headed langur (Trachypithecus leucocephalus):Call types, acoustic structures, and related social-ecological contexts.Zoological Research, 43 (5):875-879.
Feng J J, Cui L W, Ma C Y, Fei H L, Fan P F. 2014. Individuality and stability in male songs of cao vit gibbons (Nomascus nasutus) with potential to monitor population dynamics. PLoS ONE, 9 (5):e96317.
Fuentes A. 2000. Hylobatid communities:changing views on pair bonding and social organization in Hominoids. Yearbook of Physical Anthropology, 43:33-60.
Geissmann T. 2000. Gibbon songs and human music from an evolutionary perspective. In:Wallin N L, Merker B, Brown S eds. Origins of Music. MIT Press, 103-123.
Geissmann T. 2002. Duet-splitting and the evolution of gibbon songs.Biological Reviews, 77 (1):57-76.
Gittins S P, Tilson R L. 1984. The Lesser Apes:Evolutionary and Behavioural Biology. Edinburgh:Edinburgh University Press.
Guan Z H, Ma C Y, Fei H L, Huang B, Ning W H, Ni Q Y, Jiang X L, Fan P F. 2018. Ecology and social system of northern gibbons living in cold seasonal forests. Zoological Research, 39 (4):255-265.
Haimoff E H. 1983a. Gibbon Songs:An Acoustical, Organizational, and Behavior Analysis. Cambridge:Cambridge University Press.
Haimoff E H. 1983b. Some observations on the singing behaviour of the hoolock gibbon. The Journal of the Bombay Natural History Society, 82:2-12.
Haimoff E H. 1985. The organization of song in Müller's gibbon (Hylobates muelleri). International Journal of Primatology, 6 (2):173-192.
Ham S, Hedwig D, Lappan S, Choe J C. 2016. Song functions in nonduetting gibbons:Evidence from playback experiments on Javan gibbons (Hylobates moloch). International Journal of Primatology, 37 (2):225-240.
Handl J, Knowles J, Kell D B. 2005. Computational cluster validation in post-genomic data analysis. Bioinformatics, 21 (15):3201-3212.
Hradec M, Illmann G, Prikrylová M, Bolechová P, Vostrá-Vydrová H. 2023. Difference in the songs of paired and unpaired southern yellow-cheeked gibbon males (Nomascus gabriellae):Social status or age? Frontiers in Ecology and Evolution, 11:956922.
Jiang X L, Wang Y X, Wang Q. 1999. Coexistence of monogamy and polygyny in black-crested gibbon (Hylobates concolor). Primates, 40 (4):607-611.
Kassambara A. 2011. Practical Guide to Cluster Analysis in R:Unsupervised Machine Learning (Multivariate Analysis) (Volume 1).CreateSpace Independent Publishing Platform.
King A J, Sueur C. 2011. Where next? Group coordination and collective decision making by primates. International Journal of Primatology, 32 (6):1245-1267.
Kinzey W G, Robinson J G. 1983. Intergroup loud calls, range size, and spacing in Callicebus torquatus. American Journal of Physical Anthropology, 60 (4):539-544.
Li Z X, Lin Z Y. 1983. Calssification and distribution of living primates in Yunnan China. Zoological Research, 4 (2):111-120. (in Chinese)
Liebal K, Waller B M, Burrows A M, Slocombe K E. 2014. Primate Communication:A Multimodel Approach. Cambridge:Cambridge University Press.
Lwin N, Ngoprasert D, Sukumal N, Browne S, Savini T. 2022. Status and distribution of hoolock gibbon in the newly established indawgyi biosphere reserve:Implication for protected area management. Global Ecology and Conservation, 38:e02209.
Ma H G, Ma C Y, Fan P. 2021. Adult male-female social bond advertising:The primary function of coordinated singing intensity in a small ape. American Journal of Primatology, 84 (1):e23351.
Ma S L, Wang Y X. 1988. The recent disribution, status and conservation of primates in China. Acta Theriologica Sinica, 8 (4):250-260. (in Chinese)
