The long-distance calling of white-headed langurs (Trachypithecus leucocephalus) serves a defensive function for their sleeping sites
Received date: 2025-01-03
Accepted date: 2025-03-17
Online published: 2025-12-03
Long-distance calling is a distinctive vocal signal known for its loudness and long-range transmission, typically emitted by male individuals. It is often inferred to serve important socio-ecological functions, such as territory defense, protection of valuable resources, and mate attraction. The white-headed langur (Trachypithecus leucocephalus) is an endemic primate species in China, inhabiting the karst limestone forests in the southwestern of Guangxi. The role of long-distance calling in the survival and reproduction of white-headed langurs remains unclear. Between February 2023 and August 2023, we collected data on the long-distance calling locations and times of adult males from eight white-headed langur groups, as well as information on their foraging and sleeping sites, in the Banli area of the Chongzuo White-headed Langur National Nature Reserve, Guangxi. We tested the defensive function of long-distance calls concerning two important resources: food and sleeping sites. The results indicated that adult male white-headed langurs initiate their first long-distance calls an average of 38 min after the group departs from the cave, at an average distance of 43 m from the sleeping site. They make their last long-distance calls an average of 39 min before the group returns to the cave, also at an average distance of 43 m from the sleeping site. Additionally, the location of the sleeping site significantly influenced the calling location of the white-headed langurs, supporting the hypothesis that these calls serve a sleeping site defense function. However, foraging locations had no significant impact on calling locations, which did not support the food resource defense hypothesis. These findings indicate that long-distance calling in white-headed langurs is used for defending sleeping sites but not food resources. This study is the first to clarify the role of long-distance calls in defending critical survival resources in white-headed langurs. It enhances our understanding of the adaptive mechanisms and functions of vocal communication in white-headed langurs and provides scientific evidence for the conservation of rare and endangered species.
Yuqian SONG , Bojun YI , Meijie TAO , Dengpan NONG , Qihai ZHOU , Penglai FAN . The long-distance calling of white-headed langurs (Trachypithecus leucocephalus) serves a defensive function for their sleeping sites[J]. ACTA THERIOLOGICA SINICA, 2025 , 45(6) : 820 -830 . DOI: 10.16829/j.slxb.151048
| Altmann J. 1974. Observational study of behavior: sampling methods [J]. Behaviour, 49 (3): 227-267. | |
| Benítez M E, Le Roux A, Fischer J, Beehner J C, Bergman T J. 2016. Acoustic and temporal variation in gelada (Theropithecus gelada) loud calls advertise male quality [J]. International Journal of Primatology, 37 (4-5): 568-585. | |
| Brooks M E, Kristensen K, Van Benthem K J, Magnusson A, Berg C W, Nielsen A, Skaug H J, M?chler M, Bolker B M. 2017. The R journal: glmmTMB balances speed and flexibility among packages for zero?inflated generalized linear mixed modeling [J]. The R Journal, 9 (2): 378-400. | |
