Northern bats, Eptesicus nilssonii, use vision but not flutter-detection when searching for prey in clutter

We investigated the detection cues used by the aerial-hawking bat Eptesicus nilssonii foraging in a cluttered environment. The bats can detect and attack rapidly moving targets within the clutter, i.e. below grass panicles, by using prey motion as a cue. Stationary objects are attacked only above the grass, but still within the clutter overlap zone. To test if the bats were guided by flutter from moth wings or by vision when searching for stationary targets, they were presented with male ghost swifts mounted on top of steel wires. There was no difference in attack frequency on live, fluttering moths compared to dead and spread ones. However, when comparing white and dark moths, we found a significantly higher attack frequency on white ones. As the attacks always were guided by echolocation calls, we hypothesize that northern bats, at least in the initial search phase, use visual cues as a complement to detect stationary ghost swifts.     

Behavioural flexibility: the little brown bat, Myotis lucifugus, and the northern long-eared bat,M. septentrionalis , both glean and hawk prey

We present behavioural data demonstrating that the little brown bat, Myotis lucifugus, and the northern long-eared bat, M. septentrionalis, can glean prey from surfaces and take prey on the wing. Our data were collected in a large outdoor flight room mimicking a cluttered environment. We compared and analysed flight behaviours and echolocation calls used by each species of bat when aerial hawking and gleaning. Our results challenge the traditional labelling ofM. lucifugus as an obligate aerial-hawking species and show that M. septentrionalis, which is often cited as a gleaning species, can capture airborne prey. As has been shown in previous studies, prey-generated acoustic cues were necessary and sufficient for the detection and localization of perched prey. We argue that the broadband, high-frequency, downward-sweeping, frequency-modulated calls used by some bats when gleaning prey from complex surfaces resolve targets from background. First, because calls of lower frequency and narrower bandwidth are sufficient for assessing a surface before landing, and second, because there are few, if any, simple surfaces in nature from which substrate-gleaning behaviours in wild bats would be expected. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.     

Eavesdropping by Bats: The Influence of Echolocation Call Design and Foraging Strategy

We used playback presentations to free-flying bats of 3 species to assess the influence of echolocation call design and foraging strategy on the role of echolocation calls in communication. Near feeding sites over water, Myotis lucifugus and M. yumanensis responded positively only to echolocation calls of conspecifics. Near roosts, these bats did not respond before young of the year became volant, and after this responded to presentations of echolocation calls of similar and dissimilar design. At feeding sites Lasiurus borealis responded only to echolocation calls of conspecifics and particularly to “feeding buzzes”. While Myotis, particularly subadults, appear to use the echolocation calls of conspecifics to locate feeding sites, L. borealis appears to use the calls of a foraging neighbour attacking prey to identify opportunities for ‘stealing’ food.     

Echolocation calls of free-flying common vampire bats Desmodus rotundus (Chiroptera: Phyllostomidae) in Chile

We recorded and characterized the echolocation calls emitted by the common vampire bat Desmodus rotundus during foraging in natural habitats in Chile. Signal design typically shows multiple harmonics consisting of a brief quasi-constant frequency (QCF) component at the beginning of the pulse followed by a downward frequency modulated component. Calls are characterized by long durations (5.5 ms) and emitted as single pulses or in groups of 2–3 pulses at a repetition rate of 29 Hz. The higher frequency ranges (85–35 kHz) and the unusual QCF component that characterized multiharmonic signals of free-flying D. rotundus in Chile is a remarkable feature for acoustic identification with other Chilean bats.     

