570 BioScience July 2001 Vol 51 No 7

Articles

Some insects have evolved audition and evasive behaviors in response to selective pressure from bats and

other insects were preadapted to detecting ultrasonic sig-nals Some bats have evolved in turn improving the range orresolution of sonar signals and serendipitously making themless detectable by insects In other words there is a kind of evo-lutionary escalation going on between bats and insects Ouraim with this review is to present the complex interactions be-tween echolocating bats and insects with bat-detecting earsand show how these interactions may be advantageous forpredator or prey To document our examples we cite mostlynewer studies and reviews in which the reader can find ref-erences to original works

Insects occupied all terrestrial habitats at least 300 millionyears ago long before bats appeared in the Eocene about 50million years ago Ears have appeared independently 19 timesin the class Insecta In the period before bats ears and com-plex acoustical behaviors appeared independently in at leastseven orders of insects (Hoy et al 1989 Robert et al 1992 Yager1999) Antibat tactics which must have appeared in insectssince the Eocene are now known in members of four ordersLepidoptera (moths and nocturnal butterflies) Orthoptera(crickets) Dictyoptera (praying mantids) and Neuroptera(green lacewings) and possibly also in the Diptera (flies)and Coleoptera (beetles)

Insect tympanal organs or ears consist basically of an ex-ternal thin membrane (the tympanum) and associated in-ternal air sacs or tracheae The auditory (sensory) cells attachto the tympanum or to an internal membrane (Yager 1999)Tympanal organs of most modern tympanate insects re-spond to a wide band of frequencies extending well into theultrasonic range (above 20 kHz)as was probably true for pre-Eocene tympanate insects as well Tympanate insects arephysically small animals that can produce high-frequency

sounds more efficiently hence high frequencies are used bymany insects for acoustical communication between con-specifics Consequently many sonorous insects werepreadapted to the evolution of bats (Hoy 1992)

According to one possible scenario a vast larder of noc-turnal flying insects awaited exploitation and a flying mam-mal the microchiropteran bat was one successful exploiterEcholocation or biosonar was a prerequisite for success indarkness and even the first nocturnal bats probably used it(see Hoy 1992) Most of the nearly 700 microchiropteranbat species eat insects that they detect using biosonar (Schnit-zler and Kalko 2001) However bat biosonar has two majordisadvantages attenuation and forewarning

The frequencies used by echolocating bats range generallyfrom 20 kHz to 100 kHz with some outliers using frequen-

Lee A Miller (e-mail Leedoudk) and Annemarie Surlykke are as-

sociate professors at the Center for Sound Communication Institute

of Biology Odense University (SDU) DK-5230 Odense M Denmark

copy 2001 American Institute of Biological Sciences

How Some Insects Detectand Avoid Being Eaten byBats Tactics andCountertactics of Prey andPredatorLEE A MILLER AND ANNEMARIE SURLYKKE

EVOLUTIONARILY SPEAKING INSECTS

HAVE RESPONDED TO SELECTIVE PRESSURE

FROM BATS WITH NEW EVASIVE

MECHANISMS AND THESE VERY

RESPONSES IN TURN PUT PRESSURE ON

BATS TO ldquoIMPROVErdquo THEIR TACTICS

July 2001 Vol 51 No 7 BioScience 571

Articles

cies below 10 kHz or above 200 kHz Higher frequencies im-prove resolution but they attenuate at a greater rate (Surlykke1988) and the detection distance is reduced accordingly Thesource level is the sound pressure level (SPL relative to 20microPa) in decibels (dB) measured 10 cm in front of the batrsquosmouth A bat using a source level of 110 dB at 20 kHz coulddetect the echo from an object the size of a moth at more than5 m Detection would occur at no more than 24 m if the batused 100 kHz (Surlykke 1988) From the insectsrsquo perspectivebats advertise their presence with the ultrasonic pulses usedto stroboscopically probe the environment Thus insects areforewarned if they can hear ultrasound This coincidentallyexerts considerable selection pressure against those insects thateither cannot hear or do not react (Miller 1982)

Thus the stage was set in the Eocene for an evolutionaryescalation between bats and insects Evasive behaviors inexisting tympanate insects (presumably crickets locusts andmantids) probably appeared in response to selection pressureby bat predation (Hoy 1992) The same selection pressuregenerated new auditory and motor mechanisms in presum-ably earless insects (green lacewings and moths) Batstoo could have developed countermeasures for exampleshifting signals out of the preyrsquos hearing range (Fenton andFullard 1981) or modifying hunting behaviors (Miller andOlesen 1979)

Avoidance behaviors

Preadaptation Preexisting auditory systems in insectsmay have been preadaptively sensitive to bat echolocationTympanate insects that were normally diurnal may also havebecome active at night Crickets locusts and mantids areconsidered here because they were probably some of the ear-liest insects with hearing and they are mostly active during theday but often fly (migrate or disperse) at twilight and atnight However all crepuscular and nocturnal insects are po-tential prey for bats

Crickets The most intensively studied insect auditory sys-tem is that of field crickets (Figure 1a left) The majority ofthese studies concern intraspecific communication The tibiaof each foreleg contains an ear (Figure 1a middle) For ex-ample the maximum sensitivity of the cricket Gryllus bi-maculatus occurs at about 5 kHz as measured electrophysi-ologically from the auditory nerve This is also the frequencyof the calling song However the ear is sensitive to sound fre-quencies up to 100 kHz at least

Popov and Shuvalov (1977) first reported that dispersingcrickets avoid being hunted by bats Since then Ron Hoy atCornellAndrej Popov in St Petersburg and their colleagueshave documented avoidance behavior in several species ofcrickets both behaviorally and neurophysiologically (see Hoyet al 1989) Crickets in stationary flight steer away from thesource of ultrasound (negative phonotaxis) with the most ef-fective frequencies lying between about 10 kHz and 80 kHz(Figure 1a right) An interneuron in Teleogryllus oceanicus

(Int 1) initiates evasive behavior (Hoy et al 1989) and its ho-mologue in Gryllus bimaculatus (AN2 Popov et al 1994)presumably does the same The threshold for AN2 at 20 kHzis about 20 dB less than that of the behavior (Figure 1aright) meaning that the neural response is more sensitive thanthe behavior Some mole crickets hear ultrasound in part withspecial neuronal pathways and free-flying crickets showavoidance to batlike sounds (Mason et al 1998)

Bush crickets (Figure 1b left) like field crickets have theirears and associated acoustic tracheae in the tibia of the forelegs(Figure 1b middle) Some species communicate entirely inthe ultrasonic range Many bush crickets can hear bats butfew seem to react to bat echolocation However the bushcricket Neoconocephalus ensiger shows an acoustic startleresponse during tethered flight in the laboratory (Faure andHoy 2000) When the insects hear intense batlike soundswith frequencies from 15 kHz to at least 60 kHz (Figure 1bright) they dive However they exhibit no directionality withrespect to the sound source even though bush crickets havedirectional hearing A large prothoracic interneuron the T-neuronparticipates in mediating the behavior (Faure and Hoy2000) The T-neuron is most sensitive to frequencies higherthan those of the calling song (13 kHz peak frequency) for thespecies The threshold is about 50 dB less than that of the be-havior at 20 kHz (Figure 1b right)

Locusts Another primarily diurnal orthopteran the locustLocusta migratoria (Figure 1c left) has a pair of general pur-pose abdominal ears (Figure 1c middle) that are well stud-ied anatomically physically and physiologically Howeverthe role of hearing in the life of this locust remains poorly un-derstood One function of hearing may be to mediate nega-tive phonotaxis in response to batlike signals although to ourknowledge there are no published reports of locusts re-sponding to bats A locust in stationary flight rudders with itsabdomen and increases the wingbeat frequency both ofwhich produce turning in the direction opposite to the soundsource (Robert 1989) Negative phonotactic behavior occursonly at frequencies above 10 kHz (Figure 1c right) Roumlmeret al (1988) found interneurons sensitive to high frequenciesthat selectively receive input from auditory afferents Theseinterneurons control head and abdominal movements and arecandidates for controlling negative phonotaxis Figure 1c(right) shows the auditory sensitivity of one of these (SN-5)

Praying mantids Praying mantids (Figure 1d left) are pri-marily diurnal but many make dispersal flights at night(Cumming 1996) Although previously thought to be deafmany species in the suborder Mantodea actually possess ears(Yager and Hoy 1986) The tympanal organ sensitive to ul-trasound is hidden deep in a cleft between the two metatho-racic coxae (Figure 1d middle) and consists of two closely op-posed stiff tympanal membranes A cluster of sensory cellsis attached to each tympanal membraneThe ears are thoughtto function as a single organ (Hoy et al 1989) Flying man-tids (Parasphendale agrionina) react at distances as great as

572 BioScience July 2001 Vol 51 No 7

Articles

Figure 1 Insects with audition secondarily adapted for hearing bats Representative insects from the various families areshown in the left column with the location of the ear as indicated by the arrow The general anatomy of each ear is shown inthe middle column The tuning curves for avoidance behaviors (negative phonotaxis for orthopterans and nondirectionalresponses for the mantid) and interneurons thought to be involved with the behaviors are shown in the right column Thefrequency range for typical bat biosonar signals is shown on the abscissa (d right) (a middle) A cross section of the ear of acricket Gryllus bimaculatus (modified from Larsen et al 1989) (b middle) A longitudinal section of the ear of an ensiferanHemideina cassisens (modified from Ball and Field 1981) (c middle) A horizontal section through the ear of an acrididLocusta migratoria (modified from Schwabe 1906) (d middle) A partial dissection of the ventral surface of a mantidMantis religiosa (modified from Yager and Hoy 1986) (d right) The behavioral data are from Parasphendale agrioninaand the neuronal data are from M religiosa

10 m from a loudspeaker emitting batlike signals at naturalintensities They react by turning or with dives and spiral flightThe responses are all nondirectional as would be expectedfrom a functionally monaural system The lowest thresholdfor avoidance behavior occurs from 20 kHz to 80 kHz (Fig-ure 1d right Yager 1999) Yager identified an interneuronwhose tuning curve resembles that of the behavior (Figure 1dright) albeit in another species (Mantis religiosa) The neu-ron is most likely part of a neural circuit for avoidance be-havior although attempts to elicit avoidance behavior fromM religiosa to artificial bat signals have thus far failed

Flies and beetles We suspect that some flies can hearand react to bats but evidence at present is not sufficient toput them on the growing list of bat-detecting insects Thelarviparous tachinid flies Ormia ochracea and Therobialeonidei parasitize crickets and bush crickets respectively(Lakes-Harlan and Heller 1992 Robert et al 1992) The call-ing songs of their nocturnal hosts attract female flies Ormiaochracea hears best at 5 kHz as measured electrophysiologi-cally from the neck connectiveThis frequency is near the peakpower output of the hostrsquos song but the flyrsquos hearing ex-tends into the ultrasonic range The hearing of T leonidei isalso tuned to its host which sings mostly in the ultrasonicrange These flies can surely hear bats but their reactions tobatlike signals or to bats in nature are unknown

Beetles the largest order of insects are heavily preyed onby some bats and until recently ears were unknown in bee-tles The tiger beetle Cicindela marutha has ears on the firstabdominal segment that are sensitive to sound between 30 kHzand 60 kHz Batlike signals provoke changes in the beetlersquos be-havior during stationary flight which include the productionof ultrasonic clicks a property shared only with some arctiidmoths (see below Yager et al 2000) Hearing in tiger beetlesmay be used for intraspecific communication especially be-cause they also produce clicking sounds while on the groundAt present we assume that hearing in these beetles has beensecondarily adapted for detecting bats

In response to pulsed ultrasound flying scarab beetlesEutheola humilis dropped or flew toward the ground andwalking beetles stopped They hear best at 45 kHz The earsare in the neck region and have evolved independently fromthose in tiger beetles (Forrest et al 1997) perhaps specificallyfor bat detection

New auditory systems Ears have evolved independentlyin many families of eight (perhaps nine) superfamilies ofmoths (Minet and Surlykke 2002) Physiological and behav-ioral results when available for Noctuoidea PyraloideaGeometroidea Sphingoidea and Drepanoidea indicate thatthe ears are adapted specifically for hearing bat signals Veryrecently evasive behavior to batlike ultrasound was docu-mented in nocturnal butterflies of the superfamily Hedy-loidea that have ears on their wings (Yack and Fullard 2000)Green lacewings (Chrysopidae) also have ears on their wingsthat are sensitive to ultrasound and function as bat detectors

A lack of frequency sensitivity is common to all these hear-ing organs Moths and green lacewings are tone deaf In con-trast audition in orthopterans and mantids which is prob-ably secondarily adapted for hearing bats shows frequencyselectivity Nevertheless selection pressure has shaped thetuning curves the hearing or behavioral sensitivity to differ-ent sound frequencies of moth hearing Many Nearcticspecies of noctuoids hear best between 20 and 40 kHzwhereas tropical noctuoids hear best over a broader range ofultrasonic frequencies and are more sensitive than theirNearctic relatives (Fullard 1984a) A good example of this isthe noctuid Ascalapha odorata Its ear is tuned to the biosonarand social calls of the one bat species on the Hawaiian islandKauai The same or a closely related species of moth inPanama on Barro Colorado Island has a lower threshold ofhearing and a broader tuning curve This is probably anadaptation to the broader range of frequencies used by themany insectivorous bat species found there (Fullard 1984a)

Moths Ken Roeder made noctuid moths famous throughhis numerous studies of their hearing and behavior (Roeder1967a) The Noctuidae Notodontidae and Arctiidae (all inthe superfamily Noctuoidea Figure 2a left) have ears on thelateral surfaces of the metathorax (Figure 2a middle) Behindthe thin tympanal membrane is a large air sac which is sep-arated from other air sacs by tracheal membranes Two sen-sory cells A1 and A2 (but a single A cell in notodontids seeSurlykke 1988) are attached to the tympanum The two cellshave identical tuning curves (Figure 2a right) and dynamicranges but they differ by about 20 dB in sensitivity Dynamicrange is the range over which neural responses occur tosound intensity measured in dB from threshold to saturationThe noctuid and arctiid moths have a total auditory dynamicrange of about 40 dB

Freely flying unidentified moths exhibit a variety of be-havioral responses to bats and to synthetic batlike signals(Roeder 1967a for recent results refer to Acharya and Fen-ton 1992) Moths far from the source often turn and fly awaywhereas those close to the source show zigzag and loopingflight power dives or passive falls Presumably the loudersounds recruit the A2 sensory cells which trigger the switchfrom negative phonotaxis to less predictable evasive flight be-havior However Roeder (1964) indicated that the percent-age of moths showing turning-away responses decreases andthe percentage showing looping responses increases as thepulse repetition rate increases Because of this Roeder (1964)suggested that the most sensitive sensory cell (A1) actingalone could release several behaviors but further experi-mentation is needed to confirm this

Size and sensitivity are correlated in moths complicatingmatters further Big moths reflect more intense echoes thansmall moths and may be detected by bats as far away as 10 mHowever results from noctuid moths show that big moths arealso more sensitive and may detect approaching bats as faraway as 100 m Thus there seems to be a fairly constant 10-fold margin of safety that is noctuid moths can detect bats

July 2001 Vol 51 No 7 BioScience 573

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574 BioScience July 2001 Vol 51 No 7

Articles

Figure 2 Insects with audition adapted specifically for hearing bats Representative insects from the various families areshown in the left column with the location of the ear indicated by arrow The general anatomy of each ear is shown in themiddle column The tuning curves for flight cessation (behavior) the A1 sensory cells and an interneuron are shown inthe right column The frequency range for typical bat biosonar signals is shown on the abscissa (d right) (a middle) Ahorizontal section through the metathorax of a noctuid moth (modified after Eggers 1919) (b middle) A cross sectionthrough the first abdominal segment of a geometrid moth viewed from the inside (modified after Kennel and Eggers1933) A single tympanal air sac occupies the space behind the tympana (not seen in this drawing) The pyralid ear (egGalleria mellonella) is anteroabdominal like that of the geometrid (b right) Data for a geometrid Biston betularia(modified from Surlykke and Filskov 1997) as well as for a pyralid Galleria mellonella (c middle) The head of asphingid moth Celerio lineata with one labial palp in longitudinal section The sound receivers (pilifers) are seen on thelateral surface of the proboscis (modified from Roeder et al 1970) (d middle) The ventral surface of the base of the wingof the green lacewing Chrysoperla carnea (modified after Miller 1975) References for tuning curves are given in the text

at about 10 times the distance over which bats can detectmoths (Surlykke et al 1999)

Many interneurons in the thoracic and cephalic ganglia ofnoctuids have been characterized (Roeder 1975 Boyan andFullard 1986) For example two identified neurons receive di-rect input from the A1 afferent in parallelbut they process tem-poral information differently (Boyan and Miller 1991) Synap-tic input to some motor neurons controlling the upndashdownmovement of the wings occurs only when the A2 sensory cellis activated (Madsen and Miller 1987) The role individual in-terneurons play in eliciting behavior is speculative principallybecause the responses of moths are exceedingly difficult tostudy under controlled conditions (Roeder 1967b)

Arctiid moths behave like noctuids but are more reluctantto do so In addition some arctiids produce ultrasonic click-ing sounds from tymbal organs when they hear bat signals orare touched (The clicks have various effects on bats as de-scribed below) Cycnia tenera starts clicking before it stops fly-ing in response to ultrasonic stimuli (Fullard 1979) Thethreshold for flight cessation is about 10ndash20 dB above that forclicking and repetition rates from 17ndash40 pulses per secondare best at eliciting clicking (Fullard 1984b) Also the rate ofmotor spikes to the tymbal muscles increases when the stim-ulus rate increases (Northcott and Fullard 1996) So both am-plitude and pulse repetition rate of the ultrasonic stimulus in-fluence behavioral responses from noctuid and arctiid moths

The Geometridae Pyralidae and Drepanidae have ultra-sound-sensitive ears on the first abdominal segment (Minetand Surlykke 2001) In the geometrids (Figure 2b left) thetympana are adjacent to the midline and point caudally (Fig-ure 2b middle) The tympana in pyralids point rostrally andhave a slight tilt ventrallyFour sensory (A) cells attach to eachtympanum The dynamic range for hearing in the geometridBiston betularia is about 50 dB because each cell covers asmaller range (10ndash15 dB) than the A cells in a noctuid ear Thefrequency range of hearing extends to at least 100 kHz in allspecies studied thus far (Figure 2b right B betularia Surlykkeand Filskov 1997) Some geometrids show flight cessation andother responses to ultrasound (Rydell et al 1997) Pyralid waxmoths respond to bat cries (Spangler and Takessian 1983) andGalleria mellonella shows a number of behavioral responseswhile in stationary flight the most noticeable of which isflight cessation (Skals and Surlykke 2000) Flight cessationwhich is the behavior with the highest threshold occurs at +20to +25 dB with respect to the threshold for the A1 cell (Fig-ure 2b right G mellonella) Actually avoidance behavior tobat echolocation is so powerful that some pyralid (and noc-tuid) moths abort sexually oriented flight to females broad-casting pheromones (Acharya and McNeil 1998)

The bat-detecting ear of some hawk moths (Figure 2cleft) consists of air-filled labial palps that transmit sound en-ergy to the pilifers located on either side of the proboscis(Figure 2c middle) Other hawk moths have scale plates onthe labial palps rather than air-filled palps Neurophysiolog-ical recordings from the labial nerve or from interneurons re-veal the auditory characteristics in both types of hawk moths

(Figure 2c right) They are most sensitive to frequencies be-tween 20 and 30 kHz with a threshold of 40ndash50 dB sound pres-sure level The dynamic range of the single auditory sensoryneuron in the pilifer is about 20 dB resembling that in the earof notodontid moths Hawk moths in tethered flight respondto ultrasound with changes in flight speed with nondirectionalturning and sometimes by emitting sound The behavioralthreshold is about 70 dB SPL or 20 dB above the sensorythreshold (Roeder et al 1970 Goumlpfert and Wasserthal 1999)

Green lacewings The ear of the green lacewing (Figure 2dleft) is located in a bulge near the base of the radial vein in eachforewing (Figure 2d middle) It is a true tympanal organwhich is mostly fluid filled and contains a small trachea It isthe smallest tympanal organ knownPerhaps only 6 of the 25sensory cells actually respond to ultrasound (see Miller 1984for a review) Like wax moths green lacewings in stationaryflight show a number of responses to lower intensity stimulibefore ceasing their flight (Miller 1975) Flight cessation (Fig-ure 2d right) occurs most reliably to ultrasonic signals broad-cast at rates of 1ndash50 pulses per second High stimulus repe-tition rates alone were ineffective in stopping the flight ofrestrained green lacewings

A more realistic picture of behavior emerged from studieson freely flying green lacewings and bats (Figure 3) Bat sig-nals at low repetition rates possibly combined with low in-tensities cause insects to fold their wings and passively diveThe green lacewing shows this nondirectional early-warningresponse to batsrsquo searching signals (Figure 3 between flashes2 and 3) The bat increases its call rate as it approaches a fallinginsect (Figure 3 flashes 3 to 4) Just before capturing its preythe bat increases its repetition rate to a maximum of about200 signals per second in the terminal phase for most bats (Fig-ure 3 flash 5) During the terminal phase the insect suddenlyflipped open its wings (Figure 3 flash 5 arrow) presumablyin response to the high repetition rate signals This last-chance response breaks the dive and foils the bat in this caseafter which the insect continues its dive (Figure 3 flash 6)Artificial bat signals mimicking the sequence shown in Fig-ure 3 evoke the same behavior (Miller and Olesen 1979) Byrepeating the experiments with deafened green lacewingswe showed that the selective advantage of reactors over non-reactors was 47 or about the same as that found for moths(see Miller 1982) Unidentified neurons in the prothoracic gan-glion respond to ultrasound but their role in eliciting behavioris unknown (Miller 1984)

Conclusions about insect behaviorsWe can draw some conclusions and make predictions basedon what we know about avoidance behaviors Looking at allthe behavioral response types for all the insects mentionedabove we find that the best frequency the frequency at whichneural or behavioral responses have the lowest thresholdlies between about 20 and 60 kHz with thresholds betweenabout 30 and 70 dB SPL The response latencies range from40ndash70 ms at +15 dB with respect to the behavioral threshold

July 2001 Vol 51 No 7 BioScience 575

Articles

Because the distance at which the insects respond to 40 kHzsounds varies from 65ndash37 m for bats using intense signalsthe insects have several tenths of a second to avoid even fast-flying bats (Surlykke 1988) The situation is somewhat differentfor whispering bats which use intensities of less than about75 dB SPL and hunt near vegetation Here the response dis-tances for flying insects are from 01ndash27 m depending on thehearing threshold However bats can detect a moth-sizedecho at about 06 m putting the less-sensitive insects in dan-ger Many of the insects mentioned above are open-air fliersand normally do not meet whispering bats

