翼手目动物交流声波研究进展

张春棉; 郑子琪; 孙淙南; 冯江; 江廷磊

doi:10.16829/j.slxb.150970

兽类学报 >

2025 , Vol. 45 >Issue 2: 165 - 174

DOI: https://doi.org/10.16829/j.slxb.150970

综述

翼手目动物交流声波研究进展

张春棉 ,
郑子琪 ,
孙淙南 ,
冯江 ,
江廷磊

展开

1 河北师范大学, 河北省动物生理生化与分子生物学重点实验室, 石家庄 050024;
2 东北师范大学, 吉林省动物资源保护与利用重点实验室, 长春 130117;
3 吉林农业大学生命科学学院, 长春 130118

张春棉(1991-)，女，博士，助理研究员，主要从事动物行为与进化生态学研究.

收稿日期: 2024-06-19

修回日期: 2024-10-15

网络出版日期: 2025-04-01

基金资助

国家自然科学基金 (32300392, 32371562, 32400377)；河北省自然科学基金 (C2023205010, C2023205017)；河北师范大学博士科研启动基金 (L2022B16, S22B048)

收起

Research progress on communication calls in Chiroptera

ZHANG Chunmian ,
ZHENG Ziqi ,
SUN Congnan ,
FENG Jiang ,
JIANG Tinglei

Expand

1 Hebei Key Laboratory of Animal Physiology, Biochemistry and Molecular Biology, Hebei Normal University, Shijiazhuang 050024, China;
2 Jilin Provincial Key Laboratory of Animal Resource Conservation and Utilization, Northeast Normal University, Changchun 130117, China;
3 College of Life Science, Jilin Agricultural University, Changchun 130118, China

Received date: 2024-06-19

Revised date: 2024-10-15

Online published: 2025-04-01

Fold

摘要

声通讯是动物维持社群稳定的关键表型，一直是动物行为学研究领域的热点。蝙蝠是生态系统中的关键类群，主要依赖声信号在环境中活动，一直是声学研究的模式生物。本文聚焦蝙蝠交流声波，综述当前研究现状，提出未来发展方向。总的来说，蝙蝠交流声波具有多样的声谱结构，能够编码个体身份、身体大小或社会等级等多种信息，还具有防御与警报、求偶与交配及联系等多种功能。蝙蝠能通过调节叫声结构、强度和复杂性来响应噪音的干扰。蝙蝠交流叫声存在地理变化，且具有句法结构、发声节奏和复杂性。同时，蝙蝠具有发声学习以及声波发育可变能力。相比回声定位声波，交流声波研究较为缺乏，建议今后开展蝙蝠交流声波多层面进化研究，创新声波分析方法，发展高性能机载录音仪，建立全球蝙蝠声学数据库，加强多学科交叉以及开展长期系统性观测，以促进蝙蝠交流声波领域发展。

关键词： 蝙蝠; 交流声波; 功能; 语言学; 发声学习

本文引用格式

张春棉 , 郑子琪 , 孙淙南 , 冯江 , 江廷磊 . 翼手目动物交流声波研究进展[J]. 兽类学报, 2025 , 45(2) : 165 -174 . DOI: 10.16829/j.slxb.150970

Abstract

Acoustic communication is a crucial phenotype for animals to maintain social stability, and it has always been a hotspot in the field of animal behavior research. Bats, as key group in ecosystems, primarily rely on acoustic signals to move around in environments and have long been model organisms for acoustic research. Here, we provide a comprehensive overview of communication calls in bats and propose future development directions. In general, bat communication calls exhibit diverse spectral structures, encode various information about individual identity, body size, or social status, and serve functions including defense and alarm, courtship and mating, and social bonding. Bats can adjust the structure, intensity, and complexity of their calls in response to noise interference. Bat communication calls exist geographic variation and possess syntactic structure, vocal rhythm, and complexity. Additionally, bats exhibit vocal learning and variability in sound development. Compared to echolocation calls, research on bat communication calls is relatively lacking. We recommend that future studies should focus on the multi-level evolutionary aspects of bat communication calls, innovate sound analysis methods, develop high-performance on-board sound recording devices, establish a global bat acoustic database, strengthen interdisciplinary collaborations, and conduct long-term systematic observations to advance the field of bat communication calls research.