Sensory ecology of predator–prey interactions: responses of the AN2 interneuron in the field cricket, <Emphasis Type="Italic">Teleogryllus oceanicus</Emphasis> to the echolocation calls of sympatric bats

We observed the responses of the AN2 interneuron in the Pacific field cricket, Teleogryllus oceanicus, a cell implicated in eliciting avoidance flight away from bats, to acoustic stimuli representing the echolocation calls of bats as well as field recordings of search and gleaning attack calls of six species of insectivorous sympatric bats (West Australia, Australia: Tadarida australis, Chalinolobus goudii, Nyctophilus geoffroyi; Queensland, Australia: Vespadelus pumilus, Myotis adversus; Kauai, Hawaii: Lasiurus cinereus). The broad frequency sensitivity of the AN2 cell indicates that T. oceanicus has evolved to detect a wide range of echolocation call frequencies. The reduced sensitivity of this cell at frequencies higher than 70 kHz suggests that some bats (e.g., the gleaning species, N. geoffroyi) may circumvent this insects auditory defences by using frequency-mismatched (allotonic) calls. The calls of the freetail bat, T. australis evoked the strongest response in the AN2 cell but, ironically, this may allow this bat to prey upon T. oceanicus as previous studies report that under certain conditions, flying crickets exhibit ambiguous directional responses towards frequencies similar to those emitted by this bat. Short duration calls (1–2 ms) are sufficient to evoke AN2 responses with instantaneous spike periods capable of causing defensive flight behaviours; most bats tested emit calls of durations greater than this. The short calls of N. geoffroyi produced during gleaning attacks may reduce this species acoustic conspicuousness to this cricket.     

Plasticity in echolocation calls of <Emphasis Type="Italic">Myotis macrodactylus</Emphasis> (Chiroptera: Vespertilionidae): implications for acoustic identification

Poor knowledge of the intraspecific variability in echolocation calls is recognized as an important limiting factor for the accurate acoustic identification of bats. We studied the echolocation behaviors of an ecologically poorly known bat species, Myotis macrodactylus, while they were commuting in three types of habitats differing significantly in the amount of background clutter, as well as searching for prey above the water surface in a river. Results showed that M. macrodactylus altered their echolocation call structure in the same way during commuting as foraging bats do in relation to the changing level of clutter. With increasing level of clutter, M. macrodactylus generally produced echolocation calls with higher start, end, and peak frequencies; wider bandwidth; and shorter pulse duration. Compared to commuting, bats emitted significantly lower frequency calls with narrower bandwidth while searching for prey. Discriminant function analysis indicated that 79.8% of the calls from the three commuting habitats were correctly grouped, and 87% of the calls were correctly classified to the commuting and foraging contexts. Our finding has implications for those who would identify species by their calls.     

Selective Eavesdropping Behaviour in Three Neotropical Bat Species

Knowledge of interspecies information transfer in mammals is scarce compared with other taxa. We investigated whether eavesdropping on echolocation calls of bats may be used by sympatric bats with similar feeding ecology. We performed playback experiments with three free‐ranging neotropical bat species, broadcasting search phase calls or feeding buzzes of conspecifics and heterospecifics belonging either to the same or to another bat family. Both the greater fishing bat Noctilio leporinus and the lesser bulldog bat Noctilio albiventris (Noctilionidae) reacted with repeated approaches in response to playbacks of search phase calls and feeding buzzes from conspecifics and also to congeneric feeding buzzes. Noctilio leporinus also were attracted by search phase calls from its sister species N. albiventris. In contrast, the sac‐winged bat Saccopteryx bilineata (Emballonuridae) did not react to any playback sequences presented. Our results support the existence of eavesdropping behaviour for both species of Noctilio. We suggest that information transfer via eavesdropping may depend mainly on species‐specific traits, including foraging style and social behaviour (territoriality, group foraging), and on distribution and density of prey. Call design had only a minor influence on the reaction.     

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.     

Echolocation behaviours of the Japanese pipistrelle batPipistrellus abramus during foraging flight

The acoustic structure of echolocation pulses emitted by Japanese pipistrellePipistrellus abramus (Temminck, 1840) bats during different phases of aerial hawking is described here for the first time. Behavioural observations of the foraging flight in conjunction with acoustical analysis of echolocation pulses indicated a flight path consisting of four distinct phases following the reconnaissance or search phase. Short (∼4.68 ms) and relatively broadband frequencymodulated (FM) pulses (∼23.55 kHz bandwidth) were emitted at a repetition rate of 15 Hz during presumed target approach. Presumed insect capture consisted of an early and a late buzz phase. Both buzz types were emitted at high repetition rates (111 Hz in early to 222 Hz in late) and consisted of very short, broadband FM pulses (1.26 ms in early to 0.3 ms in late). There was also a characteristically sharp drop in both the peak and terminal frequencies of each echolocation pulse during the transition from early to late buzz. No pulses were recorded during the final phase of foraging referred to as a “post-buzz pause”. Thus the foraging behaviour of this species consisted of five sequential phases involving four broad types of echolocation pulses.     

