菲菊头蝠回声定位声波频率的性二态有利于性别识别
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摘要
许多动物的叫声频率呈现性二态现象。蝙蝠夜间活动,主要利用声音信号导航空间、追踪猎物、传递交流信息。本研究选择成体菲菊头蝠作为研究对象,检验回声定位声波频率性二态是否有利于性别识别。研究发现,菲菊头蝠回声定位声波频率参数具有显著性别差异。播放白噪音、雄性回声定位声波及雌性回声定位声波期间,实验个体的反应叫声数量依次递减。播放白噪音、雌性回声定位声波及雄性回声定位声波后,实验个体的反应叫声数量依次递增。白噪音诱导反应叫声强度高于回声定位声波诱导反应叫声强度。研究结果表明,菲菊头蝠回声定位声波的频率参数编码发声者性别信息,有利于种群内部的性别识别。本研究暗示,回声定位声波可能在蝙蝠配偶选择中扮演一定作用。
Sexual dimorphism in call frequency is widespread in a variety of animals. Despite possessing comparatively poor vision, bats conduct their activities at night. They primarily employ acoustic signals for spatial navigation, prey tracking, and social information transfer. Here, we use adult least horseshoe bats, Rhinolophus pusillus, to assess whether sexual dimorphism in the frequency of echolocation calls facilitates sex recognition. Analyses revealed that echolocation calls of R. pusillus showed marked gender differences in frequency parameters. In the playback periods, the number of response calls was the highest for white noise, followed by male echolocation call, and was the lowest for female echolocation call. The number of bat response calls, however, increased progressively after the playback of white noise, female echolocation call, and male echolocation call. The intensity of bat response calls showed a rapid decrease in the presence of white noise versus echolocation call stimuli. These results indicate that frequency parameters of echolocation calls encode information on caller sex in least horseshoe bats, which facilitates sex recognition within the population. Our findings provide some implications for the potential role of echolocation calls in mate choice in bats.
Sexual dimorphism in call frequency is widespread in a variety of animals. Despite possessing comparatively poor vision, bats conduct their activities at night. They primarily employ acoustic signals for spatial navigation, prey tracking, and social information transfer. Here, we use adult least horseshoe bats, Rhinolophus pusillus, to assess whether sexual dimorphism in the frequency of echolocation calls facilitates sex recognition. Analyses revealed that echolocation calls of R. pusillus showed marked gender differences in frequency parameters. In the playback periods, the number of response calls was the highest for white noise, followed by male echolocation call, and was the lowest for female echolocation call. The number of bat response calls, however, increased progressively after the playback of white noise, female echolocation call, and male echolocation call. The intensity of bat response calls showed a rapid decrease in the presence of white noise versus echolocation call stimuli. These results indicate that frequency parameters of echolocation calls encode information on caller sex in least horseshoe bats, which facilitates sex recognition within the population. Our findings provide some implications for the potential role of echolocation calls in mate choice in bats.
引文
Bailey N W, Zuk M. 2008. Acoustic experience shapes female mate choice in field crickets. Proceedings of the Royal Society B, 275(1651): 2645-2650.
Brinklv S, Kalko E K, Surlykke A. 2010. Dynamic adjustment of biosonar intensity to habitat clutter in the bat Macrophyllum macrophyllum (Phyllostomidae). Behavioral Ecology and Sociobiology, 64(11):1867-1874.
Brumm H, Slabbekoorn H. 2005. Acoustic communication in noise. Advances in the Study of Behavior, 35: 151-209.
Brumm H, Slater P J B. 2006. Animals can vary signal amplitude with receiver distance: evidence from zebra finch song. Animal Behaviour, 72(3):699-705.
Chen S F, Jones G, Rossiter S J. 2009. Determinants of echolocation call frequency variation in the Formosan lesser horseshoe bat (Rhinolophus monoceros). Proceedings of the Royal Society B, 276(1674): 3901-3909.
Eda-Fujiwara H, Yamamoto A, Sugita H, Takahashi Y, Kojima Y, Sakashita R, Ogawa H, Miyamoto T, Kimura T. 2004. Sexual dimorphism of acoustic signals in the oriental white stork: non-invasive identification of sex in birds. Zoological Science, 21 (8): 817-821.
Feng J.2001.Studies on Echolocating Behavior and Ecology in Bats.Changchun:Jilin Science & Technology Publishing House.(in Chinese)
Fitch W T, Hauser M. 2003. Unpacking “honesty”: vertebrate vocal production and the evolution of acoustic signals. In: Simmons A, Fay R, Popper A eds. Acoustic Communication. Springer New York, 65-137.