Key words： Bats; Communication call; Function; Linguistics; Vocal learning

参考文献

Altmann G. 1980. Prolegomena to Menzerath's law. Glottometrika, 2:1-10.
Amit Y, Yovel Y. 2023. Bat vocal sequences enhance contextual infor mation independently of syllable order. iScience, 26 (4). DOI:10. 1016/j. isci. 2023. 106466.
Arnold B D, Wilkinson G S. 2011. Individual specific contact calls of pallid bats (Antrozous pallidus) attract conspecifics at roosting sites. Behavioral Ecology and Sociobiology, 65:1581-1593.
Behr O, Knörnschild M, von Helversen O T. 2009. Territorial counter-singing in male sac-winged bats (Saccopteryx bilineata):low-cfrequency songs trigger a stronger response. Behavioral Ecology and Sociobiology, 63:433-442.
Behr O, von Helversen O. 2004. Bat serenades-complex courtship songs of the sac-winged bat (Saccopteryx bilineata). Behavioral Ecology and Sociobiology, 56:106-115.
Bentz C, Ferrer-i-Cancho R. 2016. Zipf's law of abbreviation as a lan guage universal. In:Bentz C, Jager G, Yanovich I eds. Proceed ings of the Leiden Workshop on Capturing Phylogenetic Algorithms for Linguistics. The Tübingen:University of Tübingen, 1-4.
Bohn K M, Schmidt-French B, Schwartz C, Smotherman M, Pollak G D. 2009. Versatility and stereotypy of free-tailed bat songs.PLoS ONE, 4 (8). DOI:10. 1371/journal. pone. 0006746.
Boughman J W. 1997. Greater spear-nosed bats give groupdistinctive calls. Behavioral Ecology and Sociobiology, 40:61-70.
Boughman J W. 1998. Vocal learning by greater spear-nosed bats.Proceedings of the Royal Society of London B:Biological Sci ences, 265 (1392):227-233.
Bradbury J W, Vehrencamp L. 2011. Principles of Animal Communi cation. Sunderland:Sinauer Associates.
Brown P E, Brown T W, Grinnell A D. 1983. Echolocation, develop ment, and vocal communication in the lesser bulldog bat, Noctilio albiventris. Behavioral Ecology and Sociobiology, 13:287-298.
Brualla N L M, Wilson L A B, Doube M, Carter R T, McElligott A G, Koyabu D. 2023. The vocal apparatus:an understudied tool to re construct the evolutionary history of echolocation in bats? Journal of Mammalian Evolution, 30 (1):79-94.
Burchardt L S, Norton P, Behr O, Scharff C, Knörnschild M. 2019.General isochronous rhythm in echolocation calls and social vo calizations of the bat Saccopteryx bilineata. Royal Society Open Science, 6 (1). DOI:10. 1098/rsos. 181076.
Carter G G, Wilkinson G S. 2016. Common vampire bat contact calls attract past food-sharing partners. Animal Behaviour, 116:45-51.
Chi T T, Liu M X, Tan X, Li Y, Xiao Y H, Sun K P, Jin L R, Feng J.2019. Vocal development of Horsfield's leaf-nosed bat pups(Hipposideros larvatus). Acta Chiropterologica, 21 (1):193-204.
Chi T T, Liu M X, Tan X, Sun K P, Jin L R, Feng J. 2020. Syllable merging during ontogeny in Hipposideros larvatus. Bioacoustics, 29 (4):387-398.
Corcoran A J, Conner W E. 2014. Bats jamming bats:food competi tion through sonar interference. Science, 346 (6210):745-747.
Corcoran A J, Weller T J, Hopkins A, Yovel Y. 2021. Silence and re duced echolocation during flight are associated with social behav iors in male hoary bats (Lasiurus cinereus). Scientific Reports, 11(1). DOI:10. 1038/s41598-021-97628-2.
