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.     

Flight performance, foraging tactics and echolocation in the trawling insectivorous bat Myotis adversus (Chiroptera: Vespertilionidae)

The bat Myotis adversus hunts for prey by aerial hawking and by taking prey from the water surface with its feet (trawling). The flight performance and echolocation of this species were studied in Queensland, Australia, and comparisons were made with Myotis daubentoni , a bat filling a similar ecological niche in the Palaearctic Region. The bats foraged in very similar ways, using the same foraging tactics and feeding in similar habitats, yet they were not geometrically similar in shape. The slightly larger Myotis adversus had relatively larger wings than M. daubentoni , conferring a slightly lower wing-loading. Nevertheless, M. adversus flew faster than M. daubentoni during the searching phase of foraging. Myotis daubentoni turned in tighter circles than M. adversus . Both species used short frequency-modulated (FM) echolocation calls of a characteristic sigmoidal structure, and nulls typically observed in the calls were an observational artefact. Myotis adversus also adopted an unusual 'long'FM call while foraging. The relations between echolocation frequencies and body size were explored in male M. adversus . Specialized morphological and acoustic adaptations for prey capture by trawling in insectivorous bats are discussed.     

Bat Avoidance in Non-Aerial Insects: The Silence Response of Signaling Males in an Acoustic Moth

While the evasive responses of many flying acoustic insects to aerial‐hawking bats are duly recognized and studied, the responses of non‐aerial insects to gleaning bats are generally overlooked. It has been assumed that acoustic insects are deaf to these predators because gleaning bat echolocation calls are typically low in amplitude, brief (1–3 ms) and very high in frequency (>60 kHz). We tested this assumption in a series of playback experiments with a moth (Achroia grisella) that uses hearing in both predator evasion and mating. We report that ultrasound pulses ≥78 dB peSPL (peak equivalent sound pressure level) and ≥1 ms in duration inhibit stationary males from broadcasting their own ultrasonic advertisement calls, provided that the pulsed stimuli are delivered at a repetition rate ≤30/s. Further analyses suggest that inhibition by pulsed ultrasound comprises two processes performed serially. First, a startle response with a latency <50 ms is elicited by a single pulse ≥1 ms duration. Here, a male misses broadcasting several calls over a 50–100 ms interval. Secondly, the startle may be extended as a silence response lasting several to many seconds if subsequent pulses occur at a rate ≤30/s. Call inhibition cannot represent a simple response to acoustic power because of the inverse interaction between pulse duration and rate. On the other hand, the temporal and energy characteristics of inhibitory stimuli match those of gleaning bat echolocation calls, and we infer that inhibition is a specialized defensive behavior by which calling males may avoid detection by eavesdropping bats.     

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.     

The relative influence of competition and prey defences on the trophic structure of animalivorous bat ensembles

Deterministic filters such as competition and prey defences should have a strong influence on the community structure of animals like animalivorous bats which have life histories characterized by low fecundity, low predation risk, long life expectancy and stable populations. We investigated the relative influence of these two deterministic filters on the trophic structure of animalivorous bat assemblages in South Africa. We used null models to test if patterns of dietary overlap were significantly different from patterns expected by chance and multivariate analyses to test the correlations between diet and phenotype (body size, wing morphology and echolocation). We found little evidence that competition structured the trophic niche of coexisting bats. Contrary to predictions from competition, dietary overlap between bats of ensembles and functional groups (open-air, clutter-edge, and clutter foragers) were significantly higher than expected by chance. Instead, we found support for the predictions of the allotonic frequency hypothesis: there were significant relationships between peak echolocation frequency and the proportion of moths in the diets of bats at local and regional scales, and peak echolocation frequency was the best predictor of diet even after we controlled for the influence of body size and phylogeny. These results suggest that echolocation frequency and prey hearing exert more influence on the trophic structure of sympatric animalivorous bats than competition. Nonetheless, differential habitat use and sensory bias may also be major determinants of trophic structure because these are also correlated with frequencies of bat calls.     

