Ontogenesis of the echolocation system in the rufous horseshoe bat,Rhinolophus rouxi (Audition and vocalization in early postnatal development)

1. The development of vocalization and hearing was studied in Sri Lankan horseshoe bats (Rhinolophus rouxi) during the first postnatal month. The young bats were caught in a nursing colony of rhinolophids in which birth took place within a two week period. 2. The new-born bats emitted isolation calls through the mouth. At the beginning these calls consisted of pure tones with frequencies below 10 kHz (Fig. 1). During the first postnatal week the call frequency increased to about 15 kHz, and the fundamental was augmented by two to four harmonics. No evoked potentials to pure tone stimuli could be elicited in the inferior colliculus of this age group, i.e., auditory processing at the midbrain level was not demonstrable. 3. Evoked potentials were first recorded in the second week, broadly tuned to 15-45 kHz, with a maximum sensitivity between 15-25 kHz. In the course of the second week, however, higher frequencies up to 60 kHz became progressively incorporated into the audiogram (Fig. 3). The fundamental frequency of the multiharmonic isolation calls, emitted strictly through the mouth, increased to about 20 kHz. 4. In the bats' third postnatal week an increased hearing sensitivity (auditory filter) emerged, sharply tuned at frequencies between 57 and 60 kHz (Fig. 4e). The same individuals were also the first to emit long constant frequency echolocation calls through the nostrils (Fig. 4c). The energy of the calls was arranged in harmonic frequency bands with the second harmonic exactly tuned to the auditory filter. These young bats continued to emit isolation calls through the mouth, which were, however, not harmonically related to the echolocation calls (Fig. 4b, d). 5. During the fourth week, both the auditory filter and the matched echolocation pulses (the second harmonic) shifted towards higher frequencies (Fig. 5). During the fifth week the fundamental frequency of the calls was progressively attenuated, and both the second harmonic of the pulses and the auditory filter reached the frequency range typical for adult bats of 73-78 kHz (Fig. 6). 6. The development of audition and vocalization is discussed with regard to possible interactions of both subsystems, and their incorporation into the active orientation system of echolocation.     

Frequency alternation and an offbeat rhythm indicate foraging behavior in the echolocating bat, <Emphasis Type="Italic">Saccopteryx bilineata</Emphasis>

The greater sac-winged bat, Saccopteryx bilineata (Emballonuridae), uses two distinct echolocation call sequences: a ‘monotonous’ sequence, where bats emit ~48 kHz calls at a relatively stable rate, and a frequency-alternating sequence, where bats emit calls at ~45 kHz (low-note call) and ~48 kHz (high-note call). The frequencies of these low–high-note pairs remain stable within sequences. In Panama, we recorded echolocation calls from S. bilineata with a multi-microphone array at two sites: one a known roosting site, the other a known foraging site. Our results indicate that this species (1) only produces monotonous sequences in non-foraging contexts and, at times, directly after emitting a feeding buzz and (2) produces frequency-alternating sequences when actively foraging. These latter sequences are also characterized by an unusual, offbeat emission rhythm. We found significant positive relationships between (1) call intensity and call duration and (2) call intensity and distance from clutter. However, these relationships were weaker than those reported for bats from other families. We speculate on how call frequency alternation and an offbeat emission rhythm might reflect a novel strategy for prey detection at the edge of complex habitat in this ancient family of bats.     

Echolocation in the large molossid bats Eumops glaucinus and Nyctinomops macrotis

Eumops glaucinus and Nyctinomops macrotis, the largest molossid bats in Cuba, were investigated. Both species of bats share the same guild in the island and are similar in size, which allow the prediction of overlapping echolocation inventories following both the "vocal plasticity hypothesis" and the "scaling hypothesis." In addition, large body size predicts the emission of low frequency calls in the human audible range. Calls recorded during hunting show that the bats' echolocation repertoires are very similar and of low frequency, with most differences in search calls. Matches were found in the calls' design, duration, slope, bandwidth, and spectral parameters. Statistical differences between search calls are consistent with the predictions from the "scaling hypothesis," considering that E. glaucinus is only slightly larger than N. macrotis. The echolocation calls emitted by both species are in the frequency range below 20-25 kHz, which identifies both species as the only ones with echolocation in the human audible range in Cuba.     

