ORIGINAL PAPERS

Behavioral response of captive Guizhou snub-nosed monkeys to noise from different sources

  • Jiangming WU ,
  • Xiaolong HUANG ,
  • Shaochuan CHENG ,
  • Wei YANG ,
  • Xu ZHANG ,
  • Jingcheng RAN
Expand
  • 1.College of Life Sciences, Guizhou Normal University, Guiyang 550025, China
    2.Guizhou Academy of Forestry, Guiyang 550005, China
    3.Key Laboratory of National Forestry and Grassland Administration on Biodiversity Conservation in Karst Mountainous Areas of Southwestern China, Guizhou Academy of Forestry, Guiyang 550005, China
    4.Guizhou Fanjingshan National Nature Reserve Administration, Jiangkou 554400, China
    5.Guizhou Fanjingshan Forest Ecosystem Observation and Research Station, Jiangkou 554400, China
    6.Guizhou Caohai Wetland Ecosystem Observation and Research Station, Weining 553100, China

Received date: 2024-11-06

  Accepted date: 2025-04-09

  Online published: 2025-12-03

Abstract

Anthropogenic noise reshapes the soundscape of natural environments, causing adverse effects on the behavior, distribution, and vigilance of wildlife. The Guizhou snub-nosed monkey (Rhinopithecus brelichi) is one of the most endangered primates globally, inhabiting only the Fanjingshan National Nature Reserve in Guizhou. To investigate the behavioral responses of Guizhou snub-nosed monkeys to different noises, from December 2023 to June 2024, we studied Guizhou snub-nosed monkeys in captivity at the Guizhou Snub-nosed Monkey Research Center. Four types of noise, including traffic noise, tourist noise, rural noise, and avian predator call, were played back with a gradient of noise levels (40 dB, 50 dB, 60 dB, and 70 dB), and behavioral changes of Guizhou snub-nosed monkeys were recorded using focal animal sampling method. The results show that the four types of noise stimuli can cause an increase in vigilance time and a decrease in rest in Guizhou snub-nosed monkeys. The vigilance time tends to increase with the intensity of the noise level, and avoidance phenomenon appears when stimulated with a 60 dB noise level. The difference in vigilance time is significant (P < 0.05) among the different types of noise, and the percentage of the total vigilance time to the avian predator is significantly higher than that to the sound of human noise such as traffic noise, tourist noise and rural noise. Captive Guizhou snub-nosed monkeys have a habituation effect on human noise to which they had been exposed for a long time. This study initially reveals the behavioral response patterns of Guizhou snub-nosed monkeys under different noise interference conditions, which provides a basis for subsequent in-depth research on their behavior, the regulation of human activities, and the formulation of conservation and management measures.

Cite this article

Jiangming WU , Xiaolong HUANG , Shaochuan CHENG , Wei YANG , Xu ZHANG , Jingcheng RAN . Behavioral response of captive Guizhou snub-nosed monkeys to noise from different sources[J]. ACTA THERIOLOGICA SINICA, 2025 , 45(6) : 810 -819 . DOI: 10.16829/j.slxb.151024