Substrate-gleaning versus aerial-hawking: plasticity in the foraging and echolocation behaviour of the long-eared bat,Myotis evotis

The foraging and echolocation behaviour of Myotis evotis was investigated during substrate-gleaning and aerial-hawking attacks. Bats gleaned moths from both the ground and a bark-covered trellis, however, they were equally adept at capturing flying moths. The calls emitted by M. evotis during substrate-gleaning sequences were short, broadband, and frequency-modulated (FM). Three behavioural phases were identified: search, hover, and attack. Gleaning search calls were significantly longer in duration, lower in highest frequency, and larger in bandwidth than hover/attack calls. Calls were detected in only 68% of gleaning sequences, and when they were emitted, bats ceased calling 200 ms before attacking. Terminal feeding buzzes, the rapid increase in pulse repetition rate associated with an attempted prey capture, were never recorded during gleaning attacks. The echolocation calls uttered by M. evotis during aerial-hawking foraging sequences were also short duration, high frequency, FM calls. Two distinct acoustic phases were identified: approach and terminal. Approach calls were significantly different from terminal calls in all variables measured. Calls were detected in 100% of aerial-hawking attacks and terminal feeding buzzes were invariably produced. Gleaning hover/attack calls were spectrally similar to aerial approach calls, but were shorter in duration and emitted at a significantly lower (but constant) repetition rate than aerial signals. Although the foraging environment (flight cage contents) remained unchanged between tasks (substrate-gleaning vs. aerial-hawking), bats emitted significantly lower amplitude calls while gleaning. We conclude that M. evotis adjusts its echolocation behaviour to meet the perceptual demands (acoustical constraints) imposed by each foraging situations.Abbreviations BW bandwidth - CF constant frequency - dB SPL decibels sound pressure level - FM frequency modulated - HF highest frequency - LF lowest frequency - PF peak frequency Presented at the meeting Acoustic Images in Bat Sonar, a conference on FM echolocation honoring Donald R. Griffin's contributions to experimental biology (June 14–16, Brown University, Providence RI).     

菲菊头蝠回声定位声波频率的性二态有利于性别识别

许多动物的叫声频率呈现性二态现象。蝙蝠夜间活动,主要利用声音信号导航空间、追踪猎物、传递交流信息。本研究选择成体菲菊头蝠作为研究对象,检验回声定位声波频率性二态是否有利于性别识别。研究发现,菲菊头蝠回声定位声波频率参数具有显著性别差异。播放白噪音、雄性回声定位声波及雌性回声定位声波期间,实验个体的反应叫声数量依次递减。播放白噪音、雌性回声定位声波及雄性回声定位声波后,实验个体的反应叫声数量依次递增。白噪音诱导反应叫声强度高于回声定位声波诱导反应叫声强度。研究结果表明,菲菊头蝠回声定位声波的频率参数编码发声者性别信息,有利于种群内部的性别识别。本研究暗示,回声定位声波可能在蝙蝠配偶选择中扮演一定作用。     

Support for the allotonic frequency hypothesis in an insectivorous bat community

The allotonic frequency hypothesis proposes that certain insectivorous bat species can prey upon moths that can hear bat echolocation calls by using echolocation frequencies outside the sensitivity range of moth ears. The hypothesis predicts that the peak frequencies of bat echolocation calls are correlated with the incidence of moths in the diets of these bats. The aim of this study was to test this prediction on a bat community dominated by bats using low duty cycle echolocation calls, i.e. aerial foraging, insectivorous species using frequency modulated calls. The community consisted of nine species, two molossids, Sauromys petrophillus and Tadarida aegyptiaca, five vespertilionids, Eptesicus capensis, Eptesicus hottentotus, Miniopteris schreibersii, Myotis tricolor, and Myotis lesueuri, one rhinolophid, Rhinolophus clivosus, and one nycterid, Nycteris thebaica. The insect fauna in the habitat used by the bat community was suited to the testing of the allotonic frequency hypothesis because more than 90% of the moths comprising the insect fauna were tympanate. These included Pyralidae (3.8%), Geometridae (44.9%), Notodontidae (3.8%), Arctiidae (4.6%), Lymantriidae (0.8%) and Noctuidae (32.4%). As predicted, peak echolocation frequency was correlated with the incidence of moths in the diets of these nine species (r=0.98, df=7, P<0.01). Furthermore, multivariate analysis revealed that echolocation frequency (t=9.91, n=129, P<0.001) was a better predictor of diet than forearm length (t=5.51, n=129, P<0.001) or wing area (t=-3.41, n=129, P<0.001). This suggests that the selection pressure exerted by moth hearing might have acted directly on call frequency and secondarily on body size and wing morphology, as part of the same adaptive complex. It is unlikely that dietary differences were due to temporal and spatial differences in the availability of prey because the pattern of differences in skull morphology of the nine species supported our dietary analyses. The skull morphology of a bat represents a historical record of the kind of diet it has become adapted to over its evolutionary history. These results suggest that prey defences may mediate other factors structuring bat communities, e.g. competition. Competition may be reduced for those species of bats that can circumvent prey defences.     