Prey-Correlated Spectral Changes in Echolocation Sounds of the Indian False Vampire Megaderma lyra

False Vampires ( Megaderma lyra ) are gleaning bats which emit brief (1 ms) and faint echolocation signals consisting of four harmonics of a shallow frequency downward modulated fundamental (27–19 kHz). The complete signal spans a frequency range from 100 to 19 kHz. In sound recordings from three experimental animals we show that Megaderma lyra shifts the dominant frequency in the echolocation signals in relation to the type of prey offered and to flight style. During roaming flights the mean peak frequency was 63.2 ± 9 kHz (third harmonic). In prey catching flights, peak frequencies were shifted into the fourth harmonic. In flights towards a dish of crawling mealworms, mean peak frequency was raised to 91.2 ± 3.3 kHz. When the bats flew towards living mice the dominant frequency was further increased to 99.8 ± 5.2 kHz, and the second and third harmonic were at least 10 dB fainter or no longer recordable. The additional frequency shift when flying towards mice was not only a consequence of the dominance of the fourth harmonic but also of an additional rise of the fundamental harmonic by nearly 2 kHz. These prey-correlated frequency shifts in echolocation calls showed little variation between the three experimental animals and were reproducible over time. They occurred at or even before take-off of the bats. This is the first report of target-correlated transient adaptations in echolocation calls of any bat species.     

三种共栖蝙蝠的回声定位信号特征及其夏季食性的比较

2005年6至9月,对桂林市郊区两个山洞中高颅鼠耳蝠(Myotissiligorensis)、菲菊头蝠(Rhinolo-phuspusillus)和黑髯墓蝠(Taphozousmelanopogon)的回声定位叫声特征和食性进行分析,并结合其形态特征与野外观察,推断其捕食生境和捕食策略。研究结果发现:黑髯墓蝠体型最大,声音特征属短调频型多谐波,一般为4个谐波,能量主要集中在第二谐波上,主频率为(32·84±1·17)kHz,选择鞘翅目和双翅目昆虫为主要食物;高颅鼠耳蝠(长调频型)和菲菊头蝠(长恒频-调频型),体型都较小,主频率分别是(84·44±8·13)kHz和(110·78±1·65)kHz,以双翅目昆虫为主要食物;而菲菊头蝠则以鞘翅目和双翅目昆虫为主要食物。上述结果证明,高颅鼠耳蝠、菲菊头蝠和黑髯墓蝠在声音和食物组成等方面出现了明显分化。     

Emergence,Echolocation, Diet and Foraging Behavior of Molossus ater (Chiroptera: Molossidae)1

Between 4 and 16 January 1996, during a period of cool weather, we studied the emergence and foraging behavior of Molossus ater at a site near Akumal, in the Yucatan Peninsula in Mexico. The bats, a colony of at least 32 individuals, roosted in a north-facing cinder block wall, and emerged about sunset. Emerging bats were usually clustered in time, while those returning usually were not. Radio-tracking revealed that the bats foraged for short periods (mean 26.8 min) and captures of returning individuals indicated that 27 of 28 had fed, taking, on average, 4.4 g of insects, mainly hydrophilid beetles. On some nights, few or none of the radio-tagged bats emerged from the roost. Calculations concerning the costs of flight and roosting show that they were more than covered by the energy intake the bats achieved. Molossus ater have high aspect ratio (8.3–9.1) wings and high wing-loadings of 17.55–24.15 N/m². When searching for prey, these bats produce long (12.3 ms), narrowband(3.8 kHz), echolocation calls that sweep from 27.6–23.8 kHz. Energy was not limiting for these bats at the time of our study.     