| Cheyne S M, H?ing A, Rinear J, Sheeran L K. 2012. Sleeping site selection by agile gibbons: the influence of tree stability, fruit availability and predation risk [J]. Folia Primatologica, 83 (3-6): 299-311. | |
| Coudrat C N Z, Nanthavong C, Ngoprasert D, Suwanwaree P, Savini T. 2015. Singing patterns of white?cheeked gibbons (Nomascus sp.) in the Annamite mountains of Laos [J]. International Journal of Primatology, 36 (4): 691-706. | |
| Delgado R A. 2006. Sexual selection in the loud calls of male primates: signal content and function [J]. International Journal of Primatology, 27 (1): 5-25. | |
| 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 [J]. 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 [J]. Zoological Research, 43 (5): 875-879. | |
| Fan P L, Lawes M J, Liu R S, Zhou Q H. 2024. Hope for limestone langurs’ conservation [J]. Science, 384 (6698): 855. DOI: 10.1126/science.ado6810 . | |
| Fan P L, Liu R S, Grueter C C, Li F, Wu F, Huang T P, Yao H, Liu D Z, Liu X C. 2019. Individuality in coo calls of adult male golden snub?nosed monkeys (Rhinopithecus roxellana) living in a multilevel society [J]. Animal Cognition, 22 (1): 71-79. | |
| Fei H L, de Guinea M, Yang L, Chapman C A, Fan P F. 2022. Where to sleep next? Evidence for spatial memory associated with sleeping sites in skywalker gibbons (Hoolock tianxing) [J]. Animal Cognition, 25 (4): 891-903. | |
| Forstmeier W, Schielzeth H. 2011. Cryptic multiple hypotheses testing in linear models: overestimated effect sizes and the winner’s curse [J]. Behavioral Ecology and Sociobiology, 65 (1): 47-55. | |
| Guo Q Y. 2024. Sex, age, and seasonal differences of gut bacteria in wild white?headed langur (Trachypithecus leucocephalus) [D]. Master thesis. Guilin: Guangxi Normal University. (in Chinese) | |
| Gittins S P. 1982. Feeding and ranging in the agile gibbon [J]. Folia Primatologica, 38 (1-2): 39-71. | |
| Harrington F H, Mech L D. 1979. Wolf howling and its role in territory maintenance [J]. Behaviour, 68 (3/4): 207-249. | |
| Huang Y, Wei X, Wu Q, Huang C M. 2021. Influences of nutritional composition on food choice of white?headed langur (Trachypithecus leucocephalus) in dry season [J]. Jornal of Guangxi Normal University (Natural Science Edition), 39 (4): 109-115. (in Chinese) | |
| Ham S, Lappan S, Hedwig D, Choe J C. 2017. Female songs of the nonduetting javan gibbons (Hylobates moloch) function for territorial defense [J]. International Journal of Primatology, 38 (3): 533-552. | |
| Huang W H, Pan W S. 2010. Habitat characteristics of Presbytis leucocephalus in Guangxi Zhuang Autonomous Region [J]. Chinese Journal of Ecology, 29 (3): 605-610. (in Chinese) | |
| Harris T R. 2006. Within? and among?male variation in roaring by black and white colobus monkeys (Colobus guereza): What does it reveal about function? [J]. Behaviour, 143 (2): 197-218. | |
| Holzmann I, Córdoba R S. 2024. Individual vocal recognition and dear enemy effect in the black?and?gold howler monkey (Alouatta caraya) [J]. Behavioral Ecology and Sociobiology, 78 (4): 51. DOI: 10.1007/s00265-024-03469-0 . | |
| Huang C M, Wei F W, Li M, Li Y B, Sun R Y. 2003. Sleeping cave selection, activity pattern and time budget of white?headed langurs [J]. International Journal of Primatology, 24 (4): 813-824. | |
| Jacobsen L, Sunde P, Rahbek C, Dabelsteen T, Thorup K. 2013. Territorial calls in the little owl (Athene noctua): spatial dispersion and social interplay of mates and neighbours [J]. Ornis Fennica, 90: 41-49. | |