The tuning of neurons suspected to be involved in avoid-ance behavior in preadapted insects such as crickets grasshop-pers and preying mantids poorly match the behavioral tun-ing This discrepancy suggests that these auditory neurons havebeen molded into an antibat circuitry as a result of selectionpressure Behaviors such as turning in midflight or flightcessation have thresholds typically 20 dB higher than thosefor sensory neurons or interneurons (except premotor in-terneurons) in the same insects Consequently yet undis-covered behaviors to low stimulus intensities may provide ad-ditional survival advantage

Insect avoidance behaviors and their underlying mecha-nisms are undoubtedly complicated Take for example the vari-ability of responses The behaviors cannot be reliably predictedand the same individual may show different responses or noresponse at all to the same stimulus Roeder called this theldquoevitabilityrdquoof behavior which provides a survival advantageby making it difficult for the predator to predict what the preywill do The characteristic feature of evitability makes it dif-ficult to study but it seems to be present in the behavior and

physiology of some moths (Roeder 1975 Madsen and Miller1987) and green lacewings (Miller and Olesen 1979)Nevertheless the auditory and behavioral mechanismspresented here found in many families in several orders ofinsects give an overall picture of convergent evolution inresponse to bat predation

Insects living in bat-free environments

Spatial isolation Some moths escape from the risk of pre-dation by insectivorous bats simply by living in places whereno bats occur Bats are found on all continents except Antarc-tica and on the majority of islands but some remote islandsare free of bats for instance the Faroe Islands in the NorthAtlantic and the islands in French Polynesia

In general moth hearing sensitivity tends to reflect thecharacteristic frequencies and intensities of the local batfaunaHowever moths from the Faroes (Surlykke 1986) as wellas those from Tahiti (French Polynesia Fullard 1994) have re-tained auditory sensitivity in complete isolation from bats Iso-lated moths have thresholds at the best frequencies that arecomparable to the thresholds of moths sympatric with batsin similar habitats temperate or tropical Moths from HighArctic areas also show evasive maneuvers to ultrasound (Ry-dell et al 2000) The reason these moths have retained sen-sitive hearing which seems totally superfluous is not knownIt may simply be due to the slow regression of a character ifthere is no selection pressure against it In contrast a characterthat has adaptive value may spread through the populationafter only a few generations as shown by melanism in the pep-pered moth Biston betularia

576 BioScience July 2001 Vol 51 No 7

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Figure 3 The behavioral responses of a green lacewing to a hunting pipistrelle bat The behavior was photographed in alarge flight cage using stroboscopic flashes at 70-ms intervals The biosonar signals that the bat emitted during the variousstages of hunting were simultaneously recorded The signals are schematic and only the intervals are accurately shownModified from Miller and Olesen 1979

Temporal isolation This is another strategy to avoidbats The Cuculliinae (Noctuidae) include moths that areactive in the winter Several species (eg Lithophane grotei andEupsilia vinulenta) were captured in Massachusetts in No-vember over a 3-week period when snow covered the groundand nightly bat censuses revealed none All captured mothshad functional ears tuned to bat sounds with thresholds as lowas their relatives flying in the summer (Surlykke and Treat1995) A study of hearing in winter-active geometrid mothsgave a similar result (Rydell et al 1997) Apparently noctur-nally active winter moths do not use their hearing even forintraspecific communication Isolated moths retain their ul-trasonic hearing which indicates that it is not very costly evo-lutionarily speaking to retain ears if they provide wintermoths with additional protection such as from the possibil-ity of occasionally overlapping with bats

The nocturnal noctuid moth Rileyana fovea (formerlyThecophora fovea) from Central Europe emerges in late Oc-tober to early November after bat activity has decreased Ri-leyana fovea communicates with ultrasound The males singin flight by scraping the file of the hind tarsus against the foveawhich is an inflated bubble on the hindwing supported by theheavily sclerotized radial vein (Figure 4) The intense sounds(80 dB at 1 m) have peak power around 30 kHz which wouldmake the moths very conspicuous to bats The moths are read-ily eaten by captive bats However by being active at a timeof the year with few bats R fovea can use ultrasound for in-traspecific communication Hence it seems that a completeconversion of hearing from a defensive context to a sexual onehas occurred secondarily in R fovea (Surlykke and Gogala1986) Ultrasound-producing organs have developed inde-pendently in distantly related species of moths that are pro-tected from bats in different ways This suggests that the pre-

existing ear prompted the development of intraspecificacoustic communication in certain moths (Conner 1999Skals and Surlykke 1999)

Some moths have changed to diurnal life a secondaryadaptation perhaps in response to predation by bats Oftendiurnal moths are protected by toxins and warning colors likesome butterflies These day fliers include many tiger moths(Arctiidae) especially from the subfamily Ctenuchinae Onlyrelatively few Noctuidae are day fliers One example is the Aus-tralian whistling moth Hecatesia thyridion (Agaristinae)which is brightly patterned and probably toxic Male whistlingmoths produce sounds that are audible but most of the en-ergy is in the ultrasonic range where their hearing is best Theyuse sounds to defend their territories and to attract females(Surlykke and Fullard 1989) Some diurnal moths are silentand apparently their hearing has no function at all For ex-ample diurnal notodontid moths in the subfamily Dioptinaefrom Venezuela show varying degrees of auditory degenera-tion ranging from almost normal sensitivity in some speciesto very reduced sensitivity especially at ultrasonic frequenciesin other species (Fullard et al 1997) Similarly the diurnalgeometrid Archiearis parthenias is practically deaf to ultrasonicfrequencies (Surlykke et al 1998)

Sound as defenseMany arctiids possess tymbal organs located on the sides ofthe metathorax (Figure 5a Conner 1999) Special musclesbuckle the tymbal membrane generating one click or a burstof clicks per activation cycle (Figure 5b) Click amplitudes varyfrom about 50ndash90 dB SPL measured at 5 cm with maxi-mum sound energy falling between 30 and 80 kHz (Figure 5cFullard and Fenton 1977 Surlykke and Miller 1985) Flyingarctiids may click when they hear the biosonar signals ofbats Thresholds for clicking can be as low as 60ndash75 dB SPLfor simulated search-phase signals (Fullard 1979 Surlykke andMiller 1985) but considerably higher for short signals (about2 ms Fullard 1984b)

Some bats and insects share the same hibernacula andmarauding bats feed on hibernating insects Nymphalid but-terflies sense the vibrations in the substratum as the batcrawls toward it The torpid butterfly opens its wings in a char-acteristic manner which produces intense ultrasonic clicksfrom a special area of the wing membrane (Moslashhl and Miller1976) What purpose do the clicks serve There are threelikely functions of clicking sounds They could startle bats theycould interfere with the batsrsquo biosonar system or they couldwarn bats of a distasteful prey as many arctiid moths containtoxins in their body tissues or in special glands

Startle and interference The clicks of nymphalid but-terflies startle bats and thus provide a chance for the insect toescape However a bat quickly habituates to the sounds andeats these butterflies (Moslashhl and Miller 1976) For experi-enced bats clicks can act as a dinner bellArctiid clicks can star-tle inexperienced and naive bats (Eptesicus fuscus) but thesebats also habituate rapidly (Bates and Fenton 1990 Miller

July 2001 Vol 51 No 7 BioScience 577

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Figure 4 Male stridulatory organ used for the productionof intraspecific communication sounds by the noctuidmoth Rileyana fovea (formerly Thecophora fovea)Sound pulses with carrier frequencies of about 30 kHzare produced by scraping the file on the tarsus of the hindleg against the stridulatory swelling (fovea) on thehindwing Modified from Surlykke and Gogala 1986

1991) Thus clicks must be used sparingly to have survivalvalue as startle signals

The ultrasonic clicks of arctiids might disturb bat biosonarin two ways by simulating multiple targets (Fullard et al1979 1994) and by interfering with range determination(Miller 1991) The arctiid Cycnia tenera produces long trainsof clicks at high rates Fullard et al (1979 1994) hypothesizedthat clicks of C tenera could function as acoustical camou-flage by simulating multiple targets (false echoes) near themoth and thus jam a batrsquos (Eptesicus fuscus) biosonar Theybased their conclusion mainly on the ability of the moth totime its clicking to the terminal phase of the batrsquos signals Milleret al (forthcoming) tested this idea using bats (Pipistrellus pip-istrellus) trained to catch catapulted meal worms after whichnatural click sequences from the arctiid Phragmatobia fulig-inosa were played back during the batsrsquo terminal phase Thebats reacted by increasing the harmonic structure of their ter-minal signals but clicks did not influence the success rate of

prey capture The results suggest that the clicks produced byP fuliginosa do not interfere with the batsrsquo sonar system per-haps because the click rate is too low However in psy-chophysical experiments the clicks from P fuliginosa did in-terfere with the ability of bats (Eptesicus fuscus) to determinerange differences (Miller 1991) When clicks triggered bythe batsrsquo own signals fall repeatedly within a critical time win-dow of about 15 ms before an echo the batrsquos discriminationof range differences deteriorated by as much as 40-fold A sin-gle artificial click placed within the critical window inter-feres with range difference determination (Tougaard et alforthcoming) and with neural responses (Tougaard et al1998) In either case a bat would miss its target if clicks rep-resent false echoes from phantom objects or if they interferewith the batrsquos ranging mechanism

Warning sounds toxins and mimicry Several factspoint to the warning function of clicks as suggested by Dun-ning (1968) The Arctiidae (including the Ctenuchinae) aregenerally unpalatable and arctiids are the only noctuoidmoths that click in response to bat sonar sounds Arctiidclicks could warn the bat of a noxious prey Evidence sup-porting a warning function comes from studies in the labo-ratory and the field In experimental studies bats (Pipistrel-lus pipistrellus and Eptesicus fuscus) habituated to arctiid clickswhen given palatable rewards (Surlykke and Miller 1985Bates and Fenton 1990) However the same bats learned veryquickly to associate moth clicks with a distasteful rewardField studies indicated that bats (Lasiurus sp) foraging aroundstreet lights often aborted their attacks in the approach or ter-minal phase when the prey was the noisy arctiid mothHypoprepia fucosa (Acharya and Fenton 1992) Wild H fucosadid not take visible evasive action to attacking bats Batsavoided more than 90 of the moths released and droppedthe few they captured usually undamaged The bats showedno evidence of habituation although H fucosa were abundantcomposing more than 30 of the moth population Hy-poprepia fucosa has classic warning coloration and patterns as-sociated with toxic species Evidence favors the assumptionthat arctiid clicks are acoustical aposematic signals warningbats that the moths taste bad (Dunning and Kruumlger 1996)

Combining acoustic defenses The startle interferenceand warning hypotheses are not mutually exclusive In areaswhere arctiid moths are scarce the clicks may mostly startlebats Because bats quickly adapt to the clicks a warning func-tion is most likely in areas where arctiid moths are abundantWarning seems especially likely for toxic arctiids like Arctia cajawhich produce few but intense clicks in response to batlikesignals (Surlykke and Miller 1985) At least some species of arc-tiids begin clicking to the searching signals of aerial hawkingbats at distances of about 2ndash4 m (Surlykke and Miller 1985)At these distances the bat should be able to hear the clicks giv-ing an experienced predator ample time to avoid the dis-tasteful prey There is sufficient time for the bat to change itsbehavior even if the warning comes during the approach or

578 BioScience July 2001 Vol 51 No 7

Articles

Figure 5 Arctiid tymbal organ and clicks (a) The tymbalorgan on the lateral surface of the metathoracic segmentof the arctiid Phragmatobia fuliginosa (b) The tymbalorgan produces a burst of clicks each time it buckles (c)The power spectrum of the burst has a maximum atabout 80 kHz (a) Modified from Surlykke and Miller1985 (b) and (c) modified from Miller 1991

terminal phases of the batrsquos pursuit (Acharya and Fenton1992) Should the mothrsquos clicks arrive at the batrsquos ear just be-fore the echoes the batrsquos estimation of range to the preyblurs perhaps causing the bat to miss the target Moths us-ing long trains of click bursts could exploit this strategy Allthree possibilities startle interference and warning offerselective advantages for arctiid moths in addition to thoseprovided by changes in flight behavior

Potential countertactics for batsThe diet of many bats contains very few moths perhaps be-cause of their effective defenses However some barbastelle batsprey almost exclusively on tympanate moths and just how theydo this is not known (Sierro and Arlettaz 1997) Here wepresent some possible double-edged strategies that may ex-plain bat adaptations

Changing signals Echolocating bats announce their pres-ence to all potential prey equipped with auditory bat detec-tors and bats may use different acoustic strategies to reducetheir conspicuousness One strategy would be an adaptationthat moved frequencies of sonar signals out of the rangewhere tympanate insects are most sensitive (Dunning andKruumlger 1996) Some bats use very high frequencies whichmake them less audible to most noctuoid moths Howeversmall moths such as some geometrids (Surlykke and Filskov1997) the pyralid Galleria mellonella (Figure 2b right) andmany tropical noctuoids (Fullard 1988) are quite sensitive tohigh frequencies The attenuation of high frequencies re-duces the useful range of bat sonar so the advantage of thisstrategy may be limited If emission of high frequencies werea countermeasure against tympanate insects one would ex-pect to find bats exploiting this strategy in temperate regionswhere many moths do have poor sensitivity at high frequen-cies (Fullard 1988) The only temperate nongleaning batsthat use relatively high frequencies are small ones (eg Pip-istrellus spp) which detect small prey While the emission ofhigh frequencies may be a response to insect defenses it mayalso be a way to increase resolution and thus increase the abil-ity of bats to detect smaller insects (Surlykke et al 1993)

A second strategy would be for bats to emit very low fre-quencies which would make them less conspicuous to moths(Rydell and Arlettaz 1994) This strategy is employed mostlyby fast-flying bats that hunt aerial insects far from the groundand vegetation (Neuweiler 1989 Fenton 1990) Low fre-quencies increase the batsrsquo range but lower the resolution ofthe batsrsquo biosonar making only large insects detectable (Bar-clay 1986)

A third strategy would be an adaptation for bats to reducethe intensity of their signals Sound intensity is a measure ofsound energy and is proportional to the sound pressure(The dB scale is adapted such that any change in sound pres-sure and the corresponding change in sound intensity resultin the same change in dB value) The advantage would be thatthe sound intensity decreases with the square of the distancebut the echo intensity decreases with the fourth power of the

distance (Surlykke 1988) making the bat less detectable to thetympanate insect We do not know if any bats exploit this strat-egy but we know that all bats studied so far when gleaninguse low-intensity sounds if they emit any signals at all(Neuweiler 1989 Miller and Treat 1993 Faure and Barclay1994) For a gleaning bat the reduction of detection range isprobably not an important restriction because reducingsound intensity gives the additional advantage of reducing clut-ter echoes from the background (see Schnitzler and Kalko2001) In contrast field studies using techniques to calculatethe distance and direction to the bat indicate that at least somebats hunting aerial insects in the open emit intense signals withsource levels up to 125 dB SPL the highest levels yet measured(Jensen and Miller 1999) Also bats that display both glean-ing and aerial-hawking modes of foraging such as for in-stance Myotis evotis (Faure and Barclay 1994) and M septen-trionalis (Miller and Treat 1993) emit high intensities whenhunting flying insects

Finally shorter echolocation signals should be less con-spicuous to prey However shorter signals mean shorterechoes with less energy which are less conspicuous to the batstoo Also short search signals are recorded mainly from batsusing frequency-modulated calls and hunting close to clut-ter (Neuweiler 1989 Fenton 1990) Hencewe believe that shortcalls probably are not a countermeasure against insect hear-ing but rather an adaptation for reducing the overlap betweenechoes from clutter and those from prey

Listening to prey sounds The most effective way for abat to sneak close to tympanate prey is to cease echolocatingaltogether and detect prey using passive sensory cues If theinsects produce sound bats may find them using passivehearing Gleaning bats such as Plecotus auritus and Myotis evo-tis usually have large pinnae (Faure and Barclay 1994) Theyreact with very fast positive phonotaxis to insect-producedsounds such as the sound of wings fluttering or of an insectcrawling on a surface Some gleaning bats emit the full reper-toire of biosonar signals including the terminal phase(Schumm et al 1991) However gleaners generally stop call-ing before the attack and produce no terminal phase(Neuweiler 1989 Faure and Barclay 1994) Whether omissionof the terminal phase reduces the insectrsquos chance of escapingis difficult to say because tympanate insects probably detectecholocating bats long before the terminal phase (Roeder1967a Surlykke et al1999) However omitting the terminalphase may prevent last-chance escape maneuvers (Miller1984) On the other hand sedentary moths stay motionlessor freeze when hearing echolocation signals Turning off thesonar in the final phase may not be a countermeasure againsttympanate insects it may simply be that the bat does not needto continuously update the estimated position of a motion-less insect In contrast the prey of aerial hunters change po-sition continuously in three dimensions thus forcing the batto use its biosonar nearly to the moment of capture

It is difficult to determine if the acoustical adaptations ofbats are responses to constraints of the environment or to the

July 2001 Vol 51 No 7 BioScience 579

Articles

batsrsquo hunting strategies or are intended to overcome insect de-fenses In any case some bat echolocation signals are lessconspicuous to tympanate prey

Concluding remarksThe evolutionary arms race continues between bats and theirinsect prey and undiscovered strategies await to be revealedSome suspected strategies such as acoustical mimicry needto be documented by laboratory and field studies Experi-mental studies in the field can elucidate some questions aboutbat and insect interactions For example wild gleaning batshunting at familiar sites (Miller and Treat 1993 Faure and Bar-clay 1994) offer unique opportunities to test some hypothe-ses about echolocation behavior and the functions of clicksas interfering or warning signals Employing modern digitalsystems that can reproduce clicks and simulate insect echoeswill assist in such studies

Some questions will be difficult to answer An individualbat can modify at least some of its strategies through learn-ing whereas insect counterstrategies appear through theslower process of natural selection Does this mean insectstrategies lag behind those of their predators Perhaps not Thevariability of an individual insectrsquos antibat behaviors might bea response to the predatorrsquos ability to learn Perhaps theldquoevitabilityrdquo of the preyrsquos behavior (Roeder 1975) makeslearning by the predator less effective

AcknowledgmentsWe thank Raymond CoxOle Naeligsbye Larsen and our students(Vibeke Futtrup Marianne E Jensen Niels Skals) for com-ments on the manuscript We also appreciate the commentsof five anonymous reviewers Our research has been sup-ported by grants from the Danish Natural Sciences ResearchCouncil the Danish National Research Foundation and theCarlsberg Foundation

References citedAcharya L Fenton MB 1992 Echolocation behaviour of vespertilionid bats

(Lasiurus cinereus and Lasiurus borealis) attacking airborne targets in-cluding arctiid moths Canadian Journal of Zoology 70 1292ndash1298

Acharya L McNeil J 1998 Predation risk and mating behavior The re-sponses of moths to batlike ultrasound Behavioral Ecology 9 552ndash558

Ball EE Field LH 1981 Structure of the auditory system of the wetaHemideina crassidens (Blanchard1851) (Orthoptera Ensifera Gryl-lacridoidea Stenopelmantidae) 1 Morphology and histology Cell Tis-sue Res 217 321ndash343

Barclay RMR 1986 The echolocation calls of hoary (Lasiurus cinereus) andsilver-haired (Lasionycteris noctivagans) bats as adaptations for long-versus short-range foraging strategies and the consequences for prey se-lection Canadian Journal of Zoology 64 2700ndash2705

Bates DL Fenton MB 1990 Aposematism or startle Predators learn their re-sponses to the defenses of prey Canadian Journal of Zoology 68 49ndash52

Boyan GS Fullard JH 1986 Interneurones responding to sound in the to-bacco budworm moth Heliothis virescens (Noctuidae) Morphological andphysiological characteristics Journal of Comparative Physiology A Sen-sory Neural and Behavioral Physiology 158 391ndash404

Boyan GS Miller LA 1991 Parallel processing of afferent input by identi-fied interneurones in the auditory pathway of the noctuid moth Noctuapronuba (L) Journal of Comparative PhysiologyA Sensory Neural andBehavioral Physiology 168 727ndash738

Conner WE 1999ldquoUn chant drsquoappel amoureusrdquo Acoustic communicationin moths Journal of Experimental Biology 202 1711ndash1723

Cumming GS 1996 Mantis movements by night and the interactions of sym-patric bats and mantises Canadian Journal of Zoology 74 1771ndash1774

Dunning DC 1968 Warning sounds of moths ZTierpsychol 25 129ndash138Dunning DC Kruumlger M 1996 Predation upon moths by free-foraging Hip-

posideros caffer Journal of Mammalogy 77 708ndash715Eggers F 1919 Das thoracale bitympanale Organ einer Gruppe der Lepi-

doptera Heterocera Zool Jb (Anat) 41 273ndash376Faure PA Barclay RMR 1994 Substrate-gleaning versus aerial-hawking

Plasticity in the foraging and echolocation behaviour of the long-earedbat Myotis evotis Journal of Comparative PhysiologyA Sensory Neuraland Behavioral Physiology 174 651ndash660

Faure PA Hoy RR 2000 Neuroethology of the katydid T-cell II Responsesto acoustic playback of conspecific and predatory signals Journal ofExperimental Biology 203 3243ndash3254

Fenton MB1990 The foraging behaviour and ecology of animal-eating batsCanadian Journal of Zoology 68 411ndash422

Fenton MB Fullard JH 1981 Moth hearing and the feeding strategies of batsAmerican Scientist 69 266ndash275

Forrest TG Read MP Farris HE Hoy RR 1997 A tympanal hearing organin scarab beetles Journal of Experimental Biology 200 601ndash606

Fullard JH 1979 Behavioral analyses of auditory sensitivity in Cycnia ten-era Huumlbner (Lepidoptera Arctiidae) Journal of Comparative Physiol-ogy A Sensory Neural and Behavioral Physiology 129 79ndash83

mdashmdashmdash 1984a Acoustic relationships between tympanate moths and theHawaiian hoary bat (Lasiurus cinereus semotus) Journal of ComparativePhysiology ASensory Neuraland Behavioral Physiology 155 795ndash801

mdashmdashmdash 1984b Listening for bats Pulse repetition rate as a cue for a defen-sive behavior in Cycnia tenera (LepidopteraArctiidae)Journal of Com-parative Physiology A Sensory Neural and Behavioral Physiology 154249ndash252

mdashmdashmdash 1988 The tuning of moth ears Experientia 44 423ndash428mdashmdashmdash 1994Auditory changes in noctuid moths endemic to a bat-free niche