皮氏菊头蝠回声定位声波与年龄的关系

皮氏菊头蝠 (Rhinolophuspearsoni)雌性成体 5只和幼体 2只采自贵州省贞丰县珉谷镇。采用超声波探测仪 (D980 ,ULTRASOUNDDETECTOR)接收皮氏菊头蝠的回声定位声波 ,转换到原频率的 1 / 1 0后导入计算机 ,然后用专业声谱分析软件 (Batsound 3 1 0 )进行分析。成蝠在飞行和悬挂状态下的声波结构相似 ,只是声波各项参数值略有不同 :它们发射FM CF FM型声波 ,具有 2～ 3个谐波 ,主频率在飞行时为 5 6 80± 0 6 2kHz ,悬挂时为 5 8 0 5± 0 2 4kHz ;声脉冲时间和间隔在飞行时分别为 3 4 6 2± 5 2 9ms和 86 5 0± 1 9 72ms ,悬挂时分别为 4 1 0 8± 5 87ms和 1 1 7 2 9± 6 6 4 4ms ;能率环飞行时为 ( 4 4 0 6± 1 2 5 8) % ,悬挂时为 ( 4 6 0 0±2 4 2 5 ) %。幼蝠声波为CF FM型 ,谐波数为 5～ 8个 ,主频率明显低于成体 ,FM带宽窄于成体 ,声脉冲时间和间隔短于成体 ,能率环低于成体。皮氏菊头蝠回声定位声波与年龄有关 ,这可能因成体的声波主要是探测食物和周围环境的详细信息 ,而幼体主要是与母蝠进行交流。     

Variation in the Sonar of an Aerial-hawking Bat (Eptesicus nilssonii)

Echolocation calls from 10 individually marked female northern bats (Eptesicus nilssonii) were recorded as the bats foraged at three distinct feeding sites (territories) near their maternity roost in southern Sweden (57° N). In addition, recordings of unmarked bats were made in northern Sweden (65° N). The frequency at maximum amplitude of “search phase” echolocation pulses was bimodally distributed, with peaks around 29–30 kHz and 31–32 kHz and was negatively correlated with pulse duration. The frequency at maximum amplitude was related to flight altitude (bats used higher frequencies when they flew near the ground) and also differed among the feeding sites. Hence, much of the variation, probably including regional differences, was behavioural and is interpreted as short term (in the order of s or min) adaptation to current foraging situations. Variation among individual bats, caused by age and size, seemed to be of less importance. Individuals did not use exclusive frequency bands.     

南蝠回声定位叫声的分析

蝙蝠科是翼手目中种类最繁多、分布最广泛、进化最成功的科之一 ,全球共有 42属 35 5种(Ｎｏｗａｋ ,1991)。该类群的大多数物种都以超声波回声定位来进行捕食 ,其回声定位行为的多样性以及捕食策略的多样性 ,一直都是动物生态学中的研究热点。南蝠 (Ｉａｉｏ)属蝙蝠科南蝠属 ,为单型种 ,主要分布于我国 (罗蓉等 ,1993)。它是蝙蝠科中体形最大者 ,以前对其生态学方面的研究非常少 ,而对其回声定位的研究则未见报道。南蝠捕食时的叫声与飞行及悬挂状态下的叫声的基本特征一致 (声谱图及谐波等 ) ,仅在叫声次数上有一定差异。因此本文将录制南…     

Auditory sensitivity and frequency selectivity in greater spear-nosed bats suggest specializations for acoustic communication

We investigated the relationship between auditory sensitivity, frequency selectivity, and the vocal repertoire of greater spear-nosed bats (Phyllostomus hastatus). P. hastatus commonly emit three types of vocalizations: group-specific foraging calls that range from 6 to 11 kHz, low amplitude echolocation calls that sweep from 80 to 40 kHz, and infant isolation calls from 15 to 100 kHz. To determine if hearing in P. hastatus is differentially sensitive or selective to frequencies in these calls, we determined absolute thresholds and masked thresholds using an operant conditioning procedure. Both absolute and masked thresholds were lowest at 15 kHz, which corresponds with the peak energy of isolation calls. Auditory and masked thresholds were higher at sound frequencies used for group-specific foraging calls and echolocation calls. Isolation calls meet the requirements of individual signatures and facilitate parent-offspring recognition. Many bat species produce isolation calls with peak energy between 10 and 25 kHz, which corresponds with the frequency region of highest sensitivity in those species for which audiogram data are available. These findings suggest that selection for accurate offspring recognition exerts a strong influence on the sensory system of P. hastatus and likely on other species of group-living bats.     

