研究论文

布氏田鼠警戒鸣叫的生态适应不支持声音适应假说

  • 李强云 ,
  • 吴金海 ,
  • 斯日古楞null ,
  • 张建平 ,
  • 柳玉明 ,
  • 肖治术 ,
  • 苏军虎 ,
  • 刘伟
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  • 1.甘肃农业大学草业学院/草业生态系统教育部重点实验室/甘肃省草业工程实验室,中美草地畜牧业可持续发展研究中心,兰州 730070
    2.中国科学院动物研究所,动物多样性保护与有害动物防控重点实验室,北京 100101
    3.内蒙古呼伦贝尔市新巴尔虎右旗草原事业发展中心,新巴尔虎右旗 021399
    4.内蒙古锡林郭勒盟太仆寺旗现代农牧业综合服务中心,太仆寺旗 027000
    5.河北石油职业技术大学,承德 067000
    6.中国科学院大学,北京 100049
李强云 (1996- ),男,硕士研究生,主要从事啮齿动物行为生态学研究.

收稿日期: 2024-06-06

  录用日期: 2024-10-15

  网络出版日期: 2025-12-03

基金资助

国家自然科学基金重大项目(32090024);中国科学院动物研究所自主部署项目(2024IOZ0105);动物多样性保护与有害动物防控全国重点实验室自主部署项目(SKLA2507)

Ecological adaptations of alarm calls in Brandt’s voles did not support the acoustic adaptation hypothesis

  • Qiangyun LI ,
  • Jinhai WU ,
  • Siriguleng ,
  • Jianping ZHANG ,
  • Yuming LIU ,
  • Zhishu XIAO ,
  • Junhu SU ,
  • Wei LIU
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  • 1.College of Grassland Science, Key Laboratory of Grassland Ecosystem (Ministry of Education), Pratacultural Engineering Laboratory of Gansu Province, Sino-U. S. Centers for Grazingland Ecosystem Sustainability, Gansu Agricultural University, Lanzhou 730070, China
    2.Key Laboratory of Animal Biodiversity Conservation and Integrated Pest Management, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
    3.Grassland Development Center of Xinbalhu Right Banner, Hulunbuir City, Inner Mongolia, Xinbalhu Right Banner 021399, China
    4.Modern Agriculture and Animal Husbandry Comprehensive Service Center of Taipusi Banner, Xilinguole League, Inner Mongolia, Taipusi Banner 027000, China
    5.Hebei Petroleum University of Technology, Chengde 067000, China
    6.University of Chinese Academy of Sciences, Beijing 100049, China

Received date: 2024-06-06

  Accepted date: 2024-10-15

  Online published: 2025-12-03

摘要

警戒鸣叫是动物重要的生存策略之一,生境植被郁闭度、气候因子、噪声和鸣叫功能等可能对动物鸣叫适应性调整发挥作用,动物警戒鸣声如何适应栖息地结构的时序变化是一个有待探究的问题。其中声音适应性假说认为动物的鸣声信号应该朝有利于在其所处环境中高效传播的方向进化,然而并非所有研究支持其预测。布氏田鼠 (Lasiopodomys brandtii) 的警戒鸣叫是其重要的反捕食行为,为检测其警戒鸣叫的声学特征和功能适应性,本研究于2023年5月、7月和9月在内蒙古新巴尔虎右旗典型草原区,采集布氏田鼠的警戒鸣叫,并结合当地历年气候参数和实时环境噪声指标,分析其警戒鸣叫特征与生境间的关系。结果发现布氏田鼠警戒鸣叫具有单音节 (占比13.1%) 和多音节 (占比86.9%) 的声学特征,且多音节鸣叫的最小基频或最大基频与生境植被指数或环境相对湿度呈显著正相关,但与风速呈显著负相关,最大基频和基频范围与环境噪声呈显著正相关,但最小基频等其他频域参数以及音节间隔与之呈负相关。夏季 (7月) 相对高温多雨、低噪声的环境条件下,布氏田鼠警戒鸣声表现为音频相对集中的长脉冲、音节松散的高频音;而在相对干燥、风急嘈杂的春季 (5月) 和秋季 (9月),尤其是9月,鸣声调整为短脉冲、音节密集的宽带低频音,布氏田鼠警戒鸣声响应了相对湿度、风速和噪声等非植被郁闭度的季节性变化,但不支持声音适应性假说,这种差异也是其权衡反捕食风险和收益的结果,与其幼仔或家族亲缘个体扩散紧密关联。本研究为布氏田鼠适应集群和季节性繁殖生活相关的反捕食声讯对策提供了依据。

