The sonar beam of Macrophyllum macrophyllum implies ecological adaptation under phylogenetic constraint.

All animals are adapted to their ecology within the bounds of their evolutionary heritage. Echolocating bats clearly show such adaptations and boundaries through their biosonar call design. Adaptations include not only the overall time-frequency structure, but also the shape of the emitted echolocation beam. Macrophyllum macrophyllum is unique within the phyllostomid family, being the only species to predominantly hunt for insects in the open, on or above water, and as such it presents an interesting case for comparing the impact of phylogeny and ecology as it originates from a family of low-intensity, high-directionality gleaning bats, but occupies a niche dominated by very loud and substantially less-directional bats. Here, we examined the sonar beam pattern of M. macrophyllum in the field and in a flight room and compared it to closely related species with very different feeding ecology and to that of the niche-sharing but distantly related Myotis daubentonii Our results show that M. macrophyllum uses higher source levels and emits less-directional calls than other phyllostomids. In the field, its call directionality is comparable to M. daubentonii, but in the flight room, M. macrophyllum is substantially more directional. Hence our results indicate that ecology influences the emitted call, pushing the bats to emit a louder and broader beam than other phyllostomids, but that phylogeny does limit the emitted intensity and flexibility of the overall beam pattern.

Convergent acoustic field of view in echolocating bats.

Most echolocating bats exhibit a strong correlation between body size and the frequency of maximum energy in their echolocation calls (peak frequency), with smaller species using signals of higher frequency than larger ones. Size-signal allometry or acoustic detection constraints imposed on wavelength by preferred prey size have been used to explain this relationship. Here we propose the hypothesis that smaller bats emit higher frequencies to achieve directional sonar beams, and that variable beam width is critical for bats. Shorter wavelengths relative to the size of the emitter translate into more directional sound beams. Therefore, bats that emit their calls through their mouths should show a relationship between mouth size and wavelength, driving smaller bats to signals of higher frequency. We found that in a flight room mimicking a closed habitat, six aerial hawking vespertilionid species (ranging in size from 4 to 21 g, ref. 5) produced sonar beams of extraordinarily similar shape and volume. Each species had a directivity index of 11 ± 1 dB (a half-amplitude angle of approximately 37°) and an on-axis sound level of 108 ± 4 dB sound pressure level referenced to 20 µPa root mean square at 10 cm. Thus all bats adapted their calls to achieve similar acoustic fields of view. We propose that the necessity for high directionality has been a key constraint on the evolution of echolocation, which explains the relationship between bat size and echolocation call frequency. Our results suggest that echolocation is a dynamic system that allows different species, regardless of their body size, to converge on optimal fields of view in response to habitat and task.

Dynamics of the echolocation beam during prey pursuit in aerial hawking bats.

In the evolutionary arms race between prey and predator, measures and countermeasures continuously evolve to increase survival on both sides. Bats and moths are prime examples. When exposed to intense ultrasound, eared moths perform dramatic escape behaviors. Vespertilionid and rhinolophid bats broaden their echolocation beam in the final stage of pursuit, presumably as a countermeasure to keep evading moths within their "acoustic field of view." In this study, we investigated if dynamic beam broadening is a general property of echolocation when catching moving prey. We recorded three species of emballonurid bats, Saccopteryx bilineata, Saccopteryx leptura, and Rhynchonycteris naso, catching airborne insects in the field. The study shows that S. bilineata and S. leptura maintain a constant beam shape during the entire prey pursuit, whereas R. naso broadens the beam by lowering the peak call frequency from 100 kHz during search and approach to 67 kHz in the buzz. Surprisingly, both Saccopteryx bats emit calls with very high energy throughout the pursuit, up to 60 times more than R. naso and Myotis daubentonii (a similar sized vespertilionid), providing them with as much, or more, peripheral "vision" than the vespertilionids, but ensonifying objects far ahead suggesting more clutter. Thus, beam broadening is not a fundamental property of the echolocation system. However, based on the results, we hypothesize that increased peripheral detection is crucial to all aerial hawking bats in the final stages of prey pursuit and speculate that beam broadening is a feature characterizing more advanced echolocation.

Fast sensory-motor reactions in echolocating bats to sudden changes during the final buzz and prey intercept.