大蹄蝠回声定位信号特征与下丘神经元频率调谐

采用超声监测仪录制超声信号和细胞外电生理记录下丘神经元的频率调谐曲线(frequency tuningcurqes,FTCs)的方法,探讨了大蹄蝠(Hipposideros armiger)回声定位信号与下丘(inferior colliculus,IC)神经元频率调谐之间的相关性.结果发现,大蹄蝠回声定位叫声为恒频-调频(consrant frequency-frequenevmodulated,CF-FM)信号,一般含有2-3个谐波,第二谐波为其主频,cF成分频率(Mean±SD,n=18)依次为:(33.3 4±0.2)、(66.5±0.3)、(99.4 4±0.5)kHz;电生理实验共获得72个神经元的频率调谐曲线,Q10-dB值的范围是0.5-95.4(9.2±14.6,rg=72),最佳频率(best frequency,BF)在回声定位主频附近的神经元具有尖锐的频率调谐特性.结果表明,大蹄蝠回声定位信号与下丘神经元频率调谐存在相关性,表现为最佳频率在回声定位信号主频附近的神经元频率调谐曲线的Q10-dB值较大,具有很强的频率分析能力.     

普通长翼蝠食性结构及其回声定位与体型特征

在普通长翼蝠(Miniopterus fuliginosus)的捕食区内用灯诱法和网捕法调查潜在食物(昆虫)种类; 用粪便分析法鉴定普通长翼蝠的食物组成,发现其主要捕食体型较大的鳞翅目和鞘翅目昆虫,体积百分比分别为55%和38%.普通长翼蝠具有相对狭长的翼,翼展比为6.94 ± 0.13;翼载为(9.85 ± 0.83)N/m2,相对较大.飞行状态下普通长翼蝠的回声定位叫声为调频下扫型,声脉冲时程为(1.45 ± 0.06)ms,脉冲间隔为(63.08 ± 21.55)ms,主频较低,为(44.50 ± 2.26)kHz.研究表明,普通长翼蝠的形态特征和回声定位特征与其捕食行为有着密切的联系.     

Different Auditory Feedback Control for Echolocation and Communication in Horseshoe Bats

Auditory feedback from the animal''s own voice is essential during bat echolocation: to optimize signal detection, bats continuously adjust various call parameters in response to changing echo signals. Auditory feedback seems also necessary for controlling many bat communication calls, although it remains unclear how auditory feedback control differs in echolocation and communication. We tackled this question by analyzing echolocation and communication in greater horseshoe bats, whose echolocation pulses are dominated by a constant frequency component that matches the frequency range they hear best. To maintain echoes within this “auditory fovea”, horseshoe bats constantly adjust their echolocation call frequency depending on the frequency of the returning echo signal. This Doppler-shift compensation (DSC) behavior represents one of the most precise forms of sensory-motor feedback known. We examined the variability of echolocation pulses emitted at rest (resting frequencies, RFs) and one type of communication signal which resembles an echolocation pulse but is much shorter (short constant frequency communication calls, SCFs) and produced only during social interactions. We found that while RFs varied from day to day, corroborating earlier studies in other constant frequency bats, SCF-frequencies remained unchanged. In addition, RFs overlapped for some bats whereas SCF-frequencies were always distinctly different. This indicates that auditory feedback during echolocation changed with varying RFs but remained constant or may have been absent during emission of SCF calls for communication. This fundamentally different feedback mechanism for echolocation and communication may have enabled these bats to use SCF calls for individual recognition whereas they adjusted RF calls to accommodate the daily shifts of their auditory fovea.     

Feeding behaviour of the bats Nycteris grandis and Nycteris thebaica (Nycteridae) in captivity

The feeding and hunting behaviour of Nycteris grandis and N. thebaica was observed in captivity at the Sengwa Wildlife Research Area in Zimbabwe in January and February 1982. Both species preferentially selected katydids and beetles over moths, and relied heavily on acoustic stimuli emanating from prey to detect targets. Nycteris grandis readily consumed frogs and bats and appeared not to use the calls of male frogs or the echolocation calls of other bats to locate prey. Both species produced echolocation calls during attacks on prey, increasing the rates of pulse repetition as they closed with targets and suggesting the use of echolocation in hunting. The echolocation calls of N. grandis are described along with general observations of the behaviour of both species.     