Fu Z Y, Dai X Y, Xu N, Shi Q, Li G J, Li B, Li J, Li J, Tang J, Jen H S. 2015. Sexual dimorphism in echolocation pulse parameters of the CF-FM bat, Hipposideros pratti. Zoological Studies, 54(5):1-9.
Gobes S M H, ter Haar S M, Vignal C, Vergne A L, Mathevon N, Bolhuis J J. 2009. Differential responsiveness in brain and behavior to sexually dimorphic long calls in male and female zebra finches. Journal of Comparative Neurology, 516(4): 312-320.
Grilliot M E, Burnett S C, Mendona M T. 2009. Sexual dimorphism in big brown bat (Eptesicus fuscus) ultrasonic vocalizations is context dependent. Journal of Mammalogy, 90(1): 203-209.
Guo X, Luo B, Liu Y, Jiang T L, Feng J. 2015. Cannot see you but can hear you: vocal identity recognition in microbats. Zoological Research, 36(5):257-262.
Hage S R, Jiang T L, Berquist S W, Feng J, Metzner W. 2013. Ambient noise induces independent shifts in call frequency and amplitude within the Lombard effect in echolocating bats. Proceedings of the National Academy of Sciences, 110(10): 4063-4068.
Jiang T L, Metzner W, You Y Y, Liu S, Lu G, Li S, Wang L, Feng J. 2010. Variation in the resting frequency of Rhinolophus pusillus in Mainland China: effect of climate and implications for conservation. Journal of the Acoustical Society of America, 128(4): 2204-2211.
Jones G, Siemers B M. 2010. The communicative potential of bat echolocation pulses. Journal of Comparative Physiology A, 197(5):447-457.
Kazial K A, Masters W M. 2004. Female big brown bats, Eptesicus fuscus, recognize sex from a caller’s echolocation signals. Animal Behaviour, 67(5): 855-863.
Knrnschild M, Jung K, Nagy M, Metz M, Kalko E. 2012. Bat echolocation calls facilitate social communication. Proceedings of the Royal Society B, 279(1748): 4827-4835.
Kunz T H, Fenton M B. 2003. Bat Ecology. University of Chicago Press, Chicago.
Liu Y, Metzner W, Feng J. 2013. Vocalization during copulation behavior in greater horseshoe bats, Rhinolophus ferrumequinum. Chinese Science Bulletin, 58(18): 2179-2184.
Luo J H, Goerlitz H R, Brumm H, Wiegrebe L. 2015. Linking the sender to the receiver: vocal adjustments by bats to maintain signal detection in noise. Scientific Reports, 5(1):18556.
Mechteld R B, Cate C T. 1997. Sex differences in the vocalizations and syrinx of the collared dove (Streptopelia decaocto).Auk, 114(1): 22-39.
Miller C T, Scarl J, Hauser M D. 2004. Sensory biases underlie sex differences in tamarin long call structure. Animal Behaviour, 68 (4): 713-720.
Neuweiler G, Metzner W, Heilmann U, Rübsamen R, Eckrich M, Costa H H. 1987. Foraging behaviour and echolocation in the rufous horseshoe bat (Rhinolophus rouxi) of Sri Lanka. Behavioral Ecology and Sociobiology, 20 (1): 53-67.
Patel E R, Owren M J. 2012. Silky sifaka (Propithecus candidus) “zzuss” vocalizations: Sexual dimorphism, individuality, and function in the alarm call of a monomorphic lemura). Journal of the Acoustical Society of America, 132 (3):1799-1810.
Puts D A, Gaulin S J, Verdolini K. 2006. Dominance and the evolution of sexual dimorphism in human voice pitch. Evolution and Human Behavior, 27(4):283-296.
Puts D A, Hill A K, Bailey D H, Walker R S, Rendall D, Wheatley J R, Welling L L M, Dawood K, Cárdenas R, Burriss R P, Jablonski N G, Shriver M D, Weiss D, Lameira A R, Apicella C L, Owren M J, Barelli C, Glenn M E, Ramos-Fernandez G. 2016. Sexual selection on male vocal fundamental frequency in humans and other anthropoids. Proceedings of the Royal Society of London B, 283(1829): 20152830.
Ryan M J. 1998. Sexual selection, receiver biases, and the evolution of sex differences. Science, 281(5385):1999-2003.
Schuchmann M, Puechmaille S J, Siemers B M. 2012. Horseshoe bats recognise the sex of conspecifics from their echolocation calls. Acta Chiropterologica, 14 (1): 161-166.
