The production and evolutionary adaptation of alarm calls in small mammals: research progress and prospect

doi:10.16829/j.slxb.151099

ACTA THERIOLOGICA SINICA ›› 2025, Vol. 45 ›› Issue (6): 723-742.DOI: 10.16829/j.slxb.151099

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The production and evolutionary adaptation of alarm calls in small mammals: research progress and prospect

Linchu TIAN¹^,², Qiangyun LI²^,³, Heping FU¹, Zhishu XIAO²^,⁴, Shuai YUAN¹(), Wei LIU²^,⁴()

^1.College of Grassland Science, Inner Mongolia Agricultural University, Key Laboratory of Grassland Rodent Ecology and Rodent Pest Control for Autonomous Region Higher Education Institutions, Hohhot 010011, China
^2.State Key Laboratory of Animal Biodiversity Conservation and Integrated Pest Management, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
^3.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
^4.University of Chinese Academy of Sciences, Beijing 100049, China

Received:2025-04-30 Accepted:2025-07-07 Online:2025-11-30 Published:2025-12-03
Contact: Shuai YUAN, Wei LIU

小型哺乳动物报警鸣叫的产生与进化适应：研究进展与展望

田琳楚¹^,², 李强云²^,³, 付和平¹, 肖治术²^,⁴, 袁帅¹(), 刘伟²^,⁴()

^1.内蒙古农业大学草业学院，草地啮齿动物生态学与鼠害控制自治区高等学校重点实验室，呼和浩特 010011
^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全国重点实验室，北京 100101
^3.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
^4.中国科学院大学，北京 100049

通讯作者: 袁帅,刘伟
作者简介:田琳楚 (2000- )，女，硕士研究生，主要从事啮齿动物行为生态学研究.
基金资助:
国家重点研发计划项目(2024YFD1400502);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)

Abstract

Abstract:

Alarm calls are a key communication behavior for animals to defend against risks, especially in response to predation threats. The study of their adaptation and evolution is of great significance for understanding the evolution of signal structure in animal vocal communication (including human language) as well as the mechanisms of signal recognition and cognition. Over the years, our understanding about the nature of alarm calls has continued to mature. Simultaneously, the function of alarm calls in conveying information in animal social interactions has been widely recognized. However, it remains unclear the production and driving mechanisms of alarm calls, not only the encoding and transmission of vocalization information but also their impact on multi-level response patterns of receivers. In recent years, with the rapid development of acoustic monitoring, digital signal processing, and artificial intelligence deep learning technologies, research on alarm calls has expanded from discriptive patterns description to a theoretical integration, validation, and mechanistic elucidation. Here, we review studies on alarm calls in small mammals over the past 20 years and briefly outline the research connotations and methods of alarm call communication. From the perspectives of call or vocalization production and adaptation, we summarize the research progress on the risk-driven effects of alarm vocalization information encoding, as well as the current status of research on the impacts of individual identity characteristics, such as age (body size), sex, and social attributes and habitat features on alarm calling. We also systematically summarize various natural selection theories and their controversies regarding the evolutionary adaptation of alarm calls. Finally, based on current application context, we discuss and prospect some key issues on the vocalization and response mechanisms and functional evolutionary adaptation of alarm calls in small mammals for the future.

Key words: Alarm call, Information encoding, Individual identity effect, Habitat effect, Natural selection

摘要：

报警鸣叫是动物抵御风险、应对捕食威胁的关键通讯行为。其适应与进化研究对于理解动物声音通讯中信号的结构演变 (包括人类语言) 以及信号识别与认知机制具有重要意义。长期以来，人们对报警鸣叫本质的认识在不断成熟，其在动物社会交流中传递信息的功能已被广泛认可。然而，报警鸣叫产生及其驱动机制，包括鸣声信息的编码和传递方式，以及对接收者多层级响应模式的影响，仍不明确。近年来，随着声学监测、数字信号处理和人工智能深度学习技术的快速发展，报警鸣叫研究已从单纯的模式描述拓展到理论整合、验证及机制阐释。本文回顾了近20年小型哺乳动物报警鸣叫的重要研究，简要概述了该领域研究的内涵与方法。从鸣声产生和适应的角度，我们归纳了报警鸣声信息编码的风险驱动效应研究进展，以及年龄 (体型)、性别和社会属性等个体身份特征和栖息环境特征对报警鸣叫的影响。同时，本文梳理了报警鸣叫进化适应的多种自然选择理论假说及其分歧。最后，我们结合当前应用背景，对小型哺乳动物报警鸣叫的发生和响应机制以及功能进化适应未来研究的重点问题和发展趋势进行了展望。

关键词: 报警鸣叫, 信息编码, 个体身份效应, 栖息地效应, 自然选择

CLC Number:

Q958.1

Linchu TIAN, Qiangyun LI, Heping FU, Zhishu XIAO, Shuai YUAN, Wei LIU. The production and evolutionary adaptation of alarm calls in small mammals: research progress and prospect[J]. ACTA THERIOLOGICA SINICA, 2025, 45(6): 723-742.

田琳楚, 李强云, 付和平, 肖治术, 袁帅, 刘伟. 小型哺乳动物报警鸣叫的产生与进化适应：研究进展与展望[J]. 兽类学报, 2025, 45(6): 723-742.

