Classification of insects by echolocating greater horseshoe bats

Summary Echolocating greater horseshoe bats (Rhinolophus ferrumequinum) detect insects by concentrating on the characteristic amplitude- and frequency modulation pattern fluttering insects impose on the returning echoes. This study shows that horseshoe bats can also further analyse insect echoes and thus recognize and categorize the kind of insect they are echolocating.Four greater horseshoe bats were trained in a twoalternative forced-choice procedure to choose the echo of one particular insect species turning its side towards the bat (Fig. 1). The bats were able to discriminate with over 90% correct choices between the reward-positive echo and the echoes of other insect species all fluttering with exactly the same wingbeat rate (Fig. 4).When the angular orientation of the reward-positive insect was changed (Fig. 2), the bats still preferred these unknown echoes over echoes from other insect species (Fig. 5) without any further training. Because the untrained bats did not show any prey preference, this indicates that the bats were able to perform an aspect-anglein-dependent classification of insects.Finally we tested what parameters in the echo were responsible for species recognition. It turned out that the bats especially used the small echo-modulations in between glints as a source of information (Fig. 7). Neither the amplitudenor the frequencymodulation of the echoes alone was sufficient for recognition of the insect species (Fig. 8). Bats performed a pattern recognition task based on complex computations of several acoustic parameters, an ability which might be termed cognitive.Abbreviations AM amplitude modulation - CF constant frequency - FM frequency modulation - S+ positive stimulus - S- negative stimulus     

Echolocation behavior of the Japanese horseshoe bat in pursuit of fluttering prey

Echolocation sounds of Rhinolophus ferrumequinum nippon as they approached a fluttering moth (Goniocraspidum pryeri) were investigated using an on-board telemetry microphone (Telemike). In 40?% of the successful moth-capture flights, the moth exhibited distinctive evasive flight behavior, but the bat pursued the moth by following its flight path. When the distance to the moth was approximately 3-4?m, the bats increased the duration of the pulses to 65-95?ms, which is 2-3 times longer than those during landing flight (30-40?ms). The mean of 5.8 long pulses were emitted before the final buzz phase of moth capture, without strengthening the sound pressure level. The mean duration of long pulses (79.9?±?7.9?ms) corresponded to three times the fluttering period of G. pryeri (26.5?×?3?=?79.5?ms). These findings indicate that the bats adjust the pulse duration to increase the number of temporal repetitions of fluttering information rather than to produce more intense sonar sounds to receive fine insect echoes. The bats exhibited Doppler-shift compensation for echoes returning from large static objects ahead, but not for echoes from target moths, even though the bats were focused on capturing the moths. Furthermore, the echoes of the Telemike recordings from target moths showed spectral glints of approximately 1-1.5?kHz caused by the fluttering of the moths but not amplitude glints because of the highly acoustical attenuation of ultrasound in the air, suggesting that spectral information may be more robust than amplitude information in echoes during moth capturing flight.     

降雨噪声对菲菊头蝠出飞行为的影响

降雨噪声属于常见的自然噪声,由雨滴撞击物体表面产生。目前,有关降雨噪声对动物的潜在影响被普遍忽视。回声定位蝙蝠主要利用声信号在黑暗环境导航空间、探测猎物及社群交流,是开展降雨噪声影响研究的理想类群。本研究选择菲菊头蝠 (Rhinolophus pusillus)作为研究对象,检验降雨噪声是否影响蝙蝠出飞行为。我们在集群栖息地外,播放强降雨噪声、空白对照和种内回声定位声波,开展野外回放实验。利用单因素方差分析及其事后检验,评价菲菊头蝠对不同回放刺激的反应差异。研究发现,相比空白对照,强降雨噪声导致菲菊头蝠的通勤数量百分比平均降低2.82倍,回声定位脉冲数量平均减少4.86倍,集群出飞时间延长3.75 min。相比空白对照,同种回声定位声波对菲菊头蝠出飞行为的影响并不显著。研究结果证实强降雨噪声抑制菲菊头蝠的出飞行为。本研究表明,降雨引起 的噪声干扰可能是导致蝙蝠躲避降雨的重要因素,为野生蝙蝠物种保育与管理提供启示。     