Journal of Evolutionary Biology 7 435ndash445Fullard JH Fenton MB 1977 Acoustic behavioural analyses of the sounds

produced by some species of Nearctic Arctiidae (Lepidoptera)CanadianJournal of Zoology 55 1213ndash1224

Fullard JH Fenton MB Simmons JA 1979 Jamming bat echolocation Theclicks of arctiid moths Canadian Journal of Zoology 57 647ndash649

Fullard JH Simmons JA Saillant PA 1994 Jamming bat echolocation Thedogbane tiger moth Cycnia tenera times its clicks to the terminal attackcalls of the big brown bat Eptesicus fuscus Journal of Experimental Bi-ology 194 285ndash298

Fullard JH Dawson JW Otero LD Surlykke A1997 Bat-deafness in day-fly-ing moths (Lepidoptera Notodontidae Dioptinae) Journal of Com-parative Physiology A Sensory Neural and Behavioral Physiology 181277ndash483

Goumlpfert MC Wasserthal LT 1999 Auditory sensory cells in hawkmoths Iden-tification physiology and structure Journal of Experimental Biology 2021579ndash1587

Hoy RR 1992 The evolution of hearing in insects as an adaptation to pre-dation from batsPages 115ndash129 in Webster DB Fay RR Popper AN edsThe Evolutionary Biology of Hearing New York Springer-Verlag

Hoy RR Nolen T Brodfuehrer P 1989 The neuroethology of acoustic star-tle and escape in flying insects Journal of Experimental Biology 146287ndash306

Jensen ME Miller LA 1999 Echolocation signals of the bat Eptesicus serot-inus recorded using a vertical microphone array Effect of flight altitudeon searching signals Behavioral Ecology and Sociobiology 47 60ndash69

Kennel JV Eggers F 1933 Die abdominalen Tympanalorgane der Lepi-dopteren Zool Jb (Anat) 57 1ndash104

Lakes-Harlan R Heller K-G 1992 Ultrasound-sensitive ears in a parasitoidfly Naturwissenschaften 79 224ndash226

Larsen ON Kleindienst H-UMichelsen A1989 Biophysical aspects of soundreception Pages 364ndash390 in Huber F Moore TELoher W eds Cricket Be-havior and Neurobiology Ithaca (NY) Cornell University Press

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July 2001 Vol 51 No 7 BioScience 571

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cies below 10 kHz or above 200 kHz Higher frequencies im-prove resolution but they attenuate at a greater rate (Surlykke1988) and the detection distance is reduced accordingly Thesource level is the sound pressure level (SPL relative to 20microPa) in decibels (dB) measured 10 cm in front of the batrsquosmouth A bat using a source level of 110 dB at 20 kHz coulddetect the echo from an object the size of a moth at more than5 m Detection would occur at no more than 24 m if the batused 100 kHz (Surlykke 1988) From the insectsrsquo perspectivebats advertise their presence with the ultrasonic pulses usedto stroboscopically probe the environment Thus insects areforewarned if they can hear ultrasound This coincidentallyexerts considerable selection pressure against those insects thateither cannot hear or do not react (Miller 1982)

Thus the stage was set in the Eocene for an evolutionaryescalation between bats and insects Evasive behaviors inexisting tympanate insects (presumably crickets locusts andmantids) probably appeared in response to selection pressureby bat predation (Hoy 1992) The same selection pressuregenerated new auditory and motor mechanisms in presum-ably earless insects (green lacewings and moths) Batstoo could have developed countermeasures for exampleshifting signals out of the preyrsquos hearing range (Fenton andFullard 1981) or modifying hunting behaviors (Miller andOlesen 1979)

Avoidance behaviors

Preadaptation Preexisting auditory systems in insectsmay have been preadaptively sensitive to bat echolocationTympanate insects that were normally diurnal may also havebecome active at night Crickets locusts and mantids areconsidered here because they were probably some of the ear-liest insects with hearing and they are mostly active during theday but often fly (migrate or disperse) at twilight and atnight However all crepuscular and nocturnal insects are po-tential prey for bats

Crickets The most intensively studied insect auditory sys-tem is that of field crickets (Figure 1a left) The majority ofthese studies concern intraspecific communication The tibiaof each foreleg contains an ear (Figure 1a middle) For ex-ample the maximum sensitivity of the cricket Gryllus bi-maculatus occurs at about 5 kHz as measured electrophysi-ologically from the auditory nerve This is also the frequencyof the calling song However the ear is sensitive to sound fre-quencies up to 100 kHz at least

Popov and Shuvalov (1977) first reported that dispersingcrickets avoid being hunted by bats Since then Ron Hoy atCornellAndrej Popov in St Petersburg and their colleagueshave documented avoidance behavior in several species ofcrickets both behaviorally and neurophysiologically (see Hoyet al 1989) Crickets in stationary flight steer away from thesource of ultrasound (negative phonotaxis) with the most ef-fective frequencies lying between about 10 kHz and 80 kHz(Figure 1a right) An interneuron in Teleogryllus oceanicus

(Int 1) initiates evasive behavior (Hoy et al 1989) and its ho-mologue in Gryllus bimaculatus (AN2 Popov et al 1994)presumably does the same The threshold for AN2 at 20 kHzis about 20 dB less than that of the behavior (Figure 1aright) meaning that the neural response is more sensitive thanthe behavior Some mole crickets hear ultrasound in part withspecial neuronal pathways and free-flying crickets showavoidance to batlike sounds (Mason et al 1998)

Bush crickets (Figure 1b left) like field crickets have theirears and associated acoustic tracheae in the tibia of the forelegs(Figure 1b middle) Some species communicate entirely inthe ultrasonic range Many bush crickets can hear bats butfew seem to react to bat echolocation However the bushcricket Neoconocephalus ensiger shows an acoustic startleresponse during tethered flight in the laboratory (Faure andHoy 2000) When the insects hear intense batlike soundswith frequencies from 15 kHz to at least 60 kHz (Figure 1bright) they dive However they exhibit no directionality withrespect to the sound source even though bush crickets havedirectional hearing A large prothoracic interneuron the T-neuronparticipates in mediating the behavior (Faure and Hoy2000) The T-neuron is most sensitive to frequencies higherthan those of the calling song (13 kHz peak frequency) for thespecies The threshold is about 50 dB less than that of the be-havior at 20 kHz (Figure 1b right)

Locusts Another primarily diurnal orthopteran the locustLocusta migratoria (Figure 1c left) has a pair of general pur-pose abdominal ears (Figure 1c middle) that are well stud-ied anatomically physically and physiologically Howeverthe role of hearing in the life of this locust remains poorly un-derstood One function of hearing may be to mediate nega-tive phonotaxis in response to batlike signals although to ourknowledge there are no published reports of locusts re-sponding to bats A locust in stationary flight rudders with itsabdomen and increases the wingbeat frequency both ofwhich produce turning in the direction opposite to the soundsource (Robert 1989) Negative phonotactic behavior occursonly at frequencies above 10 kHz (Figure 1c right) Roumlmeret al (1988) found interneurons sensitive to high frequenciesthat selectively receive input from auditory afferents Theseinterneurons control head and abdominal movements and arecandidates for controlling negative phonotaxis Figure 1c(right) shows the auditory sensitivity of one of these (SN-5)

Praying mantids Praying mantids (Figure 1d left) are pri-marily diurnal but many make dispersal flights at night(Cumming 1996) Although previously thought to be deafmany species in the suborder Mantodea actually possess ears(Yager and Hoy 1986) The tympanal organ sensitive to ul-trasound is hidden deep in a cleft between the two metatho-racic coxae (Figure 1d middle) and consists of two closely op-posed stiff tympanal membranes A cluster of sensory cellsis attached to each tympanal membraneThe ears are thoughtto function as a single organ (Hoy et al 1989) Flying man-tids (Parasphendale agrionina) react at distances as great as

572 BioScience July 2001 Vol 51 No 7

Articles

Figure 1 Insects with audition secondarily adapted for hearing bats Representative insects from the various families areshown in the left column with the location of the ear as indicated by the arrow The general anatomy of each ear is shown inthe middle column The tuning curves for avoidance behaviors (negative phonotaxis for orthopterans and nondirectionalresponses for the mantid) and interneurons thought to be involved with the behaviors are shown in the right column Thefrequency range for typical bat biosonar signals is shown on the abscissa (d right) (a middle) A cross section of the ear of acricket Gryllus bimaculatus (modified from Larsen et al 1989) (b middle) A longitudinal section of the ear of an ensiferanHemideina cassisens (modified from Ball and Field 1981) (c middle) A horizontal section through the ear of an acrididLocusta migratoria (modified from Schwabe 1906) (d middle) A partial dissection of the ventral surface of a mantidMantis religiosa (modified from Yager and Hoy 1986) (d right) The behavioral data are from Parasphendale agrioninaand the neuronal data are from M religiosa

10 m from a loudspeaker emitting batlike signals at naturalintensities They react by turning or with dives and spiral flightThe responses are all nondirectional as would be expectedfrom a functionally monaural system The lowest thresholdfor avoidance behavior occurs from 20 kHz to 80 kHz (Fig-ure 1d right Yager 1999) Yager identified an interneuronwhose tuning curve resembles that of the behavior (Figure 1dright) albeit in another species (Mantis religiosa) The neu-ron is most likely part of a neural circuit for avoidance be-havior although attempts to elicit avoidance behavior fromM religiosa to artificial bat signals have thus far failed

Flies and beetles We suspect that some flies can hearand react to bats but evidence at present is not sufficient toput them on the growing list of bat-detecting insects Thelarviparous tachinid flies Ormia ochracea and Therobialeonidei parasitize crickets and bush crickets respectively(Lakes-Harlan and Heller 1992 Robert et al 1992) The call-ing songs of their nocturnal hosts attract female flies Ormiaochracea hears best at 5 kHz as measured electrophysiologi-cally from the neck connectiveThis frequency is near the peakpower output of the hostrsquos song but the flyrsquos hearing ex-tends into the ultrasonic range The hearing of T leonidei isalso tuned to its host which sings mostly in the ultrasonicrange These flies can surely hear bats but their reactions tobatlike signals or to bats in nature are unknown

Beetles the largest order of insects are heavily preyed onby some bats and until recently ears were unknown in bee-tles The tiger beetle Cicindela marutha has ears on the firstabdominal segment that are sensitive to sound between 30 kHzand 60 kHz Batlike signals provoke changes in the beetlersquos be-havior during stationary flight which include the productionof ultrasonic clicks a property shared only with some arctiidmoths (see below Yager et al 2000) Hearing in tiger beetlesmay be used for intraspecific communication especially be-cause they also produce clicking sounds while on the groundAt present we assume that hearing in these beetles has beensecondarily adapted for detecting bats

In response to pulsed ultrasound flying scarab beetlesEutheola humilis dropped or flew toward the ground andwalking beetles stopped They hear best at 45 kHz The earsare in the neck region and have evolved independently fromthose in tiger beetles (Forrest et al 1997) perhaps specificallyfor bat detection

New auditory systems Ears have evolved independentlyin many families of eight (perhaps nine) superfamilies ofmoths (Minet and Surlykke 2002) Physiological and behav-ioral results when available for Noctuoidea PyraloideaGeometroidea Sphingoidea and Drepanoidea indicate thatthe ears are adapted specifically for hearing bat signals Veryrecently evasive behavior to batlike ultrasound was docu-mented in nocturnal butterflies of the superfamily Hedy-loidea that have ears on their wings (Yack and Fullard 2000)Green lacewings (Chrysopidae) also have ears on their wingsthat are sensitive to ultrasound and function as bat detectors

A lack of frequency sensitivity is common to all these hear-ing organs Moths and green lacewings are tone deaf In con-trast audition in orthopterans and mantids which is prob-ably secondarily adapted for hearing bats shows frequencyselectivity Nevertheless selection pressure has shaped thetuning curves the hearing or behavioral sensitivity to differ-ent sound frequencies of moth hearing Many Nearcticspecies of noctuoids hear best between 20 and 40 kHzwhereas tropical noctuoids hear best over a broader range ofultrasonic frequencies and are more sensitive than theirNearctic relatives (Fullard 1984a) A good example of this isthe noctuid Ascalapha odorata Its ear is tuned to the biosonarand social calls of the one bat species on the Hawaiian islandKauai The same or a closely related species of moth inPanama on Barro Colorado Island has a lower threshold ofhearing and a broader tuning curve This is probably anadaptation to the broader range of frequencies used by themany insectivorous bat species found there (Fullard 1984a)

Moths Ken Roeder made noctuid moths famous throughhis numerous studies of their hearing and behavior (Roeder1967a) The Noctuidae Notodontidae and Arctiidae (all inthe superfamily Noctuoidea Figure 2a left) have ears on thelateral surfaces of the metathorax (Figure 2a middle) Behindthe thin tympanal membrane is a large air sac which is sep-arated from other air sacs by tracheal membranes Two sen-sory cells A1 and A2 (but a single A cell in notodontids seeSurlykke 1988) are attached to the tympanum The two cellshave identical tuning curves (Figure 2a right) and dynamicranges but they differ by about 20 dB in sensitivity Dynamicrange is the range over which neural responses occur tosound intensity measured in dB from threshold to saturationThe noctuid and arctiid moths have a total auditory dynamicrange of about 40 dB

Freely flying unidentified moths exhibit a variety of be-havioral responses to bats and to synthetic batlike signals(Roeder 1967a for recent results refer to Acharya and Fen-ton 1992) Moths far from the source often turn and fly awaywhereas those close to the source show zigzag and loopingflight power dives or passive falls Presumably the loudersounds recruit the A2 sensory cells which trigger the switchfrom negative phonotaxis to less predictable evasive flight be-havior However Roeder (1964) indicated that the percent-age of moths showing turning-away responses decreases andthe percentage showing looping responses increases as thepulse repetition rate increases Because of this Roeder (1964)suggested that the most sensitive sensory cell (A1) actingalone could release several behaviors but further experi-mentation is needed to confirm this

Size and sensitivity are correlated in moths complicatingmatters further Big moths reflect more intense echoes thansmall moths and may be detected by bats as far away as 10 mHowever results from noctuid moths show that big moths arealso more sensitive and may detect approaching bats as faraway as 100 m Thus there seems to be a fairly constant 10-fold margin of safety that is noctuid moths can detect bats

July 2001 Vol 51 No 7 BioScience 573

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Figure 2 Insects with audition adapted specifically for hearing bats Representative insects from the various families areshown in the left column with the location of the ear indicated by arrow The general anatomy of each ear is shown in themiddle column The tuning curves for flight cessation (behavior) the A1 sensory cells and an interneuron are shown inthe right column The frequency range for typical bat biosonar signals is shown on the abscissa (d right) (a middle) Ahorizontal section through the metathorax of a noctuid moth (modified after Eggers 1919) (b middle) A cross sectionthrough the first abdominal segment of a geometrid moth viewed from the inside (modified after Kennel and Eggers1933) A single tympanal air sac occupies the space behind the tympana (not seen in this drawing) The pyralid ear (egGalleria mellonella) is anteroabdominal like that of the geometrid (b right) Data for a geometrid Biston betularia(modified from Surlykke and Filskov 1997) as well as for a pyralid Galleria mellonella (c middle) The head of asphingid moth Celerio lineata with one labial palp in longitudinal section The sound receivers (pilifers) are seen on thelateral surface of the proboscis (modified from Roeder et al 1970) (d middle) The ventral surface of the base of the wingof the green lacewing Chrysoperla carnea (modified after Miller 1975) References for tuning curves are given in the text

at about 10 times the distance over which bats can detectmoths (Surlykke et al 1999)

Many interneurons in the thoracic and cephalic ganglia ofnoctuids have been characterized (Roeder 1975 Boyan andFullard 1986) For example two identified neurons receive di-rect input from the A1 afferent in parallelbut they process tem-poral information differently (Boyan and Miller 1991) Synap-tic input to some motor neurons controlling the upndashdownmovement of the wings occurs only when the A2 sensory cellis activated (Madsen and Miller 1987) The role individual in-terneurons play in eliciting behavior is speculative principallybecause the responses of moths are exceedingly difficult tostudy under controlled conditions (Roeder 1967b)

Arctiid moths behave like noctuids but are more reluctantto do so In addition some arctiids produce ultrasonic click-ing sounds from tymbal organs when they hear bat signals orare touched (The clicks have various effects on bats as de-scribed below) Cycnia tenera starts clicking before it stops fly-ing in response to ultrasonic stimuli (Fullard 1979) Thethreshold for flight cessation is about 10ndash20 dB above that forclicking and repetition rates from 17ndash40 pulses per secondare best at eliciting clicking (Fullard 1984b) Also the rate ofmotor spikes to the tymbal muscles increases when the stim-ulus rate increases (Northcott and Fullard 1996) So both am-plitude and pulse repetition rate of the ultrasonic stimulus in-fluence behavioral responses from noctuid and arctiid moths

The Geometridae Pyralidae and Drepanidae have ultra-sound-sensitive ears on the first abdominal segment (Minetand Surlykke 2001) In the geometrids (Figure 2b left) thetympana are adjacent to the midline and point caudally (Fig-ure 2b middle) The tympana in pyralids point rostrally andhave a slight tilt ventrallyFour sensory (A) cells attach to eachtympanum The dynamic range for hearing in the geometridBiston betularia is about 50 dB because each cell covers asmaller range (10ndash15 dB) than the A cells in a noctuid ear Thefrequency range of hearing extends to at least 100 kHz in allspecies studied thus far (Figure 2b right B betularia Surlykkeand Filskov 1997) Some geometrids show flight cessation andother responses to ultrasound (Rydell et al 1997) Pyralid waxmoths respond to bat cries (Spangler and Takessian 1983) andGalleria mellonella shows a number of behavioral responseswhile in stationary flight the most noticeable of which isflight cessation (Skals and Surlykke 2000) Flight cessationwhich is the behavior with the highest threshold occurs at +20to +25 dB with respect to the threshold for the A1 cell (Fig-ure 2b right G mellonella) Actually avoidance behavior tobat echolocation is so powerful that some pyralid (and noc-tuid) moths abort sexually oriented flight to females broad-casting pheromones (Acharya and McNeil 1998)

The bat-detecting ear of some hawk moths (Figure 2cleft) consists of air-filled labial palps that transmit sound en-ergy to the pilifers located on either side of the proboscis(Figure 2c middle) Other hawk moths have scale plates onthe labial palps rather than air-filled palps Neurophysiolog-ical recordings from the labial nerve or from interneurons re-veal the auditory characteristics in both types of hawk moths

(Figure 2c right) They are most sensitive to frequencies be-tween 20 and 30 kHz with a threshold of 40ndash50 dB sound pres-sure level The dynamic range of the single auditory sensoryneuron in the pilifer is about 20 dB resembling that in the earof notodontid moths Hawk moths in tethered flight respondto ultrasound with changes in flight speed with nondirectionalturning and sometimes by emitting sound The behavioralthreshold is about 70 dB SPL or 20 dB above the sensorythreshold (Roeder et al 1970 Goumlpfert and Wasserthal 1999)

Green lacewings The ear of the green lacewing (Figure 2dleft) is located in a bulge near the base of the radial vein in eachforewing (Figure 2d middle) It is a true tympanal organwhich is mostly fluid filled and contains a small trachea It isthe smallest tympanal organ knownPerhaps only 6 of the 25sensory cells actually respond to ultrasound (see Miller 1984for a review) Like wax moths green lacewings in stationaryflight show a number of responses to lower intensity stimulibefore ceasing their flight (Miller 1975) Flight cessation (Fig-ure 2d right) occurs most reliably to ultrasonic signals broad-cast at rates of 1ndash50 pulses per second High stimulus repe-tition rates alone were ineffective in stopping the flight ofrestrained green lacewings

A more realistic picture of behavior emerged from studieson freely flying green lacewings and bats (Figure 3) Bat sig-nals at low repetition rates possibly combined with low in-tensities cause insects to fold their wings and passively diveThe green lacewing shows this nondirectional early-warningresponse to batsrsquo searching signals (Figure 3 between flashes2 and 3) The bat increases its call rate as it approaches a fallinginsect (Figure 3 flashes 3 to 4) Just before capturing its preythe bat increases its repetition rate to a maximum of about200 signals per second in the terminal phase for most bats (Fig-ure 3 flash 5) During the terminal phase the insect suddenlyflipped open its wings (Figure 3 flash 5 arrow) presumablyin response to the high repetition rate signals This last-chance response breaks the dive and foils the bat in this caseafter which the insect continues its dive (Figure 3 flash 6)Artificial bat signals mimicking the sequence shown in Fig-ure 3 evoke the same behavior (Miller and Olesen 1979) Byrepeating the experiments with deafened green lacewingswe showed that the selective advantage of reactors over non-reactors was 47 or about the same as that found for moths(see Miller 1982) Unidentified neurons in the prothoracic gan-glion respond to ultrasound but their role in eliciting behavioris unknown (Miller 1984)

Conclusions about insect behaviorsWe can draw some conclusions and make predictions basedon what we know about avoidance behaviors Looking at allthe behavioral response types for all the insects mentionedabove we find that the best frequency the frequency at whichneural or behavioral responses have the lowest thresholdlies between about 20 and 60 kHz with thresholds betweenabout 30 and 70 dB SPL The response latencies range from40ndash70 ms at +15 dB with respect to the behavioral threshold

July 2001 Vol 51 No 7 BioScience 575

Articles

Because the distance at which the insects respond to 40 kHzsounds varies from 65ndash37 m for bats using intense signalsthe insects have several tenths of a second to avoid even fast-flying bats (Surlykke 1988) The situation is somewhat differentfor whispering bats which use intensities of less than about75 dB SPL and hunt near vegetation Here the response dis-tances for flying insects are from 01ndash27 m depending on thehearing threshold However bats can detect a moth-sizedecho at about 06 m putting the less-sensitive insects in dan-ger Many of the insects mentioned above are open-air fliersand normally do not meet whispering bats

The tuning of neurons suspected to be involved in avoid-ance behavior in preadapted insects such as crickets grasshop-pers and preying mantids poorly match the behavioral tun-ing This discrepancy suggests that these auditory neurons havebeen molded into an antibat circuitry as a result of selectionpressure Behaviors such as turning in midflight or flightcessation have thresholds typically 20 dB higher than thosefor sensory neurons or interneurons (except premotor in-terneurons) in the same insects Consequently yet undis-covered behaviors to low stimulus intensities may provide ad-ditional survival advantage