Figures/Tables 1

References

	Abraham A. 2019. The Extended Theory of Cognitive Creativity: Interdisciplinary Approaches to Performativity [M]. Cham: Palgrave Macmillan, 199-216.
	Antonson N D, Enos J K, Lawson S L, Uy F M, Gill S A, Lynch K S, Hauber M E. 2024. Functional neurogenomic responses to acoustic threats, including a heterospecific referential alarm call and its referent, in the auditory forebrain of red‑winged blackbirds [J]. Scientific Reports, 14 (1): 2155. DOI: 10.1038/s41598-024-51797-y .
	Arnold K, Bar‑On D. 2020. Primate pragmatics, expressive behavior, and the evolution of language [J]. Animal Behavior and Cognition, 7 (2): 117-130.
	Artiga M, Birch J, Martínez M. 2020. The meaning of biological signals [J]. Studies in History and Philosophy of Biological and Biomedical Sciences, 84: 101348. DOI: 10.1016/j.shpsc.2020.101348 .
	Austin V I, Dalziell A H, Langmore N E, Welbergen J A. 2021. Avian vocalisations: the female perspective [J]. Biological Reviews, 96 (4): 1484-1503.
	Bergstrom C T, Lachmann M. 2001. Alarm calls as costly signals of antipredator vigilance: the watchful babbler game [J]. Animal Behaviour, 61: 535-543.
	Berthet M, Mesbah G I, Pajot A, Cäsar C, Neumann C, Zuberbühler K. 2019. Titi monkeys combine alarm calls to create probabilistic meaning [J]. Science Advances, 5 (5): eaav3991. DOI: 10.1126/sciadv.aav3991 .
	Berthet M, Mesbahi G, Csar C, Zuberbühler K. 2022. Impact of predator model presentation paradigms on titi monkey alarm sequences [J]. Behavioral Ecology and Sociobiology, 76 (11): 1-14.
	Bircher N, Oers K V, Naguib M. 2021. Anyone listening? No evidence for eavesdropping on male singing interactions in the great tit, Parus major [J]. Animal Behaviour, 176 (3): 67-76.
	Blanchard R J, Blanchard D C, Agullana R, Weiss S M. 1991. Twenty‑two kHz alarm cries to presentation of a predator, by laboratory rats living in visible burrow systems [J]. Physiology and Behavior, 50 (5): 967-972.
	Blum C R, Fitch W T, Bugnyar T. 2022. Social dynamics impact scolding behaviour in captive groups of common ravens (Corvus corax) [J]. Frontiers in Zoology, 19 (1): 32. DOI: 10.1186/s12983-022-00477-6 .
	Blumstein D T, Adler K A, Jazmine U. 2024. Costly calling: marmots who alarm call at higher rates are less likely to survive the summer and live shorter lives [J]. Current Zoology, 71 (4): 425-431.
	Blumstein D T, Armitage K B. 1997. Does sociality drive the evolution of communicative complexity? A comparative test with ground‑dwelling sciurid alarm calls [J]. The American Naturalist, 150 (2): 179-200.
	Blumstein D T, Fuong H, Palmer E. 2017. Social security: social relationship strength and connectedness influence how marmots respond to alarm calls [J]. Behavioral Ecology and Sociobiology, 71 (10): 145. DOI: 10.1007/s00265-017-2374-5 .
	Blumstein D T, Munos O. 2005. Individual, age and sex‑specific information is contained in yellow‑bellied marmot alarm calls [J]. Animal Behaviour, 69 (2): 353-361.
	Blumstein D T, Patton M L, Saltzman W. 2006. Faecal glucocorticoid metabolites and alarm calling in free‑living yellow‑bellied marmots [J]. Biology Letters, 2 (1): 29-32.
	Blumstein D T, Verneyre L, Daniel J C. 2004. Reliability and the adaptive utility of discrimination among alarm callers [J]. Proceedings of the Royal Society B: Biological Sciences, 271 (1550): 1851-1857.
	Blumstein D T, Vu N, Edica M, Voa L, Martin J G A. 2025. The sound of fear is heritable [J]. Current Zoology, 71: 49-53.
	Blumstein D T. 2007. The evolution, function, and meaning of marmot alarm communication [J]. Advances in the Study of Behavior, 37: 371-401.
	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: 134-142.
	Bouchet H, Blois‑Heulin C, Pellier A S, Zuberbühler K, Lemasson A. 2012. Acoustic variability and individual distinctiveness in the vocal repertoire of red‑capped mangabeys (Cercocebus torquatus) [J]. Journal of Comparative Psychology, 126 (1): 45-56.
	Brandler O V, Tukhbatullin A R, Nikol’Skii A A. 2019. Comparative analysis of the alarm call in different age and sexual groups of the russet ground squirrel (Spermophilus major Pallas 1778) [J]. Russian Journal of Developmental Biology, 50 (4): 173-179.