本文引用格式

李强云 , 吴金海 , 斯日古楞null , 张建平 , 柳玉明 , 肖治术 , 苏军虎 , 刘伟 . 布氏田鼠警戒鸣叫的生态适应不支持声音适应假说[J]. 兽类学报, 2025 , 45(6) : 797 -809 . DOI: 10.16829/j.slxb.150966

Abstract

Vocal alarm is one of the important survival strategies for animals, where habitat vegetation cover, climatic factors, noise, and call purpose may play a role in the adaptive tuning of animal calls. How the alarm calls of animals adapt to the temporal changes of habitat structure remains poorly explored. The acoustic adaptation hypothesis (AAH) suggests that animal calls should evolve in a direction that facilitates efficient transmission in their environment, but not all empirical reports support its predictions. The alarm calls of Brandt’s voles (Lasiopodomys brandtii) are an important anti-predator behavior. To detect the acoustic characteristics and functional adaptability of their alarm calls, in May, July, and September 2023, the alarm calls of Brandt's voles were collected in the typical steppe area of Xin Barag Right Banner, Inner Mongolia. These calls were then combined with the local historical climate parameters and real-time environmental noise indicators to analyze the relationship between the characteristics of their alarm calls and the habitat. The results showed that the alarm calls of Brandt’s voles exhibit both monosyllabic (13.1%) and multisyllabic acoustic (86.9%) characteristics. Furthermore, the minimum and maximum fundamental frequency were significantly positively correlated with habitat vegetation index and ambient relative humidity, respectively, but significantly negatively correlated with wind speed. The maximum fundamental frequency and fundamental frequency range were significantly positively correlated with ambient noise, while other frequency (i.e. the minimum fundamental frequency) and time (i.e. inter-note intervals of a call) domain parameter showed a negative correlation. Under the environmental conditions of relatively high temperature, abundant rainfall, and low noise in summer (July), the alarm calls of Brandt’s voles were characterized by long pulses with relatively concentrated audio frequencies and high-frequency sounds with loose syllables. In spring (May) and autumn (September), which were relatively dry, windy, and noisy, especially in September, the calls were adjusted to short pulses and broadband low-frequency sounds with dense syllables. The alarm calls of Brandt's voles responded to the seasonal changes in relative humidity, wind, and noise rather than vegetation canopy density, which did not support the acoustic adaptation hypothesis. This difference was also the result of their trade-off between anti-predator risks and benefits and was closely related to the dispersal of their offspring or family relatives. This study provides a basis for the anti-predator acoustic countermeasures related to the adaptation of Brandt’s voles to colonial and seasonal breeding life.