Davidson S M, Wilkinson G S. 2002. Geographic and individual variation in vocalizations by male Saccopteryx bilineata (Chirop tera:Emballonuridae). Journal of Mammalogy, 83 (2):526-535.
Esser K H, Schmidt U. 1989. Mother-infant communication in the lesser spear-nosed bat Phyllostomus discolor (Chiroptera, Phyllos tomidae) -evidence for acoustic learning. Ethology, 82 (2):156-168.
Esser K H, Schubert J. 1998. Vocal dialects in the lesser spear-nosed bat Phyllostomus discolor. Naturwissenschaften, 85:347-349.
Esser K H. 1994. Audio-vocal learning in a non-human mammal:the lesser spear-nosed bat Phyllostomus discolor. Neuroreport, 5(14):1718-1720.
Fan B Z, Wang Y J, Huang X B, Zhang X Z, Yang J T, Jiang T L.
2022. The potential to encode detailed information about para sites in the acoustic signals of Chinese horseshoe bats (Rhinolo phus sinicus). Frontiers in Ecology and Evolution, 10. DOI:10. 3389/fevo. 2022. 908209.
Fenton M B, Belwood J J, Fullard J H, Kunz T H. 1976. Responses of Myotis lucifugus (Chiroptera:Vespertilionidae) to calls of conspe cifics and to other sounds. Canadian Journal of Zoology, 54 (9):1443-1448.
Fenton M B, Grinnell A D, Popper A N, Fay R R. 2016. Bat Bioacous tics. New York:Springer.
Fernandez A A, Fasel N, Knörnschild M, Richner H. 2014. When batsare boxing:aggressive behaviour and communication in male Seba's short-tailed fruit bat. Animal Behaviour, 98:149-156.
Freeberg T M, Dunbar R I M, Ord T J. 2012. Social complexity as a proximate and ultimate factor in communicative complexity.Philosophical Transactions of the Royal Society B:Biological Sci ences, 367 (1597):1785-1801.
Genzel D, Desai J, Paras E, Yartsev M M. 2019. Long-term and per sistent vocal plasticity in adult bats. Nature Communications, 10
(1). DOI:10. 1038/s41467-019-11350-2.
Görföl T, Huang J C C, Csorba G, Győrössy D, Estók P, Kingston T, Szabadi K L, McArthur E, Senawi J, Furey N M, Tu V T, Thong V D, Khan F A A, Jinggong E R, Donnelly M, Kumaran J V, Liu J N, Chen S F, Tuanmu M N, Ho Y Y, Chang H C, Elias N A, Abdullah N I, Lim L S, Squire C D, Zsebők S. 2022. ChiroVox:a public library of bat calls. PeerJ, 10. DOI:10. 7717/peerj. 1244512445.
Gould E. 1979. Neonatal vocalizations of ten species of Malaysian bats (Megachiroptera and Microchiroptera). American Zoologist, 19 (2):481-491.
Greif S, Yovel Y. 2019. Using on-board sound recordings to infer be haviour of free-moving wild animals. Journal of Experimental Bi ology, 222. DOI:10. 1242/jeb. 184689.
Gu H, Sun C N, Gong L X, Zhao X, Feng J, Luo B, Jiang T L, Liu Y.2023. Sex ratio potentially influence the complexity of social calls in Himalayan leaf-nosed bat groups. Frontiers in Ecology and Evolution, 11. DOI:10. 3389/fevo. 2023. 955540.
Guo D G, Ding J N, Liu H, Zhou L, Feng J, Luo B, Liu Y. 2021. So cial calls influence the foraging behavior in wild big-footed myo tis. Frontiers in Zoology, 18:1-14.
Huang X B, Metzner W, Zhang K K, Wang Y J, Luo B, Sun C N, Jiang T L, Feng J. 2018. Acoustic similarity elicits responses to hetero specific distress calls in bats (Mammalia:Chiroptera). Animal Be haviour, 146:143-154.