| Janson C H, Schaik C P V. 1988. Recognizing the many faces of primate food competition: methods [J]. Behaviour, 105 (1-2): 165-186. | |
| Jin T, Wang D Z, Zhao Q, Yin L, Qin D G, Ran W Z, Pan W S. 2009. Social organization of white?headed langurs (Trachypithecus leucocephalus) in the Nongguan karst hills, Guangxi, China [J]. American Journal of Primatology, 71: 206-213. | |
| Kitchen D M, Cheney D L, Engh A L, Fischer J, Moscovice L R, Seyfarth R M. 2013. Male baboon responses to experimental manipulations of loud ‘wahoo calls’: testing an honest signal of fighting ability [J]. Behavioral Ecology and Sociobiology, 67 (11): 1825-1835. | |
| Li D Y, Zhou Q H, Tang X P, Huang H L, Huang C M. 2011. Sleeping site use of the white?headed langur Trachypithecus leucocephalus: The role of predation risk, territorial defense, and proximity to feeding sites. Current Zoology, 57 (3): 260-268. | |
| Li D Y, Yuan P S, Krzton A, Huang C M, Zhou Q H. 2016. Dietary adaptation of white?headed langurs in a fragmented limestone habitat [J]. Mammalia, 80 (2): 153-162. | |
| Li Z Y, Rogers E. 2004. Social organization of white?headed langurs Trachypithecus leucocephalus in Fusui, China [J]. Folia Primatologica, 75 (2): 97-100. | |
| Li Z Y, Rogers M E. 2005. Are limestone hills a refuge or essential habitat for white?headed langurs in Fusui, China? [J]. International Journal of Primatology, 26 (2): 437-452. | |
| Li X D, Li S Y. 2005. A primary analysis to the plants eaten by white?headed leaf monkey Presbytis leucocephalus Tan [J]. Journal of Guangxi Agricultural and Biological Science, 24 (2): 153-160. (in Chinese) | |
| Liu G H, Liu S Y, Li Y B, Huang Z H. 2022. Predator avoidance and food patch proximity influence sleeping site use of Assamese macaques in a limestone forest of southwest Guangxi, China [J]. American Journal of Physical Anthropology, 178: 244-256. | |
| Lu S Y, Lu C H, Li Y B. 2016. Impact of food availability on seasonal diet composition of white?headed langur [J]. Chinese Journal of Ecology, 35 (3): 759-766. (in Chinese) | |
| Lu S Y, Chen T, Huang Z H, Li Y B, Lu C H. 2021. Interannual variation in food choice of white?headed langur inhabiting limestone forests in Fusui, southwest Guangxi, China [J]. Ecology and Evolution, 11 (14): 9349-9360. | |
| Lutermann H, Verburgt L, Rendigs A. 2010. Resting and nesting in a small mammal: sleeping sites as a limiting resource for female grey mouse lemurs [J]. Animal Behaviour, 79 (6): 1211-1219. | |
| Ma H G, Ma C Y, Fei H L, Yang L, Fan P F. 2020. Cao vit gibbons (Nomascus nasutus) sing at higher elevation but not in peripheral areas of their home range in a karst forest [J]. International Journal of Primatology, 41 (5): 701-713. | |
| Pan W S. 2016. The Natural History of White-Head Langur [M]. Beijing: Peking University Press. (in Chinese) | |
| Pan W S. 2021a. Population restoration and social structure of white?headed langurs in the Nongguan Mountains [A]. In: Pan W S ed. The Population Ecology of White-Headed Langur [M]. Beijing: Peking University Press, 121-143. | |
| Pan W S. 2021b. The white-headed langur’s habitat and natural refuge [A]. In: Pan W S ed. The Population Ecology of White-Headed Langur [M]. Beijing: Peking University Press, 53-71. | |