	Brosseau J E, Eddington V M, Craig E C, White E R, Kloepper L N. 2024. The effect of localized disturbance on the acoustic behavior of the common tern (Sterna hirundo) [J]. JASA Express Letters, 4 (9): 1-22. DOI: 10.1121/10.0028204 .
	Brumm H, Naguib M. 2009. Environmental acoustics and the evolution of bird song [J]. Advances in the Study of Behavior, 40: 1-33.DOI: 10.1016/S0065-3454(09)40001-9 .
	Burnett A D, Koprowski J L. 2020. Ultimate causes of antipredator vocalizations in a nonhibernating squirrel [J]. Animal Behaviour, 168: 225-230.
	Carouso‑Peck S, Goldstein M H, Fitch W T. 2021. The many functions of vocal learning [J]. Philosophical Transactions of the Royal Society B, 376 (1836): 20200235.DOI: 10.1098/rstb.2020.0235 .
	Casar C, Zuberbühler K. 2012. Referential alarm calling behaviour in new world primates [J]. Current Zoology, 58 (5): 680-697.
	Charnov E L, Krebs J R. 1975. The evolution of alarm calls: altruism or manipulation? [J]. The American Naturalist, 109 (965): 107-112.
	Clarke E, Reichard U H, Zuberbühler K. 2006. The syntax and meaning of wild gibbon songs [J]. PLoS ONE, 1 (1): e73. DOI: 10.1371/journal.pone.0000073 .
	Collier K, Radford A N, Townsend S W, Manser M B. 2017. Wild dwarf mongooses produce general alert and predator‑specific alarm calls [J]. Behavioral Ecology, 28 (5): 1293-1301.
	Couchoux C, Clermont J, Garant D, Réale D, Pruitt J. 2018. Signaler and receiver boldness influence response to alarm calls in eastern chipmunks [J]. Behavioral Ecology, 29 (1): 212-220.
	Courter J R, Perruci R J, McGinnis K J, Rainieri J K. 2020. Black‑capped chickadees (Poecile atricapillus) alter alarm call duration and peak frequency in response to traffic noise [J]. PLoS ONE, 15 (10): e0241035. DOI: 10.1371/journal.pone.0241035 .
	Curio E. 1978. The adaptive significance of avian mobbing: I. Teleonomic hypotheses and predictions [J]. Zeitschrift für Tierpsychologie, 48: 175-183.
	Darwaiz T, Pasch B, Riede T. 2022. Postnatal remodeling of the laryngeal airway removes body size dependency of spectral features for ultrasonic whistling in laboratory mice [J]. Journal of Zoology, 318 (2): 114-126.
	De Rosa A, Castro I, Marsland S. 2022. The acoustic playback technique in avian fieldwork contexts: a systematic review and recommendations for best practice [J]. Ibis, 164 (2): 371-387.
	Deng K, He Y X, Wang X P, Wang T L, Wang J C, Chen Y H, Cui J G. 2024. Hainan frilled treefrogs’ calls partially conform to Menzerath‑Altmann’s law, but oppose Zipf’s law of abbreviation [J]. Animal Behaviour, 213: 51-59.
	Dent M L, Fay R R, Popper A N. 2018. Springer Handbook of Auditory Research [M]. Springer new york heidelberg dordrecht London: Springer Science Business Media.
	Diggins C. 2021. Behaviors associated with vocal communication of squirrels [J]. Ecosphere, 12 (6): e03572. DOI: 10.1002/ecs2.3572 .
	Digweed S M, Rendall D, Imbeau T. 2012. Who’s your neighbor? Acoustic cues to individual identity in red squirrel Tamiasciurus hudsonicus rattle calls [J]. Current Zoology, 58 (5): 758-764.
	Digweed S M, Rendall D. 2009. Predator‐associated vocalizations in north American red squirrels (Tamiasciurus hudsonicus): to whom are alarm calls addressed and how do they function? [J]. Ethology, 115 (12): 1190-1199.
	Dubreuil C, Notman H, Barrett L, Henzi P, Pavelka M S. 2025. Sex differences in the acoustic structure of terrestrial alarm calls in vervet monkeys (Chlorocebus pygerythrus) [J]. American J Primatol, 87 (1): e23674. DOI: DOI10.1002/ajp.23674 .
	Dunford C. 1977. Kin selection for ground squirrel alarm calls [J]. The American Naturalist, 111 (980): 782-785.
	Dutour L R, Ruth A. 2021. Australian magpies adjust their alarm calls according to predator distance [J]. Bioacoustics: The International Journal of Animal Sound and its Recording, 30 (4): 458-468.
	Dutour M, Walsh S L, Ridley A R. 2021. Australian magpies adjust their alarm calls according to predator distance [J]. Bioacoustics, 30 (4): 458-468.
	Eason P. 2010. Alarm signaling in a facultatively social mammal, the southern amazon red squirrel Sciurus spadiceus [J]. Mammalia, 74 (3): 343-345.
	Eddington V M, Nichols H K, Calistri‑Yeh A, Young V K, 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. The ‘acoustic adaptation hypothesis’: a review of the evidence from birds, anurans and mammals [J]. Bioacoustics, 19 (1-2): 21-48.