The tiny difference between foraging and communication buzzes uttered by the Mexican free-tailed bat, <Emphasis Type="Italic">Tadarida brasiliensis</Emphasis>

Echolocating insectivorous bats consummate prey captures using a distinct vocal motor pattern commonly known as the terminal or feeding buzz, which is widely considered a fixed motor pattern executed independently of auditory feedback influences. The Mexican free-tailed bat, Tadarida brasiliensis, offers an opportunity to explore the role of sensory feedback in buzzing because they emit similar buzzes both in flight during foraging and while stationary as communication sounds. Here we compared the spectral and temporal patterns of foraging and communication buzzes to address whether or not auditory feedback may influence buzz patterns. We found that while foraging buzzes uttered in open space were composed of generic FM calls, communication buzzes were composed of an adapted CF–FM call similar to the call type used by T. brasiliensis when navigating in confined spaces. This provides the first evidence that some bats can make significant context-dependent changes in the spectral parameters of calls within their buzz. We also found that inter-pulse intervals, but not call durations, were different within the two buzz types. These observations indicate that though a common pattern generator hierarchically organizes all buzzes, T. brasiliensis retains a significant capacity to adapt the spectral and temporal patterns of elements within its buzzes.     

Bidirectional Echolocation in the Bat Barbastella barbastellus: Different Signals of Low Source Level Are Emitted Upward through the Nose and Downward through the Mouth

The Barbastelle bat (Barbastella barbastellus) preys almost exclusively on tympanate moths. While foraging, this species alternates between two different signal types. We investigated whether these signals differ in emission direction or source level (SL) as assumed from earlier single microphone recordings. We used two different settings of a 16-microphone array to determine SL and sonar beam direction at various locations in the field. Both types of search signals had low SLs (81 and 82 dB SPL rms re 1 m) as compared to other aerial-hawking bats. These two signal types were emitted in different directions; type 1 signals were directed downward and type 2 signals upward. The angle between beam directions was approximately 70°. Barbastelle bats are able to emit signals through both the mouth and the nostrils. As mouth and nostrils are roughly perpendicular to each other, we conclude that type 1 signals are emitted through the mouth while type 2 signals and approach signals are emitted through the nose. We hypothesize that the “stealth” echolocation system of B. barbastellus is bifunctional. The more upward directed nose signals may be mainly used for search and localization of prey. Their low SL prevents an early detection by eared moths but comes at the expense of a strongly reduced detection range for the environment below the bat. The more downward directed mouth signals may have evolved to compensate for this disadvantage and may be mainly used for spatial orientation. We suggest that the possibly bifunctional echolocation system of B. barbastellus has been adapted to the selective foraging of eared moths and is an excellent example of a sophisticated sensory arms race between predator and prey.     

Gleaning bat echolocation calls do not elicit antipredator behaviour in the Pacific field cricket, <Emphasis Type="Italic">Teleogryllus oceanicus</Emphasis> (Orthoptera: Gryllidae)

Bats that glean prey (capture them from surfaces) produce relatively inconspicuous echolocation calls compared to aerially foraging bats and could therefore be difficult predators to detect, even for insects with ultrasound sensitive ears. In the cricket Teleogryllus oceanicus, an auditory interneuron (AN2) responsive to ultrasound is known to elicit turning behaviour, but only when the cricket is in flight. Turning would not save a cricket from a gleaning bat so we tested the hypothesis that AN2 elicits more appropriate antipredator behaviours when crickets are on the ground. The echolocation calls of Nyctophilus geoffroyi, a sympatric gleaning bat, were broadcast to singing male and walking female T. oceanicus. Males did not cease singing and females did not pause walking more than usual in response to the bat calls up to intensities of 82 dB peSPL. Extracellular recordings from the cervical connective revealed that the echolocation calls elicited AN2 action potentials at high firing rates, indicating that the crickets could hear these stimuli. AN2 appears to elicit antipredator behaviour only in flight, and we discuss possible reasons for this context-dependent function.     