Echolocation range and wingbeat period match in aerial-hawking bats

Aerial-hawking bats searching the sky for prey face the problem that flight and echolocation exert independent and possibly conflicting influences on call intervals. These bats can only exploit their full echolocation range unambiguously if they emit their next call when all echoes from the preceding call would have arrived. However, not every call interval is equally available. The need to reduce the high energetic costs of echolocation forces aerial-hawking bats to couple call emission to their wingbeat. We compared the wingbeat periods of 11 aerial-hawking bat species with the delays of the last-expected echoes. Acoustic flight-path tracking was employed to measure the source levels (SLs) of echolocation calls in the field. SLs were very high, extending the known range to 133 dB peak equivalent sound pressure level. We calculated the maximum detection distances for insects, larger flying objects and background targets. Wingbeat periods were derived from call intervals. Small and medium-sized bats in fact matched their maximum detection range for insects and larger flying targets to their wingbeat period. The tendency to skip calls correlated with the species' detection range for background targets. We argue that a species' call frequency is at such a pitch that the resulting detection range matches their wingbeat period.     

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.     

The nuclei of the lateral lemniscus in the rufous horseshoe bat,Rhinolophus rouxi

In the rufous horseshoe bat, Rhinolophus rouxi, responses to pure tones and sinusoidally frequency modulated (SFM) signals were recorded from 289 single units and 241 multiunit clusters located in the nuclei of the lateral lemniscus (NLL). The distribution of best frequencies (BFs) of units in all three nuclei of the lateral lemniscus showed an overrepresentation in the range corresponding to the constant-frequency (CF) part of the echolocation signal ('filter frequency' range): in the ventral nucleus of the lateral lemniscus (VNLL) 'filter neurons' represented 43% of all units encountered, in the intermediate nucleus (INLL) 33%, and in dorsal nucleus (DNLL) 29% (Fig. 2a). Neurons with best frequencies in the filter frequency range had highest Q10dB-values (maxima up to 400, Fig. 2c) and only in low-frequency units were values comparable to those found in other mammals. On the average, filter neurons in ventral nucleus had higher Q10dB-values (about 220) than did those in intermediate and dorsal nucleus (both about 160, Fig 2d). Response patterns and tuning properties showed higher complexity in the dorsal and intermediate nucleus than in the ventral nucleus of the lateral lemniscus (Figs. 4 and 6). Multiple best frequencies were found in 12 neurons, nine of them with harmonically related excitation maxima (Fig. 5c, d). Best frequencies of six of these harmonically tuned units could not be correlated with any harmonic components of the echolocation signal. Half of all multiple tuned neurons were located in the caudal dorsal nucleus the other half in the caudal intermediate nucleus. Synchronization of responses to sinusoidally frequency modulated (SFM) signals occurred in VNLL-units in the average up to modulation frequencies of 515 Hz (maximum about 800 Hz) whereas in the intermediate and dorsal nucleus of the lateral lemniscus responses were synchronized in the average only up to modulation frequencies of about 300 Hz (maximum about 600 Hz) (Figs. 7 and 8). A tonotopic arrangement of units was found in the intermediate nucleus of the lateral lemniscus with units having high best frequencies located medially and those with low best frequencies laterally. In the dorsal nucleus the tonotopic distribution was found to be fairly similar to that in the intermediate nucleus but much less pronounced. In more rostral parts of the dorsal nucleus additionally higher best frequencies predominated whereas in caudal areas of that nucleus and also of the intermediate nucleus low BFs were found more regularly.(ABSTRACT TRUNCATED AT 400 WORDS)     

Experimental evidence for group hunting via eavesdropping in echolocating bats

Group foraging has been suggested as an important factor for the evolution of sociality. However, visual cues are predominantly used to gain information about group members'' foraging success in diurnally foraging animals such as birds, where group foraging has been studied most intensively. By contrast, nocturnal animals, such as bats, would have to rely on other cues or signals to coordinate foraging. We investigated the role of echolocation calls as inadvertently produced cues for social foraging in the insectivorous bat Noctilio albiventris. Females of this species live in small groups, forage over water bodies for swarming insects and have an extremely short daily activity period. We predicted and confirmed that (i) free-ranging bats are attracted by playbacks of echolocation calls produced during prey capture, and that (ii) bats of the same social unit forage together to benefit from passive information transfer via the change in group members'' echolocation calls upon finding prey. Network analysis of high-resolution automated radio telemetry confirmed that group members flew within the predicted maximum hearing distance 94±6 per cent of the time. Thus, echolocation calls also serve as intraspecific communication cues. Sociality appears to allow for more effective group foraging strategies via eavesdropping on acoustical cues of group members in nocturnal mammals.     