	Fan B, Wang Y, Huang X, Zhang X, Yang J, Jiang T. 2022. The potential to encode detailed information about parasites in the acoustic signals of Chinese horseshoe bats (Rhinolophus sinicus) [J]. Frontiers in Ecology and Evolution, 10: 908209. DOI: 10.3389/fevo.2022.908209 .
	Fang W H, Hsu Y H, Lin W L, Yen S C. 2020. The function of avian mobbing: an experimental test of ‘attract the mightier’ hypothesis [J]. Animal Behaviour, 170: 229-233.
	Fichtel C. 2020. Monkey alarm calling: it ain’t all referential, or is it? [J]. Animal Behavior and Cognition, 7 (2): 101-107.
	Freeberg T M, Dunbar R I M, Ord T J. 2012. Social complexity as a proximate and ultimate factor in communicative complexity [J]. Philosophical Transactions of the Royal Society B‑Biological Sciences, 367 (1597): 1785-1801.
	Freeman A R, Hare J F, Caldwell H K. 2020. Call‐specific patterns of neural activation in auditory processing of Richardson’s ground squirrel alarm calls [J]. Brain and Behavior, 10 (6): e01629. DOI: 10.1002/brb3.1629 .
	Fuong H, Blumstein D T. 2019. Social security: less socially connected marmots produce noisier alarm calls [J]. Animal Behaviour, 154: 131-136.
	Furrer R D, Manser M B. 2009. The evolution of urgency‑based and functionally referential alarm calls in ground‑dwelling species [J]. The American Naturalist, 173 (3): 400-410.
	Garcia M, Herbst C T, Bowling D L, Dunn J C, Fitch W T. 2017. Acoustic allometry revisited: morphological determinants of fundamental frequency in primate vocal production [J]. Scientific Reports, 7 (1): 10450. DOI: 10.1038/s41598-017-11000-x .
	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 (4): 745-751.
	Garland E C, McGregor P K. 2020. Cultural transmission, evolution, and revolution in vocal displays: insights from bird and whale song [J]. Frontiers in Psychology, 11: s44929.DOI: 10.3389/fpsyg.2020.544929 .
	Gaviraghi Mussoi J, MacQueen R A, Stanley M C, Cain K E. 2024. Experimentally elevated corticosterone increases song output and complexity in common mynas [J]. Journal of Experimental Zoology Part A: Ecological and Integrative Physiology, 341 (7): 733-742.
	Goncharov D, Policht R, Hambálková L, Salovarov V, Hart V. 2021. Individual‑based acoustic variation of the alarm calls in the long‑tailed ground squirrel [J]. Royal Society Open Science, 8 (2): 200147. DOI: 10.1098/rsos.200147 .
	Grawunder S, Crockford C, Clay Z, Kalan A K, Stevens J M, Stoessel A, Hohmann G. 2018. Higher fundamental frequency in bonobos is explained by larynx morphology [J]. Current Biology, 28 (20): 1188-1189.
	Hammerschmidt K, Fischer J. 1998. The vocal repertoire of Barbary macaques: a quantitative analysis of a graded signal system [J]. Ethology, 104 (3): 203-216.
	Hardouin L A, Thompson R, Stenning M, Reby D. 2014. Anatomical bases of sex‑and size‑related acoustic variation in herring gull alarm calls [J]. Journal of Avian Biology, 45 (2): 157-166.
	Haskell E C, Bell J. 2021. A model of the burglar alarm hypothesis of prey alarm calls [J]. Theoretical Population Biology, 141: 1-13.DOI: 10.1016/j.tpb.2021.05.004 .
	Hollén L I, Clutton‑Brock T, Manser M B. 2008. Ontogenetic changes in alarm‑call production and usage in meerkats (Suricata suricatta): adaptations or constraints? [J]. Behavioral Ecology and Sociobiology, 62: 821-829.
	Hollén L I, Manser M. 2007. Motivation before meaning: motivational information encoded in meerkat alarm calls develops earlier than referential information [J]. American Naturalist, 169 (6): 758-767.
	Hollén L I, Radford A N. 2009. The development of alarm call behaviour in mammals and birds [J]. Animal Behaviour, 78 (4): 791-800.
	Huang M, Ma H, Ma C, Garber P A, Fan P. 2020. Male gibbon loud morning calls conform to Zipf’s law of brevity and Menzerath’s law: insights into the origin of human language [J]. Animal Behaviour, 160: 145-155.
	Jiang X Y, Zhang Y Y. 2024. Sounding the alarm: Functionally referential signaling in Azure‑winged Magpie [J]. Avian Research, 15 (1): 100164.
	Kelley D B, Ballagh I H, Barkan C L, Bendesky A, Elliott T M, Evans B J, Hall I C, Kwon Y M, Kwong‑Brown U, Leininger E C, Perez E C. 2020. Generation, coordination, and evolution of neural circuits for vocal communication [J]. Journal of Neuroscience, 40 (1): 22-36.