Tiger moths and the threat of bats: decision-making based on the activity of a single sensory neuron

Echolocating bats and eared moths are a model system of predator–prey interaction within an almost exclusively auditory world. Through selective pressures from aerial-hawking bats, noctuoid moths have evolved simple ears that contain one to two auditory neurons and function to detect bat echolocation calls and initiate defensive flight behaviours. Among these moths, some chemically defended and mimetic tiger moths also produce ultrasonic clicks in response to bat echolocation calls; these defensive signals are effective warning signals and may interfere with bats'' ability to process echoic information. Here, we demonstrate that the activity of a single auditory neuron (the A1 cell) provides sufficient information for the toxic dogbane tiger moth, Cycnia tenera, to decide when to initiate defensive sound production in the face of bats. Thus, despite previous suggestions to the contrary, these moths'' only other auditory neuron, the less sensitive A2 cell, is not necessary for initiating sound production. However, we found a positive linear relationship between combined A1 and A2 activity and the number of clicks the dogbane tiger moth produces.     

Frequency tracking and Doppler shift compensation in response to an artificial CF/FM echolocation sound in the CF/FM bat,Noctilio albiventris

Summary Bats of the speciesNoctilio albiventris emit short-constant frequency/frequency modulated (short-CF/FM) pulses with a CF component frequency at about 75 kHz. Bats sitting on a stationary platform were trained to discriminate target distance by means of echolocation. Loud, free-running artificial pulses, simulating the bat's natural CF/FM echolocation sounds or with systematic modifications in the frequency of the sounds, were presented to the bats during the discrimination trials. When the CF component of the artificial CF/FM sound was between 72 and 77 kHz, the bats shifted the frequency of the CF component of their own echolocation sounds toward that of the artificial pulse, tracking the frequency of the artificial CF component.Bats flying within a large laboratory flight cage were also presented with artificial pulses. Bats in flight lower the frequency of their emitted pulses to compensate for Doppler shifts caused by their own flight speed and systematically shift the frequency of their emitted CF component so that the echo CF frequency returns close to that of the CF component of the artificial CF/FM pulse, over the frequency range where tracking occurs.Abbreviations CF constant frequency - FM frequency modulation     

Molecular diet analysis finds an insectivorous desert bat community dominated by resource sharing despite diverse echolocation and foraging strategies

Interspecific differences in traits can alter the relative niche use of species within the same environment. Bats provide an excellent model to study niche use because they use a wide variety of behavioral, acoustic, and morphological traits that may lead to multi‐species, functional groups. Predatory bats have been classified by their foraging location (edge, clutter, open space), ability to use aerial hawking or substrate gleaning and echolocation call design and flexibility, all of which may dictate their prey use. For example, high frequency, broadband calls do not travel far but offer high object resolution while high intensity, low frequency calls travel further but provide lower resolution. Because these behaviors can be flexible, four behavioral categories have been proposed: (a) gleaning, (b) behaviorally flexible (gleaning and hawking), (c) clutter‐tolerant hawking, and (d) open space hawking. Many recent studies of diet in bats use molecular tools to identify prey but mainly focus on one or two species in isolation; few studies provide evidence for substantial differences in prey use despite the many behavioral, acoustic, and morphological differences. Here, we analyze the diet of 17 sympatric species in the Chihuahuan desert and test the hypothesis that peak echolocation frequency and behavioral categories are linked to differences in diet. We find no significant correlation between dietary richness and echolocation peak frequency though it spanned close to 100 kHz across species. Our data, however, suggest that bats which use both gleaning and hawking strategies have the broadest diets and are most differentiated from clutter‐tolerant aerial hawking species.     

