马铁菊头蝠生长发育及交配期交流声波行为生态研究
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摘要
马铁菊头蝠(Rhinolophus ferrumequinum)主要生活在热带、亚热带和温带地区，分布于亚洲和欧洲大部分地区，在中国分布广泛。但是近年来，马铁菊头蝠种群数量急剧下降，在欧洲大部分地区成为濒危物种，已被IUCN红色物种名录列为较少关注(Least Concern)物种。马铁菊头蝠是翼手目中声纳系统进化最完善、声脉冲形式和发声行为多样性极高、发声和听觉神经系统最复杂的种类之一，一直是蝙蝠回声定位声波、行为生态学和神经生理学研究的主要对象。但是，关于马铁菊头蝠的生长发育和交流声波行为生态的研究还比较缺乏。
本论文通过野外实验与室内驯养蝙蝠相结合的方法，于2004年-2008年分别在吉林省集安地区及美国加州大学洛杉矶分校生理学系分别开展了马铁菊头蝠幼蝠体型与声波的个体发声学及交配期交流声波与行为研究，具体内容如下。
1．首次对中国境内马铁菊头蝠幼蝠出生时间与生长发育进行研究，并准确地定量估算年龄预测方程和生长曲线。研究发现吉林省集安市治安村大砬子洞内的马铁菊头蝠幼蝠出生时间为7月8日～7月23日。初生幼蝠身体无毛，眼睛紧闭，出生23天后，能够在洞内自由地飞行，出生33天后，第一次飞出山洞进行捕食。马铁菊头蝠幼蝠中，前臂长在前19天内呈直线增长，增长率为1.42 mm／day，体重在前11天内呈直线增长，增长率为0.54g／day，第四掌骨骺间距在出生后11天前呈直线增长，出生15天后呈直线下降。前臂长与骺间距分别是估算幼蝠出生前19天及第15-35天的年龄预测方程的最适参数，Logistic曲线是最适于描述幼蝠生长发育的非线性生长曲线。幼蝠生长发育能够直接反映母蝠的哺乳状态和种群的生存能力，是研究蝙蝠生活史的重要组成部分，本研究结果能够促进对其飞行、捕食、回声定位及交配等生态行为早期发育的研究，并为探讨影响幼体发育的因素和深入研究蝙蝠生长发育期的生理、生态和行为变化提供基础数据。
2．对马铁菊头蝠幼蝠声波特征随年龄的变化进行研究，并确定幼蝠声波个体发声学特征及母婴交流方式。马铁菊头蝠初生幼蝠发出2种多谐波(5-8个)、声波主频率(16.63±4.55kHz)较低的声波，一种为声脉冲时间较长(13.56±5.29ms)的不连续叫声，主要用于母婴交流，一种为声脉冲时间较短(3.28±0.49ms)的回声定位声波雏形，发育为回声定位声波。幼蝠声波主频率、声脉冲持续时间及各谐波频率均与前臂长呈显著正相关，声波谐波数随年龄增加而减少。幼蝠只在出生后前二周内发出伴有可听声的不连续叫声，随着幼蝠的生长，其叫声中可听声部分逐渐减少，年龄在2周以上的幼蝠只发出纯音超声波，带有可听声的不连续叫声主要用于母婴识别与交流。马铁菊头蝠母蝠只哺乳自己的幼蝠。本研究通过对马铁菊头蝠幼蝠在无母蝠干扰下自然发声声波随年龄发育的研究，发现马铁菊头蝠幼蝠既发出用于母婴交流的不连续声波，又发出回声定位声波雏形。这一结果对解决关于幼蝠发声类型的争议和明确蝙蝠回声定位声波的起源与发声的神经生理学机制具有重要意义。
3．首次对马铁菊头蝠交配过程中的交流声波与行为进行了录制与分析，并探讨其功能。成体雄蝠和雌蝠单独置于笼中后，雄蝠首先接近雌蝠，不断用翼或嘴碰触雌蝠，接触之后开始交配。交配时，雄蝠和雌蝠均倒挂在笼项，雄蝠弓起背部，用翼和后足从雌蝠背后抱住雌蝠。交配过程中，雄蝠在试图将阴茎插入雌蝠身体时发出短交配声波(16.48±4.8ms～17.79±4.03ms)，阴茎插入后交配过程中持续发出长交配声波(42.08±12.67ms～43.02±11.44ms)，2种类型的声波波型均较稳定。雌蝠在交配过程中很少发声，只在交配初始阶段偶尔发出带有噪音的交流声波。雄蝠交配时发出的波型和频率均较稳定的交配声波主要对雌蝠起到指示作用，向雌蝠传递求偶和安抚信号，可能是配偶重聚和识别的重要线索。研究结果是对被普遍忽视的蝙蝠声学交流行为的重要补充，能够为深入开展蝙蝠生殖行为生态学提供理论依据。
4．在8只马铁菊头蝠个体(6雄，2雌)中发现了短交流声波。在这8只个体中，回声定位声波主频变化较大，短交流声波的主频率相对稳定，且不同个体间的短交流叫声频率不同，每个个体都有自己相对固定的叫声频率。比较回声定位声波和短交流声波主频率和声脉冲持续时间的CV值显示，短交流声波主频率的CV值较稳定，不随回声定位声波主频率的CV值变化，而声脉冲持续时间的CV值则随回声定位声波的CV值变化较大。研究结果提出了一个从未被研究者发现的问题：蝙蝠的交流声波发声神经控制系统可能比其回声定位声波控制系统更精确，是关于蝙蝠交流声波发声的重要发现，能够为完善蝙蝠发声系统的神经生物学机制研究提供有力的行为生态学证据。
The greater horseshoe bat, Rhinolophus ferrumequinum maily inhabitats in tropic,semi-tropic and temperate zones, especially spreads widely in China. Recently, thepopulation decreasedly sharply. It has been the rare species in most European areas and hasbeen listed as the Least Concern species in the Red list of Rare Species by IUCN.Rhinolophus ferrumequinum is one of the species having the most developed sonar system,the most multiple echolocation calls and the most complex auditory neuron mechanisms,which makes it a focused object for studying on echolocation calls, behavioral ecology andneurophysiology. However, the studies on postnatal growth and communication calls arestill scarce.
From 2004 to 2008, we investigated on the ontogeny of morphology andvocalization and mating communication calls in infant and adult bats of Rhinolophusferrumequinum using methods of field studies and feeding bats in labs at Ji'an, China andDepartment of Neurophysiology, University of California, Los Angeles, USA, respectively.The details are as followed.