Jiang T L, Guo X, Lin A Q, Wu H, Sun C N, Feng J, Kanwal J S.2019. Bats increase vocal amplitude and decrease vocal complex ity to mitigate noise interference during social communication.Animal Cognition, 22:199-212.
Jin L R, Lin A Q, Sun K P, Liu Y, Feng J. 2011. Postnatal develop ment of morphological features and vocalization in the pomona leaf-nosed bat Hipposideros pomona. Acta Theriologica, 56:13-22.
Jin L R, Wang J, Zhang Z Z, Sun K P, Kanwal J S, Feng J. 2012. Post natal development of morphological and vocal features in Asian particolored bat, Vespertilio sinensis. Mammalian Biology, 77:339-5344.
Jin L R, Yang S L, Kimball R T, Xie L F, Yue X K, Luo B, Sun K P, Feng J. 2015. Do pups recognize maternal calls in pomona leaf-nosed bats, Hipposideros pomona? Animal Behaviour, 100:200-207.
Jones G, Hughes P M, Rayner J M V. 1991. The development of vo calizations in Pipistrellus pipistrellus (Chiroptera:Vespertilioni dae) during postnatal growth and the maintenance of individual vocal signatures. Journal of Zoology, 225 (1):71-84.
Kanwal J S, Matsumura S, Ohlemiller K, Suga N. 1994. Analysis of acoustic elements and syntax in communication sounds emitted by mustached bats. The Journal of the Acoustical Society of America, 96 (3):1229-1254.
Kerth G, Perony N, Schweitzer F. 2011. Bats are able to maintain long-term social relationships despite the high fissionfusion dy namics of their groups. Philosophical Transactions of the Royal Society B:Biological Sciences, 278:2761-2767.
Knörnschild M, Blüml S, Steidl P, Eckenweber M, Nagy M. 2017.
Bat songs as acoustic beacons-male territorial songs attract dis persing females. Scientific Reports, 7. DOI:10. 1038/s41598-017-14434-5.
Knörnschild M, Feifel M, Kalko E K V. 2014. Male courtship dis plays and vocal communication in the polygynous bat Carollia perspicillata. Behaviour, 151 (6):781-798.
Knörnschild M, Fernandez A A, Nagy M. 2020. Vocal information and the navigation of social decisions in bats:Is social complexity linked to vocal complexity? Functional Ecology, 34 (2):322-331.
Knörnschild M, Nagy M, Metz M, Mayer F, von Helversen O. 2010.Complex vocal imitation during ontogeny in a bat. Biology Let ters, 6 (2):156-159.
Knörnschild M, Von Helversen O, Mayer F. 2007. Twin siblings sound alike:isolation call variation in the noctule bat, Nyctalus noctula. Animal Behaviour, 74 (4):1055-1063.
Knörnschild M, Von Helversen O. 2008. Nonmutual vocal mother-pup recognition in the greater sac-winged bat. Animal Behaviour, 76 (3):1001-1009.
Knörnschild M. 2014. Vocal production learning in bats. Current Opinion in Neurobiology, 28:80-85.
Lin A Q, Jiang T L, Feng J, Kanwal J S. 2016. Acoustically diverse vocalization repertoire in the Himalayan leaf-nosed bat, a widely distributed Hipposideros species. The Journal of the Acoustical Society of America, 140 (5):3765-3774.
Liu Y, Feng J, Jiang Y L, Wu L, Sun K P. 2007. Vocalization develop ment of greater horseshoe bat, Rhinolophus ferrumequinum (Rhi nolophidae, Chiroptera). Folia Zoologica, 56 (2):126-136.
Luo B, Jiang T L, Liu Y, Wang J, Lin A Q, Wei X W, Feng J. 2013.Brevity is prevalent in bat short-range communication. Journal of Comparative Physiology A, 199:325-333.