References

Alecia J C, Harry H M, Robert H, Guy C. 2012. How not to measure boldness: novel object and antipredator responses are not the same in wild baboons [J]. Animal Behaviour, 84 (3): 603-609.
  Allan A T L, Bailey A L, Hill R A. 2020. Habituation is not neutral or equal: individual differences in tolerance suggest an overlooked personality trait [J]. Science Advances, 6 (28): eaaz0870. DOI: 10.1126/sciadv.aaz0870 .
  Audet J N, Ducatez S, Lefebvre L. 2015. The town bird and the country bird: problem solving and immunocompetence vary with urbanization [J]. Behavioral Ecology, 27 (2): 637-644.
  Bates D, M?chler M, Bolker B, Walker S. 2015. Fitting lnear mixed?effects models using lme4 [J]. Journal of Statistical Software, 67 (1): 1-48.
  Blackburn G, Ashton B J, Thornton A, Woodiss?Field S, Ridley A R. 2023. Cognition mediates response to anthropogenic noise in wild Western Australian magpies (Gmynorhina tibicen dorsalis) [J]. Global Change Biology, 29 (24): 6912-6930.
  Bunkley J P, Mcclure C J W, Kawahara Y, Francis C D, Barber J R. 2017. Anthropogenic noise changes arthropod abundances [J]. Ecology and Evolution, 7 (9): 2977-2985.
  Campos F A, Fedigan L M. 2014. Spatial ecology of perceived predation risk and vigilance behavior in white?faced capuchins [J]. Behavioral Ecology, 25 (3): 477-486.
  Chen H L, Koprowski J L. 2015. Animal occurrence and space use change in the landscape of anthropogenic noise [J]. Biological Conservation, 192: 315-322.
  Cronin K A, Bethell E J, Jacobson S L, Egelkamp C, Hopper L M, Ross S R. 2018. Evaluating mood changes in response to anthropogenic noise with a response?slowing task in three species of zoo?housed primates [J]. Animal Behavior and Cognition, 5 (2): 209-221.
  Daniel T B. 2016. Habituation and sensitization: new thoughts about old ideas [J]. Animal Behaviour, 120: 255-262.
  Dias P A D, Gómez E E E, Chavira R D R, Rangel N A. 2024. Noise intensity modulates the responses of mantled howler monkeys to anthropophony [J]. American Journal of Primatology, 86 (1): e23568.DOI: 10.1002/ajp.23568 .
  Duarte M H L, Vecci M A, Hirsch A, Young R J. 2011. Noisy human neighbours affect where urban monkeys live [J]. Biology Letters, 7 (6): 840-842.
  Duarte M H L, Kaizer M C, Young R J, Rodrigues M, Sousa?Lima R S. 2018. Mining noise affects loud call structures and emission patterns of wild black?fronted titi monkeys [J]. Primates, 59 (1): 89-97.
  Francis C D, Ortega C P, Cruz A. 2009. Noise pollution changes avian communities and species interactions [J]. Current Biology, 19 (16): 1415-1419.
  Francis C D, Kleist N J, Ortega C P, Cruz A. 2012. Noise pollution alters ecological services: enhanced pollination and disrupted seed dispersal [J]. Proceedings of the Royal Society B: Biological Sciences, 279: 2727-2735.
  Francis C D, Barber J R. 2013. A framework for understanding noiseimpacts on wildlife: an urgent conservation priority [J]. Frontiers in Ecology and the Environment, 11 (6): 305-313.
  Grenat P, Michelli M, Pollo F, Otero M, Baraquet M, Martino A. 2023. Traffic noise and breeding site characteristics influencing assemblage composition of anuran species associated to roads [J]. Biodiversity and Conservation, 32 (6): 1931-1947.
  Hawkins E, Papworth S. 2022. Little evidence to support the risk?disturbance hypothesis as an explanation for responses to anthropogenic noise by pygmy marmosets (Cebuella niveiventris) at a tourism site in the Peruvian Amazon [J]. International Journal of Primatology, 43 (6): 1110-1132.