Siemers B M, Beedholm K, Dietz C, Dietz I, Ivanova T. 2005. Is species identity, sex, age or individual quality conveyed by echolocation call frequency in European horseshoe bats? Acta Chiropterologica, 7 (Sep 2005): 259-274.
Smith A T,Xie Y.2009. A Guide to the Mammals of China. Changsha: Hunan Education Press.(in Chinese)
Sun K P, Luo L, Kimball R T, Wei X W, Jin L R, Jiang T L, Li G H, Feng J. 2013. Geographic variation in the acoustic traits of greater horseshoe bats: testing the importance of drift and ecological selection in evolutionary processes. PLoS ONE, 8 (8): e70368.
Tobias M L, Viswanathan S S, Kelley D B. 1998. Rapping, a female receptive call, initiates male-female duets in the South African clawedfrog. Proceedings of the National Academy of Sciences, 95 (4): 1870-1875.
Wu H, Jiang T L, Huang X B, Feng J. 2018. Patterns of sexual size dimorphism in horseshoe bats: testing Rensch’s rule and potential causes. Scientific Reports, 8(1):2616.
Smith A T, 解焱. 2009. 中国兽类野外手册. 长沙:湖南教育出版社.
冯江. 2001. 蝙蝠回声定位行为生态研究. 长春:吉林科学技术出版社.
张劲硕, 李钢, 刘洋, 张俊鹏, 韩乃坚, 赵华斌, 张树义. 2007. 菲菊头蝠在中国北方的新纪录. 动物学杂志, 42 (6):102.
Brinklv S, Kalko E K, Surlykke A. 2010. Dynamic adjustment of biosonar intensity to habitat clutter in the bat Macrophyllum macrophyllum (Phyllostomidae). Behavioral Ecology and Sociobiology, 64(11):1867-1874.
Brumm H, Slabbekoorn H. 2005. Acoustic communication in noise. Advances in the Study of Behavior, 35: 151-209.
Brumm H, Slater P J B. 2006. Animals can vary signal amplitude with receiver distance: evidence from zebra finch song. Animal Behaviour, 72(3):699-705.
Chen S F, Jones G, Rossiter S J. 2009. Determinants of echolocation call frequency variation in the Formosan lesser horseshoe bat (Rhinolophus monoceros). Proceedings of the Royal Society B, 276(1674): 3901-3909.
Eda-Fujiwara H, Yamamoto A, Sugita H, Takahashi Y, Kojima Y, Sakashita R, Ogawa H, Miyamoto T, Kimura T. 2004. Sexual dimorphism of acoustic signals in the oriental white stork: non-invasive identification of sex in birds. Zoological Science, 21 (8): 817-821.
Feng J.2001.Studies on Echolocating Behavior and Ecology in Bats.Changchun:Jilin Science & Technology Publishing House.(in Chinese)
Fitch W T, Hauser M. 2003. Unpacking “honesty”: vertebrate vocal production and the evolution of acoustic signals. In: Simmons A, Fay R, Popper A eds. Acoustic Communication. Springer New York, 65-137.
Fu Z Y, Dai X Y, Xu N, Shi Q, Li G J, Li B, Li J, Li J, Tang J, Jen H S. 2015. Sexual dimorphism in echolocation pulse parameters of the CF-FM bat, Hipposideros pratti. Zoological Studies, 54(5):1-9.
Gobes S M H, ter Haar S M, Vignal C, Vergne A L, Mathevon N, Bolhuis J J. 2009. Differential responsiveness in brain and behavior to sexually dimorphic long calls in male and female zebra finches. Journal of Comparative Neurology, 516(4): 312-320.
Grilliot M E, Burnett S C, Mendona M T. 2009. Sexual dimorphism in big brown bat (Eptesicus fuscus) ultrasonic vocalizations is context dependent. Journal of Mammalogy, 90(1): 203-209.
Guo X, Luo B, Liu Y, Jiang T L, Feng J. 2015. Cannot see you but can hear you: vocal identity recognition in microbats. Zoological Research, 36(5):257-262.
Hage S R, Jiang T L, Berquist S W, Feng J, Metzner W. 2013. Ambient noise induces independent shifts in call frequency and amplitude within the Lombard effect in echolocating bats. Proceedings of the National Academy of Sciences, 110(10): 4063-4068.
Jiang T L, Metzner W, You Y Y, Liu S, Lu G, Li S, Wang L, Feng J. 2010. Variation in the resting frequency of Rhinolophus pusillus in Mainland China: effect of climate and implications for conservation. Journal of the Acoustical Society of America, 128(4): 2204-2211.