Echolocation is an active sense enabling bats and toothed whales to orient in darkness through echo returns from their ultrasonic signals. Immediately before prey capture, both bats and whales emit a buzz with such high emission rates (≥ 180 Hz) and overall duration so short that its functional significance remains an enigma. To investigate sensory-motor control during the buzz of the insectivorous bat Myotis daubentonii, we removed prey, suspended in air or on water, before expected capture. The bats responded by shortening their echolocation buzz gradually; the earlier prey was removed down to approximately 100 ms (30 cm) before expected capture, after which the full buzz sequence was emitted both in air and over water. Bats trawling over water also performed the full capture behavior, but in-air capture motions were aborted, even at very late prey removals (<20 ms = 6 cm before expected contact). Thus, neither the buzz nor capture movements are stereotypical, but dynamically adapted based on sensory feedback. The results indicate that echolocation is controlled mainly by acoustic feedback, whereas capture movements are adjusted according to both acoustic and somatosensory feedback, suggesting separate (but coordinated) central motor control of the two behaviors based on multimodal input. Bat echolocation, especially the terminal buzz, provides a unique window to extremely fast decision processes in response to sensory feedback and modulation through attention in a naturally behaving animal.

Big brown bats (Eptesicus fuscus) emit intense search calls and fly in stereotyped flight paths as they forage in the wild.

The big brown bat, Eptesicus fuscus, uses echolocation for orientation and foraging, and scans its surroundings by aiming its sonar beam at obstacles and prey. All call parameters are highly adaptable and determine the bat's acoustic field of view and hence its perception of the echo scene. The intensity (source level) and directionality of the emitted calls directly contribute to the bat's acoustic field of view; however, the source level and directionality of the big brown bat's sonar signals have not been measured in the field. In addition, for bats, navigation and prey capture require that they process several streams of acoustic information. By using stereotypic flight paths in known areas, bats may be able to reduce the sensory processing load for orientation and therefore allocate echo processing resources to prey. Here we recorded the echolocation calls from foraging E. fuscus in the field with a microphone array and estimated call intensity and directionality, based on reconstructed flight trajectories. The source levels were intense with an average maximum source level of 138 dB (root mean square re. 20 µPa at 0.1 m). Furthermore, measurements taken from a subset of calls indicate that the echolocation signals in the field may be more directional than estimated in the laboratory (half-amplitude angle 30 deg at 35 kHz). We also observed that E. fuscus appear to follow stereotypic flight paths, and propose that this could be a strategy to optimize foraging efficiency by minimizing the sensory processing load.

Moth hearing and sound communication.

Active echolocation enables bats to orient and hunt the night sky for insects. As a counter-measure against the severe predation pressure many nocturnal insects have evolved ears sensitive to ultrasonic bat calls. In moths bat-detection was the principal purpose of hearing, as evidenced by comparable hearing physiology with best sensitivity in the bat echolocation range, 20-60 kHz, across moths in spite of diverse ear morphology. Some eared moths subsequently developed sound-producing organs to warn/startle/jam attacking bats and/or to communicate intraspecifically with sound. Not only the sounds for interaction with bats, but also mating signals are within the frequency range where bats echolocate, indicating that sound communication developed after hearing by "sensory exploitation". Recent findings on moth sound communication reveal that close-range (~ a few cm) communication with low-intensity ultrasounds "whispered" by males during courtship is not uncommon, contrary to the general notion of moths predominantly being silent. Sexual sound communication in moths may apply to many eared moths, perhaps even a majority. The low intensities and high frequencies explain that this was overlooked, revealing a bias towards what humans can sense, when studying (acoustic) communication in animals.

Sound-sensitive neurons innervate the ventro-lateral protocerebrum of the heliothine moth brain.

Many noctuid moth species perceive ultrasound via tympanic ears that are located at the metathorax. Whereas the neural processing of auditory information is well studied at the peripheral and first synaptic level, little is known about the features characterizing higher order sound-sensitive neurons in the moth brain. During intracellular recordings from the lateral protocerebrum in the brain of three noctuid moth species, Heliothis virescens, Helicoverpa armigera and Helicoverpa assulta, we found an assembly of neurons responding to transient sound pulses of broad bandwidth. The majority of the auditory neurons ascended from the ventral cord and ramified densely within the anterior region of the ventro-lateral protocerebrum. The physiological and morphological characteristics of these auditory neurons were similar. We detected one additional sound-sensitive neuron, a brain interneuron with its soma positioned near the calyces of mushroom bodies and with numerous neuronal processes in the ventro-lateral protocerebrum. Mass-staining of ventral-cord neurons supported the assumption that the ventro-lateral region of the moth brain was the main target for the auditory projections ascending from the ventral cord.

Bats coordinate sonar and flight behavior as they forage in open and cluttered environments.

