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     

The adaptive value of increasing pulse repetition rate during hunting by echolocating bats

During hunting, bats of suborder Microchiropetra emit intense ultrasonic pulses and analyze the weak returning echoes with their highly developed auditory system to extract the information about insects or obstacles. These bats progressively shorten the duration, lower the frequency, decrease the intensity and increase the repetition rate of emitted pulses as they search, approach, and finally intercept insects or negotiate obstacles. This dynamic variation in multiple parameters of emitted pulses predicts that analysis of an echo parameter by the bat would be inevitably affected by other co-varying echo parameters. The progressive increase in the pulse repetition rate throughout the entire course of hunting would presumably enable the bat to extract maximal information from the increasing number of echoes about the rapid changes in the target or obstacle position for successful hunting. However, the increase in pulse repetition rate may make it difficult to produce intense short pulse at high repetition rate at the end of long-held breath. The increase in pulse repetition rate may also make it difficult to produce high frequency pulse due to the inability of the bat laryngeal muscles to reach its full extent of each contraction and relaxation cycle at a high repetition rate. In addition, the increase in pulse repetition rate increases the minimum threshold (i.e. decrease auditory sensitivity) and the response latency of auditory neurons. In spite of these seemingly physiological disadvantages in pulse emission and auditory sensitivity, these bats do progressively increase pulse repetition rate throughout a target approaching sequence. Then, what is the adaptive value of increasing pulse repetition rate during echolocation? What are the underlying mechanisms for obtaining maximal information about the target features during increasing pulse repetition rate? This article reviews the electrophysiological studies of the effect of pulse repetition rate on multiple-parametric selectivity of neurons in the central nucleus of the inferior colliculus of the big brown bat, Eptesicus fuscus using single repetitive sound pulses and temporally patterned trains of sound pulses. These studies show that increasing pulse repetition rate improves multiple-parametric selectivity of inferior collicular neurons. Conceivably, this improvement of multiple-parametric selectivity of collicular neurons with increasing pulse repetition rate may serve as the underlying mechanisms for obtaining maximal information about the prey features for successful hunting by bats.     

Some comments on the proposed perception of phase and nanosecond time disparities by echolocating bats

In a series of recent reports, Simmons and his colleagues propose that bats are able to accurately encode the spectral, temporal and phase information of their emitted calls and echoes. The information so encoded is then extracted by the networks of the auditory system with specialized processing. They propose that bats use this information to determine the distance to their target by crosscorrelating the entire structure of the emitted call with the structure of the echo. The idea is that slight deviations in the correlation function can be detected by the bat and the degree of mismatch provides an accurate measure of temporal disparity and hence range. The data in the reports purport to show that bats perceive the phase of ultrasonic signals and that they can resolve temporal disparities of about 10 ns, and thus can distinguish range differences as small as 2 m.The hypothesis also attempts to explain how a variety of acoustic cues are processed and represented in the auditory system and how they are combined to form a unitary percept of space and fine structure. The theory incorporates some time honored processes of extracting information, such as crosscorrelations. The implications of. the hypothesis, however, go far beyond a theory of neural processing and representation of information by ensembles of cells. The hypothesis requires some remarkable abilities, such as the phase coding of ultrasonic signals and a temporal acuity on the order of 10 ns. These features have never been seen in any neurophysiological study of any animal nor has its existence been implied in behavioral studies of other animals. If bats, in fact, detect and process those signals in the manner proposed by Simmons and his colleagues, it would suggest that bats are supermammals whose auditory systems have evolved new and extraordinary mechanisms not possessed by other animals.In view of the extraordinary implications of the hypothesis, it seems prudent to critically evaluate the data upon which the hypothesis is based. The purpose of this review is to point out a number of technical problems and deficiencies in those experiments which undermine the veracity of the purported demonstration of phase perception and nanosecond time resolution by bats.     

Variability of the approach phase of landing echolocating Greater Mouse-eared bats

The approach phase of landing vespertilionid bats ends with a group of calls, which either consists of buzz I alone or buzz I and buzz II. To understand the possible role of buzz II, we trained Myotis myotis to land on a vertical grid, and compared the flight and echolocation behavior during approach in trials with and without buzz II. During the approach, we did not find any differences in the echolocation behavior until the end of buzz I which indicated whether buzz II was emitted or not. However, bats flying from the periphery of the flight channel, such that they had to make a small turn at the very last moment, finished the sequence with a buzz II. Bats flying on a rather stereotyped trajectory near the center of the flight channel without last instant corrections emitted buzz I alone. Our results indicate that buzz II occurred only on trajectories that implied a higher risk to fail at landing. The information delivered by buzz II reaches the bat too late to be used for landing. Therefore, we hypothesize that buzz II may help the bats to evaluate unsuccessful attempts and to eventually react adequately.     