Insect avoidance behaviors and their underlying mecha-nisms are undoubtedly complicated Take for example the vari-ability of responses The behaviors cannot be reliably predictedand the same individual may show different responses or noresponse at all to the same stimulus Roeder called this theldquoevitabilityrdquoof behavior which provides a survival advantageby making it difficult for the predator to predict what the preywill do The characteristic feature of evitability makes it dif-ficult to study but it seems to be present in the behavior and

physiology of some moths (Roeder 1975 Madsen and Miller1987) and green lacewings (Miller and Olesen 1979)Nevertheless the auditory and behavioral mechanismspresented here found in many families in several orders ofinsects give an overall picture of convergent evolution inresponse to bat predation

Insects living in bat-free environments

Spatial isolation Some moths escape from the risk of pre-dation by insectivorous bats simply by living in places whereno bats occur Bats are found on all continents except Antarc-tica and on the majority of islands but some remote islandsare free of bats for instance the Faroe Islands in the NorthAtlantic and the islands in French Polynesia

In general moth hearing sensitivity tends to reflect thecharacteristic frequencies and intensities of the local batfaunaHowever moths from the Faroes (Surlykke 1986) as wellas those from Tahiti (French Polynesia Fullard 1994) have re-tained auditory sensitivity in complete isolation from bats Iso-lated moths have thresholds at the best frequencies that arecomparable to the thresholds of moths sympatric with batsin similar habitats temperate or tropical Moths from HighArctic areas also show evasive maneuvers to ultrasound (Ry-dell et al 2000) The reason these moths have retained sen-sitive hearing which seems totally superfluous is not knownIt may simply be due to the slow regression of a character ifthere is no selection pressure against it In contrast a characterthat has adaptive value may spread through the populationafter only a few generations as shown by melanism in the pep-pered moth Biston betularia

576 BioScience July 2001 Vol 51 No 7

Articles

Figure 3 The behavioral responses of a green lacewing to a hunting pipistrelle bat The behavior was photographed in alarge flight cage using stroboscopic flashes at 70-ms intervals The biosonar signals that the bat emitted during the variousstages of hunting were simultaneously recorded The signals are schematic and only the intervals are accurately shownModified from Miller and Olesen 1979

Temporal isolation This is another strategy to avoidbats The Cuculliinae (Noctuidae) include moths that areactive in the winter Several species (eg Lithophane grotei andEupsilia vinulenta) were captured in Massachusetts in No-vember over a 3-week period when snow covered the groundand nightly bat censuses revealed none All captured mothshad functional ears tuned to bat sounds with thresholds as lowas their relatives flying in the summer (Surlykke and Treat1995) A study of hearing in winter-active geometrid mothsgave a similar result (Rydell et al 1997) Apparently noctur-nally active winter moths do not use their hearing even forintraspecific communication Isolated moths retain their ul-trasonic hearing which indicates that it is not very costly evo-lutionarily speaking to retain ears if they provide wintermoths with additional protection such as from the possibil-ity of occasionally overlapping with bats

The nocturnal noctuid moth Rileyana fovea (formerlyThecophora fovea) from Central Europe emerges in late Oc-tober to early November after bat activity has decreased Ri-leyana fovea communicates with ultrasound The males singin flight by scraping the file of the hind tarsus against the foveawhich is an inflated bubble on the hindwing supported by theheavily sclerotized radial vein (Figure 4) The intense sounds(80 dB at 1 m) have peak power around 30 kHz which wouldmake the moths very conspicuous to bats The moths are read-ily eaten by captive bats However by being active at a timeof the year with few bats R fovea can use ultrasound for in-traspecific communication Hence it seems that a completeconversion of hearing from a defensive context to a sexual onehas occurred secondarily in R fovea (Surlykke and Gogala1986) Ultrasound-producing organs have developed inde-pendently in distantly related species of moths that are pro-tected from bats in different ways This suggests that the pre-

existing ear prompted the development of intraspecificacoustic communication in certain moths (Conner 1999Skals and Surlykke 1999)

Some moths have changed to diurnal life a secondaryadaptation perhaps in response to predation by bats Oftendiurnal moths are protected by toxins and warning colors likesome butterflies These day fliers include many tiger moths(Arctiidae) especially from the subfamily Ctenuchinae Onlyrelatively few Noctuidae are day fliers One example is the Aus-tralian whistling moth Hecatesia thyridion (Agaristinae)which is brightly patterned and probably toxic Male whistlingmoths produce sounds that are audible but most of the en-ergy is in the ultrasonic range where their hearing is best Theyuse sounds to defend their territories and to attract females(Surlykke and Fullard 1989) Some diurnal moths are silentand apparently their hearing has no function at all For ex-ample diurnal notodontid moths in the subfamily Dioptinaefrom Venezuela show varying degrees of auditory degenera-tion ranging from almost normal sensitivity in some speciesto very reduced sensitivity especially at ultrasonic frequenciesin other species (Fullard et al 1997) Similarly the diurnalgeometrid Archiearis parthenias is practically deaf to ultrasonicfrequencies (Surlykke et al 1998)

Sound as defenseMany arctiids possess tymbal organs located on the sides ofthe metathorax (Figure 5a Conner 1999) Special musclesbuckle the tymbal membrane generating one click or a burstof clicks per activation cycle (Figure 5b) Click amplitudes varyfrom about 50ndash90 dB SPL measured at 5 cm with maxi-mum sound energy falling between 30 and 80 kHz (Figure 5cFullard and Fenton 1977 Surlykke and Miller 1985) Flyingarctiids may click when they hear the biosonar signals ofbats Thresholds for clicking can be as low as 60ndash75 dB SPLfor simulated search-phase signals (Fullard 1979 Surlykke andMiller 1985) but considerably higher for short signals (about2 ms Fullard 1984b)

Some bats and insects share the same hibernacula andmarauding bats feed on hibernating insects Nymphalid but-terflies sense the vibrations in the substratum as the batcrawls toward it The torpid butterfly opens its wings in a char-acteristic manner which produces intense ultrasonic clicksfrom a special area of the wing membrane (Moslashhl and Miller1976) What purpose do the clicks serve There are threelikely functions of clicking sounds They could startle bats theycould interfere with the batsrsquo biosonar system or they couldwarn bats of a distasteful prey as many arctiid moths containtoxins in their body tissues or in special glands

Startle and interference The clicks of nymphalid but-terflies startle bats and thus provide a chance for the insect toescape However a bat quickly habituates to the sounds andeats these butterflies (Moslashhl and Miller 1976) For experi-enced bats clicks can act as a dinner bellArctiid clicks can star-tle inexperienced and naive bats (Eptesicus fuscus) but thesebats also habituate rapidly (Bates and Fenton 1990 Miller

July 2001 Vol 51 No 7 BioScience 577

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Figure 4 Male stridulatory organ used for the productionof intraspecific communication sounds by the noctuidmoth Rileyana fovea (formerly Thecophora fovea)Sound pulses with carrier frequencies of about 30 kHzare produced by scraping the file on the tarsus of the hindleg against the stridulatory swelling (fovea) on thehindwing Modified from Surlykke and Gogala 1986

1991) Thus clicks must be used sparingly to have survivalvalue as startle signals

The ultrasonic clicks of arctiids might disturb bat biosonarin two ways by simulating multiple targets (Fullard et al1979 1994) and by interfering with range determination(Miller 1991) The arctiid Cycnia tenera produces long trainsof clicks at high rates Fullard et al (1979 1994) hypothesizedthat clicks of C tenera could function as acoustical camou-flage by simulating multiple targets (false echoes) near themoth and thus jam a batrsquos (Eptesicus fuscus) biosonar Theybased their conclusion mainly on the ability of the moth totime its clicking to the terminal phase of the batrsquos signals Milleret al (forthcoming) tested this idea using bats (Pipistrellus pip-istrellus) trained to catch catapulted meal worms after whichnatural click sequences from the arctiid Phragmatobia fulig-inosa were played back during the batsrsquo terminal phase Thebats reacted by increasing the harmonic structure of their ter-minal signals but clicks did not influence the success rate of

prey capture The results suggest that the clicks produced byP fuliginosa do not interfere with the batsrsquo sonar system per-haps because the click rate is too low However in psy-chophysical experiments the clicks from P fuliginosa did in-terfere with the ability of bats (Eptesicus fuscus) to determinerange differences (Miller 1991) When clicks triggered bythe batsrsquo own signals fall repeatedly within a critical time win-dow of about 15 ms before an echo the batrsquos discriminationof range differences deteriorated by as much as 40-fold A sin-gle artificial click placed within the critical window inter-feres with range difference determination (Tougaard et alforthcoming) and with neural responses (Tougaard et al1998) In either case a bat would miss its target if clicks rep-resent false echoes from phantom objects or if they interferewith the batrsquos ranging mechanism

Warning sounds toxins and mimicry Several factspoint to the warning function of clicks as suggested by Dun-ning (1968) The Arctiidae (including the Ctenuchinae) aregenerally unpalatable and arctiids are the only noctuoidmoths that click in response to bat sonar sounds Arctiidclicks could warn the bat of a noxious prey Evidence sup-porting a warning function comes from studies in the labo-ratory and the field In experimental studies bats (Pipistrel-lus pipistrellus and Eptesicus fuscus) habituated to arctiid clickswhen given palatable rewards (Surlykke and Miller 1985Bates and Fenton 1990) However the same bats learned veryquickly to associate moth clicks with a distasteful rewardField studies indicated that bats (Lasiurus sp) foraging aroundstreet lights often aborted their attacks in the approach or ter-minal phase when the prey was the noisy arctiid mothHypoprepia fucosa (Acharya and Fenton 1992) Wild H fucosadid not take visible evasive action to attacking bats Batsavoided more than 90 of the moths released and droppedthe few they captured usually undamaged The bats showedno evidence of habituation although H fucosa were abundantcomposing more than 30 of the moth population Hy-poprepia fucosa has classic warning coloration and patterns as-sociated with toxic species Evidence favors the assumptionthat arctiid clicks are acoustical aposematic signals warningbats that the moths taste bad (Dunning and Kruumlger 1996)

Combining acoustic defenses The startle interferenceand warning hypotheses are not mutually exclusive In areaswhere arctiid moths are scarce the clicks may mostly startlebats Because bats quickly adapt to the clicks a warning func-tion is most likely in areas where arctiid moths are abundantWarning seems especially likely for toxic arctiids like Arctia cajawhich produce few but intense clicks in response to batlikesignals (Surlykke and Miller 1985) At least some species of arc-tiids begin clicking to the searching signals of aerial hawkingbats at distances of about 2ndash4 m (Surlykke and Miller 1985)At these distances the bat should be able to hear the clicks giv-ing an experienced predator ample time to avoid the dis-tasteful prey There is sufficient time for the bat to change itsbehavior even if the warning comes during the approach or

578 BioScience July 2001 Vol 51 No 7

Articles

Figure 5 Arctiid tymbal organ and clicks (a) The tymbalorgan on the lateral surface of the metathoracic segmentof the arctiid Phragmatobia fuliginosa (b) The tymbalorgan produces a burst of clicks each time it buckles (c)The power spectrum of the burst has a maximum atabout 80 kHz (a) Modified from Surlykke and Miller1985 (b) and (c) modified from Miller 1991

terminal phases of the batrsquos pursuit (Acharya and Fenton1992) Should the mothrsquos clicks arrive at the batrsquos ear just be-fore the echoes the batrsquos estimation of range to the preyblurs perhaps causing the bat to miss the target Moths us-ing long trains of click bursts could exploit this strategy Allthree possibilities startle interference and warning offerselective advantages for arctiid moths in addition to thoseprovided by changes in flight behavior

Potential countertactics for batsThe diet of many bats contains very few moths perhaps be-cause of their effective defenses However some barbastelle batsprey almost exclusively on tympanate moths and just how theydo this is not known (Sierro and Arlettaz 1997) Here wepresent some possible double-edged strategies that may ex-plain bat adaptations

Changing signals Echolocating bats announce their pres-ence to all potential prey equipped with auditory bat detec-tors and bats may use different acoustic strategies to reducetheir conspicuousness One strategy would be an adaptationthat moved frequencies of sonar signals out of the rangewhere tympanate insects are most sensitive (Dunning andKruumlger 1996) Some bats use very high frequencies whichmake them less audible to most noctuoid moths Howeversmall moths such as some geometrids (Surlykke and Filskov1997) the pyralid Galleria mellonella (Figure 2b right) andmany tropical noctuoids (Fullard 1988) are quite sensitive tohigh frequencies The attenuation of high frequencies re-duces the useful range of bat sonar so the advantage of thisstrategy may be limited If emission of high frequencies werea countermeasure against tympanate insects one would ex-pect to find bats exploiting this strategy in temperate regionswhere many moths do have poor sensitivity at high frequen-cies (Fullard 1988) The only temperate nongleaning batsthat use relatively high frequencies are small ones (eg Pip-istrellus spp) which detect small prey While the emission ofhigh frequencies may be a response to insect defenses it mayalso be a way to increase resolution and thus increase the abil-ity of bats to detect smaller insects (Surlykke et al 1993)

A second strategy would be for bats to emit very low fre-quencies which would make them less conspicuous to moths(Rydell and Arlettaz 1994) This strategy is employed mostlyby fast-flying bats that hunt aerial insects far from the groundand vegetation (Neuweiler 1989 Fenton 1990) Low fre-quencies increase the batsrsquo range but lower the resolution ofthe batsrsquo biosonar making only large insects detectable (Bar-clay 1986)

A third strategy would be an adaptation for bats to reducethe intensity of their signals Sound intensity is a measure ofsound energy and is proportional to the sound pressure(The dB scale is adapted such that any change in sound pres-sure and the corresponding change in sound intensity resultin the same change in dB value) The advantage would be thatthe sound intensity decreases with the square of the distancebut the echo intensity decreases with the fourth power of the

distance (Surlykke 1988) making the bat less detectable to thetympanate insect We do not know if any bats exploit this strat-egy but we know that all bats studied so far when gleaninguse low-intensity sounds if they emit any signals at all(Neuweiler 1989 Miller and Treat 1993 Faure and Barclay1994) For a gleaning bat the reduction of detection range isprobably not an important restriction because reducingsound intensity gives the additional advantage of reducing clut-ter echoes from the background (see Schnitzler and Kalko2001) In contrast field studies using techniques to calculatethe distance and direction to the bat indicate that at least somebats hunting aerial insects in the open emit intense signals withsource levels up to 125 dB SPL the highest levels yet measured(Jensen and Miller 1999) Also bats that display both glean-ing and aerial-hawking modes of foraging such as for in-stance Myotis evotis (Faure and Barclay 1994) and M septen-trionalis (Miller and Treat 1993) emit high intensities whenhunting flying insects

Finally shorter echolocation signals should be less con-spicuous to prey However shorter signals mean shorterechoes with less energy which are less conspicuous to the batstoo Also short search signals are recorded mainly from batsusing frequency-modulated calls and hunting close to clut-ter (Neuweiler 1989 Fenton 1990) Hencewe believe that shortcalls probably are not a countermeasure against insect hear-ing but rather an adaptation for reducing the overlap betweenechoes from clutter and those from prey

Listening to prey sounds The most effective way for abat to sneak close to tympanate prey is to cease echolocatingaltogether and detect prey using passive sensory cues If theinsects produce sound bats may find them using passivehearing Gleaning bats such as Plecotus auritus and Myotis evo-tis usually have large pinnae (Faure and Barclay 1994) Theyreact with very fast positive phonotaxis to insect-producedsounds such as the sound of wings fluttering or of an insectcrawling on a surface Some gleaning bats emit the full reper-toire of biosonar signals including the terminal phase(Schumm et al 1991) However gleaners generally stop call-ing before the attack and produce no terminal phase(Neuweiler 1989 Faure and Barclay 1994) Whether omissionof the terminal phase reduces the insectrsquos chance of escapingis difficult to say because tympanate insects probably detectecholocating bats long before the terminal phase (Roeder1967a Surlykke et al1999) However omitting the terminalphase may prevent last-chance escape maneuvers (Miller1984) On the other hand sedentary moths stay motionlessor freeze when hearing echolocation signals Turning off thesonar in the final phase may not be a countermeasure againsttympanate insects it may simply be that the bat does not needto continuously update the estimated position of a motion-less insect In contrast the prey of aerial hunters change po-sition continuously in three dimensions thus forcing the batto use its biosonar nearly to the moment of capture

It is difficult to determine if the acoustical adaptations ofbats are responses to constraints of the environment or to the

July 2001 Vol 51 No 7 BioScience 579

Articles

batsrsquo hunting strategies or are intended to overcome insect de-fenses In any case some bat echolocation signals are lessconspicuous to tympanate prey

Concluding remarksThe evolutionary arms race continues between bats and theirinsect prey and undiscovered strategies await to be revealedSome suspected strategies such as acoustical mimicry needto be documented by laboratory and field studies Experi-mental studies in the field can elucidate some questions aboutbat and insect interactions For example wild gleaning batshunting at familiar sites (Miller and Treat 1993 Faure and Bar-clay 1994) offer unique opportunities to test some hypothe-ses about echolocation behavior and the functions of clicksas interfering or warning signals Employing modern digitalsystems that can reproduce clicks and simulate insect echoeswill assist in such studies

Some questions will be difficult to answer An individualbat can modify at least some of its strategies through learn-ing whereas insect counterstrategies appear through theslower process of natural selection Does this mean insectstrategies lag behind those of their predators Perhaps not Thevariability of an individual insectrsquos antibat behaviors might bea response to the predatorrsquos ability to learn Perhaps theldquoevitabilityrdquo of the preyrsquos behavior (Roeder 1975) makeslearning by the predator less effective

AcknowledgmentsWe thank Raymond CoxOle Naeligsbye Larsen and our students(Vibeke Futtrup Marianne E Jensen Niels Skals) for com-ments on the manuscript We also appreciate the commentsof five anonymous reviewers Our research has been sup-ported by grants from the Danish Natural Sciences ResearchCouncil the Danish National Research Foundation and theCarlsberg Foundation

References citedAcharya L Fenton MB 1992 Echolocation behaviour of vespertilionid bats

(Lasiurus cinereus and Lasiurus borealis) attacking airborne targets in-cluding arctiid moths Canadian Journal of Zoology 70 1292ndash1298

Acharya L McNeil J 1998 Predation risk and mating behavior The re-sponses of moths to batlike ultrasound Behavioral Ecology 9 552ndash558

Ball EE Field LH 1981 Structure of the auditory system of the wetaHemideina crassidens (Blanchard1851) (Orthoptera Ensifera Gryl-lacridoidea Stenopelmantidae) 1 Morphology and histology Cell Tis-sue Res 217 321ndash343

Barclay RMR 1986 The echolocation calls of hoary (Lasiurus cinereus) andsilver-haired (Lasionycteris noctivagans) bats as adaptations for long-versus short-range foraging strategies and the consequences for prey se-lection Canadian Journal of Zoology 64 2700ndash2705

Bates DL Fenton MB 1990 Aposematism or startle Predators learn their re-sponses to the defenses of prey Canadian Journal of Zoology 68 49ndash52

Boyan GS Fullard JH 1986 Interneurones responding to sound in the to-bacco budworm moth Heliothis virescens (Noctuidae) Morphological andphysiological characteristics Journal of Comparative Physiology A Sen-sory Neural and Behavioral Physiology 158 391ndash404

Boyan GS Miller LA 1991 Parallel processing of afferent input by identi-fied interneurones in the auditory pathway of the noctuid moth Noctuapronuba (L) Journal of Comparative PhysiologyA Sensory Neural andBehavioral Physiology 168 727ndash738

Conner WE 1999ldquoUn chant drsquoappel amoureusrdquo Acoustic communicationin moths Journal of Experimental Biology 202 1711ndash1723

Cumming GS 1996 Mantis movements by night and the interactions of sym-patric bats and mantises Canadian Journal of Zoology 74 1771ndash1774

Dunning DC 1968 Warning sounds of moths ZTierpsychol 25 129ndash138Dunning DC Kruumlger M 1996 Predation upon moths by free-foraging Hip-

posideros caffer Journal of Mammalogy 77 708ndash715Eggers F 1919 Das thoracale bitympanale Organ einer Gruppe der Lepi-

doptera Heterocera Zool Jb (Anat) 41 273ndash376Faure PA Barclay RMR 1994 Substrate-gleaning versus aerial-hawking

Plasticity in the foraging and echolocation behaviour of the long-earedbat Myotis evotis Journal of Comparative PhysiologyA Sensory Neuraland Behavioral Physiology 174 651ndash660

Faure PA Hoy RR 2000 Neuroethology of the katydid T-cell II Responsesto acoustic playback of conspecific and predatory signals Journal ofExperimental Biology 203 3243ndash3254

Fenton MB1990 The foraging behaviour and ecology of animal-eating batsCanadian Journal of Zoology 68 411ndash422

Fenton MB Fullard JH 1981 Moth hearing and the feeding strategies of batsAmerican Scientist 69 266ndash275

Forrest TG Read MP Farris HE Hoy RR 1997 A tympanal hearing organin scarab beetles Journal of Experimental Biology 200 601ndash606

Fullard JH 1979 Behavioral analyses of auditory sensitivity in Cycnia ten-era Huumlbner (Lepidoptera Arctiidae) Journal of Comparative Physiol-ogy A Sensory Neural and Behavioral Physiology 129 79ndash83

mdashmdashmdash 1984a Acoustic relationships between tympanate moths and theHawaiian hoary bat (Lasiurus cinereus semotus) Journal of ComparativePhysiology ASensory Neuraland Behavioral Physiology 155 795ndash801

mdashmdashmdash 1984b Listening for bats Pulse repetition rate as a cue for a defen-sive behavior in Cycnia tenera (LepidopteraArctiidae)Journal of Com-parative Physiology A Sensory Neural and Behavioral Physiology 154249ndash252

mdashmdashmdash 1988 The tuning of moth ears Experientia 44 423ndash428mdashmdashmdash 1994Auditory changes in noctuid moths endemic to a bat-free niche

Journal of Evolutionary Biology 7 435ndash445Fullard JH Fenton MB 1977 Acoustic behavioural analyses of the sounds

produced by some species of Nearctic Arctiidae (Lepidoptera)CanadianJournal of Zoology 55 1213ndash1224

Fullard JH Fenton MB Simmons JA 1979 Jamming bat echolocation Theclicks of arctiid moths Canadian Journal of Zoology 57 647ndash649