Echolocating bats use active sensing as they emit sounds and listen to the returning echoes to probe their environment for navigation, obstacle avoidance and pursuit of prey. The sensing behavior of bats includes the planning of 3D spatial trajectory paths, which are guided by echo information. In this study, we examined the relationship between active sonar sampling and flight motor output as bats changed environments from open space to an artificial forest in a laboratory flight room. Using high-speed video and audio recordings, we reconstructed and analyzed 3D flight trajectories, sonar beam aim and acoustic sonar emission patterns as the bats captured prey. We found that big brown bats adjusted their sonar call structure, temporal patterning and flight speed in response to environmental change. The sonar beam aim of the bats predicted the flight turn rate in both the open room and the forest. However, the relationship between sonar beam aim and turn rate changed in the forest during the final stage of prey pursuit, during which the bat made shallower turns. We found flight stereotypy developed over multiple days in the forest, but did not find evidence for a reduction in active sonar sampling with experience. The temporal patterning of sonar sound groups was related to path planning around obstacles in the forest. Together, these results contribute to our understanding of how bats coordinate echolocation and flight behavior to represent and navigate their environment.

Development of vocalization and hearing in American mink (Neovison vison).

American mink (Neovison vison) kits are born altricial and fully dependent on maternal care, for which the kits' vocalizations appear essential. We used auditory brainstem responses (ABRs) to determine: (1) hearing sensitivity of adult females from two breeding lines known to differ in maternal behaviour and (2) development of hearing in kits 8-52 days of age. We also studied sound production in 20 kits throughout postnatal days 1 to 44. Adult female mink had a broad hearing range from 1 kHz to above 70 kHz, with peak sensitivity (threshold of 20 dB SPL) at 8-10 kHz, and no difference in sensitivity between the two breeding lines (P>0.22) to explain the difference in maternal care. Mink kits showed no signs of hearing up to postnatal day 24. From day 30, all kits had ABRs indicative of hearing. Hearing sensitivity increased with age, but was still below the adult level at postnatal day 52. When separated from their mothers, kits vocalized loudly. Until the age of 22 days, 90% of all kits vocalized with no significant decline with age (P=0.27). From day 25, concurrent with the start of hearing, the number of vocalizing kits decreased with age (P<0.001), in particular in kits that were re-tested (P=0.004). Large numbers of mink are kept in fur industry farms, and our results are important to the understanding of sound communication, which is part of their natural behaviour. Our results also suggest mink as an interesting model for studying the development of mammalian hearing and its correlation to sound production.

The simple ears of noctuoid moths are tuned to the calls of their sympatric bat community.

Insects with bat-detecting ears are ideal animals for investigating sensory system adaptations to predator cues. Noctuid moths have two auditory receptors (A1 and A2) sensitive to the ultrasonic echolocation calls of insectivorous bats. Larger moths are detected at greater distances by bats than smaller moths. Larger moths also have lower A1 best thresholds, allowing them to detect bats at greater distances and possibly compensating for their increased conspicuousness. Interestingly, the sound frequency at the lowest threshold is lower in larger than in smaller moths, suggesting that the relationship between threshold and size might vary across frequencies used by different bat species. Here, we demonstrate that the relationships between threshold and size in moths were only significant at some frequencies, and these frequencies differed between three locations (UK, Canada and Denmark). The relationships were more likely to be significant at call frequencies used by proportionately more bat species in the moths' specific bat community, suggesting an association between the tuning of moth ears and the cues provided by sympatric predators. Additionally, we found that the best threshold and best frequency of the less sensitive A2 receptor are also related to size, and that these relationships hold when controlling for evolutionary relationships. The slopes of best threshold versus size differ, however, such that the difference in threshold between A1 and A2 is greater for larger than for smaller moths. The shorter time from A1 to A2 excitation in smaller than in larger moths could potentially compensate for shorter absolute detection distances in smaller moths.

How the bat got its buzz.

Since the discovery of echolocation in bats, the final phase of an attack on a flying insect, the 'terminal buzz', has proved enigmatic. During the buzz, bats increase information update rates by producing vocalizations up to 220 times s(-1). The buzz's ubiquity in hawking and trawling bats implies its importance for hunting success. Superfast muscles, previously unknown in mammals, are responsible for the extreme vocalization rate. Some bats produce a second phase-buzz II-defined by a large drop in the fundamental frequency (F(0)) of their calls. By doing so, bats broaden their acoustic field of view and should thereby reduce the likelihood of insect escape. We make the case that the buzz was a critical adaptation for capturing night-flying insects, and suggest that the drop in F(0) during buzz II requires novel, unidentified laryngeal mechanisms in order to counteract increasing muscle tension. Furthermore, we propose that buzz II represents a countermeasure against the evasive flight of eared prey in the evolutionary arms-race that saw the independent evolution of bat-detecting ears in various groups of night-flying insects.