	Kershenbaum A, Blumstein D T, Roch M A, Akçay Ç, Backus G, Bee M A, Bohn K, Cao Y, Carter G, Cäsar C, Coen M, DeRuiter S L, Doyle L, Edelman S, Ferrer‑i‑Cancho R, Freeberg T M, Garland E C, Gustison M, Harley H E, Huetz C, Hughes M, Hyland B J, Ilany A, Jin D Z, Johnson M, Ju C, Karnowski J, Lohr B, Manser M B, McCowan B, Mercado E, Narins P M, Piel A, Rice M, Salmi R, Sasahara K, Sayigh L, Shiu Y, Taylor C, Vallejo E E, Waller S, Zamora‑Gutierrez V. 2016. Acoustic sequences in non‐human animals:a tutorial review and prospectus [J]. Biological Reviews, 91 (1): 13-52.
	Klump G M, Shalter M D. 1984. Acoustic behaviour of birds and mammals in the predator context; I.Factors affecting the structure of alarm signals.II.The functional significance and evolution of alarm signals [J]. Zeitschrift für Tierpsychologie, 66 (3): 189-226.
	Laine M A, Mitchell J R, Rhyner J, Clark R, Kannan A, Keith J, Pikus M, Bergeron E, Ravaglia I, Ulgenturk E, Shinde A. 2022. Sounding the alarm: sex differences in rat ultrasonic vocalizations during pavlovian fear conditioning and extinction [J]. ENeuro, 9 (6): H5. DOI: 10.1523/ENEURO.0382-22.2022 .
	Lameira A R, Santamaría‑Bonfil Guillermo, Galeone D, Gamba M, Hardus M, Knott C D, Morrogh‑Bernard H, Nowak M G, Campbell‑Smith G, Wich S A. 2022. Sociality predicts orangutan vocal phenotype [J]. Nature Ecology and Evolution, 6 (5): 644-652.
	Lea A J, Blumstein D T. 2011. Ontogenetic and sex differences influence alarm call responses in mammals: a meta‑analysis [J]. Ethology, 117: 839-851.
	Lissovsky A A. 2005. Comparative analyses of the vocalization of pikas (Ochotona, Mammalia) from alpina‑hyperborea group [J]. Byulleten’Moskovskogo Obshchestva Ispytateley Prirody. Otdel Biologicheskii, 110 (6): 12-26.
	Locke J L. 2021. The indexical voice: communication of personal states and traits in humans and other primates [J]. Frontiers in Psychology, 12: 651108. DOI: 10.3389/fpsyg.2021.651108 .
	López‑Cuamatzi I L, Vega‑Gutiérrez V H, Cabrera‑Campos I, RuizSanchez E, Ayala‑Berdon J, Saldaña‑Vázquez R A. 2020. Does body mass restrict call peak frequency in echolocating bats? [J]. Mammal Review, 50: 304-313.
	Loughry W J, Oeser M, Anderson C D, Hoogland J L. 2019. The importance of individual variation in the alarm calls of Gunnison’s prairie dogs [J]. Animal Behaviour, 150: 59-68.
	Luo J, Goerlitz H R, Brumm H, Wiegrebe L. 2015. Linking the sender to the receiver: vocal adjustments by bats to maintain signal detection in noise [J]. Scientific Reports, 5 (1): 18556. DOI: 10.1038/srep18556 .
	Luo J, Lu M, Wang X, Moss C F. 2022. Doppler shift compensation performance in Hipposideros pratti across experimental paradigms [J]. Frontiers in Systems Neuroscience, 16: 920703. DOI: 10.3389/fnsys.2022.920703 .
	Ma M, Hua R, Bao D, Ye G, Tang Z, Hua L. 2023. Alarm calling in plateau pika (Ochotona curzoniae): evidence from field observations and simulated predator and playback experiments [J]. Animals, 13: 1271. DOI: 10.3390/ani13071271 .
	Madhusudhana S, Shiu Y, Klinck H, Fleishman E, Liu X, Nosal E M, Roch M A. 2021. Improve automatic detection of animal call sequences with temporal context [J]. Journal of the Royal Society Interface, 18 (180): 20210297. DOI: 10.1098/rsif.2021.0297 .
	Manser M B, Seyfarth R M, Cheney D L. 2002. Suricate alarm calls signal predator class and urgency [J]. Trends in Cognitive Sciences, 6 (2): 55-57.
	Marten K, Marler P. 1977. Sound transmission and its significance for animal vocalization: I. Temperate habitats [J]. Behavioral Ecology and Sociobiology, 2: 271-290.
	Martin K, Tucker M A, Rogers T L. 2016. Does size matter? examining the drivers of mammalian vocalizations [J]. Evolution, 71 (2): 249-260.
	Matrosova V A, Blumstein D T, Volodin I A, Volodina E V. 2011. The potential to encode sex, age, and individual identity in the alarm calls of three species of Marmotinae [J]. Naturwissenschaften, 98: 181-192.
	Matrosova V A, Rusin M Y, Volodina E V, Proyavka S V, Savinetskaya L E, Shekarova O N, Rashevska H V, Volodin I A. 2016. Genetic and alarm call diversity across scattered populations of speckled ground squirrels (Spermophilus suslicus) [J]. Mammalian Biology, 81: 255-265.
	Matrosova V A, Schneiderová I, Volodin I A, Volodina E V. 2012. Species‑specific and shared features in vocal repertoires of three Eurasian ground squirrels (genus Spermophilus) [J]. Mammal Research, 57 (1): 65-78.