Luo B, Huang X B, Li Y Y, Lu G J, Zhao J L, Zhang K K, Zhao H B, Liu Y, Feng J. 2017a. Social call divergence in bats:a compara tive analysis. Behavioral Ecology, 28 (2):533-540.
Luo B, Lu G, Chen K, Guo D G, Huang X B, Liu Y, Feng J. 2017b.Social calls honestly signal female competitive ability in Asian particoloured bats. Animal Behaviour, 127:101-108.
Luo J H, Lingner A, Firzlaff U, Wiegrebe L. 2017. The Lombard ef fect emerges early in young bats:implications for the develop ment of audio-vocal integration. Journal of Experimental Biol ogy, 220 (6):1032-1037.
Ma J, Kobayasi K, Zhang S Y, Metzner W. 2006. Vocal communica tion in adult greater horseshoe bats, Rhinolophus ferrumequinum.Journal of Comparative Physiology A, 192:535-550.
Middleton N, Froud A, French K. 2022. Social Calls of the Bats ofBritain and Ireland. London:Pelagic Publishing Ltd.
Montero B K, Sagot M, Phillips C D, Baker R J, Gillam E H. 2018.Geographic variation of contact calls suggest distinct modes of vo cal transmission in a leaf-roosting bat. Behavioral Ecology and Sociobiology, 72 (8). DOI:10. 1007/s00265-018-2543-1.
Moss C F, Redish D, Gounden C, Kunz T. 1997. Ontogeny of vocal signals in the little brown bat, Myotis lucifugus. Animal Behav iour, 54 (1):131-141.
Nowicki S, Searcy W A. 2014. The evolution of vocal learning. Cur rent Opinion in Neurobiology, 28:48-53.
Patel A D. 2008. Music, Language and the Brain. New York:Oxford University Press.
Peckre L, Kappeler P M, Fichtel C. 2019. Clarifying and expanding the social complexity hypothesis for communicative complexity.Behavioral Ecology and Sociobiology, 73 (1):1-19.
Pfalzer G, Kusch J. 2003. Structure and variability of bat social calls:implications for specificity and individual recognition. Journal of Zoology, 261 (1):21-33.
Prat Y, Taub M, Yovel Y. 2015. Vocal learning in a social mammal:Demonstrated by isolation and playback experiments in bats. Sci ence Advances, 1 (2). DOI:10. 1126/sciadv. 1500019.
Prat Y, Taub M, Yovel Y. 2016. Everyday bat vocalizations contain in formation about emitter, addressee, context, and behavior. Scien tific Reports, 6 (1):1-10.
Sagot M, Schöner C R, Jago A J, Razik I, Chaverri G. 2018. The im portance of group vocal behaviour in roost finding. Animal Be haviour, 142:157-164.
Simmons N B, Cirranello A L. 2024. Bat Species of the World:A taxonomic and geographic database. Version 1. 5. Accessed on05/26/2024.
Sun C N, Jiang T L, Gu H, Guo X, Zhang C M, Gong L X, Shi B Y, Feng J. 2020. Geographical variation of social calls and vocal discrimination in male Himalayan leaf-nosed bats. Animal Behav iour, 170:15-26.
Sun C N, Jiang T L, Kanwal J S, Guo X, Luo B, Lin A Q, Feng J.2018. Great Himalayan leaf-nosed bats modify vocalizations to communicate threat escalation during agonistic interactions. Be havioural Processes, 157:180-187.
Sun C N, Zhang C M, Lucas J R, Lin A Q, Feng J, Jiang T L. 2021.
Territorial calls of the bat Hipposideros armiger may encode mul tiple types of information:body mass, dominance rank and indi vidual identity. Animal Cognition, 24:689-702.