Jones G, Siemers B M. 2010. The communicative potential of bat echolocation pulses. Journal of Comparative Physiology A, 197(5):447-457.
Kazial K A, Masters W M. 2004. Female big brown bats, Eptesicus fuscus, recognize sex from a caller’s echolocation signals. Animal Behaviour, 67(5): 855-863.
Knrnschild M, Jung K, Nagy M, Metz M, Kalko E. 2012. Bat echolocation calls facilitate social communication. Proceedings of the Royal Society B, 279(1748): 4827-4835.
Kunz T H, Fenton M B. 2003. Bat Ecology. University of Chicago Press, Chicago.
Liu Y, Metzner W, Feng J. 2013. Vocalization during copulation behavior in greater horseshoe bats, Rhinolophus ferrumequinum. Chinese Science Bulletin, 58(18): 2179-2184.
Luo J H, Goerlitz H R, Brumm H, Wiegrebe L. 2015. Linking the sender to the receiver: vocal adjustments by bats to maintain signal detection in noise. Scientific Reports, 5(1):18556.
Mechteld R B, Cate C T. 1997. Sex differences in the vocalizations and syrinx of the collared dove (Streptopelia decaocto).Auk, 114(1): 22-39.
Miller C T, Scarl J, Hauser M D. 2004. Sensory biases underlie sex differences in tamarin long call structure. Animal Behaviour, 68 (4): 713-720.
Neuweiler G, Metzner W, Heilmann U, Rübsamen R, Eckrich M, Costa H H. 1987. Foraging behaviour and echolocation in the rufous horseshoe bat (Rhinolophus rouxi) of Sri Lanka. Behavioral Ecology and Sociobiology, 20 (1): 53-67.
Patel E R, Owren M J. 2012. Silky sifaka (Propithecus candidus) “zzuss” vocalizations: Sexual dimorphism, individuality, and function in the alarm call of a monomorphic lemura). Journal of the Acoustical Society of America, 132 (3):1799-1810.
Puts D A, Gaulin S J, Verdolini K. 2006. Dominance and the evolution of sexual dimorphism in human voice pitch. Evolution and Human Behavior, 27(4):283-296.
Puts D A, Hill A K, Bailey D H, Walker R S, Rendall D, Wheatley J R, Welling L L M, Dawood K, Cárdenas R, Burriss R P, Jablonski N G, Shriver M D, Weiss D, Lameira A R, Apicella C L, Owren M J, Barelli C, Glenn M E, Ramos-Fernandez G. 2016. Sexual selection on male vocal fundamental frequency in humans and other anthropoids. Proceedings of the Royal Society of London B, 283(1829): 20152830.
Ryan M J. 1998. Sexual selection, receiver biases, and the evolution of sex differences. Science, 281(5385):1999-2003.
Schuchmann M, Puechmaille S J, Siemers B M. 2012. Horseshoe bats recognise the sex of conspecifics from their echolocation calls. Acta Chiropterologica, 14 (1): 161-166.
Siemers B M, Beedholm K, Dietz C, Dietz I, Ivanova T. 2005. Is species identity, sex, age or individual quality conveyed by echolocation call frequency in European horseshoe bats? Acta Chiropterologica, 7 (Sep 2005): 259-274.
Smith A T,Xie Y.2009. A Guide to the Mammals of China. Changsha: Hunan Education Press.(in Chinese)
Sun K P, Luo L, Kimball R T, Wei X W, Jin L R, Jiang T L, Li G H, Feng J. 2013. Geographic variation in the acoustic traits of greater horseshoe bats: testing the importance of drift and ecological selection in evolutionary processes. PLoS ONE, 8 (8): e70368.
Tobias M L, Viswanathan S S, Kelley D B. 1998. Rapping, a female receptive call, initiates male-female duets in the South African clawedfrog. Proceedings of the National Academy of Sciences, 95 (4): 1870-1875.
Wu H, Jiang T L, Huang X B, Feng J. 2018. Patterns of sexual size dimorphism in horseshoe bats: testing Rensch’s rule and potential causes. Scientific Reports, 8(1):2616.
Smith A T, 解焱. 2009. 中国兽类野外手册. 长沙:湖南教育出版社.
冯江. 2001. 蝙蝠回声定位行为生态研究. 长春:吉林科学技术出版社.
张劲硕, 李钢, 刘洋, 张俊鹏, 韩乃坚, 赵华斌, 张树义. 2007. 菲菊头蝠在中国北方的新纪录. 动物学杂志, 42 (6):102.