Fullard JH Simmons JA Saillant PA 1994 Jamming bat echolocation Thedogbane tiger moth Cycnia tenera times its clicks to the terminal attackcalls of the big brown bat Eptesicus fuscus Journal of Experimental Bi-ology 194 285ndash298

Fullard JH Dawson JW Otero LD Surlykke A1997 Bat-deafness in day-fly-ing moths (Lepidoptera Notodontidae Dioptinae) Journal of Com-parative Physiology A Sensory Neural and Behavioral Physiology 181277ndash483

Goumlpfert MC Wasserthal LT 1999 Auditory sensory cells in hawkmoths Iden-tification physiology and structure Journal of Experimental Biology 2021579ndash1587

Hoy RR 1992 The evolution of hearing in insects as an adaptation to pre-dation from batsPages 115ndash129 in Webster DB Fay RR Popper AN edsThe Evolutionary Biology of Hearing New York Springer-Verlag

Hoy RR Nolen T Brodfuehrer P 1989 The neuroethology of acoustic star-tle and escape in flying insects Journal of Experimental Biology 146287ndash306

Jensen ME Miller LA 1999 Echolocation signals of the bat Eptesicus serot-inus recorded using a vertical microphone array Effect of flight altitudeon searching signals Behavioral Ecology and Sociobiology 47 60ndash69

Kennel JV Eggers F 1933 Die abdominalen Tympanalorgane der Lepi-dopteren Zool Jb (Anat) 57 1ndash104

Lakes-Harlan R Heller K-G 1992 Ultrasound-sensitive ears in a parasitoidfly Naturwissenschaften 79 224ndash226

Larsen ON Kleindienst H-UMichelsen A1989 Biophysical aspects of soundreception Pages 364ndash390 in Huber F Moore TELoher W eds Cricket Be-havior and Neurobiology Ithaca (NY) Cornell University Press

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572 BioScience July 2001 Vol 51 No 7

Articles

Figure 1 Insects with audition secondarily adapted for hearing bats Representative insects from the various families areshown in the left column with the location of the ear as indicated by the arrow The general anatomy of each ear is shown inthe middle column The tuning curves for avoidance behaviors (negative phonotaxis for orthopterans and nondirectionalresponses for the mantid) and interneurons thought to be involved with the behaviors are shown in the right column Thefrequency range for typical bat biosonar signals is shown on the abscissa (d right) (a middle) A cross section of the ear of acricket Gryllus bimaculatus (modified from Larsen et al 1989) (b middle) A longitudinal section of the ear of an ensiferanHemideina cassisens (modified from Ball and Field 1981) (c middle) A horizontal section through the ear of an acrididLocusta migratoria (modified from Schwabe 1906) (d middle) A partial dissection of the ventral surface of a mantidMantis religiosa (modified from Yager and Hoy 1986) (d right) The behavioral data are from Parasphendale agrioninaand the neuronal data are from M religiosa

10 m from a loudspeaker emitting batlike signals at naturalintensities They react by turning or with dives and spiral flightThe responses are all nondirectional as would be expectedfrom a functionally monaural system The lowest thresholdfor avoidance behavior occurs from 20 kHz to 80 kHz (Fig-ure 1d right Yager 1999) Yager identified an interneuronwhose tuning curve resembles that of the behavior (Figure 1dright) albeit in another species (Mantis religiosa) The neu-ron is most likely part of a neural circuit for avoidance be-havior although attempts to elicit avoidance behavior fromM religiosa to artificial bat signals have thus far failed

Flies and beetles We suspect that some flies can hearand react to bats but evidence at present is not sufficient toput them on the growing list of bat-detecting insects Thelarviparous tachinid flies Ormia ochracea and Therobialeonidei parasitize crickets and bush crickets respectively(Lakes-Harlan and Heller 1992 Robert et al 1992) The call-ing songs of their nocturnal hosts attract female flies Ormiaochracea hears best at 5 kHz as measured electrophysiologi-cally from the neck connectiveThis frequency is near the peakpower output of the hostrsquos song but the flyrsquos hearing ex-tends into the ultrasonic range The hearing of T leonidei isalso tuned to its host which sings mostly in the ultrasonicrange These flies can surely hear bats but their reactions tobatlike signals or to bats in nature are unknown

Beetles the largest order of insects are heavily preyed onby some bats and until recently ears were unknown in bee-tles The tiger beetle Cicindela marutha has ears on the firstabdominal segment that are sensitive to sound between 30 kHzand 60 kHz Batlike signals provoke changes in the beetlersquos be-havior during stationary flight which include the productionof ultrasonic clicks a property shared only with some arctiidmoths (see below Yager et al 2000) Hearing in tiger beetlesmay be used for intraspecific communication especially be-cause they also produce clicking sounds while on the groundAt present we assume that hearing in these beetles has beensecondarily adapted for detecting bats

In response to pulsed ultrasound flying scarab beetlesEutheola humilis dropped or flew toward the ground andwalking beetles stopped They hear best at 45 kHz The earsare in the neck region and have evolved independently fromthose in tiger beetles (Forrest et al 1997) perhaps specificallyfor bat detection

New auditory systems Ears have evolved independentlyin many families of eight (perhaps nine) superfamilies ofmoths (Minet and Surlykke 2002) Physiological and behav-ioral results when available for Noctuoidea PyraloideaGeometroidea Sphingoidea and Drepanoidea indicate thatthe ears are adapted specifically for hearing bat signals Veryrecently evasive behavior to batlike ultrasound was docu-mented in nocturnal butterflies of the superfamily Hedy-loidea that have ears on their wings (Yack and Fullard 2000)Green lacewings (Chrysopidae) also have ears on their wingsthat are sensitive to ultrasound and function as bat detectors

A lack of frequency sensitivity is common to all these hear-ing organs Moths and green lacewings are tone deaf In con-trast audition in orthopterans and mantids which is prob-ably secondarily adapted for hearing bats shows frequencyselectivity Nevertheless selection pressure has shaped thetuning curves the hearing or behavioral sensitivity to differ-ent sound frequencies of moth hearing Many Nearcticspecies of noctuoids hear best between 20 and 40 kHzwhereas tropical noctuoids hear best over a broader range ofultrasonic frequencies and are more sensitive than theirNearctic relatives (Fullard 1984a) A good example of this isthe noctuid Ascalapha odorata Its ear is tuned to the biosonarand social calls of the one bat species on the Hawaiian islandKauai The same or a closely related species of moth inPanama on Barro Colorado Island has a lower threshold ofhearing and a broader tuning curve This is probably anadaptation to the broader range of frequencies used by themany insectivorous bat species found there (Fullard 1984a)

Moths Ken Roeder made noctuid moths famous throughhis numerous studies of their hearing and behavior (Roeder1967a) The Noctuidae Notodontidae and Arctiidae (all inthe superfamily Noctuoidea Figure 2a left) have ears on thelateral surfaces of the metathorax (Figure 2a middle) Behindthe thin tympanal membrane is a large air sac which is sep-arated from other air sacs by tracheal membranes Two sen-sory cells A1 and A2 (but a single A cell in notodontids seeSurlykke 1988) are attached to the tympanum The two cellshave identical tuning curves (Figure 2a right) and dynamicranges but they differ by about 20 dB in sensitivity Dynamicrange is the range over which neural responses occur tosound intensity measured in dB from threshold to saturationThe noctuid and arctiid moths have a total auditory dynamicrange of about 40 dB

Freely flying unidentified moths exhibit a variety of be-havioral responses to bats and to synthetic batlike signals(Roeder 1967a for recent results refer to Acharya and Fen-ton 1992) Moths far from the source often turn and fly awaywhereas those close to the source show zigzag and loopingflight power dives or passive falls Presumably the loudersounds recruit the A2 sensory cells which trigger the switchfrom negative phonotaxis to less predictable evasive flight be-havior However Roeder (1964) indicated that the percent-age of moths showing turning-away responses decreases andthe percentage showing looping responses increases as thepulse repetition rate increases Because of this Roeder (1964)suggested that the most sensitive sensory cell (A1) actingalone could release several behaviors but further experi-mentation is needed to confirm this

Size and sensitivity are correlated in moths complicatingmatters further Big moths reflect more intense echoes thansmall moths and may be detected by bats as far away as 10 mHowever results from noctuid moths show that big moths arealso more sensitive and may detect approaching bats as faraway as 100 m Thus there seems to be a fairly constant 10-fold margin of safety that is noctuid moths can detect bats

July 2001 Vol 51 No 7 BioScience 573

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574 BioScience July 2001 Vol 51 No 7

Articles

Figure 2 Insects with audition adapted specifically for hearing bats Representative insects from the various families areshown in the left column with the location of the ear indicated by arrow The general anatomy of each ear is shown in themiddle column The tuning curves for flight cessation (behavior) the A1 sensory cells and an interneuron are shown inthe right column The frequency range for typical bat biosonar signals is shown on the abscissa (d right) (a middle) Ahorizontal section through the metathorax of a noctuid moth (modified after Eggers 1919) (b middle) A cross sectionthrough the first abdominal segment of a geometrid moth viewed from the inside (modified after Kennel and Eggers1933) A single tympanal air sac occupies the space behind the tympana (not seen in this drawing) The pyralid ear (egGalleria mellonella) is anteroabdominal like that of the geometrid (b right) Data for a geometrid Biston betularia(modified from Surlykke and Filskov 1997) as well as for a pyralid Galleria mellonella (c middle) The head of asphingid moth Celerio lineata with one labial palp in longitudinal section The sound receivers (pilifers) are seen on thelateral surface of the proboscis (modified from Roeder et al 1970) (d middle) The ventral surface of the base of the wingof the green lacewing Chrysoperla carnea (modified after Miller 1975) References for tuning curves are given in the text

at about 10 times the distance over which bats can detectmoths (Surlykke et al 1999)

Many interneurons in the thoracic and cephalic ganglia ofnoctuids have been characterized (Roeder 1975 Boyan andFullard 1986) For example two identified neurons receive di-rect input from the A1 afferent in parallelbut they process tem-poral information differently (Boyan and Miller 1991) Synap-tic input to some motor neurons controlling the upndashdownmovement of the wings occurs only when the A2 sensory cellis activated (Madsen and Miller 1987) The role individual in-terneurons play in eliciting behavior is speculative principallybecause the responses of moths are exceedingly difficult tostudy under controlled conditions (Roeder 1967b)

Arctiid moths behave like noctuids but are more reluctantto do so In addition some arctiids produce ultrasonic click-ing sounds from tymbal organs when they hear bat signals orare touched (The clicks have various effects on bats as de-scribed below) Cycnia tenera starts clicking before it stops fly-ing in response to ultrasonic stimuli (Fullard 1979) Thethreshold for flight cessation is about 10ndash20 dB above that forclicking and repetition rates from 17ndash40 pulses per secondare best at eliciting clicking (Fullard 1984b) Also the rate ofmotor spikes to the tymbal muscles increases when the stim-ulus rate increases (Northcott and Fullard 1996) So both am-plitude and pulse repetition rate of the ultrasonic stimulus in-fluence behavioral responses from noctuid and arctiid moths

The Geometridae Pyralidae and Drepanidae have ultra-sound-sensitive ears on the first abdominal segment (Minetand Surlykke 2001) In the geometrids (Figure 2b left) thetympana are adjacent to the midline and point caudally (Fig-ure 2b middle) The tympana in pyralids point rostrally andhave a slight tilt ventrallyFour sensory (A) cells attach to eachtympanum The dynamic range for hearing in the geometridBiston betularia is about 50 dB because each cell covers asmaller range (10ndash15 dB) than the A cells in a noctuid ear Thefrequency range of hearing extends to at least 100 kHz in allspecies studied thus far (Figure 2b right B betularia Surlykkeand Filskov 1997) Some geometrids show flight cessation andother responses to ultrasound (Rydell et al 1997) Pyralid waxmoths respond to bat cries (Spangler and Takessian 1983) andGalleria mellonella shows a number of behavioral responseswhile in stationary flight the most noticeable of which isflight cessation (Skals and Surlykke 2000) Flight cessationwhich is the behavior with the highest threshold occurs at +20to +25 dB with respect to the threshold for the A1 cell (Fig-ure 2b right G mellonella) Actually avoidance behavior tobat echolocation is so powerful that some pyralid (and noc-tuid) moths abort sexually oriented flight to females broad-casting pheromones (Acharya and McNeil 1998)

The bat-detecting ear of some hawk moths (Figure 2cleft) consists of air-filled labial palps that transmit sound en-ergy to the pilifers located on either side of the proboscis(Figure 2c middle) Other hawk moths have scale plates onthe labial palps rather than air-filled palps Neurophysiolog-ical recordings from the labial nerve or from interneurons re-veal the auditory characteristics in both types of hawk moths

(Figure 2c right) They are most sensitive to frequencies be-tween 20 and 30 kHz with a threshold of 40ndash50 dB sound pres-sure level The dynamic range of the single auditory sensoryneuron in the pilifer is about 20 dB resembling that in the earof notodontid moths Hawk moths in tethered flight respondto ultrasound with changes in flight speed with nondirectionalturning and sometimes by emitting sound The behavioralthreshold is about 70 dB SPL or 20 dB above the sensorythreshold (Roeder et al 1970 Goumlpfert and Wasserthal 1999)

Green lacewings The ear of the green lacewing (Figure 2dleft) is located in a bulge near the base of the radial vein in eachforewing (Figure 2d middle) It is a true tympanal organwhich is mostly fluid filled and contains a small trachea It isthe smallest tympanal organ knownPerhaps only 6 of the 25sensory cells actually respond to ultrasound (see Miller 1984for a review) Like wax moths green lacewings in stationaryflight show a number of responses to lower intensity stimulibefore ceasing their flight (Miller 1975) Flight cessation (Fig-ure 2d right) occurs most reliably to ultrasonic signals broad-cast at rates of 1ndash50 pulses per second High stimulus repe-tition rates alone were ineffective in stopping the flight ofrestrained green lacewings

A more realistic picture of behavior emerged from studieson freely flying green lacewings and bats (Figure 3) Bat sig-nals at low repetition rates possibly combined with low in-tensities cause insects to fold their wings and passively diveThe green lacewing shows this nondirectional early-warningresponse to batsrsquo searching signals (Figure 3 between flashes2 and 3) The bat increases its call rate as it approaches a fallinginsect (Figure 3 flashes 3 to 4) Just before capturing its preythe bat increases its repetition rate to a maximum of about200 signals per second in the terminal phase for most bats (Fig-ure 3 flash 5) During the terminal phase the insect suddenlyflipped open its wings (Figure 3 flash 5 arrow) presumablyin response to the high repetition rate signals This last-chance response breaks the dive and foils the bat in this caseafter which the insect continues its dive (Figure 3 flash 6)Artificial bat signals mimicking the sequence shown in Fig-ure 3 evoke the same behavior (Miller and Olesen 1979) Byrepeating the experiments with deafened green lacewingswe showed that the selective advantage of reactors over non-reactors was 47 or about the same as that found for moths(see Miller 1982) Unidentified neurons in the prothoracic gan-glion respond to ultrasound but their role in eliciting behavioris unknown (Miller 1984)

Conclusions about insect behaviorsWe can draw some conclusions and make predictions basedon what we know about avoidance behaviors Looking at allthe behavioral response types for all the insects mentionedabove we find that the best frequency the frequency at whichneural or behavioral responses have the lowest thresholdlies between about 20 and 60 kHz with thresholds betweenabout 30 and 70 dB SPL The response latencies range from40ndash70 ms at +15 dB with respect to the behavioral threshold

July 2001 Vol 51 No 7 BioScience 575

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Because the distance at which the insects respond to 40 kHzsounds varies from 65ndash37 m for bats using intense signalsthe insects have several tenths of a second to avoid even fast-flying bats (Surlykke 1988) The situation is somewhat differentfor whispering bats which use intensities of less than about75 dB SPL and hunt near vegetation Here the response dis-tances for flying insects are from 01ndash27 m depending on thehearing threshold However bats can detect a moth-sizedecho at about 06 m putting the less-sensitive insects in dan-ger Many of the insects mentioned above are open-air fliersand normally do not meet whispering bats

The tuning of neurons suspected to be involved in avoid-ance behavior in preadapted insects such as crickets grasshop-pers and preying mantids poorly match the behavioral tun-ing This discrepancy suggests that these auditory neurons havebeen molded into an antibat circuitry as a result of selectionpressure Behaviors such as turning in midflight or flightcessation have thresholds typically 20 dB higher than thosefor sensory neurons or interneurons (except premotor in-terneurons) in the same insects Consequently yet undis-covered behaviors to low stimulus intensities may provide ad-ditional survival advantage

Insect avoidance behaviors and their underlying mecha-nisms are undoubtedly complicated Take for example the vari-ability of responses The behaviors cannot be reliably predictedand the same individual may show different responses or noresponse at all to the same stimulus Roeder called this theldquoevitabilityrdquoof behavior which provides a survival advantageby making it difficult for the predator to predict what the preywill do The characteristic feature of evitability makes it dif-ficult to study but it seems to be present in the behavior and

physiology of some moths (Roeder 1975 Madsen and Miller1987) and green lacewings (Miller and Olesen 1979)Nevertheless the auditory and behavioral mechanismspresented here found in many families in several orders ofinsects give an overall picture of convergent evolution inresponse to bat predation

Insects living in bat-free environments

Spatial isolation Some moths escape from the risk of pre-dation by insectivorous bats simply by living in places whereno bats occur Bats are found on all continents except Antarc-tica and on the majority of islands but some remote islandsare free of bats for instance the Faroe Islands in the NorthAtlantic and the islands in French Polynesia

In general moth hearing sensitivity tends to reflect thecharacteristic frequencies and intensities of the local batfaunaHowever moths from the Faroes (Surlykke 1986) as wellas those from Tahiti (French Polynesia Fullard 1994) have re-tained auditory sensitivity in complete isolation from bats Iso-lated moths have thresholds at the best frequencies that arecomparable to the thresholds of moths sympatric with batsin similar habitats temperate or tropical Moths from HighArctic areas also show evasive maneuvers to ultrasound (Ry-dell et al 2000) The reason these moths have retained sen-sitive hearing which seems totally superfluous is not knownIt may simply be due to the slow regression of a character ifthere is no selection pressure against it In contrast a characterthat has adaptive value may spread through the populationafter only a few generations as shown by melanism in the pep-pered moth Biston betularia

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Figure 3 The behavioral responses of a green lacewing to a hunting pipistrelle bat The behavior was photographed in alarge flight cage using stroboscopic flashes at 70-ms intervals The biosonar signals that the bat emitted during the variousstages of hunting were simultaneously recorded The signals are schematic and only the intervals are accurately shownModified from Miller and Olesen 1979

Temporal isolation This is another strategy to avoidbats The Cuculliinae (Noctuidae) include moths that areactive in the winter Several species (eg Lithophane grotei andEupsilia vinulenta) were captured in Massachusetts in No-vember over a 3-week period when snow covered the groundand nightly bat censuses revealed none All captured mothshad functional ears tuned to bat sounds with thresholds as lowas their relatives flying in the summer (Surlykke and Treat1995) A study of hearing in winter-active geometrid mothsgave a similar result (Rydell et al 1997) Apparently noctur-nally active winter moths do not use their hearing even forintraspecific communication Isolated moths retain their ul-trasonic hearing which indicates that it is not very costly evo-lutionarily speaking to retain ears if they provide wintermoths with additional protection such as from the possibil-ity of occasionally overlapping with bats

The nocturnal noctuid moth Rileyana fovea (formerlyThecophora fovea) from Central Europe emerges in late Oc-tober to early November after bat activity has decreased Ri-leyana fovea communicates with ultrasound The males singin flight by scraping the file of the hind tarsus against the foveawhich is an inflated bubble on the hindwing supported by theheavily sclerotized radial vein (Figure 4) The intense sounds(80 dB at 1 m) have peak power around 30 kHz which wouldmake the moths very conspicuous to bats The moths are read-ily eaten by captive bats However by being active at a timeof the year with few bats R fovea can use ultrasound for in-traspecific communication Hence it seems that a completeconversion of hearing from a defensive context to a sexual onehas occurred secondarily in R fovea (Surlykke and Gogala1986) Ultrasound-producing organs have developed inde-pendently in distantly related species of moths that are pro-tected from bats in different ways This suggests that the pre-

existing ear prompted the development of intraspecificacoustic communication in certain moths (Conner 1999Skals and Surlykke 1999)

Some moths have changed to diurnal life a secondaryadaptation perhaps in response to predation by bats Oftendiurnal moths are protected by toxins and warning colors likesome butterflies These day fliers include many tiger moths(Arctiidae) especially from the subfamily Ctenuchinae Onlyrelatively few Noctuidae are day fliers One example is the Aus-tralian whistling moth Hecatesia thyridion (Agaristinae)which is brightly patterned and probably toxic Male whistlingmoths produce sounds that are audible but most of the en-ergy is in the ultrasonic range where their hearing is best Theyuse sounds to defend their territories and to attract females(Surlykke and Fullard 1989) Some diurnal moths are silentand apparently their hearing has no function at all For ex-ample diurnal notodontid moths in the subfamily Dioptinaefrom Venezuela show varying degrees of auditory degenera-tion ranging from almost normal sensitivity in some speciesto very reduced sensitivity especially at ultrasonic frequenciesin other species (Fullard et al 1997) Similarly the diurnalgeometrid Archiearis parthenias is practically deaf to ultrasonicfrequencies (Surlykke et al 1998)

Sound as defenseMany arctiids possess tymbal organs located on the sides ofthe metathorax (Figure 5a Conner 1999) Special musclesbuckle the tymbal membrane generating one click or a burstof clicks per activation cycle (Figure 5b) Click amplitudes varyfrom about 50ndash90 dB SPL measured at 5 cm with maxi-mum sound energy falling between 30 and 80 kHz (Figure 5cFullard and Fenton 1977 Surlykke and Miller 1985) Flyingarctiids may click when they hear the biosonar signals ofbats Thresholds for clicking can be as low as 60ndash75 dB SPLfor simulated search-phase signals (Fullard 1979 Surlykke andMiller 1985) but considerably higher for short signals (about2 ms Fullard 1984b)

Some bats and insects share the same hibernacula andmarauding bats feed on hibernating insects Nymphalid but-terflies sense the vibrations in the substratum as the batcrawls toward it The torpid butterfly opens its wings in a char-acteristic manner which produces intense ultrasonic clicksfrom a special area of the wing membrane (Moslashhl and Miller1976) What purpose do the clicks serve There are threelikely functions of clicking sounds They could startle bats theycould interfere with the batsrsquo biosonar system or they couldwarn bats of a distasteful prey as many arctiid moths containtoxins in their body tissues or in special glands