Vespertilionid bats control the width of their biosonar sound beam dynamically during prey pursuit.

Animals using sound for communication emit directional signals, focusing most acoustic energy in one direction. Echolocating bats are listening for soft echoes from insects. Therefore, a directional biosonar sound beam greatly increases detection probability in the forward direction and decreases off-axis echoes. However, high directionality has context-specific disadvantages: at close range the detection space will be vastly reduced, making a broad beam favorable. Hence, a flexible system would be very advantageous. We investigated whether bats can dynamically change directionality of their biosonar during aerial pursuit of insects. We trained five Myotis daubentonii and one Eptesicus serotinus to capture tethered mealworms and recorded their echolocation signals with a multimicrophone array. The results show that the bats broaden the echolocation beam drastically in the terminal phase of prey pursuit. M. daubentonii increased the half-amplitude angle from approximately 40 degrees to approximately 90 degrees horizontally and from approximately 45 degrees to more than 90 degrees vertically. The increase in beam width is achieved by lowering the frequency by roughly one octave from approximately 55 kHz to approximately 27.5 kHz. The E. serotinus showed beam broadening remarkably similar to that of M. daubentonii. Our results demonstrate dynamic control of beam width in both species. Hence, we propose directionality as an explanation for the frequency decrease observed in the buzz of aerial hawking vespertilionid bats. We predict that future studies will reveal dynamic control of beam width in a broad range of acoustically communicating animals.

Ultrasonic recording system without intrinsic limits.

Today state-of-the-art bioacoustic research requires high-sample-rate, multi-channel, and often long-term recording systems. Commercial systems are very costly. This paper proposes and demonstrates an ultrasonic recording system design that is arbitrarily scalable. The system is modular and based on retail components and open source software/hardware. Each module has four microphones and modules can be combined to extend the coverage area, obtain higher spatial recording resolution, and/or add recording redundancy. The system is designed to have no inherent scalability limits. The system has been deployed in four different test settings. The first setup tests the system's ability to make medium-term recordings (1 to 2 min) with many microphones. The second setup tests the robustness of the system, being deployed throughout the Danish winter with only minor issues. The third setup integrates the system in a mobile robot as an echolocating guidance system, while the fourth setup demonstrates full-spectrum transducer calibration. In most respects this system's hardware specification surpasses all competitors on the market at a quarter of the price. Tests demonstrate that large deployments are feasible and accurate ultrasonic measurements can be obtained.

New model for gain control of signal intensity to object distance in echolocating bats.

Echolocating bats emit ultrasonic calls and listen for the returning echoes to orient and localize prey in darkness. The emitted source level, SL (estimated signal intensity 10 cm from the mouth), is adjusted dynamically from call to call in response to sensory feedback as bats approach objects. A logarithmic relationship of SL=20 log(10)(x), i.e. 6 dB output reduction per halving of distance, x, has been proposed as a model for the relationship between emitted intensity and object distance, not only for bats but also for echolocating toothed whales. This logarithmic model suggests that the approaching echolocator maintains a constant intensity impinging upon the object, but it also implies ever-increasing source levels with distance, a physical and biological impossibility. We developed a new model for intensity compensation with an exponential rise to the maximum source level: SL=SL(max)-ae(-)(bx). In addition to providing a method for estimating maximum output, the new model also offers a tool for estimating a minimum detection distance where intensity compensation starts. We tested the new exponential model against the 'conventional' logarithmic model on data from five bat species. The new model performed better in 77% of the trials and as good as the conventional model in the rest (23%). We found much steeper rates of compensation when fitting the model to individual rather than pooled data, with slopes often steeper than -20 dB per halving of distance. This emphasizes the importance of analyzing individual events. The results are discussed in light of habitat constraints and the interaction between bats and their eared prey.

Frequency alternation and an offbeat rhythm indicate foraging behavior in the echolocating bat, Saccopteryx bilineata.

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.

Directional escape behavior in allis shad (Alosa alosa) exposed to ultrasonic clicks mimicking an approaching toothed whale.