  Huang X L, Meng B S, Li H B, Ran W, Yang W, Wang C, Xie B, Zhang X, Ran J C, Zhang M M. 2024. Interspecific associations between Rhinopithecus brelichi and its sympatric species using infrared cameras [J]. Biodiversity Science, 32 (2): 73-84.(in Chinese)
  Jakob?Hoff R, Kingan M, Fenemore C, Schmid G, Cockrem J F, Crackle A, Bemmel E V, Connor R, Descovich K. 2019. Potential impact of construction noise on selected zoo animals [J]. Animals, 9 (8): 504.DOI: 10.3390/ani9080504 .
  Kolleck J, Yang M, Zinner D, Roos C. 2013. Genetic diversity in endangered Guizhou snub?nosed monkeys (Rhinopithecus brelichi): contrasting results from microsatellite and mitochondrial DNA data [J]. PLoS ONE, 8 (8): e73647.DOI: 10.1371/journal.pone.0073647 .
  Lazerte S E, Otter K A, Slabbekoorn H. 2017. Mountain chickadees adjust songs, calls and chorus composition with increasing ambient and experimental anthropogenic noise [J]. Urban Ecosystems, 20 (5): 989-1000.
  Li J Y, Deng J, He X B, Tan K, Long X B, Li Y P, Huang Z P, Xiao W. 2021. The noise influence to black snub?nosed monkeys (Rinopithecus bieti) during the development of ecotourism activities [J].Chinese Journal of Zoology, 56 (6): 801-807.(in Chinese)
  Li X J. 2023. Study on the response of Rhinopithecus brelichi habitat changes [D]. Master thesis. Guiyang: Guizhou University.(in Chinese)
  L?schner J, Pomberger T, Hage S R. 2023. Marmoset monkeys use different avoidance strategies to cope with ambient noise during vocal behavior [J]. iScience, 26 (3): 106219.DOI: 10.1016/j.isci.2023.106219 .
  Mcclure C J W, Ware H E, Carlisle J, Kaltenecker G, Barber J R. 2013. An experimental investigation into the effects of traffic noise on distributions of birds: avoiding the phantom road [J]. Proceedings of the Royal Society B: Biological Sciences, 280 (1773): 20132290.DOI: 10.1098/rspb.2013.2290 .
  Niu K F, Tan C L, Yang Y Q. 2010. Altitudinal movements of Guizhou snub?nosed monkeys (Rhinopihecus brelichi) in Fanjingshan National Nature Reserve, China: implicationsfor conservation management of a fagship species [J]. Folia Primatologica, 81: 233-244.
  Niu K F, Tan C L, Cui D Y, Shi L, Yang M Y, Qiu Y, Zhang W Y, Yang Y Q. 2014. Utilization of food on snow?covered ground by Guizhou snub?nosed monkey (Rhinopithecus brelichi) during winter in Fanjingshan Nature Reserve,China [J]. Chinese Journal of Wildlife, 35 (1): 31-37. (in Chinese)
  Oliveira F G, Mathias M D L, Rychlik L, Tapisso J T, Merten S V. 2020. Metabolic and behavioral adaptations of greater white?toothed shrews to urban conditions [J]. Behavioral Ecology, 31 (6): 1334-1343.
  Palacios G, Lowenstine L J, Cranfield M R, Gilardi K, Spelman L, Lukasik?Braum M, Kinani J F, Mudakikwa A, Nyirakaragire E, Bussetti A V, Savji N, Hutchison S, Egholm M, Lipkin W. 2011. Human metapneumovirus infection in Wild Mountain Gorillas, Rwanda [J]. Emerging Infectious Diseases, 17 (4): 711-713.
  Phillips J N, Termondt S E, Francis C D. 2021. Long?term noise pollution affects seedling recruitment and community composition, with negative effects persisting after removal [J]. Proceedings of the Royal Society B: Biological Sciences, 288 (1948): 20202906.DOI: 10.1098/rspb.2020.2906 .
  Proppe D S, Sturdy C B, St Ckair C C. 2011. Flexibility in animal signals facilitates adaptation to rapidly changing environments [J]. PLoS ONE, 6 (9): e25413.DOI: 10.1371/journal.pone.0025413 .
  Rachel T B, Mckenna M F, Menitt D, Fristrup K, Crooks K, Angeloni L, Wittemyer G. 2017. Noise pollution is pervasive in U.S. protected areas [J]. Science, 356 (6337): 531-533.
  Robbins L, Margulis S W. 2014. The effects of auditory enrichment on gorillas [J]. Zoo Biology, 33 (3): 197-203.