The foraging ecology of the mountain long-eared bat Plecotus macrobullaris revealed with DNA mini-barcodes

Molecular analysis of diet overcomes the considerable limitations of traditional techniques for identifying prey remains in bat faeces. We collected faeces from individual Mountain Long-eared Bats Plecotus macrobullaris trapped using mist nets during the summers of 2009 and 2010 in the Pyrenees. We analysed their diet using DNA mini-barcodes to identify prey species. In addition, we inferred some basic features of the bat's foraging ecology that had not yet been addressed. P. macrobullaris fed almost exclusively on moths (97.8%). As prey we detected one dipteran genus (Tipulidae) and 29 moth taxa: 28 were identified at species level (23 Noctuidae, 1 Crambidae, 1 Geometridae, 1 Pyralidae, 1 Sphingidae, 1 Tortricidae), and one at genus level (Rhyacia sp., Noctuidae). Known ecological information about the prey species allowed us to determine that bats had foraged at elevations between 1,500 and 2,500 m amsl (above mean sea level), mostly in subalpine meadows, followed by other open habitats such as orophilous grasslands and alpine meadows. No forest prey species were identified in the diet. As 96.4% of identified prey species were tympanate moths and no evidence of gleaning behaviour was revealed, we suggest P. macrobullaris probably forages by aerial hawking using faint echolocation pulses to avoid detection by hearing moths. As we could identify 87.8% of the analysed sequences (64.1% of the MOTUs, Molecular Operational Taxonomic Units) at species level, we conclude that DNA mini-barcodes are a very useful tool to analyse the diet of moth-specialist 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.     

Strategy-switching in the gaffing bat

Foraging in Daubenton's bats Myotis daubentonii , at two altitudinal locations along a river gradient in North Wales was investigated in relation to aerial insect density and to the density of prey on the water surface. Prey capture in Daubenton's bats consisted of aerial hawking, where prey was taken in the air, and trawling, where bats gaffed invertebrates from the water surface. Aerial hawking accounted for 86% of all prey capture attempts, despite aerial insect availability falling close to zero for much of the night. Conversely, prey density on the water surface was an order of magnitude higher than aerial prey density and increased through the night due to aquatic invertebrate drift. At the higher altitude site, M. daubentonii switched prey capture strategy to gaffing, possibly to reflect this change in prey availability on the water's surface, but at the lower altitude site, they maintained aerial hawking as the preferred strategy. The switch to gaffing may be inhibited by the significant downstream accumulation of large numbers of inedible exuviae of caddis flies, Trichoptera, at the low-altitude site, which form both acoustic clutter and increase the probability of capturing inedible prey, making foraging less efficient. These small altitudinal differences in foraging strategy should be factored into the design of future altitudinal bat foraging studies and if found to be a widespread strategy, taken into consideration by conservation planners when reviewing the habitat requirements of Daubenton's bats in river valleys within the United Kingdom.     

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

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

Functional differences in echolocation call design in an adaptive radiation of bats

All organisms have specialized systems to sense their environment. Most bat species use echolocation for navigation and foraging, but which and how ecological factors shaped echolocation call diversity remains unclear for the most diverse clades, including the adaptive radiation of neotropical leaf‐nosed bats (Phyllostomidae). This is because phyllostomids emit low‐intensity echolocation calls and many inhabit dense forests, leading to low representation in acoustic surveys. We present a field‐collected, echolocation call dataset spanning 35 species and all phyllostomid dietary guilds. We analyze these data under a phylogenetic framework to test the hypothesis that echolocation call design and parameters are specialized for the acoustic demands of different diets, and investigate the contributions of phylogeny and body size to echolocation call diversity. We further link call parameters to dietary ecology by contrasting minimum detectable prey size estimates (MDPSE) across species. We find phylogeny and body size explain a substantial proportion of echolocation call parameter diversity, but most species can be correctly assigned to taxonomic (61%) or functional (77%) dietary guilds based on call parameters. This suggests a degree of acoustic ecological specialization, albeit with interspecific similarities in call structure. Theoretical MDPSE are greatest for omnivores and smallest for insectivores. Omnivores significantly differ from other dietary guilds in MDPSE when phylogeny is not considered, but there are no differences among taxonomic dietary guilds within a phylogenetic context. Similarly, predators of non‐mobile/non‐evasive prey and predators of mobile/evasive prey differ in estimated MDPSE when phylogeny is not considered. Phyllostomid echolocation call structure may be primarily specialized for overcoming acoustic challenges of foraging in dense habitats, and then secondarily specialized for the detection of food items according to functional dietary guilds. Our results give insight into the possible ecological mechanisms shaping the diversity of sensory systems, and their reciprocal influence on resource use.     