Predation risk and mating behavior: the responses of moths to bat-like ultrasound

In the presence of predators, animals may reduce or alter theirmating activities. There has been little experimental studyof whether mating behavior varies with the level of predationrisk. Two species of moths, Pseudaletia unipuncta (Noctuidae)and Ostrinia nubilalis (Pyralidae), significantly reduced theirmate-seeking behavior under high levels of simulated predationrisk. Male moths aborted upwind flight in a pheromone plume,and females stopped releasing pheromone in response to soundssimulating the echolocation calls of bats. For O. nubilalis,but not for P. unipuncta, the response varied significantlywith the level of predation risk. Interspecific differencesin behavioral responses likely reflect differences in physiologicalauditory sensitivity and/or behavioral thresholds. Female behavioralresponses to sounds simulating the calls of bats that gleantheir prey from surfaces were significantly weaker than theirresponses to sounds resembling the calls of aerially hawkingbats; these results support the neurophysiological data thatthe calls of gleaning bats are relatively inaudible to moths.This study indicates that some animals can modify their reproductiveactivities in response to auditory cues from predators.     

Nocturnal activity positively correlated with auditory sensitivity in noctuoid moths

We investigated the relationship between predator detection threshold and antipredator behaviour in noctuoid moths. Moths with ears sensitive to the echolocation calls of insectivorous bats use avoidance manoeuvres in flight to evade these predators. Earless moths generally fly less than eared species as a primary defence against predation by bats. For eared moths, however, there is interspecific variation in auditory sensitivity. At the species level, and when controlling for shared evolutionary history, nocturnal flight time and auditory sensitivity were positively correlated in moths, a relationship that most likely reflects selection pressure from aerial-hawking bats. We suggest that species-specific differences in the detection of predator cues are important but often overlooked factors in the evolution and maintenance of antipredator behaviour.     

Variations in the echolocation calls of the European free-tailed bat

The echolocation calls of Tadarida teniotis were studied in an outdoor flight enclosure (captive individuals) and in the wild using single microphones or an array of four microphones. Calls were characterized by measures of 10 call variables. Comparison of individual calls recorded on four microphones arrayed in a tetrahedron with 1 m between each microphone revealed that all calls were not equally detectable by all microphones but that there were no significant differences in call features obtained from calls recorded on all four microphones. A comparison of 47 calls recorded by all four microphones showed no significant differences in the features of the four recordings of each call. Analysis of calls of five individuals flying individually in an outdoor flight cage revealed significant individual differences in call features. In the field, T. teniotis used long, narrowband search-phase calls, usually without harmonics. Analysis of 1876 search-phase echolocation calls of T. teniotis recorded in the field in Israel and Greece in 2002, 2005 and 2006 showed significant year-to-year and site-to-site differences in some call features. When flying in the presence of conspecifics, T. teniotis changed their echolocation calls. We found a range of different buzzes in the wild, and based on their structure we attempted to classify them as feeding and social buzzes. The features of individual calls comprising buzzes differed significantly among buzzes, and yet there were no consistent differences between what we classified as feeding and social buzzes.     

Seasonal patterns of habitat use by insectivorous bats in a subtropical African agro‐ecosystem dominated by macadamia orchards

We report on acoustic surveys of insectivorous bats conducted during seven months of the year using ANABAT recordings in two habitats (macadamia orchards and adjacent riparian bush) in a subtropical agro‐ecosystem in northern South Africa. We defined two functional foraging groups of bats based on their echolocation calls: (i) open‐air foragers (family Molossidae) having narrow‐band, low‐frequency, low duty cycle calls; and (ii) clutter‐edge foragers (families Miniopteridae and Vespertilionidae), having broad‐band, higher frequency, low duty cycle calls. Bat activity (number of bat passes) was not significantly influenced by habitat. Total bat activity and activity of both functional groups varied significantly between seasons, being highest in summer and autumn (coinciding with annual peaks in numbers of Twin spotted (Bathycoelia natalicola) and Green (Nezara spp) Stinkbugs, order Heteroptera, family Pentatomidae, and Macadamia Nut Borer moths, Cryptophlebia ombrodelta) and lower in winter and spring. No significant effect of moon phase was detected, either on total activity or activity of the two functional groups. We postulate that the significant pattern of seasonality of commuting and/or foraging activity of bats in macadamia orchards (which is more marked in open‐air foragers) may be driven by the seasonal abundance of pest insects such as stinkbugs and Macadamia Nut Borer moths.