Noseleaf dynamics during pulse emission in horseshoe bats

Horseshoe bats emit their biosonar pulses nasally and diffract the outgoing ultrasonic waves by conspicuous structures that surrounded the nostrils. Here, we report quantitative experimental data on the motion of a prominent component of these structures, the anterior leaf, using synchronized laser Doppler vibrometry and acoustic recordings in the greater horseshoe bat (Rhinolophus ferrumequinum). The vibrometry data has demonstrated non-random motion patterns in the anterior leaf. In these patterns, the outer rim of the walls of the anterior leaf twitches forward and inwards to decrease the aperture of the noseleaf and increase the curvature of its surfaces. Noseleaf displacements were correlated with the emitted ultrasonic pulses. After their onset, the inward displacements increased monotonically towards their maximum value which was always reached within the duration of the biosonar pulse, typically towards its end. In other words, the anterior leaf's surfaces were moving inwards during most of the pulse. Non-random motions were not present in all recorded pulse trains, but could apparently be switched on or off. Such switches happened between sequences of consecutive pulses but were never observed between individual pulses within a sequence. The amplitudes of the emitted biosonar pulse and accompanying noseleaf movement were not correlated in the analyzed data set. The measured velocities of the noseleaf surface were too small to induce Doppler shifts of a magnitude with a likely significance. However, the displacement amplitudes were significant in comparison with the overall size of the anterior leaf and the sound wavelengths. These results indicate the possibility that horseshoe bats use dynamic sensing principles on the emission side of their biosonar system. Given the already available evidence that such mechanisms exist for biosonar reception, it may be hypothesized that time-variant mechanisms play a pervasive role in the biosonar sensing of horseshoe bats.     

Fine control of call frequency by horseshoe bats

The auditory system of horseshoe bats is narrowly tuned to the sound of their own echoes. During flight these bats continuously adjust the frequency of their echolocation calls to compensate for Doppler-effects in the returning echo. Horseshoe bats can accurately compensate for changes in echo frequency up to 5 kHz, but they do so through a sequence of small, temporally-independent, step changes in call frequency. The relationship between an echo's frequency and its subsequent impact on the frequency of the very next call is fundamental to how Doppler-shift compensation behavior works. We analyzed how horseshoe bats control call frequency by measuring the changes occurring between many successive pairs of calls during Doppler-shift compensation and relating the magnitude of these changes to the frequency of each intervening echo. The results indicate that Doppler-shift compensation is mediated by a pair of (echo)frequency-specific sigmoidal functions characterized by a threshold, a slope, and an upper limit to the maximum change in frequency that may occur between successive calls. The exact values of these parameters necessarily reflect properties of the underlying neural circuitry of Doppler-shift compensation and the motor control of vocalization, and provide insight into how neural feedback can accommodate the need for speed without sacrificing stability.     

Echolocation call description of 15 species of Middle-Eastern desert dwelling insectivorous bats

Modern advances in acoustic technology have made possible new and broad ranges of research in bioacoustics, particularly with regard to echolocating bats. In the present study, we present an acoustic guide to the calls of 15 species of bats in the Arava rift valley, Israel, with a focus on their bioacoustics, habitat use and explaining differences between similar species. We also describe a potential case of frequency separation where four bat species using six call types appear to separate the frequencies of their calls to minimize overlap. The studied community of bat species is also found in other Middle Eastern deserts including the deserts of Jordan, Syria and Saudi Arabia and we hope that data gathered will benefit other bat researchers in the region.     

Control of echolocation pulses by neurons of the nucleus ambiguus in the rufous horseshoe bat,Rhinolophus rouxi

Horseradish peroxidase was applied by inotophoretic injections to physiologically identified regions of the laryngeal motor nucleus, the nucleus ambiguus in the CF/FM bat Rhinolophus rouxi. The connections of the nucleus ambiguus were analysed with regards to their possible functional significance in the vocal control system, in the respiration control system, and in mediating information from the central auditory system. The nucleus ambiguus is reciprocally interconnected with nuclei involved in the generation of the vocal motor pattern, i.e., the homonomous contralateral nucleus and the area of the lateral reticular formation. Similarly, reciprocal connections are found with the nuclei controlling the rhythm of respiration, i.e., medial parts of the medulla oblongata and the parabrachial nuclei. Afferents to the nucleus ambiguus derive from nuclei of the 'descending vocalization system' (periaqueductal gray and cuneiform nuclei) and from motor control centers (red nucleus and frontal cortex). Afferents to the nucleus ambiguus, possibly mediating auditory influence to the motor control of vocalization, come from the superior colliculus and from the pontine nuclei. The efferents from the pontine nuclei are restricted to rostral parts of the nucleus ambiguus, which hosts the motoneurons of the cricothyroid muscle controlling the call frequency.     