1. We quantified the length of the forearm, the body mass and the length of the totalgap of the fourth metacarpal-phalangeal joint of marked individuals of the greaterhorseshoe bat (Rhinolophus ferrumequinum) from birth to flight. By using these data, wedevelop empirical growth curves, derive growth rates, establish age-predictive equations,and compare growth parameters based on three nonlinear growth models. Young of R.ferrumequinum were born within a half-month period, with length of forearm averaging ca.42.31% of the size of adult females and body mass averaging ca. 30.75% of their mother'sbody mass. Length of forearm increased linearly until 19 days after birth (growth rate=1.42mm/day), as did body mass until 11 days after birth (growth rate=0.54g/day). Thelength of the total gap of the fourth metacarpal-phalangeal joint decreased linearly from 15days to 35 days of birth. Two most appropriate linear regression equations predicting theage of young bats were derived from forearm length from 1 to 19 days and the length ofthe epiphyseal gap from 15 to 35days. These two equations make it possible to estimate theage of pups from 1 to 35 days of age in R. ferrumequinum. Of the three nonlinear growthmodels (logistic, Gompertz, and von Bertalanffy), the logistic equation provides the best fitto the empirical curves for length of forearm and body mass. Postnatal growth has beenconsidered as an important trait for understanding the life history in mammals. Our resultsare important understanding various internal and external factors influencing the pattern of growth and provide the background data on the pattern of postnatal growth for bats fromChina. It also can reveal key aspects of physiology, behavior, and ecology of the bats.
2. We studied on the variation in infant vocalization with the age and themother-infant recognition in R. ferrumequinum. In contrast to adult bats, infant bats of thegreater horseshoe bat emitted calls characterized by multiharmonics and variable harmonicpatterns. With the physical growth of infants, the dominant frequency, pulse duration andfrequency of each harmonic of spontaneous calls increased, the number of harmonicsdecreased from 5-8 to 1-2 and dominant harmonic switched from first to the second withpeak frequency increasing. Vocalizations of infant bats of the greater horseshoe bat couldbe categorized to those serving as precursors of echolocation sounds (short calls:3.28±0.49ms) and those serving as isolation calls (long calls: 13.56±5.29ms) used to attracttheir mothers. According to observation on mother-infant reunion, the female adult batsonly suckled their own babies, but not other pups in the same colony. And the motherrecognized their own infants through both odor and vocal cues indicating that the isolationcalls emitted by infant bats played an important role in mother-infant communication. Thestudy is very significant for clarify the augment about the origin and vocalneurophysiology of echolocation calls in infant bats.