Vernes S C, Devanna P, Hörpel S G, Tussenbroek I A, Firzlaff U, Ha goort P, Hiller M, Hoeksema N, Hughes G M, Lavrichenko K, Mengede J, Morales A E, Hughes G M, Lavrichenko K, Mengede J, Morales A E, Wiesmann M. 2022. The pale spearnosed bat:A neuromolecular and transgenic model for vocal learning. Annals of the New York Academy of Sciences, 1517 (1):125-142.
Vernes S C, Wilkinson G S. 2020. Behaviour, biology and evolution of vocal learning in bats. Philosophical Transactions of the Royal Society B, 375 (1789). DOI:10. 1098/rstb. 2019. 0061.
Wilkinson G S. 2003. Social and vocal complexity in bats. In:De Waal F B M, Tyack P L eds. Animal Social Complexity:Intelli gence, Culture, and Individualized Societies. Cambridge:Har vard University Press, 322-341.
Wu X, Pang Y, Luo B, Wang M, Feng J. 2018. Function of distress calls in least horseshoe bats:a field study using playback experi ments. Acta Chiropterologica, 20 (2):455-464.
Yovel Y, Rechavi O. 2023. AI and the doctor dolittle challenge. Cur rent Biology, 33 (15):R783-R787.
Zhang C M, Ji L G, Li Z J, Lucas J R, Feng J, Sun C N, Jiang T L.2024. Resting posture drives the evolution of agonistic displays in bats. Evolution, 78 (5):964-970.
Zhang C M, Sun C N, Wang Z Q, Lin P C, Xiao Y H, Metzner W, Feng J, Jiang T L. 2021. Minor modification of frequency modulated call parameters underlies a shift in behavioral response in the Great Himalayan leaf-nosed bats, Hipposideros armiger. Journal of Mammalogy, 102 (2):457-467.
Zhang C M, Zheng Z Q, Lucas J R, Wang Y C, Fan X, Zhao X, Feng J, Sun C N, Jiang T L. 2024. Do bats'social vocalizations conform to Zipf's law and the Menzerath-Altmann law? iScience, 27 (7).DOI:10. 1016/j. isci. 2024. 110401.
Zhang K K, Liu T, Liu M X, Li A Q, Xiao Y H, Metzner W, Liu Y.2019. Comparing context-dependent call sequences employing machine learning methods:An indication of syntactic structure of greater horseshoe bats. Journal of Experimental Biology, 222
(24). DOI:10. 1242/jeb. 214072.
Zhang K K, Yu Y P, Liu T, Ding J N, Gu H, Feng J, Liu Y. 2024. Uni versal patterns and differences in graded aggressive calls of greater horseshoe bats from distant populations. Animal Behav iour, 210:153-178.
Zhang L B, Jones G, Parsons S, Liang B, Zhang S Y. 2005. Develop ment of vocalizations in the flat-headed bats, Tylonycteris pachy pus and T. robustula (Chiroptera:Vespertilionidae). Acta Chirop terologica, 7 (1):91-99.
Zhao X, Jiang T L, Gu H, Liu H, Sun C N, Liu Y, Feng J. 2018. Are aggressive vocalizations the honest signals of body size and qual ity in female Asian particoloured bats? Behavioral Ecology and Sociobiology, 72:1-16.
Zhao X, Jiang T L, Liu H, Wang Y Z, Liu Y, Feng J. 2019. Acoustic signalling of aggressive intent in the agonistic encounters of fe male Asian particoloured bats. Animal Behaviour, 149:65-75.
Zuberbühler K. 2020. Syntax and compositionality in animal commu nication. Philosophical Transactions of the Royal Society B, 375(1789). DOI:10. 1098/rstb. 2019. 0062.
江廷磊, 赵华斌, 何彪, 张礼标, 罗金红, 刘颖, 孙克萍, 余文华, 吴毅, 冯江. 2020. 中国蝙蝠生物学研究进展及其保护对策. 兽类学报, 40 (6):539-559.
魏辅文, 杨奇森, 吴毅, 蒋学龙, 刘少英, 胡义波, 葛德燕, 李保国, 杨光, 李明, 周江, 李松, 李晟, 余文华, 陈炳耀, 张泽钧, 周材权, 吴诗宝, 张立, 陈中正, 陈顺德, 邓怀庆, 江廷磊, 张礼标, 石红艳, 卢学理, 李权, 刘铸, 崔雅倩, 李玉春, 何锴. 2025. 中国兽类名录 (2024 版). 兽类学报, 45 (1):1-16.

Options

文章导航

模态框（Modal）标题

摘要

本文引用格式

Abstract

参考文献