Harmonic and frequency structure used for echolocation sound pattern recognition and distance information processing in the rufous horseshoe bat

Summary The rufous horseshoe bat, Rhinolophus rouxi, was trained to discriminate differences in target distance. During the discrimination trials, the bats emitted complex FM/CF/FM pulses containing first harmonic and dominant second harmonic components.Loud free running artificial pulses, simulating the CF/FM part of the natural echolocation components, interfered with the ability of the bat to discriminate target distance. Changes in the frequency or frequency pattern of the artificial pulses resulted in systematic changes in the degree of interference. Interference occurred when artificial CF/FM pulses were presented at frequencies near those of the bat's own first or second harmonic components.These findings suggest that Rhinolophus rouxi uses both the first and second harmonic components of its complex multiharmonic echolocation sound for distance discrimination. For interference to occur, the sound pattern of each harmonic component must contain a CF signal followed by an FM sweep beginning near the frequency of the CF.Abbreviations CF constant frequency - FM frequency modulated     

Vocal communication in adult greater horseshoe bats, Rhinolophus ferrumequinum

Whereas echolocation in horseshoe bats is well studied, virtually nothing is known about characteristics and function of their communication calls. Therefore, the communication calls produced by a group of captive adult greater horseshoe bats were recorded during various social interactions in a free-flight facility. Analysis revealed that this species exhibited an amazingly rich repertoire of vocalizations varying in numerous spectro-temporal aspects. Calls were classified into 17 syllable types (ten simple syllables and seven composites). Syllables were combined into six types of simple phrases and four combination phrases. The majority of syllables had durations of more than 100 ms with multiple harmonics and fundamental frequencies usually above 20 kHz, although some of them were also audible to humans. Preliminary behavioral observations indicated that many calls were emitted during direct interaction with and in response to social calls from conspecifics without requiring physical contact. Some echolocation-like vocalizations also appeared to clearly serve a communication role. These results not only shed light upon a so far widely neglected aspect of horseshoe bat vocalizations, but also provide the basis for future studies on the neural control of the production of communicative vocalizations in contrast to the production of echolocation pulse sequences.     

Ectoparasitic insects of bats in British Columbia, Canada

One species of parasitic bug (Hemiptera : Cimicidae), 3 species of fleas (Siphonaptera: Ischnopsyllidae), and 2 species of parasitic flies (Diptera : Nycteribiidae) were collected from 9 species of bats (Chiroptera : Vespertilionidae) in southern interior and northeastern British Columbia, Canada. Female bats that return daily to maternity roosts were more frequently infested with both cimicids and ischnopsyllids than were male bats. Some differences in ectoparasite infestation can be attributed to differences in roosting behavior of the host. New national records for 2 parasite species, and 8 new host records are established for Canada.     

Control of echolocation pulses by neurons of the nucleus ambiguus in the rufous horseshoe bat,Rhinolophus rouxi