Startle and interference The clicks of nymphalid but-terflies startle bats and thus provide a chance for the insect toescape However a bat quickly habituates to the sounds andeats these butterflies (Moslashhl and Miller 1976) For experi-enced bats clicks can act as a dinner bellArctiid clicks can star-tle inexperienced and naive bats (Eptesicus fuscus) but thesebats also habituate rapidly (Bates and Fenton 1990 Miller

July 2001 Vol 51 No 7 BioScience 577

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Figure 4 Male stridulatory organ used for the productionof intraspecific communication sounds by the noctuidmoth Rileyana fovea (formerly Thecophora fovea)Sound pulses with carrier frequencies of about 30 kHzare produced by scraping the file on the tarsus of the hindleg against the stridulatory swelling (fovea) on thehindwing Modified from Surlykke and Gogala 1986

1991) Thus clicks must be used sparingly to have survivalvalue as startle signals

The ultrasonic clicks of arctiids might disturb bat biosonarin two ways by simulating multiple targets (Fullard et al1979 1994) and by interfering with range determination(Miller 1991) The arctiid Cycnia tenera produces long trainsof clicks at high rates Fullard et al (1979 1994) hypothesizedthat clicks of C tenera could function as acoustical camou-flage by simulating multiple targets (false echoes) near themoth and thus jam a batrsquos (Eptesicus fuscus) biosonar Theybased their conclusion mainly on the ability of the moth totime its clicking to the terminal phase of the batrsquos signals Milleret al (forthcoming) tested this idea using bats (Pipistrellus pip-istrellus) trained to catch catapulted meal worms after whichnatural click sequences from the arctiid Phragmatobia fulig-inosa were played back during the batsrsquo terminal phase Thebats reacted by increasing the harmonic structure of their ter-minal signals but clicks did not influence the success rate of

prey capture The results suggest that the clicks produced byP fuliginosa do not interfere with the batsrsquo sonar system per-haps because the click rate is too low However in psy-chophysical experiments the clicks from P fuliginosa did in-terfere with the ability of bats (Eptesicus fuscus) to determinerange differences (Miller 1991) When clicks triggered bythe batsrsquo own signals fall repeatedly within a critical time win-dow of about 15 ms before an echo the batrsquos discriminationof range differences deteriorated by as much as 40-fold A sin-gle artificial click placed within the critical window inter-feres with range difference determination (Tougaard et alforthcoming) and with neural responses (Tougaard et al1998) In either case a bat would miss its target if clicks rep-resent false echoes from phantom objects or if they interferewith the batrsquos ranging mechanism

Warning sounds toxins and mimicry Several factspoint to the warning function of clicks as suggested by Dun-ning (1968) The Arctiidae (including the Ctenuchinae) aregenerally unpalatable and arctiids are the only noctuoidmoths that click in response to bat sonar sounds Arctiidclicks could warn the bat of a noxious prey Evidence sup-porting a warning function comes from studies in the labo-ratory and the field In experimental studies bats (Pipistrel-lus pipistrellus and Eptesicus fuscus) habituated to arctiid clickswhen given palatable rewards (Surlykke and Miller 1985Bates and Fenton 1990) However the same bats learned veryquickly to associate moth clicks with a distasteful rewardField studies indicated that bats (Lasiurus sp) foraging aroundstreet lights often aborted their attacks in the approach or ter-minal phase when the prey was the noisy arctiid mothHypoprepia fucosa (Acharya and Fenton 1992) Wild H fucosadid not take visible evasive action to attacking bats Batsavoided more than 90 of the moths released and droppedthe few they captured usually undamaged The bats showedno evidence of habituation although H fucosa were abundantcomposing more than 30 of the moth population Hy-poprepia fucosa has classic warning coloration and patterns as-sociated with toxic species Evidence favors the assumptionthat arctiid clicks are acoustical aposematic signals warningbats that the moths taste bad (Dunning and Kruumlger 1996)

Combining acoustic defenses The startle interferenceand warning hypotheses are not mutually exclusive In areaswhere arctiid moths are scarce the clicks may mostly startlebats Because bats quickly adapt to the clicks a warning func-tion is most likely in areas where arctiid moths are abundantWarning seems especially likely for toxic arctiids like Arctia cajawhich produce few but intense clicks in response to batlikesignals (Surlykke and Miller 1985) At least some species of arc-tiids begin clicking to the searching signals of aerial hawkingbats at distances of about 2ndash4 m (Surlykke and Miller 1985)At these distances the bat should be able to hear the clicks giv-ing an experienced predator ample time to avoid the dis-tasteful prey There is sufficient time for the bat to change itsbehavior even if the warning comes during the approach or

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Figure 5 Arctiid tymbal organ and clicks (a) The tymbalorgan on the lateral surface of the metathoracic segmentof the arctiid Phragmatobia fuliginosa (b) The tymbalorgan produces a burst of clicks each time it buckles (c)The power spectrum of the burst has a maximum atabout 80 kHz (a) Modified from Surlykke and Miller1985 (b) and (c) modified from Miller 1991

terminal phases of the batrsquos pursuit (Acharya and Fenton1992) Should the mothrsquos clicks arrive at the batrsquos ear just be-fore the echoes the batrsquos estimation of range to the preyblurs perhaps causing the bat to miss the target Moths us-ing long trains of click bursts could exploit this strategy Allthree possibilities startle interference and warning offerselective advantages for arctiid moths in addition to thoseprovided by changes in flight behavior

Potential countertactics for batsThe diet of many bats contains very few moths perhaps be-cause of their effective defenses However some barbastelle batsprey almost exclusively on tympanate moths and just how theydo this is not known (Sierro and Arlettaz 1997) Here wepresent some possible double-edged strategies that may ex-plain bat adaptations

Changing signals Echolocating bats announce their pres-ence to all potential prey equipped with auditory bat detec-tors and bats may use different acoustic strategies to reducetheir conspicuousness One strategy would be an adaptationthat moved frequencies of sonar signals out of the rangewhere tympanate insects are most sensitive (Dunning andKruumlger 1996) Some bats use very high frequencies whichmake them less audible to most noctuoid moths Howeversmall moths such as some geometrids (Surlykke and Filskov1997) the pyralid Galleria mellonella (Figure 2b right) andmany tropical noctuoids (Fullard 1988) are quite sensitive tohigh frequencies The attenuation of high frequencies re-duces the useful range of bat sonar so the advantage of thisstrategy may be limited If emission of high frequencies werea countermeasure against tympanate insects one would ex-pect to find bats exploiting this strategy in temperate regionswhere many moths do have poor sensitivity at high frequen-cies (Fullard 1988) The only temperate nongleaning batsthat use relatively high frequencies are small ones (eg Pip-istrellus spp) which detect small prey While the emission ofhigh frequencies may be a response to insect defenses it mayalso be a way to increase resolution and thus increase the abil-ity of bats to detect smaller insects (Surlykke et al 1993)

A second strategy would be for bats to emit very low fre-quencies which would make them less conspicuous to moths(Rydell and Arlettaz 1994) This strategy is employed mostlyby fast-flying bats that hunt aerial insects far from the groundand vegetation (Neuweiler 1989 Fenton 1990) Low fre-quencies increase the batsrsquo range but lower the resolution ofthe batsrsquo biosonar making only large insects detectable (Bar-clay 1986)

A third strategy would be an adaptation for bats to reducethe intensity of their signals Sound intensity is a measure ofsound energy and is proportional to the sound pressure(The dB scale is adapted such that any change in sound pres-sure and the corresponding change in sound intensity resultin the same change in dB value) The advantage would be thatthe sound intensity decreases with the square of the distancebut the echo intensity decreases with the fourth power of the

distance (Surlykke 1988) making the bat less detectable to thetympanate insect We do not know if any bats exploit this strat-egy but we know that all bats studied so far when gleaninguse low-intensity sounds if they emit any signals at all(Neuweiler 1989 Miller and Treat 1993 Faure and Barclay1994) For a gleaning bat the reduction of detection range isprobably not an important restriction because reducingsound intensity gives the additional advantage of reducing clut-ter echoes from the background (see Schnitzler and Kalko2001) In contrast field studies using techniques to calculatethe distance and direction to the bat indicate that at least somebats hunting aerial insects in the open emit intense signals withsource levels up to 125 dB SPL the highest levels yet measured(Jensen and Miller 1999) Also bats that display both glean-ing and aerial-hawking modes of foraging such as for in-stance Myotis evotis (Faure and Barclay 1994) and M septen-trionalis (Miller and Treat 1993) emit high intensities whenhunting flying insects

Finally shorter echolocation signals should be less con-spicuous to prey However shorter signals mean shorterechoes with less energy which are less conspicuous to the batstoo Also short search signals are recorded mainly from batsusing frequency-modulated calls and hunting close to clut-ter (Neuweiler 1989 Fenton 1990) Hencewe believe that shortcalls probably are not a countermeasure against insect hear-ing but rather an adaptation for reducing the overlap betweenechoes from clutter and those from prey

Listening to prey sounds The most effective way for abat to sneak close to tympanate prey is to cease echolocatingaltogether and detect prey using passive sensory cues If theinsects produce sound bats may find them using passivehearing Gleaning bats such as Plecotus auritus and Myotis evo-tis usually have large pinnae (Faure and Barclay 1994) Theyreact with very fast positive phonotaxis to insect-producedsounds such as the sound of wings fluttering or of an insectcrawling on a surface Some gleaning bats emit the full reper-toire of biosonar signals including the terminal phase(Schumm et al 1991) However gleaners generally stop call-ing before the attack and produce no terminal phase(Neuweiler 1989 Faure and Barclay 1994) Whether omissionof the terminal phase reduces the insectrsquos chance of escapingis difficult to say because tympanate insects probably detectecholocating bats long before the terminal phase (Roeder1967a Surlykke et al1999) However omitting the terminalphase may prevent last-chance escape maneuvers (Miller1984) On the other hand sedentary moths stay motionlessor freeze when hearing echolocation signals Turning off thesonar in the final phase may not be a countermeasure againsttympanate insects it may simply be that the bat does not needto continuously update the estimated position of a motion-less insect In contrast the prey of aerial hunters change po-sition continuously in three dimensions thus forcing the batto use its biosonar nearly to the moment of capture

It is difficult to determine if the acoustical adaptations ofbats are responses to constraints of the environment or to the

July 2001 Vol 51 No 7 BioScience 579

Articles

batsrsquo hunting strategies or are intended to overcome insect de-fenses In any case some bat echolocation signals are lessconspicuous to tympanate prey

Concluding remarksThe evolutionary arms race continues between bats and theirinsect prey and undiscovered strategies await to be revealedSome suspected strategies such as acoustical mimicry needto be documented by laboratory and field studies Experi-mental studies in the field can elucidate some questions aboutbat and insect interactions For example wild gleaning batshunting at familiar sites (Miller and Treat 1993 Faure and Bar-clay 1994) offer unique opportunities to test some hypothe-ses about echolocation behavior and the functions of clicksas interfering or warning signals Employing modern digitalsystems that can reproduce clicks and simulate insect echoeswill assist in such studies

Some questions will be difficult to answer An individualbat can modify at least some of its strategies through learn-ing whereas insect counterstrategies appear through theslower process of natural selection Does this mean insectstrategies lag behind those of their predators Perhaps not Thevariability of an individual insectrsquos antibat behaviors might bea response to the predatorrsquos ability to learn Perhaps theldquoevitabilityrdquo of the preyrsquos behavior (Roeder 1975) makeslearning by the predator less effective

AcknowledgmentsWe thank Raymond CoxOle Naeligsbye Larsen and our students(Vibeke Futtrup Marianne E Jensen Niels Skals) for com-ments on the manuscript We also appreciate the commentsof five anonymous reviewers Our research has been sup-ported by grants from the Danish Natural Sciences ResearchCouncil the Danish National Research Foundation and theCarlsberg Foundation

References citedAcharya L Fenton MB 1992 Echolocation behaviour of vespertilionid bats

(Lasiurus cinereus and Lasiurus borealis) attacking airborne targets in-cluding arctiid moths Canadian Journal of Zoology 70 1292ndash1298

Acharya L McNeil J 1998 Predation risk and mating behavior The re-sponses of moths to batlike ultrasound Behavioral Ecology 9 552ndash558

Ball EE Field LH 1981 Structure of the auditory system of the wetaHemideina crassidens (Blanchard1851) (Orthoptera Ensifera Gryl-lacridoidea Stenopelmantidae) 1 Morphology and histology Cell Tis-sue Res 217 321ndash343

Barclay RMR 1986 The echolocation calls of hoary (Lasiurus cinereus) andsilver-haired (Lasionycteris noctivagans) bats as adaptations for long-versus short-range foraging strategies and the consequences for prey se-lection Canadian Journal of Zoology 64 2700ndash2705

Bates DL Fenton MB 1990 Aposematism or startle Predators learn their re-sponses to the defenses of prey Canadian Journal of Zoology 68 49ndash52

Boyan GS Fullard JH 1986 Interneurones responding to sound in the to-bacco budworm moth Heliothis virescens (Noctuidae) Morphological andphysiological characteristics Journal of Comparative Physiology A Sen-sory Neural and Behavioral Physiology 158 391ndash404

Boyan GS Miller LA 1991 Parallel processing of afferent input by identi-fied interneurones in the auditory pathway of the noctuid moth Noctuapronuba (L) Journal of Comparative PhysiologyA Sensory Neural andBehavioral Physiology 168 727ndash738

Conner WE 1999ldquoUn chant drsquoappel amoureusrdquo Acoustic communicationin moths Journal of Experimental Biology 202 1711ndash1723

Cumming GS 1996 Mantis movements by night and the interactions of sym-patric bats and mantises Canadian Journal of Zoology 74 1771ndash1774

Dunning DC 1968 Warning sounds of moths ZTierpsychol 25 129ndash138Dunning DC Kruumlger M 1996 Predation upon moths by free-foraging Hip-

posideros caffer Journal of Mammalogy 77 708ndash715Eggers F 1919 Das thoracale bitympanale Organ einer Gruppe der Lepi-

doptera Heterocera Zool Jb (Anat) 41 273ndash376Faure PA Barclay RMR 1994 Substrate-gleaning versus aerial-hawking

Plasticity in the foraging and echolocation behaviour of the long-earedbat Myotis evotis Journal of Comparative PhysiologyA Sensory Neuraland Behavioral Physiology 174 651ndash660

Faure PA Hoy RR 2000 Neuroethology of the katydid T-cell II Responsesto acoustic playback of conspecific and predatory signals Journal ofExperimental Biology 203 3243ndash3254

Fenton MB1990 The foraging behaviour and ecology of animal-eating batsCanadian Journal of Zoology 68 411ndash422

Fenton MB Fullard JH 1981 Moth hearing and the feeding strategies of batsAmerican Scientist 69 266ndash275

Forrest TG Read MP Farris HE Hoy RR 1997 A tympanal hearing organin scarab beetles Journal of Experimental Biology 200 601ndash606

Fullard JH 1979 Behavioral analyses of auditory sensitivity in Cycnia ten-era Huumlbner (Lepidoptera Arctiidae) Journal of Comparative Physiol-ogy A Sensory Neural and Behavioral Physiology 129 79ndash83

mdashmdashmdash 1984a Acoustic relationships between tympanate moths and theHawaiian hoary bat (Lasiurus cinereus semotus) Journal of ComparativePhysiology ASensory Neuraland Behavioral Physiology 155 795ndash801

mdashmdashmdash 1984b Listening for bats Pulse repetition rate as a cue for a defen-sive behavior in Cycnia tenera (LepidopteraArctiidae)Journal of Com-parative Physiology A Sensory Neural and Behavioral Physiology 154249ndash252

mdashmdashmdash 1988 The tuning of moth ears Experientia 44 423ndash428mdashmdashmdash 1994Auditory changes in noctuid moths endemic to a bat-free niche

Journal of Evolutionary Biology 7 435ndash445Fullard JH Fenton MB 1977 Acoustic behavioural analyses of the sounds

produced by some species of Nearctic Arctiidae (Lepidoptera)CanadianJournal of Zoology 55 1213ndash1224

Fullard JH Fenton MB Simmons JA 1979 Jamming bat echolocation Theclicks of arctiid moths Canadian Journal of Zoology 57 647ndash649

Fullard JH Simmons JA Saillant PA 1994 Jamming bat echolocation Thedogbane tiger moth Cycnia tenera times its clicks to the terminal attackcalls of the big brown bat Eptesicus fuscus Journal of Experimental Bi-ology 194 285ndash298

Fullard JH Dawson JW Otero LD Surlykke A1997 Bat-deafness in day-fly-ing moths (Lepidoptera Notodontidae Dioptinae) Journal of Com-parative Physiology A Sensory Neural and Behavioral Physiology 181277ndash483

Goumlpfert MC Wasserthal LT 1999 Auditory sensory cells in hawkmoths Iden-tification physiology and structure Journal of Experimental Biology 2021579ndash1587

Hoy RR 1992 The evolution of hearing in insects as an adaptation to pre-dation from batsPages 115ndash129 in Webster DB Fay RR Popper AN edsThe Evolutionary Biology of Hearing New York Springer-Verlag

Hoy RR Nolen T Brodfuehrer P 1989 The neuroethology of acoustic star-tle and escape in flying insects Journal of Experimental Biology 146287ndash306

Jensen ME Miller LA 1999 Echolocation signals of the bat Eptesicus serot-inus recorded using a vertical microphone array Effect of flight altitudeon searching signals Behavioral Ecology and Sociobiology 47 60ndash69

Kennel JV Eggers F 1933 Die abdominalen Tympanalorgane der Lepi-dopteren Zool Jb (Anat) 57 1ndash104

Lakes-Harlan R Heller K-G 1992 Ultrasound-sensitive ears in a parasitoidfly Naturwissenschaften 79 224ndash226

Larsen ON Kleindienst H-UMichelsen A1989 Biophysical aspects of soundreception Pages 364ndash390 in Huber F Moore TELoher W eds Cricket Be-havior and Neurobiology Ithaca (NY) Cornell University Press

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10 m from a loudspeaker emitting batlike signals at naturalintensities They react by turning or with dives and spiral flightThe responses are all nondirectional as would be expectedfrom a functionally monaural system The lowest thresholdfor avoidance behavior occurs from 20 kHz to 80 kHz (Fig-ure 1d right Yager 1999) Yager identified an interneuronwhose tuning curve resembles that of the behavior (Figure 1dright) albeit in another species (Mantis religiosa) The neu-ron is most likely part of a neural circuit for avoidance be-havior although attempts to elicit avoidance behavior fromM religiosa to artificial bat signals have thus far failed

Flies and beetles We suspect that some flies can hearand react to bats but evidence at present is not sufficient toput them on the growing list of bat-detecting insects Thelarviparous tachinid flies Ormia ochracea and Therobialeonidei parasitize crickets and bush crickets respectively(Lakes-Harlan and Heller 1992 Robert et al 1992) The call-ing songs of their nocturnal hosts attract female flies Ormiaochracea hears best at 5 kHz as measured electrophysiologi-cally from the neck connectiveThis frequency is near the peakpower output of the hostrsquos song but the flyrsquos hearing ex-tends into the ultrasonic range The hearing of T leonidei isalso tuned to its host which sings mostly in the ultrasonicrange These flies can surely hear bats but their reactions tobatlike signals or to bats in nature are unknown

Beetles the largest order of insects are heavily preyed onby some bats and until recently ears were unknown in bee-tles The tiger beetle Cicindela marutha has ears on the firstabdominal segment that are sensitive to sound between 30 kHzand 60 kHz Batlike signals provoke changes in the beetlersquos be-havior during stationary flight which include the productionof ultrasonic clicks a property shared only with some arctiidmoths (see below Yager et al 2000) Hearing in tiger beetlesmay be used for intraspecific communication especially be-cause they also produce clicking sounds while on the groundAt present we assume that hearing in these beetles has beensecondarily adapted for detecting bats

In response to pulsed ultrasound flying scarab beetlesEutheola humilis dropped or flew toward the ground andwalking beetles stopped They hear best at 45 kHz The earsare in the neck region and have evolved independently fromthose in tiger beetles (Forrest et al 1997) perhaps specificallyfor bat detection

New auditory systems Ears have evolved independentlyin many families of eight (perhaps nine) superfamilies ofmoths (Minet and Surlykke 2002) Physiological and behav-ioral results when available for Noctuoidea PyraloideaGeometroidea Sphingoidea and Drepanoidea indicate thatthe ears are adapted specifically for hearing bat signals Veryrecently evasive behavior to batlike ultrasound was docu-mented in nocturnal butterflies of the superfamily Hedy-loidea that have ears on their wings (Yack and Fullard 2000)Green lacewings (Chrysopidae) also have ears on their wingsthat are sensitive to ultrasound and function as bat detectors

A lack of frequency sensitivity is common to all these hear-ing organs Moths and green lacewings are tone deaf In con-trast audition in orthopterans and mantids which is prob-ably secondarily adapted for hearing bats shows frequencyselectivity Nevertheless selection pressure has shaped thetuning curves the hearing or behavioral sensitivity to differ-ent sound frequencies of moth hearing Many Nearcticspecies of noctuoids hear best between 20 and 40 kHzwhereas tropical noctuoids hear best over a broader range ofultrasonic frequencies and are more sensitive than theirNearctic relatives (Fullard 1984a) A good example of this isthe noctuid Ascalapha odorata Its ear is tuned to the biosonarand social calls of the one bat species on the Hawaiian islandKauai The same or a closely related species of moth inPanama on Barro Colorado Island has a lower threshold ofhearing and a broader tuning curve This is probably anadaptation to the broader range of frequencies used by themany insectivorous bat species found there (Fullard 1984a)

Moths Ken Roeder made noctuid moths famous throughhis numerous studies of their hearing and behavior (Roeder1967a) The Noctuidae Notodontidae and Arctiidae (all inthe superfamily Noctuoidea Figure 2a left) have ears on thelateral surfaces of the metathorax (Figure 2a middle) Behindthe thin tympanal membrane is a large air sac which is sep-arated from other air sacs by tracheal membranes Two sen-sory cells A1 and A2 (but a single A cell in notodontids seeSurlykke 1988) are attached to the tympanum The two cellshave identical tuning curves (Figure 2a right) and dynamicranges but they differ by about 20 dB in sensitivity Dynamicrange is the range over which neural responses occur tosound intensity measured in dB from threshold to saturationThe noctuid and arctiid moths have a total auditory dynamicrange of about 40 dB