Social calls used by a leaf-roosting bat to signal location

Social calls in bats have many functions, including mate attraction and maintaining contact during flight. Research suggests that social calls may also be used to transfer information about roosts, but no studies have yet demonstrated that calls are used to actively attract conspecifics to roosting locations. We document the social calls used by Spix''s disc-winged bat (Thyroptera tricolor) to actively recruit group members to roosts. In acoustic trials, we recorded two sets of calls; one from flying individuals termed ‘inquiry calls’, and another from roosting bats termed ‘response calls’. Inquiry calls were emitted by flying bats immediately upon release, and quickly (i.e. 178 ms) elicited production of response calls from roosting individuals. Most flying bats entered the roost when roosting individuals responded, while few bats entered the roost in the absence of a response. We argue that information transfer concerning roost location may facilitate sociality in T. tricolor, given the ephemeral nature of roosting structures used by this species.     

Female big brown bats, Eptesicus fuscus, recognize sex from a caller's echolocation signals

The echolocation calls of bats function in prey capture and navigation but are not commonly regarded as communicative signals. However, because bats' echolocation calls show patterns of variability, they may transmit information about a bat, such as its age, individual identity or sex. For echolocation calls to function in this manner, variation in calls must be reliably linked to the characteristics of the bat, as has been shown in a number of studies. However, few studies have asked whether bats respond to this variation. We tested whether female big brown bats can identify the sex of an unfamiliar bat from playbacks of its echolocation calls. Playback consisted of a 30-s preplayback period, a 60-s playback period of either male or female echolocation calls, and a 30-s postplayback period. In the playback and postplayback periods the vocalization rates of female bats changed significantly relative to the preplayback period depending on the sex of the playback stimulus, indicating that they could determine sex from the echolocation calls. These findings support the possibility that echolocation calls play a role in communication in big brown bats.     

Genetic divergence and echolocation call frequency in cryptic species of Hipposideros larvatus s.l. (Chiroptera: Hipposideridae) from the Indo-Malayan region

The intermediate leaf-nosed bat ( Hipposideros larvatus ) is a medium-sized bat distributed throughout the Indo-Malay region. In north-east India, bats identified as H. larvatus captured at a single cave emitted echolocation calls with a bimodal distribution of peak frequencies, around either 85 kHz or 98 kHz. Individuals echolocating at 85 kHz had larger ears and longer forearms than those echolocating at 98 kHz, although no differences were detected in either wing morphology or diet, suggesting limited resource partitioning. A comparison of mitochondrial control region haplotypes of the two phonic types with individuals sampled from across the Indo-Malay range supports the hypothesis that, in India, two cryptic species are present. The Indian 98-kHz phonic bats formed a monophyletic clade with bats from all other regional populations sampled, to the exclusion of the Indian 85-kHz bats. In India, the two forms showed 12–13% sequence divergence and we propose that the name Hipposideros khasiana for bats of the 85-kHz phonic type. Bats of the 98-kHz phonic type formed a monophyletic group with bats from Myanmar, and corresponded to Hipposideros grandis , which is suggested to be a species distinct from Hipposideros larvatus . Differences in echolocation call frequency among populations did not reflect phylogenetic relationships, indicating that call frequency is a poor indicator of evolutionary history. Instead, divergence in call frequency probably occurs in allopatry, possibly augmented by character displacement on secondary contact to facilitate intraspecific communication.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 119–130.     

菲菊头蝠回声定位声波频率的性二态有利于性别识别

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。     

两种同域分布蹄蝠在开阔度不同的环境中回声定位声波的可塑性

在广西桂林研究了同域分布的大蹄蝠(Hipposideros armiger)和中蹄蝠(H.larvatus)在不同开阔度环境中回声定位声波信号的变化。用超声波仪录制自由悬挂和分别释放于人工"大棚"和"小棚"内飞行的蝙蝠的回声定位声波,使用超声分析软件分析声脉冲时程、主频率及声脉冲间隔,通过重复测量方差分析比较不同状态下的声波参数。结果表明:中蹄蝠声波的主频在悬挂状态下最高,小棚内飞行时次之,大棚内飞行最低;两种蹄蝠声波的脉冲时程和脉冲间隔在悬挂状态下最长,大棚内飞行次之,小棚内飞行最低。总之,这两种蹄蝠的回声定位声波能够随所处状态的变化而变化,可根据生境的复杂度调节声讯号,具有明显的声波可塑性。