| Rasoloharijaona S, Randrianambinina B, Braune P, Zimmermann E. 2006. Loud calling, spacing, and cohesiveness in a nocturnal primate, the Milne Edwards’ sportive lemur (Lepilemur edwardsi) [J]. American Journal of Physical Anthropology, 129 (4): 591-600. | |
| Rasoloharijaona S, Randrianambinina B, Joly?Radko M. 2010. Does nonnutritive tree gouging in a rainforest?dwelling lemur convey resource ownership as does loud calling in a dry forest?dwelling lemur? [J]. American Journal of Primatology, 72 (12): 1062-1072. | |
| Reid D S, Wood C M, Whitmore S A, Berigan W J, Kramer H A, Kryshak N F, Keane J J, Sawyer S C, Gutiérrez R J, Klinck H, Peery M Z. 2022. Breeding status shapes territoriality and vocalization patterns in spotted owls [J]. Journal of Avian Biology, 2022 (8): e02952. DOI: 10.1111/jav.02952 . | |
| Tang H X, Huang H L, Wang Z X, Wu J B, Wang A L, Nong D P, Garber P A, Zhou Q H, Huang C M. 2023. Population dynamics and conservation status of the white?headed langur in the Chongzuo forest fragments, Guangxi, China [J]. Oryx, 58 (2): 179-182. | |
| Van Schaik C P, Assink P R, Salafsky N. 1992. Territorial behavior in Southeast Asian langurs: Resource defense or mate defense? [J]. American Journal of Primatology, 26 (4): 233-242. | |
| Van Belle S, Estrada A, Garber P A. 2014. The function of loud calls in black howler monkeys (Alouatta pigra): food, mate, or infant defense? [J]. American Journal of Primatology, 76 (12): 1196-1206. | |
| Wang W R, Yao M. 2017. Fine?scale genetic structure analyses reveal dispersal patterns in a critically endangered primate, Trachypithecus leucocephalus [J]. American Journal of Primatology, 79 (5): e22635. DOI: 10.1002/ajp.22635 . | |
| Yin L J, Liu W, Zhao Q, Qin D G, Li X D, Wang D Z, Jin T, Chen M, Pan W S. 2011. A video?aided study of the diet of wild white?headed langurs (Trachypithecus leucocephalus) [J]. Folia Primatologica, 82 (1): 33-44. | |
| Zhou Q H, Huang C M. 2021. Advances in ecological research on the limestone langurs in China [J]. Acta Theriologica Sinica, 41 (1): 59-70. (in Chinese) | |
| Zhou Q H, Huang Z H, Wei X S, Wei F W, Huang C M. 2009. Factors influencing interannual and intersite variability in the diet of Trachypithecus francoisi [J]. International Journal of Primatology, 30 (4): 583-599. | |
| Zhao Q, Tan C L, Pan W S. 2008. Weaning age, infant care, and behavioral development in Trachypithecus leucocephalus [J]. International Journal of Primatology, 29 (3): 583-591. | |
| Zhang K C, Yuan P S, Huang H L, Tang X P, Zhou Q H, Huang Z H. 2018. Inter?site variation in dietary composition of white?headed langurs (Trachypithecus leucocephalus) [J]. Jornal of Guangxi Normal University (Natural Science Edition), 35 (1): 75-81. (in Chinese) | |
| 张克处, 袁培松, 黄恒连, 唐小平, 周岐海, 黄中豪. 2018. 白头叶猴食物组成的地域性差异比较 [J]. 广西师范大学学报 (自然科学版), 35 (1): 75-81. | |
| 陆施毅, 鲁长虎, 李友邦. 2016.食物可获得性对白头叶猴 (Trachypithecus leucocephalus) 食物季节性组成的影响 [J]. 生态学杂志, 35 (3): 759-766. | |
| 周岐海, 黄乘明. 2021. 中国石山叶猴生态学研究进展 [J]. 兽类学报, 41 (1): 59-70. | |
| 郭秋艳. 2024. 野生白头叶猴肠道微生物的性别、年龄和季节性差异 [D]. 桂林: 广西师范大学硕士学位论文. | |
| 黄万辉, 潘文石. 2010. 广西白头叶猴栖息地特征 [J]. 生态学杂志, 29 (3): 605-610. | |
| 黄颖, 韦晓, 吴茜, 黄乘明. 2021. 白头叶猴旱季食物营养对食物选择的影响 [J]. 广西师范大学学报 (自然科学版), 39 (4): 109-115. | |
| 黎向东, 李士諹. 2005. 白头叶猴采食植物初析 [J]. 广西农业生物科学, 24 (2): 153-160. | |
| 潘文石. 2016. 白头叶猴自然史 [M]. 北京: 北京大学出版社. |
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