The vocal motor control of the larynx was studied with single unit recordings from the efferent motor nucleus (nucleus ambiguus) in the CF-FM-bat Rhinolophus rouxi, spontaneously emitting echolocation sounds. The experiments were performed in a stereotaxic apparatus that allowed differentiation of activities in the recorded nucleus depending on the electrode position (Fig. 1). Echolocation calls and respiration activity were monitored simultaneously, thus it was possible to compare the time course of the motor control activity during respiration with and without concurrent vocalization. Unit discharges were classified as laryngeal motoneuron activity according to their correlation with the time course (onset and end) of echolocation calls and their discharge rate as: Pre-off-tonic, pre-off-phasic, off-pauser, off-tonic, on-chopper, on-tonic, prior-tonic and inhibitory (Fig. 4). The on-chopper and on-tonic discharge patterns were assigned to the motor activity of the lateral cricoarytenoid muscle and the off-pauser and off-tonic discharge patterns to the motor activity of the posterior cricoarytenoid muscle controlling the time course of vocal pulses. Motoneuron activities recorded under the condition of systematically shifted frequencies in the emitted echolocation calls were investigated in Doppler-shift compensating bats responding to electronically simulated echoes. Of all neurons classified as motor control, only units of the pre-off-tonic discharge type (cricothyroid muscle) changed their activity with frequency shifts in the vocalized pulses; they showed a positive linear correlation with the emitted sound frequency (Fig. 6). In addition, single unit activities in strict synchronization to vocalization were recorded, that by their low discharge rate were not valid as motor control, and were considered to represent activities of interneurons or internuclear neurons connecting the nucleus ambiguus with other vocalization- and respiration-centers (Fig. 3c). Electric lesions in the brain stem and iontophoretically applied horseradish peroxidase (HRP) served as references for localization and morphological identification of the recording sites in cell stained brain slices.     

A gating mechanism for sound pattern recognition is correlated with the temporal structure of echolocation sounds in the rufous horseshoe bat

Summary The rufous horseshoe bat, Rhinolophus rouxi, was trained to discriminate differences in target distance. Loud free running artificial pulses, simulating the bat's natural long-CF/FM echolocation sounds, interfered with the ability of the bat to discriminate target distance. Interference occurred when the duration of the CF component of the CF/FM artificial pulse was between 2 and 70 ms. A brief (2.0 ms) CF signal 2–68 ms before an isolated FM signal was as effective as a continuous CF component of the same duration. When coupled with the bat's own emissions, a 2 ms FM sweep alone was effective in interfering when it came 42 to 69 ms after the onset of the bat's pulse. The coupled FM artificial pulses did not interfere when they began during the bat's own emissions.It appears that the onset of the CF component activates a gating mechanism that establishes a time window during which FM component signals must occur for proper neural processing. A comparison with a similar gating mechanism in Noctillo albiventris, which emits short-CF/FM echolocation sounds, reveals that the temporal parameters of the time window of the gating mechanism are species specific and specified by the temporal structure of the echolocation sound pattern of each species.Abbreviations FM frequency modulated - CF constant frequency     

Echolocation sounds and hearing of the greater Japanese horseshoe bat (Rhinolophus ferrumequinum nippon)

Summary The relationship between the orientation sounds and hearing sensitivity in the greater Japanese horseshoe bat,Rhinolophus ferrumequinum nippon was studied.An orientation pulse consisted of a constant frequency (CF) component followed by a short downward frequency-modulated (FM) component. Sometimes, an initial upward FM component preceded the CF component. Duration of pulses was about 30 ms and the CF of resting pulses (RF) averaged 65.5 kHz. The best frequency (BF) at the lowest threshold in audiograms as measured by the pinna reflex averaged 66.1 kHz. Audiograms showed remarkable sharp cut-offs on both sides near the BF. The frequency difference between the BF and the RF was about 0.6 kHz, and the RF was always below the BF. The values of RF and BF were characteristically different from those of the European subspecies,Rhinolophus ferrumequinum ferrumequinum.Abbreviations BF best frequency - CF constant frequency - FM frequency modulated - RF resting frequency     

Echolocation calls in Central American emballonurid bats: signal design and call frequency alternation

In southern Central America, 10 species of emballonurid bats occur, which are all aerial insectivores: some hunt flying insects preferably away from vegetation in open space, others hunt in edge space near vegetation and one species forages mainly over water. We present a search call design of each species and link signal structure to foraging habitat. All emballonurid bats use a similar type of echolocation call that consists of a central, narrowband component and one or two short, frequency-modulated sweeps. All calls are multi-harmonic, generally with most energy concentrated in the second harmonic. The design of search calls is closely related to habitat type, in particular to distance of clutter. Emballonurid bats foraging in edge space near vegetation and over water used higher frequencies, shorter call durations and shorter pulse intervals compared with species mostly hunting in open, uncluttered habitats. Peak frequency correlated negatively with body size. Regular frequency alternation between subsequent calls was typical in the search sequences of four out of 10 species. We discuss several hypotheses regarding the possible role of this frequency alternation, including species identification and partitioning of acoustic channels. Furthermore, we propose a model of how frequency alternation could increase the maximum detection distance of obstacles by marking search calls with different frequencies.