3. We initially recorded and analized the mating communication calls and behaviourin R. ferrumequinum, also discussing the fuction of the calls. When the adult male andfemale were put into a single small cage, the male one approached to the female, touchingher with his wings and mouth, and then they mated. Both the male and female hang on theceiling of the cage during mating. The male arched his back and surrounded the femalewith wings and hind feet from the back. The male emitted very short communication calls(16.48±4.8ms～17.79±4.03ms) when he tried to insert the pinnea into female and then keptemitting long communication calls (42.08±12.67ms～43.02±11.44ms) during the copulation.The female seldomly vocalled when mated. The female only emitted noise burstcommunication calls at the beginning of the copulation. We suggested that the matingcommunication calls of male bats play important roles in comforting females when theymating.
4. We found short communication calls in 8 individuals (6 males and 2 females). Inthese 8 individuals, the dominant frequency of their echolocation calls changed day by day,but the dominant frequency of the short communication calls was relatively constant.Although the dominant frequency of echolocation calls in some bats were overlapped, theyhave privacy constant dominant frequency in their short communication calls.Although thepulse durations of short communication calls were very short, they varied in a wide rangewith large value of SD, as well as those of echolocation calls. The pulse duration was notso constant as the dominant frequency of the short communication calls in the 8 bats. Comparing the CV value of dominant frequency and pulse duration between echolocationcalls and short communication calls showed that CV values of SCF were relativelyconstant, and they didn't change a lot with CV of ECF, while the CV values of durations ofshort communication calls changed greatly with CV of echolocation calls. The interestingpoint is that horseshoe bats which are famous for controlling their echolocation call CF inan extremely precise way (= Doppler-shift compensation) appear to vary this CF muchmore during echolocation than they do in their communication calls. Our result implies thatthe neural control mechanisms for communication calls have to function extremelyprecisely, which is something nobody has considered so far.
本论文通过野外实验与室内驯养蝙蝠相结合的方法，于2004年-2008年分别在吉林省集安地区及美国加州大学洛杉矶分校生理学系分别开展了马铁菊头蝠幼蝠体型与声波的个体发声学及交配期交流声波与行为研究，具体内容如下。