Marler P, Tenaza R. 1976. How Animals Communicate. Indiana:Indiana University Press Marshall J T J, Marshall E R. 1976. Gibbons and their territory songs. Science, 193:237.
Mathevon N, Koralek A, Weldele M, Glickman S E, Theunissen F E. 2010. What the hyena's laugh tells:Sex age dominance and signature in the giggling call of Crocuta crocuta. BMC Ecology, 10(1):1-16.
Moos-Heilen R, Sossinka R. 2010. The influence of oestrus on the vocalization of female gelada baboons (Theropithecus gelada).Ethology, 84 (1):35-46.
Niu X W, Guan Z H, Ning W H, Li X Y, Sun G Z, Ni Q Y, Liu G Q, Jiang X L. 2023. Experimental evidence for nasty neighbour effect in western black crested gibbons (Nomascus concolor). Behavioral Ecology and Sociobiology, 77 (3):33.
Reichard U H, Barelli C, Hirai H, Nowak M G. 2016. The Evolution of Gibbons and Siamang. Springer.
Rendall D, Rodman P S, Emond E R. 1996. Vocal recognition of individuals and kin in free-ranging rhesus monkeys. Animal Behaviour, (51):1007-1015.
Rousseeuw P J. 1987. Silhouettes a graphical aid to the interpretation and validation of cluster validation. Journal of Computational and Applied Mathematics, 20:53-65.
Schubert E, Rousseeuw P J. 2021. Fast and eager k-medoids clustering:O (k) runtime improvement of the PAM, CLARA, and CLARANS algorithms. Information Systems, 101:101804.
Sun Z Q, Tian F D. 1994. Medical Systematic Evaluation. China Science and Technology Press.
Taylor A M, Reby D. 2010. The contribution of source-filter theory to mammal vocal communication research. Journal of Zoology, 280(3):221-236.
Terleph T A, Malaivijitnond S, Reichard U H. 2016. Age related decline in female lar gibbon great call performance suggests that call features correlate with physical condition. BMC Evolutionary Biology, 16 (1):1-13.
Terleph T A, Malaivijitnond S, Reichard U. 2015. Lar gibbon (Hylobates lar) great call reveals individual caller identity. American Journal of Primatology, 77 (7):811-821.
Vu T T, Doherty P F. 2021. Using bioacoustics to monitor gibbons.Biodiversity and Conservation, 30 (4):1189-1198.
Wanelik K M, Azis A, Cheyne S M. 2013. Note-, phrase- and song-specific acoustic variables contributing to the individuality of male duet song in the Bornean southern gibbon (Hylobates albibarbis). Primates, 54 (2):159-170.
Yang J H, Huang X Y, Jin S H, Chan B P L. 2020. Filling a longstanding knowledge gap:Population size and conservation status of the endangered Gaoligong hoolock gibbon (Hoolock tianxing) in Houqiao Town, Yunnan. Global Ecology and Conservation, 24:e01347.
Yin L Y, Fei H L, Chen G S, Li J H, Cui L W, Fan P F. 2016. Effects of group density, hunting, and temperature on the singing patterns of eastern hoolock gibbons (Hoolock leuconedys) in Gaoligongshan, Southwest China. American Journal of Primatology, 78 (8):861-871.
Yuan S D, Fei H L, Zhu S H, Cui L W, Ai H S, Fan P F. 2013. Effects of tsaoko cultivating on tree diversity and canopy structure in the habitats of eastern hoolock gibbon. Zoological Research, 35 (3):231-239.
Zhang L, Guan Z H, Fei H L, Yan L, Turvey S T, Fan P F. 2020. Influence of traditional ecological knowledge on conservation of the skywalker hoolock gibbon (Hoolock tianxing) outside Nature Reserves. Biological Conservation, 241:108267.
李致祥, 林正玉. 1983. 云南灵长类的分类与分布. 动物学研究, 4(2):111-120.
马世来, 王应祥. 1986. 中国南部长臂猿的分类与分布:附三个新亚种的描记. 动物学研究, 7 (4):393-408.
马世来, 王应祥. 1988. 中国现代灵长类的分布、现状与保护. 兽类学报, 8 (4):250-260.

Options

文章导航

模态框（Modal）标题

摘要

本文引用格式

Abstract

参考文献