	Mcgregor P K. 2000. Playback experiments: design and analysis [J]. Acta Ethologica, 3 (1): 3-8.
	McLachlan J R, Magrath R D. 2020. Speedy revelations: how alarm calls can convey rapid, reliable information about urgent danger [J]. Proceedings of the Royal Society B, 287 (1921): 20192772. DOI: 10.1098/rspb.2019.2772 .
	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, Petrusková 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]. Ecology Letters, 24 (3): 477-486.
	Morris‑Drake A, Bracken A, Kern J, Radford A. 2017. Anthropogenic noise alters dwarf mongoose responses to heterospecific alarm calls [J]. Environment Pollution, 223: 476-483
	Morton E S. 1975. Ecological sources of selection on avian sounds [J]. The American Naturalist, 109 (965): 17-34.
	Morton E S. 1977. On the occurrence and significance of motivation‑structural rules in some bird and mammal sounds [J]. American Naturalist, 111 (981): 855-869.
	Mussoi G J, Macqueen R A, Stanley M C, Cain K E. 2024. Experimentally elevated corticosterone increases song output and complexity in common mynas [J]. Journal of Experimental Zoology: Part A Ecological and Integrative Physiology, 341 (7): 733-742.
	Niemczura A C, Grimsley J M, Kim C, Alkhawaga A, Poth A, Carvalho A, Wenstrup J J. 2020. Physiological and behavioral responses to vocalization playback in mice [J]. Frontiers in Behavioral Neuroscience, 14: 155. DOI: 10.3389/fnbeh.2020.00155 .
	Nouri K, Blumstein D T. 2019. Parasites are associated with noisy alarm calls [J]. Frontiers in Ecology and Evolution, 7: 28. DOI: 10.3389/fevo.2019.00028 .
	Oestreich W K, Oliver R Y, Chapman M S, Go M C, Mckenna M F. 2024. Listening to animal behavior to understand changing ecosystems [J]. Trends in Ecology and Evolution, 39 (10): 961-973.
	Olszyński K H, Polowy R, Małż M, Boguszewski P M, Filipkowski R K. 2020. Playback of alarm and appetitive calls differentially impacts vocal, heart‑rate, and motor response in rats [J]. iScience, 23 (10): 101577. DOI: 10.1016/j.isci.2020.101577 .
	Palazzolo G. 2024. A case for animal reference: beyond functional reference and meaning attribution [J]. Synthese, 203 (2): 59. DOI: 10.1007/s11229-023-04469-9 .
	Pandourski I. 2011. Case of alarm vocalization in a colony of Microtus guentheri (Danford and Alston, 1880) (Mammalia, Rodentia, Arvicolidae) from Southern Bulgaria [J]. ZooNotes, 19: 1-34.
	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.
	Pollard K A. 2011. Making the most of alarm signals: the adaptive value of individual discrimination in an alarm context [J]. Behavioral Ecology, 22 (1): 93-100.
	Prat Y, Taub M, Yovel Y. 2015. Vocal learning in a social mammal: Demonstrated by isolation and playback experiments in bats [J]. Science Advances, 1 (2): e1500019. DOI: 10.1126/sciadv.1500019 .
	Qian Q, Li J, Fu M, Zou M, Tian T, Yan Y, Newman C, Zou D, Zhou Y. 2024. Ultrasonic differentiation between two species of Chinese pygmy dormice (genus Typhlomys) with support for the size‑signal allometry hypothesis [J]. Integrative Zoology, 53: 34. DOI: 10.1111/1749-4877.12937 .
	Randall J A, McCowan B, Collins K C, Hooper S L, Rogovin K. 2005. Alarm signals of the great gerbil: acoustic variation by predator context, sex, age, individual, and family group [J]. The Journal of the Acoustical Society of America, 118 (4): 2706-2714.
	Randall J A, Rogovin K A. 2002. Variation in and meaning of alarm calls in a social desert rodent Rhombomys opimus [J]. Ethology, 108 (6): 513-527.
	Rauber R, Kranstauber B, Manser M B. 2020. Call order within vocal sequences of meerkats contains temporary contextual and individual information [J]. BMC Biology, 18 (1): 1190.DOI: 10.1186/s12915-020-00847-8 .
	Robert T. 2015. The SAGE Handbook of Evolutionary Psychology: Foundations of Evolutionary Psychology [M]. London: SAGE Publications, 137-154.
	Robinson B. 1980. Antipredator behaviour and predator recognition in Belding’s ground squirrels [J]. Animal Behaviour, 28 (3): 840-852.
	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.
	Ruff Z J, Lesmeister D B, Duchac L S, Padmaraju B K, Sullivan C M. 2020. Automated identification of avian vocalizations with deep convolutional neural networks [J]. Remote Sensing in Ecology and Conservation, 6 (1): 79-92.