Freely flying unidentified moths exhibit a variety of be-havioral responses to bats and to synthetic batlike signals(Roeder 1967a for recent results refer to Acharya and Fen-ton 1992) Moths far from the source often turn and fly awaywhereas those close to the source show zigzag and loopingflight power dives or passive falls Presumably the loudersounds recruit the A2 sensory cells which trigger the switchfrom negative phonotaxis to less predictable evasive flight be-havior However Roeder (1964) indicated that the percent-age of moths showing turning-away responses decreases andthe percentage showing looping responses increases as thepulse repetition rate increases Because of this Roeder (1964)suggested that the most sensitive sensory cell (A1) actingalone could release several behaviors but further experi-mentation is needed to confirm this

Size and sensitivity are correlated in moths complicatingmatters further Big moths reflect more intense echoes thansmall moths and may be detected by bats as far away as 10 mHowever results from noctuid moths show that big moths arealso more sensitive and may detect approaching bats as faraway as 100 m Thus there seems to be a fairly constant 10-fold margin of safety that is noctuid moths can detect bats

July 2001 Vol 51 No 7 BioScience 573

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574 BioScience July 2001 Vol 51 No 7

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Figure 2 Insects with audition adapted specifically for hearing bats Representative insects from the various families areshown in the left column with the location of the ear indicated by arrow The general anatomy of each ear is shown in themiddle column The tuning curves for flight cessation (behavior) the A1 sensory cells and an interneuron are shown inthe right column The frequency range for typical bat biosonar signals is shown on the abscissa (d right) (a middle) Ahorizontal section through the metathorax of a noctuid moth (modified after Eggers 1919) (b middle) A cross sectionthrough the first abdominal segment of a geometrid moth viewed from the inside (modified after Kennel and Eggers1933) A single tympanal air sac occupies the space behind the tympana (not seen in this drawing) The pyralid ear (egGalleria mellonella) is anteroabdominal like that of the geometrid (b right) Data for a geometrid Biston betularia(modified from Surlykke and Filskov 1997) as well as for a pyralid Galleria mellonella (c middle) The head of asphingid moth Celerio lineata with one labial palp in longitudinal section The sound receivers (pilifers) are seen on thelateral surface of the proboscis (modified from Roeder et al 1970) (d middle) The ventral surface of the base of the wingof the green lacewing Chrysoperla carnea (modified after Miller 1975) References for tuning curves are given in the text

at about 10 times the distance over which bats can detectmoths (Surlykke et al 1999)

Many interneurons in the thoracic and cephalic ganglia ofnoctuids have been characterized (Roeder 1975 Boyan andFullard 1986) For example two identified neurons receive di-rect input from the A1 afferent in parallelbut they process tem-poral information differently (Boyan and Miller 1991) Synap-tic input to some motor neurons controlling the upndashdownmovement of the wings occurs only when the A2 sensory cellis activated (Madsen and Miller 1987) The role individual in-terneurons play in eliciting behavior is speculative principallybecause the responses of moths are exceedingly difficult tostudy under controlled conditions (Roeder 1967b)

Arctiid moths behave like noctuids but are more reluctantto do so In addition some arctiids produce ultrasonic click-ing sounds from tymbal organs when they hear bat signals orare touched (The clicks have various effects on bats as de-scribed below) Cycnia tenera starts clicking before it stops fly-ing in response to ultrasonic stimuli (Fullard 1979) Thethreshold for flight cessation is about 10ndash20 dB above that forclicking and repetition rates from 17ndash40 pulses per secondare best at eliciting clicking (Fullard 1984b) Also the rate ofmotor spikes to the tymbal muscles increases when the stim-ulus rate increases (Northcott and Fullard 1996) So both am-plitude and pulse repetition rate of the ultrasonic stimulus in-fluence behavioral responses from noctuid and arctiid moths

The Geometridae Pyralidae and Drepanidae have ultra-sound-sensitive ears on the first abdominal segment (Minetand Surlykke 2001) In the geometrids (Figure 2b left) thetympana are adjacent to the midline and point caudally (Fig-ure 2b middle) The tympana in pyralids point rostrally andhave a slight tilt ventrallyFour sensory (A) cells attach to eachtympanum The dynamic range for hearing in the geometridBiston betularia is about 50 dB because each cell covers asmaller range (10ndash15 dB) than the A cells in a noctuid ear Thefrequency range of hearing extends to at least 100 kHz in allspecies studied thus far (Figure 2b right B betularia Surlykkeand Filskov 1997) Some geometrids show flight cessation andother responses to ultrasound (Rydell et al 1997) Pyralid waxmoths respond to bat cries (Spangler and Takessian 1983) andGalleria mellonella shows a number of behavioral responseswhile in stationary flight the most noticeable of which isflight cessation (Skals and Surlykke 2000) Flight cessationwhich is the behavior with the highest threshold occurs at +20to +25 dB with respect to the threshold for the A1 cell (Fig-ure 2b right G mellonella) Actually avoidance behavior tobat echolocation is so powerful that some pyralid (and noc-tuid) moths abort sexually oriented flight to females broad-casting pheromones (Acharya and McNeil 1998)

The bat-detecting ear of some hawk moths (Figure 2cleft) consists of air-filled labial palps that transmit sound en-ergy to the pilifers located on either side of the proboscis(Figure 2c middle) Other hawk moths have scale plates onthe labial palps rather than air-filled palps Neurophysiolog-ical recordings from the labial nerve or from interneurons re-veal the auditory characteristics in both types of hawk moths

(Figure 2c right) They are most sensitive to frequencies be-tween 20 and 30 kHz with a threshold of 40ndash50 dB sound pres-sure level The dynamic range of the single auditory sensoryneuron in the pilifer is about 20 dB resembling that in the earof notodontid moths Hawk moths in tethered flight respondto ultrasound with changes in flight speed with nondirectionalturning and sometimes by emitting sound The behavioralthreshold is about 70 dB SPL or 20 dB above the sensorythreshold (Roeder et al 1970 Goumlpfert and Wasserthal 1999)

Green lacewings The ear of the green lacewing (Figure 2dleft) is located in a bulge near the base of the radial vein in eachforewing (Figure 2d middle) It is a true tympanal organwhich is mostly fluid filled and contains a small trachea It isthe smallest tympanal organ knownPerhaps only 6 of the 25sensory cells actually respond to ultrasound (see Miller 1984for a review) Like wax moths green lacewings in stationaryflight show a number of responses to lower intensity stimulibefore ceasing their flight (Miller 1975) Flight cessation (Fig-ure 2d right) occurs most reliably to ultrasonic signals broad-cast at rates of 1ndash50 pulses per second High stimulus repe-tition rates alone were ineffective in stopping the flight ofrestrained green lacewings

A more realistic picture of behavior emerged from studieson freely flying green lacewings and bats (Figure 3) Bat sig-nals at low repetition rates possibly combined with low in-tensities cause insects to fold their wings and passively diveThe green lacewing shows this nondirectional early-warningresponse to batsrsquo searching signals (Figure 3 between flashes2 and 3) The bat increases its call rate as it approaches a fallinginsect (Figure 3 flashes 3 to 4) Just before capturing its preythe bat increases its repetition rate to a maximum of about200 signals per second in the terminal phase for most bats (Fig-ure 3 flash 5) During the terminal phase the insect suddenlyflipped open its wings (Figure 3 flash 5 arrow) presumablyin response to the high repetition rate signals This last-chance response breaks the dive and foils the bat in this caseafter which the insect continues its dive (Figure 3 flash 6)Artificial bat signals mimicking the sequence shown in Fig-ure 3 evoke the same behavior (Miller and Olesen 1979) Byrepeating the experiments with deafened green lacewingswe showed that the selective advantage of reactors over non-reactors was 47 or about the same as that found for moths(see Miller 1982) Unidentified neurons in the prothoracic gan-glion respond to ultrasound but their role in eliciting behavioris unknown (Miller 1984)

Conclusions about insect behaviorsWe can draw some conclusions and make predictions basedon what we know about avoidance behaviors Looking at allthe behavioral response types for all the insects mentionedabove we find that the best frequency the frequency at whichneural or behavioral responses have the lowest thresholdlies between about 20 and 60 kHz with thresholds betweenabout 30 and 70 dB SPL The response latencies range from40ndash70 ms at +15 dB with respect to the behavioral threshold

July 2001 Vol 51 No 7 BioScience 575

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Because the distance at which the insects respond to 40 kHzsounds varies from 65ndash37 m for bats using intense signalsthe insects have several tenths of a second to avoid even fast-flying bats (Surlykke 1988) The situation is somewhat differentfor whispering bats which use intensities of less than about75 dB SPL and hunt near vegetation Here the response dis-tances for flying insects are from 01ndash27 m depending on thehearing threshold However bats can detect a moth-sizedecho at about 06 m putting the less-sensitive insects in dan-ger Many of the insects mentioned above are open-air fliersand normally do not meet whispering bats

The tuning of neurons suspected to be involved in avoid-ance behavior in preadapted insects such as crickets grasshop-pers and preying mantids poorly match the behavioral tun-ing This discrepancy suggests that these auditory neurons havebeen molded into an antibat circuitry as a result of selectionpressure Behaviors such as turning in midflight or flightcessation have thresholds typically 20 dB higher than thosefor sensory neurons or interneurons (except premotor in-terneurons) in the same insects Consequently yet undis-covered behaviors to low stimulus intensities may provide ad-ditional survival advantage

Insect avoidance behaviors and their underlying mecha-nisms are undoubtedly complicated Take for example the vari-ability of responses The behaviors cannot be reliably predictedand the same individual may show different responses or noresponse at all to the same stimulus Roeder called this theldquoevitabilityrdquoof behavior which provides a survival advantageby making it difficult for the predator to predict what the preywill do The characteristic feature of evitability makes it dif-ficult to study but it seems to be present in the behavior and

physiology of some moths (Roeder 1975 Madsen and Miller1987) and green lacewings (Miller and Olesen 1979)Nevertheless the auditory and behavioral mechanismspresented here found in many families in several orders ofinsects give an overall picture of convergent evolution inresponse to bat predation

Insects living in bat-free environments

Spatial isolation Some moths escape from the risk of pre-dation by insectivorous bats simply by living in places whereno bats occur Bats are found on all continents except Antarc-tica and on the majority of islands but some remote islandsare free of bats for instance the Faroe Islands in the NorthAtlantic and the islands in French Polynesia

In general moth hearing sensitivity tends to reflect thecharacteristic frequencies and intensities of the local batfaunaHowever moths from the Faroes (Surlykke 1986) as wellas those from Tahiti (French Polynesia Fullard 1994) have re-tained auditory sensitivity in complete isolation from bats Iso-lated moths have thresholds at the best frequencies that arecomparable to the thresholds of moths sympatric with batsin similar habitats temperate or tropical Moths from HighArctic areas also show evasive maneuvers to ultrasound (Ry-dell et al 2000) The reason these moths have retained sen-sitive hearing which seems totally superfluous is not knownIt may simply be due to the slow regression of a character ifthere is no selection pressure against it In contrast a characterthat has adaptive value may spread through the populationafter only a few generations as shown by melanism in the pep-pered moth Biston betularia

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Figure 3 The behavioral responses of a green lacewing to a hunting pipistrelle bat The behavior was photographed in alarge flight cage using stroboscopic flashes at 70-ms intervals The biosonar signals that the bat emitted during the variousstages of hunting were simultaneously recorded The signals are schematic and only the intervals are accurately shownModified from Miller and Olesen 1979

Temporal isolation This is another strategy to avoidbats The Cuculliinae (Noctuidae) include moths that areactive in the winter Several species (eg Lithophane grotei andEupsilia vinulenta) were captured in Massachusetts in No-vember over a 3-week period when snow covered the groundand nightly bat censuses revealed none All captured mothshad functional ears tuned to bat sounds with thresholds as lowas their relatives flying in the summer (Surlykke and Treat1995) A study of hearing in winter-active geometrid mothsgave a similar result (Rydell et al 1997) Apparently noctur-nally active winter moths do not use their hearing even forintraspecific communication Isolated moths retain their ul-trasonic hearing which indicates that it is not very costly evo-lutionarily speaking to retain ears if they provide wintermoths with additional protection such as from the possibil-ity of occasionally overlapping with bats

The nocturnal noctuid moth Rileyana fovea (formerlyThecophora fovea) from Central Europe emerges in late Oc-tober to early November after bat activity has decreased Ri-leyana fovea communicates with ultrasound The males singin flight by scraping the file of the hind tarsus against the foveawhich is an inflated bubble on the hindwing supported by theheavily sclerotized radial vein (Figure 4) The intense sounds(80 dB at 1 m) have peak power around 30 kHz which wouldmake the moths very conspicuous to bats The moths are read-ily eaten by captive bats However by being active at a timeof the year with few bats R fovea can use ultrasound for in-traspecific communication Hence it seems that a completeconversion of hearing from a defensive context to a sexual onehas occurred secondarily in R fovea (Surlykke and Gogala1986) Ultrasound-producing organs have developed inde-pendently in distantly related species of moths that are pro-tected from bats in different ways This suggests that the pre-

existing ear prompted the development of intraspecificacoustic communication in certain moths (Conner 1999Skals and Surlykke 1999)

Some moths have changed to diurnal life a secondaryadaptation perhaps in response to predation by bats Oftendiurnal moths are protected by toxins and warning colors likesome butterflies These day fliers include many tiger moths(Arctiidae) especially from the subfamily Ctenuchinae Onlyrelatively few Noctuidae are day fliers One example is the Aus-tralian whistling moth Hecatesia thyridion (Agaristinae)which is brightly patterned and probably toxic Male whistlingmoths produce sounds that are audible but most of the en-ergy is in the ultrasonic range where their hearing is best Theyuse sounds to defend their territories and to attract females(Surlykke and Fullard 1989) Some diurnal moths are silentand apparently their hearing has no function at all For ex-ample diurnal notodontid moths in the subfamily Dioptinaefrom Venezuela show varying degrees of auditory degenera-tion ranging from almost normal sensitivity in some speciesto very reduced sensitivity especially at ultrasonic frequenciesin other species (Fullard et al 1997) Similarly the diurnalgeometrid Archiearis parthenias is practically deaf to ultrasonicfrequencies (Surlykke et al 1998)

Sound as defenseMany arctiids possess tymbal organs located on the sides ofthe metathorax (Figure 5a Conner 1999) Special musclesbuckle the tymbal membrane generating one click or a burstof clicks per activation cycle (Figure 5b) Click amplitudes varyfrom about 50ndash90 dB SPL measured at 5 cm with maxi-mum sound energy falling between 30 and 80 kHz (Figure 5cFullard and Fenton 1977 Surlykke and Miller 1985) Flyingarctiids may click when they hear the biosonar signals ofbats Thresholds for clicking can be as low as 60ndash75 dB SPLfor simulated search-phase signals (Fullard 1979 Surlykke andMiller 1985) but considerably higher for short signals (about2 ms Fullard 1984b)

Some bats and insects share the same hibernacula andmarauding bats feed on hibernating insects Nymphalid but-terflies sense the vibrations in the substratum as the batcrawls toward it The torpid butterfly opens its wings in a char-acteristic manner which produces intense ultrasonic clicksfrom a special area of the wing membrane (Moslashhl and Miller1976) What purpose do the clicks serve There are threelikely functions of clicking sounds They could startle bats theycould interfere with the batsrsquo biosonar system or they couldwarn bats of a distasteful prey as many arctiid moths containtoxins in their body tissues or in special glands

Startle and interference The clicks of nymphalid but-terflies startle bats and thus provide a chance for the insect toescape However a bat quickly habituates to the sounds andeats these butterflies (Moslashhl and Miller 1976) For experi-enced bats clicks can act as a dinner bellArctiid clicks can star-tle inexperienced and naive bats (Eptesicus fuscus) but thesebats also habituate rapidly (Bates and Fenton 1990 Miller

July 2001 Vol 51 No 7 BioScience 577

Articles

Figure 4 Male stridulatory organ used for the productionof intraspecific communication sounds by the noctuidmoth Rileyana fovea (formerly Thecophora fovea)Sound pulses with carrier frequencies of about 30 kHzare produced by scraping the file on the tarsus of the hindleg against the stridulatory swelling (fovea) on thehindwing Modified from Surlykke and Gogala 1986

1991) Thus clicks must be used sparingly to have survivalvalue as startle signals

The ultrasonic clicks of arctiids might disturb bat biosonarin two ways by simulating multiple targets (Fullard et al1979 1994) and by interfering with range determination(Miller 1991) The arctiid Cycnia tenera produces long trainsof clicks at high rates Fullard et al (1979 1994) hypothesizedthat clicks of C tenera could function as acoustical camou-flage by simulating multiple targets (false echoes) near themoth and thus jam a batrsquos (Eptesicus fuscus) biosonar Theybased their conclusion mainly on the ability of the moth totime its clicking to the terminal phase of the batrsquos signals Milleret al (forthcoming) tested this idea using bats (Pipistrellus pip-istrellus) trained to catch catapulted meal worms after whichnatural click sequences from the arctiid Phragmatobia fulig-inosa were played back during the batsrsquo terminal phase Thebats reacted by increasing the harmonic structure of their ter-minal signals but clicks did not influence the success rate of

prey capture The results suggest that the clicks produced byP fuliginosa do not interfere with the batsrsquo sonar system per-haps because the click rate is too low However in psy-chophysical experiments the clicks from P fuliginosa did in-terfere with the ability of bats (Eptesicus fuscus) to determinerange differences (Miller 1991) When clicks triggered bythe batsrsquo own signals fall repeatedly within a critical time win-dow of about 15 ms before an echo the batrsquos discriminationof range differences deteriorated by as much as 40-fold A sin-gle artificial click placed within the critical window inter-feres with range difference determination (Tougaard et alforthcoming) and with neural responses (Tougaard et al1998) In either case a bat would miss its target if clicks rep-resent false echoes from phantom objects or if they interferewith the batrsquos ranging mechanism

Warning sounds toxins and mimicry Several factspoint to the warning function of clicks as suggested by Dun-ning (1968) The Arctiidae (including the Ctenuchinae) aregenerally unpalatable and arctiids are the only noctuoidmoths that click in response to bat sonar sounds Arctiidclicks could warn the bat of a noxious prey Evidence sup-porting a warning function comes from studies in the labo-ratory and the field In experimental studies bats (Pipistrel-lus pipistrellus and Eptesicus fuscus) habituated to arctiid clickswhen given palatable rewards (Surlykke and Miller 1985Bates and Fenton 1990) However the same bats learned veryquickly to associate moth clicks with a distasteful rewardField studies indicated that bats (Lasiurus sp) foraging aroundstreet lights often aborted their attacks in the approach or ter-minal phase when the prey was the noisy arctiid mothHypoprepia fucosa (Acharya and Fenton 1992) Wild H fucosadid not take visible evasive action to attacking bats Batsavoided more than 90 of the moths released and droppedthe few they captured usually undamaged The bats showedno evidence of habituation although H fucosa were abundantcomposing more than 30 of the moth population Hy-poprepia fucosa has classic warning coloration and patterns as-sociated with toxic species Evidence favors the assumptionthat arctiid clicks are acoustical aposematic signals warningbats that the moths taste bad (Dunning and Kruumlger 1996)

Combining acoustic defenses The startle interferenceand warning hypotheses are not mutually exclusive In areaswhere arctiid moths are scarce the clicks may mostly startlebats Because bats quickly adapt to the clicks a warning func-tion is most likely in areas where arctiid moths are abundantWarning seems especially likely for toxic arctiids like Arctia cajawhich produce few but intense clicks in response to batlikesignals (Surlykke and Miller 1985) At least some species of arc-tiids begin clicking to the searching signals of aerial hawkingbats at distances of about 2ndash4 m (Surlykke and Miller 1985)At these distances the bat should be able to hear the clicks giv-ing an experienced predator ample time to avoid the dis-tasteful prey There is sufficient time for the bat to change itsbehavior even if the warning comes during the approach or

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Articles

Figure 5 Arctiid tymbal organ and clicks (a) The tymbalorgan on the lateral surface of the metathoracic segmentof the arctiid Phragmatobia fuliginosa (b) The tymbalorgan produces a burst of clicks each time it buckles (c)The power spectrum of the burst has a maximum atabout 80 kHz (a) Modified from Surlykke and Miller1985 (b) and (c) modified from Miller 1991

terminal phases of the batrsquos pursuit (Acharya and Fenton1992) Should the mothrsquos clicks arrive at the batrsquos ear just be-fore the echoes the batrsquos estimation of range to the preyblurs perhaps causing the bat to miss the target Moths us-ing long trains of click bursts could exploit this strategy Allthree possibilities startle interference and warning offerselective advantages for arctiid moths in addition to thoseprovided by changes in flight behavior

Potential countertactics for batsThe diet of many bats contains very few moths perhaps be-cause of their effective defenses However some barbastelle batsprey almost exclusively on tympanate moths and just how theydo this is not known (Sierro and Arlettaz 1997) Here wepresent some possible double-edged strategies that may ex-plain bat adaptations

Changing signals Echolocating bats announce their pres-ence to all potential prey equipped with auditory bat detec-tors and bats may use different acoustic strategies to reducetheir conspicuousness One strategy would be an adaptationthat moved frequencies of sonar signals out of the rangewhere tympanate insects are most sensitive (Dunning andKruumlger 1996) Some bats use very high frequencies whichmake them less audible to most noctuoid moths Howeversmall moths such as some geometrids (Surlykke and Filskov1997) the pyralid Galleria mellonella (Figure 2b right) andmany tropical noctuoids (Fullard 1988) are quite sensitive tohigh frequencies The attenuation of high frequencies re-duces the useful range of bat sonar so the advantage of thisstrategy may be limited If emission of high frequencies werea countermeasure against tympanate insects one would ex-pect to find bats exploiting this strategy in temperate regionswhere many moths do have poor sensitivity at high frequen-cies (Fullard 1988) The only temperate nongleaning batsthat use relatively high frequencies are small ones (eg Pip-istrellus spp) which detect small prey While the emission ofhigh frequencies may be a response to insect defenses it mayalso be a way to increase resolution and thus increase the abil-ity of bats to detect smaller insects (Surlykke et al 1993)

A second strategy would be for bats to emit very low fre-quencies which would make them less conspicuous to moths(Rydell and Arlettaz 1994) This strategy is employed mostlyby fast-flying bats that hunt aerial insects far from the groundand vegetation (Neuweiler 1989 Fenton 1990) Low fre-quencies increase the batsrsquo range but lower the resolution ofthe batsrsquo biosonar making only large insects detectable (Bar-clay 1986)