Toothed whales emit high-powered ultrasonic clicks to echolocate a wide range of prey. It may be hypothesized that some of their prey species have evolved capabilities to detect and respond to such ultrasonic pulses in a way that reduces predation, akin to the situation for many nocturnal insects and echolocating bats. Using high-speed film recordings and controlled exposures, we obtained behavioural evidence that simulated toothed whale biosonar clicks elicit highly directional anti-predator responses in an ultrasound-sensitive allis shad (Alosa alosa). Ten shad were exposed to 192 dB re. 1 µPa (pp) clicks centred at 40 kHz at repetition rates of 1, 20, 50 and 250 clicks s(-1) with summed energy flux density levels of 148, 161, 165 and 172 dB re. 1 µPa(2) s. The exposures mimicked the acoustic exposure from a delphinid toothed whale in different phases of prey search and capture. The response times of allis shad were faster for higher repetition rates of clicks with the same sound pressure level. None of the fish responded to a single click, but had median response times of 182, 93 and 57 ms when exposed to click rates of 20, 50 and 250 clicks s(-1), respectively. This suggests that the ultrasound detector of allis shad is an energy detector and that shad respond faster when exposed to a nearby fast-clicking toothed whale than to a slow-clicking toothed whale far away. The findings are thus consistent with the hypothesis that shad ultrasound detection is used for reducing predation from echolocating toothed whales.

Moths produce extremely quiet ultrasonic courtship songs by rubbing specialized scales.

Insects have evolved a marked diversity of mechanisms to produce loud conspicuous sounds for efficient communication. However, the risk of eavesdropping by competitors and predators is high. Here, we describe a mechanism for producing extremely low-intensity ultrasonic songs (46 dB sound pressure level at 1 cm) adapted for private sexual communication in the Asian corn borer moth, Ostrinia furnacalis. During courtship, the male rubs specialized scales on the wing against those on the thorax to produce the songs, with the wing membrane underlying the scales possibly acting as a sound resonator. The male's song suppresses the escape behavior of the female, thereby increasing his mating success. Our discovery of extremely low-intensity ultrasonic communication may point to a whole undiscovered world of private communication, using "quiet" ultrasound.

A method for estimating the orientation of a directional sound source from source directivity and multi-microphone recordings: principles and application.

Taking into account directivity of real sound sources makes it possible to try solving an interesting and biologically relevant problem: estimating the orientation in three-dimensional space of a directional sound source. The source, of known directivity, produces a broadband signal (in the ultrasonic range, in this application) that is recorded by microphones whose position with respect to source is known. An analytical method to process the recorded signals and estimate source orientation is developed in this paper. Experiments testing method performance in estimating source orientation were performed both in a laboratory environment with a Polaroid transducer as source and in a flight room with a Myotis daubentonii bat. In the first case, results showed the estimation method to be accurate and pointed out its limitations. The latter case is significant as an example biological application of the method for extracting behavioral features from bats; results are compared with alternative calculations based on microphone root-mean-square (rms)-pressure values.

Echolocation call intensity and directionality in flying short-tailed fruit bats, Carollia perspicillata (Phyllostomidae).

The directionality of bat echolocation calls defines the width of bats' sonar "view," while call intensity directly influences detection range since adequate sound energy must impinge upon objects to return audible echoes. Both are thus crucial parameters for understanding biosonar signal design. Phyllostomid bats have been classified as low intensity or "whispering bats," but recent data indicate that this designation may be inaccurate. Echolocation beam directionality in phyllostomids has only been measured through electrode brain-stimulation of restrained bats, presumably excluding active beam control via the noseleaf. Here, a 12-microphone array was used to measure echolocation call intensity and beam directionality in the frugivorous phyllostomid, Carollia perspicillata, echolocating in flight. The results showed a considerably narrower beam shape (half-amplitude beam angles of approximately 16° horizontally and 14° vertically) and louder echolocation calls [source levels averaging 99 dB sound pressure level (SPL) root mean square] for C. perspicillata than was found for this species when stationary. This suggests that naturally behaving phyllostomids shape their sound beam to achieve a longer and narrower sonar range than previously thought. C. perspicillata orient and forage in the forest interior and the narrow beam might be adaptive in clutter, by reducing the number and intensity of off-axis echoes.

To females of a noctuid moth, male courtship songs are nothing more than bat echolocation calls.

It has been proposed that intraspecific ultrasonic communication observed in some moths evolved, through sexual selection, subsequent to the development of ears sensitive to echolocation calls of insectivorous bats. Given this scenario, the receiver bias model of signal evolution argues that acoustic communication in moths should have evolved through the exploitation of receivers' sensory bias towards bat ultrasound. We tested this model using a noctuid moth Spodoptera litura, males of which were recently found to produce courtship ultrasound. We first investigated the mechanism of sound production in the male moth, and subsequently the role of the sound with reference to the female's ability to discriminate male courtship songs from bat calls. We found that males have sex-specific tymbals for ultrasound emission, and that the broadcast of either male songs or simulated bat calls equally increased the acceptance of muted males by the female. It was concluded that females of this moth do not distinguish between male songs and bat calls, supporting the idea that acoustic communication in this moth evolved through a sensory exploitation process.