1．首次对中国境内马铁菊头蝠幼蝠出生时间与生长发育进行研究，并准确地定量估算年龄预测方程和生长曲线。研究发现吉林省集安市治安村大砬子洞内的马铁菊头蝠幼蝠出生时间为7月8日～7月23日。初生幼蝠身体无毛，眼睛紧闭，出生23天后，能够在洞内自由地飞行，出生33天后，第一次飞出山洞进行捕食。马铁菊头蝠幼蝠中，前臂长在前19天内呈直线增长，增长率为1.42 mm／day，体重在前11天内呈直线增长，增长率为0.54g／day，第四掌骨骺间距在出生后11天前呈直线增长，出生15天后呈直线下降。前臂长与骺间距分别是估算幼蝠出生前19天及第15-35天的年龄预测方程的最适参数，Logistic曲线是最适于描述幼蝠生长发育的非线性生长曲线。幼蝠生长发育能够直接反映母蝠的哺乳状态和种群的生存能力，是研究蝙蝠生活史的重要组成部分，本研究结果能够促进对其飞行、捕食、回声定位及交配等生态行为早期发育的研究，并为探讨影响幼体发育的因素和深入研究蝙蝠生长发育期的生理、生态和行为变化提供基础数据。
2．对马铁菊头蝠幼蝠声波特征随年龄的变化进行研究，并确定幼蝠声波个体发声学特征及母婴交流方式。马铁菊头蝠初生幼蝠发出2种多谐波(5-8个)、声波主频率(16.63±4.55kHz)较低的声波，一种为声脉冲时间较长(13.56±5.29ms)的不连续叫声，主要用于母婴交流，一种为声脉冲时间较短(3.28±0.49ms)的回声定位声波雏形，发育为回声定位声波。幼蝠声波主频率、声脉冲持续时间及各谐波频率均与前臂长呈显著正相关，声波谐波数随年龄增加而减少。幼蝠只在出生后前二周内发出伴有可听声的不连续叫声，随着幼蝠的生长，其叫声中可听声部分逐渐减少，年龄在2周以上的幼蝠只发出纯音超声波，带有可听声的不连续叫声主要用于母婴识别与交流。马铁菊头蝠母蝠只哺乳自己的幼蝠。本研究通过对马铁菊头蝠幼蝠在无母蝠干扰下自然发声声波随年龄发育的研究，发现马铁菊头蝠幼蝠既发出用于母婴交流的不连续声波，又发出回声定位声波雏形。这一结果对解决关于幼蝠发声类型的争议和明确蝙蝠回声定位声波的起源与发声的神经生理学机制具有重要意义。
3．首次对马铁菊头蝠交配过程中的交流声波与行为进行了录制与分析，并探讨其功能。成体雄蝠和雌蝠单独置于笼中后，雄蝠首先接近雌蝠，不断用翼或嘴碰触雌蝠，接触之后开始交配。交配时，雄蝠和雌蝠均倒挂在笼项，雄蝠弓起背部，用翼和后足从雌蝠背后抱住雌蝠。交配过程中，雄蝠在试图将阴茎插入雌蝠身体时发出短交配声波(16.48±4.8ms～17.79±4.03ms)，阴茎插入后交配过程中持续发出长交配声波(42.08±12.67ms～43.02±11.44ms)，2种类型的声波波型均较稳定。雌蝠在交配过程中很少发声，只在交配初始阶段偶尔发出带有噪音的交流声波。雄蝠交配时发出的波型和频率均较稳定的交配声波主要对雌蝠起到指示作用，向雌蝠传递求偶和安抚信号，可能是配偶重聚和识别的重要线索。研究结果是对被普遍忽视的蝙蝠声学交流行为的重要补充，能够为深入开展蝙蝠生殖行为生态学提供理论依据。
4．在8只马铁菊头蝠个体(6雄，2雌)中发现了短交流声波。在这8只个体中，回声定位声波主频变化较大，短交流声波的主频率相对稳定，且不同个体间的短交流叫声频率不同，每个个体都有自己相对固定的叫声频率。比较回声定位声波和短交流声波主频率和声脉冲持续时间的CV值显示，短交流声波主频率的CV值较稳定，不随回声定位声波主频率的CV值变化，而声脉冲持续时间的CV值则随回声定位声波的CV值变化较大。研究结果提出了一个从未被研究者发现的问题：蝙蝠的交流声波发声神经控制系统可能比其回声定位声波控制系统更精确，是关于蝙蝠交流声波发声的重要发现，能够为完善蝙蝠发声系统的神经生物学机制研究提供有力的行为生态学证据。
The greater horseshoe bat, Rhinolophus ferrumequinum maily inhabitats in tropic,semi-tropic and temperate zones, especially spreads widely in China. Recently, thepopulation decreasedly sharply. It has been the rare species in most European areas and hasbeen listed as the Least Concern species in the Red list of Rare Species by IUCN.Rhinolophus ferrumequinum is one of the species having the most developed sonar system,the most multiple echolocation calls and the most complex auditory neuron mechanisms,which makes it a focused object for studying on echolocation calls, behavioral ecology andneurophysiology. However, the studies on postnatal growth and communication calls arestill scarce.
From 2004 to 2008, we investigated on the ontogeny of morphology andvocalization and mating communication calls in infant and adult bats of Rhinolophusferrumequinum using methods of field studies and feeding bats in labs at Ji'an, China andDepartment of Neurophysiology, University of California, Los Angeles, USA, respectively.The details are as followed.