参考文献

Blumstein D T, Armitage K B. 1997. Alarm calling in yellow?bellied marmots: I. The meaning of situationally variable alarm calls [J]. Animal Behaviour, 53: 143-171.
  Blumstein D T. 2007. The evolution of alarm communication in rodents: Structure, function, and the puzzle of apparently altruistic calling [A]. In: Wolff J O, Sherman P W eds. Rodent Societies–An Ecological & Evolutionary Perspective [M]. The University of Chicago Press, 317-327.
  Boncoraglio G, Saino N. 2007. Habitat structure and the evolution of bird song: a meta?analysis of the evidence for the acoustic adaptation hypothesis [J]. Functional Ecology, 21 (1): 134-142.
  Braune P, Schmidt S, Zimmermann E. 2008. Acoustic divergence in the communication of cryptic species of nocturnal primates (Microcebus ssp.) [J]. BMC Biology, 6 (1): 1-10.
  Brown C H, Gomez R, Wasser P M. 1995. Old world monkey vocalizations: adaptation to the local habitat? [J]. Animal Behaviour, 50: 945-961.
  Brown T, Handford P. 1996. Acoustic signal amplitude patterns: a computer simulation investigation of the acoustic adaptation hypothesis [J]. Condor, 98: 608-623.
  Chu C J, Lutz J A, Kral K, Vrska T, Yin X, Myers J A, Abiem I, Alonso A, Bourg N, Burslem D F R P, Cao M, Chapman H, Condit R, Fang S Q, Fischer G A, Gao L M, Hao Z Q, Hau B C H, He Q, Hector A, Hubbell S P, Jiang M X, Jin G Z, Kenfack D, Lai J S, Li B H, Li X K, Li Y D, Lian J Y, Lin L X, Liu Y K, Liu Y, Luo Y H, Ma K P, McShea W, Memiaghe H, Mi X C, Ni M, O’Brien M J, de Oliveira A A, Orwig D A, Parker G G, Qiao X J, Ren H B, Reynolds G, Sang W G, Shen G C, Su Z Y, Sui X H, Sun I F, Tian S Y, Wang B, Wang X H, Wang X G, Wang Y S, Weiblen G D, Wen S J, Xi N X, Xiang W S, Xu H, Xu K, Ye W H, Zhang B W, Zhang J X, Zhang X T, Zhang Y M, Zhu K, Zimmerman J, Storch D, Baltzer J L, Anderson?Teixeira K J, Mittelbach G G, He F L. 2018. Direct and indirect effects of climate on richness drive the latitudinal diversity gradient in forest trees [J]. Ecology Letters, 22 (2): 245-255.
  Deng K, Wang X P, Zhu B C, Zhao L H, Yang Y, Cai Y L, Sun X Q, Wang T L, Cui J G. 2023. A dataset on the call characteristics of 43 anuran species [J]. Biodiversity Science, 31 (1): 179-182. (in Chinese)
  Di Z L, Wu Y N, Song Y T, Huo G W, Zhang F J, Wang X G, Zhang X H. 2017. Variation of temperature and precipitation in the Xin Barag Right Banner of the Hulunbeier Grassland during 1958-2016 [J]. Journal of Desert Research, 37 (5): 1006-1015.
  Eddington V M, Nichols H K, Calistri?Yeh A, Young V K H, Kloepper L N. 2024. Graded alarm call behavior in wild fox squirrels (Sciurus niger) [J]. Journal of the Acoustical Society of America, 155 (2): 1308-1314.
  Ey E, Fischer J. 2009. ‘TheAcoustic Adaptation Hypothesis’- a review of the evidence from birds, anurans and mammals [J]. Bioacoustics, 19 (1): 21-48.
  Fei H L. 2010. The research on singing behavior of eastern black crested gibbon (Nomascus nasutus) [D]. Master thesis. Changsha: Central South University of Forestry and Technology. (in Chinese)