	Ruff Z J, Lesmeister D B, Jenkins J M, Sullivan C M. 2023. PNW‑Cnet v4: Automated species identification for passive acoustic monitoring [J]. SoftwareX, 23: 101473. DOI: 10.1016/j.softx.2023.101473 .
	Scarantino A. 2013. Rethinking functional reference [J]. Philosophy of Science, 80 (5): 1006-1018
	Schibler F, Manser M B. 2007. The irrelevance of individual discrimination in meerkat alarm calls [J]. Animal Behaviour, 74 (5): 1259-1268.
	Schneider S, Goettlich S, Diercks C, Dierkes P W. 2021. Discrimination of acoustic stimuli and maintenance of graded alarm call structure in captive meerkats [J]. Animals, 11 (11): 3064. DOI: 10.3390/ani11113064 .
	Seyfarth R M, Cheney D L. 2003.Signalers and receivers in animal communication [J]. Annual Review Psychology, 54: 145-173.
	Seyfarth R, Cheney D, Marler P. 1980. Monkey responses to three different alarm calls: evidence of predator classification and semantic communication [J]. Science, 210 (4471): 801-803.
	Shackelford T K. 2016. Encyclopedia of Evolutionary Psychological Science [M]. Cham: Springer International Publishing, 1-5.
	Shannon G, Mckenna M F, Wilson‑Henjum G E, Angeloni L M, Crooks K R, Wittemyer G. 2020. Vocal characteristics of prairie dog alarm calls across an urban noise gradient [J]. Behavioral Ecology, 31 (2): 393-400.
	Shelley E L, Blumstein D T. 2005. The evolution of vocal alarm communication in rodents [J]. Behavioral Ecology, 16: 169-177.
	Sherman P W. 1977. Nepotism and the evolution of alarm calls: alarm calls of Belding’s ground squirrels warn relatives, and thus are expressions of nepotism [J]. Science, 197 (4310): 1246-1253.
	Sierro J, Gil D, Sáez‑Gómez P, Hidalgo‑Rodríguez P, Rabadán‑González J, Camacho C. 2024. Call for your life: acoustic structure and age‑sex differences in distress calls of red‑necked nightjars [J]. Ethology, 130 (12): e13513. DOI: 10.1111/eth.13513 .
	Slobodchikoff C N, Briggs W R, Dennis P A, Hodge A M C. 2012. Size and shape information serve as labels in the alarm calls of gunnison’s prairie dogs Cynomys gunnisoni [J]. Current Zoology, 58 (5): 741-748.
	Smith J M. 1965. The evolution of alarm calls [J]. American Naturalist, 99 (904): 59-63.
	Snowdon C T. 2020 Vervet monkey alarm calls: setting the historical context [J]. Animal Behavior and Cognition, 7 (2): 87-94.
	Stein R M, Rachlow J L. 2023. Acoustic ecology of terrestrial mammals: a new signaller‑receiver conceptual framework [J]. Mammal Review, 53: 143-157.
	Suzuki T N. 2018. Alarm calls evoke a visual search image of a predator in birds [J]. Proceedings of the National Academy of Sciences, 115 (7): 1541-1545.
	Tang‑Martínez Z. 2016. Rethinking Bateman’s principles: challenging persistent myths of sexually reluctant females and promiscuous males [J]. The Journal of Sex Research, 53 (4-5): 532-559.
	Taylor A M, Reby D. 2010. The contribution of source‑filter theory to mammal vocal communication research [J]. Journal of Zoology, 280 (3): 221-236.
	Taylor R J, Balph D F, Balph M H. 1990. The evolution of alarm calling: a cost‑benefit analysis [J]. Animal Behaviour, 39 (5): 860-868.
	Tchernichovski O, Marcus G. 2014. Vocal learning beyond imitation: mechanisms of adaptive vocal development in songbirds and human infants [J]. Current Opinion in Neurobiology, 28: 42-47.
	Thompson A B, Hare J F. 2010. Neighbourhood watch: multiple alarm callers communicate directional predator movement in Richardson’s ground squirrels, Spermophilus richardsonii [J]. Animal Behaviour, 80 (2): 269-275.
	Toledo L F D, Haddad F C B. 2009. Defensive vocalizations of neotropical anurans [J]. South American Journal of Herpetology, 4 (1): 25-42.
	Trefry S A, Hik D S. 2010. Variation in pika (Ochotona collaris, O. princeps) vocalizations within and between populations [J]. Ecography, 33 (4): 784-795.
	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, 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, 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.
	Volodin I A, Volodina E V, Frey R, Karaseva K D, Kirilyuk V E. 2021. Daurian pika (Ochotona dauurica) alarm calls: individual acoustic variation in a lagomorph with audible through ultrasonic vocalizations [J]. Journal of Mammalogy, 102 (3): 947-959.
	Vonk J. 2020. Forty years on from the question of referential signals in nonhuman communication [J]. Animal Behavior and Cognition, 7 (2): 82-86.