1. We quantified the length of the forearm, the body mass and the length of the totalgap of the fourth metacarpal-phalangeal joint of marked individuals of the greaterhorseshoe bat (Rhinolophus ferrumequinum) from birth to flight. By using these data, wedevelop empirical growth curves, derive growth rates, establish age-predictive equations,and compare growth parameters based on three nonlinear growth models. Young of R.ferrumequinum were born within a half-month period, with length of forearm averaging ca.42.31% of the size of adult females and body mass averaging ca. 30.75% of their mother'sbody mass. Length of forearm increased linearly until 19 days after birth (growth rate=1.42mm/day), as did body mass until 11 days after birth (growth rate=0.54g/day). Thelength of the total gap of the fourth metacarpal-phalangeal joint decreased linearly from 15days to 35 days of birth. Two most appropriate linear regression equations predicting theage of young bats were derived from forearm length from 1 to 19 days and the length ofthe epiphyseal gap from 15 to 35days. These two equations make it possible to estimate theage of pups from 1 to 35 days of age in R. ferrumequinum. Of the three nonlinear growthmodels (logistic, Gompertz, and von Bertalanffy), the logistic equation provides the best fitto the empirical curves for length of forearm and body mass. Postnatal growth has beenconsidered as an important trait for understanding the life history in mammals. Our resultsare important understanding various internal and external factors influencing the pattern of growth and provide the background data on the pattern of postnatal growth for bats fromChina. It also can reveal key aspects of physiology, behavior, and ecology of the bats.
2. We studied on the variation in infant vocalization with the age and themother-infant recognition in R. ferrumequinum. In contrast to adult bats, infant bats of thegreater horseshoe bat emitted calls characterized by multiharmonics and variable harmonicpatterns. With the physical growth of infants, the dominant frequency, pulse duration andfrequency of each harmonic of spontaneous calls increased, the number of harmonicsdecreased from 5-8 to 1-2 and dominant harmonic switched from first to the second withpeak frequency increasing. Vocalizations of infant bats of the greater horseshoe bat couldbe categorized to those serving as precursors of echolocation sounds (short calls:3.28±0.49ms) and those serving as isolation calls (long calls: 13.56±5.29ms) used to attracttheir mothers. According to observation on mother-infant reunion, the female adult batsonly suckled their own babies, but not other pups in the same colony. And the motherrecognized their own infants through both odor and vocal cues indicating that the isolationcalls emitted by infant bats played an important role in mother-infant communication. Thestudy is very significant for clarify the augment about the origin and vocalneurophysiology of echolocation calls in infant bats.
3. We initially recorded and analized the mating communication calls and behaviourin R. ferrumequinum, also discussing the fuction of the calls. When the adult male andfemale were put into a single small cage, the male one approached to the female, touchingher with his wings and mouth, and then they mated. Both the male and female hang on theceiling of the cage during mating. The male arched his back and surrounded the femalewith wings and hind feet from the back. The male emitted very short communication calls(16.48±4.8ms～17.79±4.03ms) when he tried to insert the pinnea into female and then keptemitting long communication calls (42.08±12.67ms～43.02±11.44ms) during the copulation.The female seldomly vocalled when mated. The female only emitted noise burstcommunication calls at the beginning of the copulation. We suggested that the matingcommunication calls of male bats play important roles in comforting females when theymating.
4. We found short communication calls in 8 individuals (6 males and 2 females). Inthese 8 individuals, the dominant frequency of their echolocation calls changed day by day,but the dominant frequency of the short communication calls was relatively constant.Although the dominant frequency of echolocation calls in some bats were overlapped, theyhave privacy constant dominant frequency in their short communication calls.Although thepulse durations of short communication calls were very short, they varied in a wide rangewith large value of SD, as well as those of echolocation calls. The pulse duration was notso constant as the dominant frequency of the short communication calls in the 8 bats. Comparing the CV value of dominant frequency and pulse duration between echolocationcalls and short communication calls showed that CV values of SCF were relativelyconstant, and they didn't change a lot with CV of ECF, while the CV values of durations ofshort communication calls changed greatly with CV of echolocation calls. The interestingpoint is that horseshoe bats which are famous for controlling their echolocation call CF inan extremely precise way (= Doppler-shift compensation) appear to vary this CF muchmore during echolocation than they do in their communication calls. Our result implies thatthe neural control mechanisms for communication calls have to function extremelyprecisely, which is something nobody has considered so far.
引文
[1] Simmons N B Order Chiroptera[A]. In: Wilson, D E,Reeder D M, eds. Mammal species of the world: a taxonomic and geographic reference[C], Maryland: The John Hopking University Press, 2005; 312-529.
[2] 张劲硕，张俊鹏，梁冰，et al．世界翼手目动物分类系统和种类最新报道[J]．动物学杂志，2005，40：79-79．
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