Prey pursuit strategy of Japanese horseshoe bats during an in-flight target-selection task

The prey pursuit behavior of Japanese horseshoe bats (Rhinolophus ferrumequinum nippon) was investigated by tasking bats during flight with choosing between two tethered fluttering moths. Echolocation pulses were recorded using a telemetry microphone mounted on the bat combined with a 17-channel horizontal microphone array to measure pulse directions. Flight paths of the bat and moths were monitored using two high-speed video cameras. Acoustical measurements of returning echoes from fluttering moths were first collected using an ultrasonic loudspeaker, turning the head direction of the moth relative to the loudspeaker from 0° (front) to 180° (back) in the horizontal plane. The amount of acoustical glints caused by moth fluttering varied with the sound direction, reaching a maximum at 70°–100° in the horizontal plane. In the flight experiment, moths chosen by the bat fluttered within or moved across these angles relative to the bat’s pulse direction, which would cause maximum dynamic changes in the frequency and amplitude of acoustical glints during flight. These results suggest that echoes with acoustical glints containing the strongest frequency and amplitude modulations appear to attract bats for prey selection.     

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.     

Peripheral control of acoustic signals in the auditory system of echolocating bats.

Many species of echolocating bats emit intense orientation sounds. If such intense sounds directly stimulated their ears, detection of faint echoes would be impaired. Therefore, possible mechanisms for the attenuation of self-stimulation were studied with Myotis lucifugus. The acoustic middle-ear-muscle reflex could perfectly and transiently regulate the amplitude of an incoming signal only at its beginning. However, its shortest latency in terms of electromyograms and of the attenuation of the cochlear microphonic was 3-4 and 4-8 msec, respectively, so that these muscles failed to attenuate orientation signals by the reflex. The muscles, however, received a message from the vocalization system when the bat vocalized, and contracted synchronously with vocalization. The duration of the contraction-relaxation was so short that the self-stimulation was attenuated, but the echoes were not. The tetanus-fusion frequency of tha stapedium muscle ranged between 260 and 320/sec. Unlike the efferent fibres in the lateral-line and vestibular systems, the olivo-cochlear bundle showed no sign of attenuation of self-stimulation.     

Neural responses in the inferior colliculus of echolocating bats to artificial orientation sounds and echoes

The responses of single units and evoked potentials to a pair of artificial sounds, mimicking theorientation sound and echo, and to tape recorded actual orientation sounds were studied in terms of recovery cycle. the recovery cycle of single units could be classified into four groups: (1) short suppression (4%), (2) delayed inhibition (11%), (3) temporal recovery with or without a supernormal phase (7%), and (4) undelayed inhibition (78%) lasting 4 to 26 msec. therefore the majority of neurons were not excited by the second sound (echo) of a pair when it was delivered within several milliseconds after the first (out-going orientation sound). the duration of the recovery cycle was a function of the intensity of a pair of sounds. the weaker the first tone pulse relative to the second, the more rapid the recovery to the second. therefore, the reception of echoes is probably improved by contraction of middle ear muscles resulting in attenuation of self-stimulation by the out-going pulse. The collicular evoked potential consisted of two components, a fast one mainly due to the incoming fibers from lower levels and a slow one due to the main body of the inferior colliculus. The slow component showed slow recovery cycles as did the majority of single units while the fast one recovered very quickly. No noticeable difference in recovery cycles was found between awake and anesthetized animals. The functional meaning of inhibitory periods in the recovery cycle and role of the inferior colliculus in echo-location are discussed.     

Lipidomics: new tools and applications

Once viewed simply as a reservoir for carbon storage, lipids are no longer cast as bystanders in the drama of biological systems. The emerging field of lipidomics is driven by technology, most notably mass spectrometry, but also by complementary approaches for the detection and characterization of lipids and their biosynthetic enzymes in living cells. The development of these integrated tools promises to greatly advance our understanding of the diverse biological roles of lipids.     