	Vu T T, Doherty P F, Nguyen H T, Clink D J, Nguyen M D, Dong H T, Cheyne S M, Giang T T, Phan D V, Ta N T, Tran D V. 2023. Passive acoustic monitoring using smartphones reveals an alarming gibbon decline in a protected area in the central Annamite Mountains, Vietnam [J]. American Journal of Primatology, 85 (11): e23544. DOI: 10.1002/ajp.23544 .
	Wang T T, Kong Y C, Zhang H, Li Y H, Hou R, Dunn D W, Hou X D, Huang K, Li B G. 2023. Do golden snub‑nosed monkeys use deceptive alarm calls during competition for food? [J]. iScience, 26 (2): 23. DOI: 10.1016/j.isci.2023.106098 .
	Wascher C A, Reynolds S. 2025. Vocal communication in corvids: a systematic review [J]. Animal Behaviour, 221: 123073. DOI: 10.1016/j.anbehav.2024.123073 .
	Watson S K, Zali M, Falk N, Widmer P, Manse M B. 2024. Inter‑call intervals, but not call durations, adhere to Menzerath’s law in the submissive vocal bouts of meerkats [J]. Royal Society Open Science, 11 (12): 241351. DOI: 10.1098/rsos.241351/v1/review2 .
	Watve M, Prati S, Taborsky B. 2019. Simulating more realistic predation threat using attack playbacks [J]. Peer J, 7 (6): e8149. DOI: 10.7717/peerj.8149 .
	Wheeler B C, Fischer J. 2012. Functionally referential signals: a promising paradigm whose time has passed [J]. Evolutionary Anthropology: Issues, News, and Reviews, 21 (5): 195-205.
	Wilkins M R, Seddon N, Safran R J. 2013. Evolutionary divergence in acoustic signals: causes and consequences [J]. Trends in Ecology and Evolution, 28 (3): 156-166.
	Wilson D R, Hare J F. 2004. Ground squirrel uses ultrasonic alarms [J]. Nature, 430 (6999): 523-523.
	Wilson‑Henjum G E, Job J R, Mckenna M F, Shannon G, Wittemyer G. 2019. Alarm call modification by prairie dogs in the presence of juveniles [J]. Journal of Ethology, 37 (2): 167-174
	Wyman M T, Walkenhorst B, Manser M B. 2022. Selection levels on vocal individuality: strategic use or byproduct [J]. Current Opinion in Behavioral Sciences, 46: 101140. DOI: 10.1016/j.cobeha.2022.101140 .
	Zhang C, Zheng Z, Lucas J R, Wang Y, Fan X, Zhao X, Feng J, Sun C, Jiang T. 2024. Do bats’ social vocalizations conform to Zipf’s law and the Menzerath‑Altmann Denlaw? [J]. iScience, 27 (7): 110401. DOI: 10.1016/j.isci.2024.110401 .
	Zhang H, Zhu B, Zhou Y, He Q, Sun X, Wang J, Cui J. 2021. Females and males respond differently to calls impaired by noise in a tree frog [J]. Ecology and Evolution, 11 (13): 9159-9167.
	Zhu B C, Qu J P, Cui J G. 2023. Plateau pikas near roads are bold and silent when facing a potential predator [J]. Current Zoology, 69 (5): 552-558
	Zuberbühler K. 2009. Survivor signals: the biology and psychology of animal alarm calling [J]. Advances in the Study of Behavior, 40 (9): 277-322.
	马梅娜, 花蕊, 包达尔罕, 叶国辉, 唐庄生, 花立民. 2024. 高原鼠兔警戒鸣声识别 [J].草原与草坪, 44 (5): 166-173.
	田苗, 夏灿玮. 2023. 回放实验在鸟类鸣声研究中的应用与设计 [J]. 北京师范大学学报 (自然科学版), 59 (4): 614-622.
	刘慕勋, 刘恒, 谭笑, 孙克萍, 冯江, 金龙如. 2017. 动物发声学习研究进展 [J]. 四川动物, 36 (3): 351-360.
	李昱. 2020. 东方蝙蝠声波发育的影响因素研究 [D]. 长春: 东北师范大学硕士学位论文.
	李强云, 吴金海, 斯日古楞, 张建平, 柳玉明, 肖治术, 苏军虎, 刘伟. 2025. 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, 45 (6): 797-809.
	肖治术. 2024. 被动声学技术在生物多样性监测与研究中的应用 [J]. 生物多样性, 32 (10): 4-8.
	汪松, 谢焱, 王家骏. 2001. 世界哺乳动物名典 (拉汉英) [M]. 长沙: 湖南教育出版社.
	张海珠, 刘永波, 狄建军, 张文, 赵新华, 姚花荣, 李红梅. 2005. 不同生长发育期的虎皮鹦鹉发声行为与发声控制神经核团的研究 [J]. 生物学杂志, 22 (6): 15-16.
	陈毅, 刘全生. 2016. 鼠类超声通讯在鼠害防治中的应用 [J]. 中国媒介生物学及控制杂志, 27 (4): 407-410.
	赵莹, 申小莉, 李晟, 张雁云, 彭任华, 马克平. 2020. 声景生态学研究进展和展望 [J]. 生物多样性, 28 (7): 806-820.
	费汉榄, 范朋飞, 向左甫, 马长勇, 张文, 黄涛. 2010. 东黑冠长臂猿鸣叫特征及气象因子对鸣叫的影响 [J]. 兽类学报, 30 (4): 377-383.
	蒋天一, 丁由中, 王正寰, 何桂芳, 赵金萍, 马凤琴, 王小明. 2011. 人为干扰下宁夏贺兰山岩羊反应的群体差异 [J]. 动物学研究, 32 (2): 157-162.
	魏万红, 曹伊凡, 张堰铭, 殷宝法, 王金龙. 2004. 捕食风险对高原鼠兔行为的影响 [J]. 动物学报, (3): 319-325.

[1]	Qiangyun LI, Jinhai WU, Siriguleng, Jianping ZHANG, Yuming LIU, Zhishu XIAO, Junhu SU, Wei LIU. Ecological adaptations of alarm calls in Brandt’s voles did not support the acoustic adaptation hypothesis [J]. ACTA THERIOLOGICA SINICA, 2025, 45(6): 797-809.
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[3]	ZHAO Yingchun SU Yanjie. Alarm Calls of Nonhuman Primates [J]. , 2005, 25(1): 81-85.

The production and evolutionary adaptation of alarm calls in small mammals: research progress and prospect

小型哺乳动物报警鸣叫的产生与进化适应：研究进展与展望

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