  Fitch T W. 2006. Production of vocalizations in mammals [J]. Encyclopedia of Language & Lingus, 115-121.
  Fu H P, Bu S, Yuan S, Wang H L, Li X, NaShun M K, Wang Z H, Wei J, Hu S L. 2022. Advances in population ecology of Brandt’s vole (Lasiopodomys brandtii) in Typical Steppe [J]. Journal of Inner Mongolia Agricultural University (Natural Science Edition), 43 (5): 71-79. (in Chinese)
  García?Navas V, Blumstein D T. 2016. The effect of body size and habitat on the evolution of alarm vocalizations in rodents [J]. Biological Journal of the Linnean Society, 118: 745-751.
  Gillard G L, Rowley J J L. 2023. Assessment of the acoustic adaptation hypothesis in frogsusing large?scale citizen science data [J]. Journal of Zoology, 32 (2): 271-281.
  Guo T Y, Ma H J, Han P, Wang Z D, Zhu C Y, Chu Y M R, Zhang L X, Li R X, Qi J R, Li J H, Fan P F. 2024. Spectral characteristics and sex differences in the song of Skywalker hoolock gibbon (Hoolock tianxing) [J]. Acta Theriologica Sinica, 44 (1): 14-25. (in Chinese)
  Handford S C L. 1992. Vocal dialects and the structure of geographic variation in morphological and allozymic characters in the rufous?collared sparrow, Zonotrichia capensis [J]. Evolution, 46 (5): 1443-1456.
  Hansen P. 1979. Vocal learning: its role in adapting sound structures to long?distance propagation and a hypothesis on its evolution [J]. Animal Behaviour, 27: 1270-1271.
  Hollén L I, Radford A N. 2009. The development of alarm call behaviour in mammals and birds [J]. Animal Behaviour, 78 (4): 791-800.
  Holzmann I, Areta J I. 2020. Reduced geographic variation in roars in different habitats rejects the acoustic adaptation hypothesis in the black?and?gold howler monkey (Alouatta caraya) [J]. Ethology, 126 (1): 76-87.
  Hua X Z, Zhou R, Ye G H, Hua R, Bao D R H, Hua L M. 2020. The temporal distribution of the long call and its influencing factors in male plateau pika (Ochotona curzoniae) [J]. Acta Theriologica Sinica, 40 (6): 606-614. (in Chinese)
  Li M R, Deng Z K, Du J M. 2021.Study on the vegetation cover change in Xin Barag Right Banner [J]. Grassland and Prataculture, 33 (1): 29-34. (in Chinese)
  Loannou C C, Tosh C R, Neville L, Krause J. 2008. The confusion effect?from neural networks to reduced predation risk [J]. Behavioral Ecology, 19 (1): 126-130.
  Marten K, Marler P. 1977. Sound transmission and its significance for animal vocalization [J]. Behavioral Ecology and Sociobiology, 2 (3): 271-290.
  McRae T R, Green S M. 2017. Gray squirrel alarm call composition differs in response to simulated aerial versus terrestrial predator attacks [J]. Ethology Ecology & Evolution, 29: 54-63.
  McRae T R. 2020. A review of squirrel alarm?calling behavior: What we know and what we do not know about how predator attributes affect alarm calls [J]. Animal Behavior and Cognition, 7 (2): 168-191.