  Santiago S C, Dias P A D, Garau S, Fuentes A C, Chavira Ramírez D R, Espinosa D C, Negrín A R. 2019. Behavioral and physiological stress responses to local spatial disturbance and human activities by howler monkeys at Los Tuxtlas, Mexico [J].Animal Conservation, 23 (3): 297-306.
  Shannon G, Angeloni L M, Wittemyer G, Fristrup K M, Crooks K R. 2014. Road traffic noise modifies behaviour of a keystone species [J]. Animal Behaviour, 94: 135-141.
  Shannon G, Mckenna M F, Angeloni L M, Crooks K R, Fristrup K M, Brown E, Warner K A, Nelson M D, White C, Briggs J, Mcfarland S, Wittemyer G. 2015. A synthesis of two decades of research documenting the effects of noise on wildlife [J]. Biological Reviews, 91 (4): 982-1005.
  Sheehan R L, Papworth S. 2019. Human speech reduces pygmy marmoset (Cebuella pygmaea) feeding and resting at a Peruvian tourist site, with louder volumes decreasing visibility [J]. American Journal of Primatology, 81 (4): e22967.DOI: 10.1002/ajp.22967 .
  Siemers B M, Schaub A. 2011. Hunting at the highway: traffic noise reduces foraging efficiency in acoustic predators [J]. Proceedings of the Royal Society B: Biological Sciences, 278 (1712): 1646-1652.
  Smith J A, Gaynor K M, Suraci J P. 2021. Mismatch between risk and response may amplify lethal and non?lethal effects of humans on wild animal populations [J]. Frontiers in Ecology and Evolution, 9: 604973.DOI: 10.3389/fevo.2021.604973 .
  Steinbrecher F, Dunn J C, Price E C, Buck L H, Wascher C A F, Ckark F E. 2023. The effect of anthropogenic noise on foraging and vigilance in zoo housed pied tamarins [J]. Applied Animal Behaviour Science, 265: 105989.DOI: 10.1016/j.applanim.2023.105989 .
  Uchida K, Suzuki K K, Shimamoto T, Yanagawa H, Koizumi I. 2019. Decreased vigilance or habituation to humans? Mechanisms on increased boldness in urban animals [J]. Behavioral Ecology, 30 (6): 1583-1590.
  Wang C, LiI H B, Yang Z H, Bi X, Fan H, Su H J, Hu C S, Zhang M M. 2022. Temporal and spatial distribution pattemns of Rhinopithecus brelichi and Macaca thibetana in the sameregion of the northeast Fanjingshan [J]. Scientia Silvae Sinicae, 58 (3): 117-128.(in Chinese)
  Wilson M C, Chen XY, Corlett R T, Didham K R, Ding P, Holt R D, Holyoakm, Hu G, Hughes A C, Jiang L, Laurance W F, Liu J J, Pimm S L, Robinson S K, Russo S E, Si X F, Wilcove D S, Wu J G, Yu M J. 2016. Habitat fragmentation and biodiversity conservation: key findings and future challenges [J]. Landscape Ecology, 31: 219-227.
  Xiang Z, Liang W B, Nie S G, Li M. 2012. Diet and feeding behavior of Rhinopithecus brelichi at Yangaoping, Guizhou [J]. American Journal of Primatology, 74 (6): 551-560.
  Yang Y Q, Lei X P, Yang C D. 2002. Fanjing Mountain Research: The Wild Ecology of Guizhou Golden Monkey [M]. Guiyang: Guizhou Science and Technology Publishing House.(in Chinese)
  Zeng X Q. 2018. Research on glucocorticoid and behavior adaptation strategies of Yunnan snub?nosed monkey under human behaviors [D]. Master thesis. Nanchong: China West Normal University.(in Chinese)
  王丞, 李海波, 杨朝辉, 毕兴, 樊涵, 粟海军, 胡灿实, 张明明.2022. 梵净山东北部同域黔金丝猴与藏酋猴的时空分布格局 [J]. 林业科学, 58 (3): 117-128.
  牛克锋, Tan C L, 崔多英, 石磊, Yang M, 邱阳, 张维勇, 杨业勤.2014. 黔金丝猴 (Rhinopithecus brelichi) 雪季地表食物利用 [J].野生动物学报, 35 (1): 31-37.
  李金燕, 邓静, 和晓斌, 谭坤, 龙晓斌, 李延鹏, 黄志旁, 肖文. 2021.生态旅游活动中游客噪声对滇金丝猴的影响 [J].动物学杂志, 56 (6): 801-807.
  李晓婕. 2023. 黔金丝猴生境变化的响应研究 [D].贵阳: 贵州大学硕士学位论文.
  杨业勤, 雷孝平, 杨传东.2002. 梵净山研究: 黔金丝猴的野外生态 [M]. 贵阳: 贵州科技出版社.
  黄小龙, 蒙秉顺, 李海波, 冉伟, 杨伟, 王丞, 谢波, 张旭, 冉景丞, 张明明. 2024. 基于红外相机的黔金丝猴及其同域分布物种种间关联 [J]. 生物多样性, 32 (2): 73-84.
  曾小琴. 2018. 人为干扰下滇金丝猴 (Rhinopithecus bieti) 皮质醇激素变化与行为适应策略研究 [D]. 南充: 西华师范大学硕士学位论文.
Outlines

/

〈 〉