Auditory fovea and Doppler shift compensation: adaptations for flutter detection in echolocating bats using CF-FM signals

Rhythmical modulations in insect echoes caused by the moving wings of fluttering insects are behaviourally relevant information for bats emitting CF-FM signals with a high duty cycle. Transmitter and receiver of the echolocation system in flutter detecting foragers are especially adapted for the processing of flutter information. The adaptations of the transmitter are indicated by a flutter induced increase in duty cycle, and by Doppler shift compensation (DSC) that keeps the carrier frequency of the insect echoes near a reference frequency. An adaptation of the receiver is the auditory fovea on the basilar membrane, a highly expanded frequency representation centred to the reference frequency. The afferent projections from the fovea lead to foveal areas with an overrepresentation of sharply tuned neurons with best frequencies near the reference frequency throughout the entire auditory pathway. These foveal neurons are very sensitive to stimuli with natural and simulated flutter information. The frequency range of the foveal areas with their flutter processing neurons overlaps exactly with the frequency range where DS compensating bats most likely receive echoes from fluttering insects. This tight match indicates that auditory fovea and DSC are adaptations for the detection and evaluation of insects flying in clutter.     

Female greater wax moths reduce sexual display behavior in relation to the potential risk of predation by echolocating bats

Female greater wax moths Galleria mellonella display by wing fanning in response to bursts of ultrasonic calls produced bymales. The temporal and spectral characteristics of these callsshow some similarities with the echolocation calls of batsthat emit frequency-modulated (FM) signals. Female G. mellonellatherefore need to distinguish between the attractive signalsof male conspecifics, which may lead to mating opportunities,and similar sounds made by predatory bats. We therefore predictedthat (1) females would display in response to playbacks of male calls; (2) females would not display in response to playbacksof the calls of echolocating bats (we used the calls of Daubenton'sbat Myotis daubentonii as representative of a typical FM echolocatingbat); and (3) when presented with male calls and bat callsduring the same time block, females would display more whenperceived predation risk was lower. We manipulated predationrisk in two ways. First, we varied the intensity of bat callsto represent a nearby (high risk) or distant (low risk) bat.Second, we played back calls of bats searching for prey (lowrisk) and attacking prey (high risk). All predictions weresupported, suggesting that female G. mellonella are able todistinguish conspecific male mating calls from bat calls, andthat they modify display rate in relation to predation risk.The mechanism (s) by which the moths separate the calls ofbat and moth must involve temporal cues. Bat and moth signalsdiffer considerably in duration, and differences in durationcould be encoded by the moth's nervous system and used in discrimination.     

Leaf-mining and gall-forming insects: tools for teaching population ecology

Groups of Israeli and Australian science educationists, practising secondary school science teachers, practising scientists, and science graduates preparing to become science teachers were questioned as to the suitability of teleologically and anthropomorphically formulated statements for inclusion in fourth/fifth-form (14–16 year olds) level study material. Respondents' awareness of the dangers involved (i.e. literal acceptance by pupils of such statements) was acute in the science educationist group, but progressively less so with the teachers, the scientists, and the prospective teachers. It was recommended that all persons connected with science teaching become more aware of the problem, in particular persons engaged in teacher training, and those responsible for preparing texts.     

The ecosystem services provided by social insects: traits,management tools and knowledge gaps

Social insects, i.e. ants, bees, wasps and termites, are key components of ecological communities, and are important ecosystem services (ESs) providers. Here, we review the literature in order to (i) analyse the particular traits of social insects that make them good suppliers of ESs; (ii) compile and assess management strategies that improve the services provided by social insects; and (iii) detect gaps in our knowledge about the services that social insects provide. Social insects provide at least 10 ESs; however, many of them are poorly understood or valued. Relevant traits of social insects include high biomass and numerical abundance, a diversity of mutualistic associations, the ability to build important biogenic structures, versatile production of chemical defences, the simultaneous delivery of several ESs, the presence of castes and division of labour, efficient communication and cooperation, the capacity to store food, and a long lifespan. All these characteristics enhance social insects as ES providers, highlighting their potential, constancy and efficiency as suppliers of these services. In turn, many of these traits make social insects stress tolerant and easy to manage, so increasing the ESs they provide. We emphasise the need for a conservation approach to the management of the services, as well as the potential use of social insects to help restore habitats degraded by human activities. In addition, we stress the need to evaluate both services and disservices in an integrated way, because some species of social insects are among the most problematic invasive species and native pests. Finally, we propose two areas of research that will lead to a greater and more efficient use of social insects as ES providers, and to a greater appreciation of them by producers and decision‐makers.