  Mikula P, Valcu M, Brumm H, Bulla M, Forstmeier W, Petruskova T, Kempenaers B, Albrecht T. 2021. A global analysis of song frequency in passerines provides no support for the acoustic adaptation hypothesis but suggests a role for sexual selection [J]. Wiley, 24 (3): 477-486.
  Morton E S. 1975. Ecological sources of selection on avian sounds [J]. American Naturalist, 109: 17-34.
  Pan X Q. 1992. Hulunbuir Grassland, China [M]. Changchun: Jilin Science and Technology Press. (in Chinese)
  Pang Y L, Luo B, Wang M, Wu X, Feng J. 2019. Sexual dimorphism in the frequency of echolocation calls facilitates sex recognition in least horseshoe bats [J]. Acta Theriologica Sinica, 39 (2): 155-161. (in Chinese)
  Pen N Y. 1987. Discussion on cluster sampling method [J]. The Theory and Practice of Finance and Economics, (1): 65-68. (in Chinese)
  Perla B S, Slobodchikoff C N. 2002. Habitat structure and alarm call dialects in Gunnison’s prairie dog (Cynomys gunnisoni) [J]. Behavioral Ecology, 13 (6): 844-850.
  Pollard K A, Blumstein D T. 2012. Evolving communicative complexity: insights from rodents and beyond [J]. Philosophical Transactions of the Royal Society B: Biological Sciences, 367 (1597): 1869-1878.
  Prestwich K N. 1994. The energetics of acoustic signaling in anurans and insects [J]. American Zoologist, 34 (6): 625-643.
  Reme? V, Harmá?ková L. 2018. Disentangling direct and indirect effects of water availability, vegetation, and topography on avian diversity [J]. Scientific Reports, 8. DOI: 10.1038/s41598-018-33671-w .
  Roca I T, Desrochers L, Giacomazzo M, Bertolo A, Bolduc P, Deschesnes R, Martin C A, Rainville V, Rheault G, Proulx R. 2016. Shifting song frequencies in response to anthropogenic noise: a meta?analysis on birds and anurans [J]. Behavioral Ecology, 27 (5): 1269-1274.
  Shelley E L, Blumstein D T. 2005. The evolution of vocal alarm communication in rodents [J]. Behavioral Ecology, 16 (1): 169-177.
  Slabbekoorn H. 2004. Singing in the wild: the ecology of birdsong [A]. In: MarlerP, edsSlabbekoorn H. Nature’s Music. The Science of Birdsong [M]. San Diego, Elsevier Academic Press, 178-205.
  Townsend S W, Maria R, Tim C B, Manser M B. 2012. Flexible alarm calling in meerkats: the role of the social environment and predation urgency [J]. Behavioral Ecology, 23 (6): 1360-1364.
  Volodin I A, Matrosova V A, Frey R, Kozhevnikova J D, Isaeva I L, Volodina E V. 2018. Altai pika (Ochotona alpina) alarm calls: individual acoustic variation and the phenomenon of call?synchronous ear folding behavior [J]. The Science of Nature, 105: 1-13.
  Volodin I A, Kirilyuk V E, Vasilieva N A, Volodina E V. 2025. Individual identity of alarm calls in wild?living Brandt’s voles (Lasiopodomys brandtii) [J]. The Science of Nature, 112 (1): 1-15.
  Volodin I A, Klenova A V, Kirilyuk V E, Ilchenko O G, Volodina E V. 2024a. Ultrasonic alarm call of Mongolian gerbils (Meriones ungiuculatus) in the wild and in captivity: a potential tool for detecting inhabited colonies during population depression [J]. Mammalian Biology, 104 (4): 407-416.