蝙蝠回声定位声波的可塑性及其生态适应

蝙蝠通过调节回声定位声波特征来满足自身的感官需求,表现出回声定位声波的可塑性及其对生态环境与需求的适应。声波频率、强度、脉冲持续时间和间隔时间等特征与蝙蝠所处的生态位密切相关,声波可塑性在蝙蝠进化过程中起着至关重要的作用。本文结合马铁菊头蝠(Rhinolophus ferrumequinum)和大趾鼠耳蝠(Myotis macrodactylus)回声定位声波可塑性的研究,从回声定位声波的方向性、目标距离、环境复杂度和应对干扰4个方面总结了蝙蝠如何通过改变回声定位声波特征来满足自身在导航和捕捉猎物过程中的感官需求与生态适应,并阐述了回声定位声波可塑性的研究现状,为开展蝙蝠声学和行为学研究提供参考。     

Bat echolocation calls: adaptation and convergent evolution

Bat echolocation calls provide remarkable examples of 'good design' through evolution by natural selection. Theory developed from acoustics and sonar engineering permits a strong predictive basis for understanding echolocation performance. Call features, such as frequency, bandwidth, duration and pulse interval are all related to ecological niche. Recent technological breakthroughs have aided our understanding of adaptive aspects of call design in free-living bats. Stereo videogrammetry, laser scanning of habitat features and acoustic flight path tracking permit reconstruction of the flight paths of echolocating bats relative to obstacles and prey in nature. These methods show that echolocation calls are among the most intense airborne vocalizations produced by animals. Acoustic tracking has clarified how and why bats vary call structure in relation to flight speed. Bats using broadband echolocation calls adjust call design in a range-dependent manner so that nearby obstacles are localized accurately. Recent phylogenetic analyses based on gene sequences show that particular types of echolocation signals have evolved independently in several lineages of bats. Call design is often influenced more by perceptual challenges imposed by the environment than by phylogeny, and provides excellent examples of convergent evolution. Now that whole genome sequences of bats are imminent, understanding the functional genomics of echolocation will become a major challenge.     

The role of echolocation in the hunting of terrestrial prey – new evidence for an underestimated strategy in the gleaning bat, Megaderma lyra

The observation that gleaning bats detect prey by its noises, together with difficulties in recording their faint sonar calls, have led some authors to conclude that gleaning bats may not use echolocation in certain hunting situations. In particular, it is conjectured that echolocation plays no role in the classification and tracking of prey. In the present study, we show that the gleaning bat, Megaderma lyra, is able to find silent and motionless prey on the ground. The significance of sonar for catching a variety of terrestrial prey is established in a standardized situation. Sonar calls were found to be emitted during all stages, i.e. approach, hovering above the prey, and return to the roost, of every hunting flight. The harmonic pattern of the calls differed significantly between these stages, calls with three or more prominent components prevailing during hovering. Bats identified prey and rejected dummies while hovering above them. During this stage, increased call rates and reduced call durations were found. Echolocation activity during, and the duration of, the hovering phase depended on prey type, in particular on prey movement. The prey-dependent shifts in sonar activity, the broadband call structure with an emphasis on higher harmonics, and a systematic shift of the calls' peak frequencies during hovering, are discussed as adaptations to identifying prey by sonar.     

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.     

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.     

Flight performance, echolocation and foraging behaviour in noctule bats Nyctalus noctula

The noctule Nyctulus noctula (Schreber, 1774) is a relatively large (c. 25 g) insectivorous bat which catches insects on the wing (by aerial hawking). Emergence at a maternity roost was earliest relative to sunset when females were lactating, and bats may then have risked predation by flying at higher light levels during a period of high energy demand. Flight performance was quantified by using stereophotogrammetry. At feeding sites bats flew at 6.0 ± 2.1 m/s. This was faster than predicted minimum power speed (V _mp), and either between V _mp and maximum range speed (V _mr), or close to their predicted V _mr, depending on which aerodynamic model of flight power requirements was used. The echolocation behaviour of noctules is flexible. Long duration, low frequency calls (c. 20 kHz) with little frequency modulation were emitted while cruising, but at foraging sites the calls became more frequency-modulated. As the noctule is traditionally thought of as using low frequency echolocation, it was expected to receive weak echoes from small targets and therefore to specialize in eating large insect prey. Although the bats ate mainly beetles, large numbers of small dipterans were also eaten. The noctule is probably able to detect such small items because, when foraging, its calls become broadband and sweep from high frequencies. Higher harmonics are also present, and these may assist in the detection of small prey. In noctules, as in many bats, there appears to be a 1:1 link between wingbeat and call production during the search phase of foraging.