  Volodin I A, Rutovskaya M V, Golenishchev F N, Volodina E V. 2024b. Startle together, shout in chorus: collective bursts of alarm calls in a social rodent, the Harting’s vole (Microtus hartingi) [J]. Behaviour, 161 (8-9): 587-611.
  Wan X R, Liu W, Wang G H, Wang M J, Zhong W Q. 2006. Seasonal changes of the activity patternes of Brandt’s voles(Lasiopodomys brandtii) in the typical steppe in Inner Monglia [J]. Acta Agrestia Sinica, 26 (3): 226-234. (in Chinese)
  Wan X R, Zhong W Q. 1998. Ecology and management of Brandt’s voles [A]. In: ZhangZ B, WangZ W eds. Ecology and Management of Rodent Pests in Agriculture [M]. Beijing: Ocean Press. (in Chinese)
  Wang T T, Baima C R, Hai S Z, Wang D. 2015. Construction for the ethogram of Brandt’s voles (Lasiopodomys brandtii) [J]. Acta Agrestia Sinica, 23 (3): 646-652. (in Chinese)
  Wu X D. 1990. A study on the population ecology of Brandt’s voles [J]. Acta Theriologica Sinica, 10 (1): 54-59. (in Chinese)
  Xu R G. 2016. Fauna Inner Mongolia, Volume 5 Mammal (Rodentia, Lagomorpha) [M]. Hohhot: Inner Mongolia University Press, 171-181. (in Chinese)
  Zhang F, Chen P, Chen Z Q, Zhao J. 2015. Ultrasonic frogs call at a higher pitch in noisier ambiance [J]. Current Zoology, 61 (6): 996-1003.
  Zhao L H, Sun X Q, Chen Q H, Yang Y, Wang J C, Ran J H, Brauth S E, Tang Y Z, Cui J G. 2018. Males increase call frequency, not intensity, in response to noise, revealing no Lombard effect in the little torrent frog [J]. Ecology and Evolution, 8 (23): 11733-11741.
  Zhao Y C, Su Y J. 2005. Alarm calls of nonhuman primates [J]. Acta Theriologica Sinica, 25 (1): 81-85. (in Chinese)
  王涛涛, 白玛次仁, 海淑珍, 王登. 2015. 布氏田鼠行为谱的构建 [J]. 草地学报, 23 (3): 646-652.
  邓可, 汪小萍, 朱弼成, 赵龙辉, 杨悦, 蔡炎林, 孙晓倩, 王同亮, 崔建国. 2023. 中国43种蛙类鸣声特征数据集 [J]. 生物多样性, 31 (1): 179-182.
  邸择雷, 乌云娜, 宋彦涛, 霍光伟, 张凤杰, 王晓光, 张小红. 2017. 1958—2016 年呼伦贝尔草原新巴尔虎右旗气温和降水变化特征 [J]. 中国沙漠, 37 (5): 1006-1015.
  付和平, 卜凡, 袁帅, 王海龙, 李鑫, 那顺孟克, 王占海, 伟军, 胡斯勒. 2022. 典型草原布氏田鼠种群生态学研究进展 [J]. 内蒙古农业大学学报 (自然科学版), 43 (5): 71-79.
  华铣泽, 周睿, 叶国辉, 花蕊, 包达尔罕, 花立民. 2020. 雄性高原鼠兔长鸣时间分配及其影响因素 [J].兽类学报, 40 (6): 606-614.
  旭日干. 2016. 内蒙古动物志第5卷哺乳纲 (啮齿目、兔形目) [M]. 呼和浩特: 内蒙古大学出版社, 171-181.
  李梦茹, 邓泽坤, 杜佳梦. 2021. 新巴尔虎右旗植被覆盖变化研究 [J]. 草原与草业, 33 (1): 29-34.
  武晓东. 1990. 布氏田鼠种群生态研究 [J]. 兽类学报, 10 (1): 54-59.
  庞育兰, 罗波, 王漫, 吴秀, 冯江. 2019. 菲菊头蝠回声定位声波频率的性二态有利于性别识别 [J]. 兽类学报, 39 (2): 155-161.
  宛新荣, 刘伟, 王广和, 王梦军, 钟文勤. 2006. 典型草原区布氏田鼠的活动节律及其季节变化 [J]. 兽类学报, 26 (3): 226-234.
  宛新荣, 钟文勤. 1998. 布氏田鼠的生态学及控制对策 [A]. 见: 张知彬, 王祖望. 农业重要害鼠的生态学及控制对策 [M]. 北京: 海洋出版社.
  赵迎春, 苏彦捷. 2005. 非人灵长类动物的警报叫声 [J]. 兽类学报, 25 (1): 81-85.
  费汉榄. 2010. 东黑冠长臂猿Nomascus nasutus鸣叫行为研究 [D]. 长沙: 中南林业科技大学硕士学位论文.
  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. 2024. 天行长臂猿鸣唱的声谱特征与性别差异 [J]. 兽类学报, 44 (1): 14-25.
  彭念一. 1987. 整群抽样法浅谈 [J]. 财经理论与实践, (1): 65-68.
  潘学清. 1992. 中国呼伦贝尔草地 [M] . 长春: 吉林科学技术出版社.
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