A third strategy would be an adaptation for bats to reducethe intensity of their signals Sound intensity is a measure ofsound energy and is proportional to the sound pressure(The dB scale is adapted such that any change in sound pres-sure and the corresponding change in sound intensity resultin the same change in dB value) The advantage would be thatthe sound intensity decreases with the square of the distancebut the echo intensity decreases with the fourth power of the

distance (Surlykke 1988) making the bat less detectable to thetympanate insect We do not know if any bats exploit this strat-egy but we know that all bats studied so far when gleaninguse low-intensity sounds if they emit any signals at all(Neuweiler 1989 Miller and Treat 1993 Faure and Barclay1994) For a gleaning bat the reduction of detection range isprobably not an important restriction because reducingsound intensity gives the additional advantage of reducing clut-ter echoes from the background (see Schnitzler and Kalko2001) In contrast field studies using techniques to calculatethe distance and direction to the bat indicate that at least somebats hunting aerial insects in the open emit intense signals withsource levels up to 125 dB SPL the highest levels yet measured(Jensen and Miller 1999) Also bats that display both glean-ing and aerial-hawking modes of foraging such as for in-stance Myotis evotis (Faure and Barclay 1994) and M septen-trionalis (Miller and Treat 1993) emit high intensities whenhunting flying insects

Finally shorter echolocation signals should be less con-spicuous to prey However shorter signals mean shorterechoes with less energy which are less conspicuous to the batstoo Also short search signals are recorded mainly from batsusing frequency-modulated calls and hunting close to clut-ter (Neuweiler 1989 Fenton 1990) Hencewe believe that shortcalls probably are not a countermeasure against insect hear-ing but rather an adaptation for reducing the overlap betweenechoes from clutter and those from prey

Listening to prey sounds The most effective way for abat to sneak close to tympanate prey is to cease echolocatingaltogether and detect prey using passive sensory cues If theinsects produce sound bats may find them using passivehearing Gleaning bats such as Plecotus auritus and Myotis evo-tis usually have large pinnae (Faure and Barclay 1994) Theyreact with very fast positive phonotaxis to insect-producedsounds such as the sound of wings fluttering or of an insectcrawling on a surface Some gleaning bats emit the full reper-toire of biosonar signals including the terminal phase(Schumm et al 1991) However gleaners generally stop call-ing before the attack and produce no terminal phase(Neuweiler 1989 Faure and Barclay 1994) Whether omissionof the terminal phase reduces the insectrsquos chance of escapingis difficult to say because tympanate insects probably detectecholocating bats long before the terminal phase (Roeder1967a Surlykke et al1999) However omitting the terminalphase may prevent last-chance escape maneuvers (Miller1984) On the other hand sedentary moths stay motionlessor freeze when hearing echolocation signals Turning off thesonar in the final phase may not be a countermeasure againsttympanate insects it may simply be that the bat does not needto continuously update the estimated position of a motion-less insect In contrast the prey of aerial hunters change po-sition continuously in three dimensions thus forcing the batto use its biosonar nearly to the moment of capture

It is difficult to determine if the acoustical adaptations ofbats are responses to constraints of the environment or to the

July 2001 Vol 51 No 7 BioScience 579

Articles

batsrsquo hunting strategies or are intended to overcome insect de-fenses In any case some bat echolocation signals are lessconspicuous to tympanate prey

Concluding remarksThe evolutionary arms race continues between bats and theirinsect prey and undiscovered strategies await to be revealedSome suspected strategies such as acoustical mimicry needto be documented by laboratory and field studies Experi-mental studies in the field can elucidate some questions aboutbat and insect interactions For example wild gleaning batshunting at familiar sites (Miller and Treat 1993 Faure and Bar-clay 1994) offer unique opportunities to test some hypothe-ses about echolocation behavior and the functions of clicksas interfering or warning signals Employing modern digitalsystems that can reproduce clicks and simulate insect echoeswill assist in such studies

Some questions will be difficult to answer An individualbat can modify at least some of its strategies through learn-ing whereas insect counterstrategies appear through theslower process of natural selection Does this mean insectstrategies lag behind those of their predators Perhaps not Thevariability of an individual insectrsquos antibat behaviors might bea response to the predatorrsquos ability to learn Perhaps theldquoevitabilityrdquo of the preyrsquos behavior (Roeder 1975) makeslearning by the predator less effective

AcknowledgmentsWe thank Raymond CoxOle Naeligsbye Larsen and our students(Vibeke Futtrup Marianne E Jensen Niels Skals) for com-ments on the manuscript We also appreciate the commentsof five anonymous reviewers Our research has been sup-ported by grants from the Danish Natural Sciences ResearchCouncil the Danish National Research Foundation and theCarlsberg Foundation

References citedAcharya L Fenton MB 1992 Echolocation behaviour of vespertilionid bats

(Lasiurus cinereus and Lasiurus borealis) attacking airborne targets in-cluding arctiid moths Canadian Journal of Zoology 70 1292ndash1298

Acharya L McNeil J 1998 Predation risk and mating behavior The re-sponses of moths to batlike ultrasound Behavioral Ecology 9 552ndash558

Ball EE Field LH 1981 Structure of the auditory system of the wetaHemideina crassidens (Blanchard1851) (Orthoptera Ensifera Gryl-lacridoidea Stenopelmantidae) 1 Morphology and histology Cell Tis-sue Res 217 321ndash343

Barclay RMR 1986 The echolocation calls of hoary (Lasiurus cinereus) andsilver-haired (Lasionycteris noctivagans) bats as adaptations for long-versus short-range foraging strategies and the consequences for prey se-lection Canadian Journal of Zoology 64 2700ndash2705

Bates DL Fenton MB 1990 Aposematism or startle Predators learn their re-sponses to the defenses of prey Canadian Journal of Zoology 68 49ndash52

Boyan GS Fullard JH 1986 Interneurones responding to sound in the to-bacco budworm moth Heliothis virescens (Noctuidae) Morphological andphysiological characteristics Journal of Comparative Physiology A Sen-sory Neural and Behavioral Physiology 158 391ndash404

Boyan GS Miller LA 1991 Parallel processing of afferent input by identi-fied interneurones in the auditory pathway of the noctuid moth Noctuapronuba (L) Journal of Comparative PhysiologyA Sensory Neural andBehavioral Physiology 168 727ndash738

Conner WE 1999ldquoUn chant drsquoappel amoureusrdquo Acoustic communicationin moths Journal of Experimental Biology 202 1711ndash1723

Cumming GS 1996 Mantis movements by night and the interactions of sym-patric bats and mantises Canadian Journal of Zoology 74 1771ndash1774

Dunning DC 1968 Warning sounds of moths ZTierpsychol 25 129ndash138Dunning DC Kruumlger M 1996 Predation upon moths by free-foraging Hip-

posideros caffer Journal of Mammalogy 77 708ndash715Eggers F 1919 Das thoracale bitympanale Organ einer Gruppe der Lepi-

doptera Heterocera Zool Jb (Anat) 41 273ndash376Faure PA Barclay RMR 1994 Substrate-gleaning versus aerial-hawking

Plasticity in the foraging and echolocation behaviour of the long-earedbat Myotis evotis Journal of Comparative PhysiologyA Sensory Neuraland Behavioral Physiology 174 651ndash660

Faure PA Hoy RR 2000 Neuroethology of the katydid T-cell II Responsesto acoustic playback of conspecific and predatory signals Journal ofExperimental Biology 203 3243ndash3254

Fenton MB1990 The foraging behaviour and ecology of animal-eating batsCanadian Journal of Zoology 68 411ndash422

Fenton MB Fullard JH 1981 Moth hearing and the feeding strategies of batsAmerican Scientist 69 266ndash275

Forrest TG Read MP Farris HE Hoy RR 1997 A tympanal hearing organin scarab beetles Journal of Experimental Biology 200 601ndash606

Fullard JH 1979 Behavioral analyses of auditory sensitivity in Cycnia ten-era Huumlbner (Lepidoptera Arctiidae) Journal of Comparative Physiol-ogy A Sensory Neural and Behavioral Physiology 129 79ndash83

mdashmdashmdash 1984a Acoustic relationships between tympanate moths and theHawaiian hoary bat (Lasiurus cinereus semotus) Journal of ComparativePhysiology ASensory Neuraland Behavioral Physiology 155 795ndash801

mdashmdashmdash 1984b Listening for bats Pulse repetition rate as a cue for a defen-sive behavior in Cycnia tenera (LepidopteraArctiidae)Journal of Com-parative Physiology A Sensory Neural and Behavioral Physiology 154249ndash252

mdashmdashmdash 1988 The tuning of moth ears Experientia 44 423ndash428mdashmdashmdash 1994Auditory changes in noctuid moths endemic to a bat-free niche

Journal of Evolutionary Biology 7 435ndash445Fullard JH Fenton MB 1977 Acoustic behavioural analyses of the sounds

produced by some species of Nearctic Arctiidae (Lepidoptera)CanadianJournal of Zoology 55 1213ndash1224

Fullard JH Fenton MB Simmons JA 1979 Jamming bat echolocation Theclicks of arctiid moths Canadian Journal of Zoology 57 647ndash649

Fullard JH Simmons JA Saillant PA 1994 Jamming bat echolocation Thedogbane tiger moth Cycnia tenera times its clicks to the terminal attackcalls of the big brown bat Eptesicus fuscus Journal of Experimental Bi-ology 194 285ndash298

Fullard JH Dawson JW Otero LD Surlykke A1997 Bat-deafness in day-fly-ing moths (Lepidoptera Notodontidae Dioptinae) Journal of Com-parative Physiology A Sensory Neural and Behavioral Physiology 181277ndash483

Goumlpfert MC Wasserthal LT 1999 Auditory sensory cells in hawkmoths Iden-tification physiology and structure Journal of Experimental Biology 2021579ndash1587

Hoy RR 1992 The evolution of hearing in insects as an adaptation to pre-dation from batsPages 115ndash129 in Webster DB Fay RR Popper AN edsThe Evolutionary Biology of Hearing New York Springer-Verlag

Hoy RR Nolen T Brodfuehrer P 1989 The neuroethology of acoustic star-tle and escape in flying insects Journal of Experimental Biology 146287ndash306

Jensen ME Miller LA 1999 Echolocation signals of the bat Eptesicus serot-inus recorded using a vertical microphone array Effect of flight altitudeon searching signals Behavioral Ecology and Sociobiology 47 60ndash69

Kennel JV Eggers F 1933 Die abdominalen Tympanalorgane der Lepi-dopteren Zool Jb (Anat) 57 1ndash104

Lakes-Harlan R Heller K-G 1992 Ultrasound-sensitive ears in a parasitoidfly Naturwissenschaften 79 224ndash226

Larsen ON Kleindienst H-UMichelsen A1989 Biophysical aspects of soundreception Pages 364ndash390 in Huber F Moore TELoher W eds Cricket Be-havior and Neurobiology Ithaca (NY) Cornell University Press

580 BioScience July 2001 Vol 51 No 7

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574 BioScience July 2001 Vol 51 No 7

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Figure 2 Insects with audition adapted specifically for hearing bats Representative insects from the various families areshown in the left column with the location of the ear indicated by arrow The general anatomy of each ear is shown in themiddle column The tuning curves for flight cessation (behavior) the A1 sensory cells and an interneuron are shown inthe right column The frequency range for typical bat biosonar signals is shown on the abscissa (d right) (a middle) Ahorizontal section through the metathorax of a noctuid moth (modified after Eggers 1919) (b middle) A cross sectionthrough the first abdominal segment of a geometrid moth viewed from the inside (modified after Kennel and Eggers1933) A single tympanal air sac occupies the space behind the tympana (not seen in this drawing) The pyralid ear (egGalleria mellonella) is anteroabdominal like that of the geometrid (b right) Data for a geometrid Biston betularia(modified from Surlykke and Filskov 1997) as well as for a pyralid Galleria mellonella (c middle) The head of asphingid moth Celerio lineata with one labial palp in longitudinal section The sound receivers (pilifers) are seen on thelateral surface of the proboscis (modified from Roeder et al 1970) (d middle) The ventral surface of the base of the wingof the green lacewing Chrysoperla carnea (modified after Miller 1975) References for tuning curves are given in the text

at about 10 times the distance over which bats can detectmoths (Surlykke et al 1999)

Many interneurons in the thoracic and cephalic ganglia ofnoctuids have been characterized (Roeder 1975 Boyan andFullard 1986) For example two identified neurons receive di-rect input from the A1 afferent in parallelbut they process tem-poral information differently (Boyan and Miller 1991) Synap-tic input to some motor neurons controlling the upndashdownmovement of the wings occurs only when the A2 sensory cellis activated (Madsen and Miller 1987) The role individual in-terneurons play in eliciting behavior is speculative principallybecause the responses of moths are exceedingly difficult tostudy under controlled conditions (Roeder 1967b)

Arctiid moths behave like noctuids but are more reluctantto do so In addition some arctiids produce ultrasonic click-ing sounds from tymbal organs when they hear bat signals orare touched (The clicks have various effects on bats as de-scribed below) Cycnia tenera starts clicking before it stops fly-ing in response to ultrasonic stimuli (Fullard 1979) Thethreshold for flight cessation is about 10ndash20 dB above that forclicking and repetition rates from 17ndash40 pulses per secondare best at eliciting clicking (Fullard 1984b) Also the rate ofmotor spikes to the tymbal muscles increases when the stim-ulus rate increases (Northcott and Fullard 1996) So both am-plitude and pulse repetition rate of the ultrasonic stimulus in-fluence behavioral responses from noctuid and arctiid moths

The Geometridae Pyralidae and Drepanidae have ultra-sound-sensitive ears on the first abdominal segment (Minetand Surlykke 2001) In the geometrids (Figure 2b left) thetympana are adjacent to the midline and point caudally (Fig-ure 2b middle) The tympana in pyralids point rostrally andhave a slight tilt ventrallyFour sensory (A) cells attach to eachtympanum The dynamic range for hearing in the geometridBiston betularia is about 50 dB because each cell covers asmaller range (10ndash15 dB) than the A cells in a noctuid ear Thefrequency range of hearing extends to at least 100 kHz in allspecies studied thus far (Figure 2b right B betularia Surlykkeand Filskov 1997) Some geometrids show flight cessation andother responses to ultrasound (Rydell et al 1997) Pyralid waxmoths respond to bat cries (Spangler and Takessian 1983) andGalleria mellonella shows a number of behavioral responseswhile in stationary flight the most noticeable of which isflight cessation (Skals and Surlykke 2000) Flight cessationwhich is the behavior with the highest threshold occurs at +20to +25 dB with respect to the threshold for the A1 cell (Fig-ure 2b right G mellonella) Actually avoidance behavior tobat echolocation is so powerful that some pyralid (and noc-tuid) moths abort sexually oriented flight to females broad-casting pheromones (Acharya and McNeil 1998)

The bat-detecting ear of some hawk moths (Figure 2cleft) consists of air-filled labial palps that transmit sound en-ergy to the pilifers located on either side of the proboscis(Figure 2c middle) Other hawk moths have scale plates onthe labial palps rather than air-filled palps Neurophysiolog-ical recordings from the labial nerve or from interneurons re-veal the auditory characteristics in both types of hawk moths

(Figure 2c right) They are most sensitive to frequencies be-tween 20 and 30 kHz with a threshold of 40ndash50 dB sound pres-sure level The dynamic range of the single auditory sensoryneuron in the pilifer is about 20 dB resembling that in the earof notodontid moths Hawk moths in tethered flight respondto ultrasound with changes in flight speed with nondirectionalturning and sometimes by emitting sound The behavioralthreshold is about 70 dB SPL or 20 dB above the sensorythreshold (Roeder et al 1970 Goumlpfert and Wasserthal 1999)

Green lacewings The ear of the green lacewing (Figure 2dleft) is located in a bulge near the base of the radial vein in eachforewing (Figure 2d middle) It is a true tympanal organwhich is mostly fluid filled and contains a small trachea It isthe smallest tympanal organ knownPerhaps only 6 of the 25sensory cells actually respond to ultrasound (see Miller 1984for a review) Like wax moths green lacewings in stationaryflight show a number of responses to lower intensity stimulibefore ceasing their flight (Miller 1975) Flight cessation (Fig-ure 2d right) occurs most reliably to ultrasonic signals broad-cast at rates of 1ndash50 pulses per second High stimulus repe-tition rates alone were ineffective in stopping the flight ofrestrained green lacewings

A more realistic picture of behavior emerged from studieson freely flying green lacewings and bats (Figure 3) Bat sig-nals at low repetition rates possibly combined with low in-tensities cause insects to fold their wings and passively diveThe green lacewing shows this nondirectional early-warningresponse to batsrsquo searching signals (Figure 3 between flashes2 and 3) The bat increases its call rate as it approaches a fallinginsect (Figure 3 flashes 3 to 4) Just before capturing its preythe bat increases its repetition rate to a maximum of about200 signals per second in the terminal phase for most bats (Fig-ure 3 flash 5) During the terminal phase the insect suddenlyflipped open its wings (Figure 3 flash 5 arrow) presumablyin response to the high repetition rate signals This last-chance response breaks the dive and foils the bat in this caseafter which the insect continues its dive (Figure 3 flash 6)Artificial bat signals mimicking the sequence shown in Fig-ure 3 evoke the same behavior (Miller and Olesen 1979) Byrepeating the experiments with deafened green lacewingswe showed that the selective advantage of reactors over non-reactors was 47 or about the same as that found for moths(see Miller 1982) Unidentified neurons in the prothoracic gan-glion respond to ultrasound but their role in eliciting behavioris unknown (Miller 1984)

Conclusions about insect behaviorsWe can draw some conclusions and make predictions basedon what we know about avoidance behaviors Looking at allthe behavioral response types for all the insects mentionedabove we find that the best frequency the frequency at whichneural or behavioral responses have the lowest thresholdlies between about 20 and 60 kHz with thresholds betweenabout 30 and 70 dB SPL The response latencies range from40ndash70 ms at +15 dB with respect to the behavioral threshold

July 2001 Vol 51 No 7 BioScience 575

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Because the distance at which the insects respond to 40 kHzsounds varies from 65ndash37 m for bats using intense signalsthe insects have several tenths of a second to avoid even fast-flying bats (Surlykke 1988) The situation is somewhat differentfor whispering bats which use intensities of less than about75 dB SPL and hunt near vegetation Here the response dis-tances for flying insects are from 01ndash27 m depending on thehearing threshold However bats can detect a moth-sizedecho at about 06 m putting the less-sensitive insects in dan-ger Many of the insects mentioned above are open-air fliersand normally do not meet whispering bats

The tuning of neurons suspected to be involved in avoid-ance behavior in preadapted insects such as crickets grasshop-pers and preying mantids poorly match the behavioral tun-ing This discrepancy suggests that these auditory neurons havebeen molded into an antibat circuitry as a result of selectionpressure Behaviors such as turning in midflight or flightcessation have thresholds typically 20 dB higher than thosefor sensory neurons or interneurons (except premotor in-terneurons) in the same insects Consequently yet undis-covered behaviors to low stimulus intensities may provide ad-ditional survival advantage

Insect avoidance behaviors and their underlying mecha-nisms are undoubtedly complicated Take for example the vari-ability of responses The behaviors cannot be reliably predictedand the same individual may show different responses or noresponse at all to the same stimulus Roeder called this theldquoevitabilityrdquoof behavior which provides a survival advantageby making it difficult for the predator to predict what the preywill do The characteristic feature of evitability makes it dif-ficult to study but it seems to be present in the behavior and

physiology of some moths (Roeder 1975 Madsen and Miller1987) and green lacewings (Miller and Olesen 1979)Nevertheless the auditory and behavioral mechanismspresented here found in many families in several orders ofinsects give an overall picture of convergent evolution inresponse to bat predation

Insects living in bat-free environments

Spatial isolation Some moths escape from the risk of pre-dation by insectivorous bats simply by living in places whereno bats occur Bats are found on all continents except Antarc-tica and on the majority of islands but some remote islandsare free of bats for instance the Faroe Islands in the NorthAtlantic and the islands in French Polynesia

In general moth hearing sensitivity tends to reflect thecharacteristic frequencies and intensities of the local batfaunaHowever moths from the Faroes (Surlykke 1986) as wellas those from Tahiti (French Polynesia Fullard 1994) have re-tained auditory sensitivity in complete isolation from bats Iso-lated moths have thresholds at the best frequencies that arecomparable to the thresholds of moths sympatric with batsin similar habitats temperate or tropical Moths from HighArctic areas also show evasive maneuvers to ultrasound (Ry-dell et al 2000) The reason these moths have retained sen-sitive hearing which seems totally superfluous is not knownIt may simply be due to the slow regression of a character ifthere is no selection pressure against it In contrast a characterthat has adaptive value may spread through the populationafter only a few generations as shown by melanism in the pep-pered moth Biston betularia

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Figure 3 The behavioral responses of a green lacewing to a hunting pipistrelle bat The behavior was photographed in alarge flight cage using stroboscopic flashes at 70-ms intervals The biosonar signals that the bat emitted during the variousstages of hunting were simultaneously recorded The signals are schematic and only the intervals are accurately shownModified from Miller and Olesen 1979

Temporal isolation This is another strategy to avoidbats The Cuculliinae (Noctuidae) include moths that areactive in the winter Several species (eg Lithophane grotei andEupsilia vinulenta) were captured in Massachusetts in No-vember over a 3-week period when snow covered the groundand nightly bat censuses revealed none All captured mothshad functional ears tuned to bat sounds with thresholds as lowas their relatives flying in the summer (Surlykke and Treat1995) A study of hearing in winter-active geometrid mothsgave a similar result (Rydell et al 1997) Apparently noctur-nally active winter moths do not use their hearing even forintraspecific communication Isolated moths retain their ul-trasonic hearing which indicates that it is not very costly evo-lutionarily speaking to retain ears if they provide wintermoths with additional protection such as from the possibil-ity of occasionally overlapping with bats

The nocturnal noctuid moth Rileyana fovea (formerlyThecophora fovea) from Central Europe emerges in late Oc-tober to early November after bat activity has decreased Ri-leyana fovea communicates with ultrasound The males singin flight by scraping the file of the hind tarsus against the foveawhich is an inflated bubble on the hindwing supported by theheavily sclerotized radial vein (Figure 4) The intense sounds(80 dB at 1 m) have peak power around 30 kHz which wouldmake the moths very conspicuous to bats The moths are read-ily eaten by captive bats However by being active at a timeof the year with few bats R fovea can use ultrasound for in-traspecific communication Hence it seems that a completeconversion of hearing from a defensive context to a sexual onehas occurred secondarily in R fovea (Surlykke and Gogala1986) Ultrasound-producing organs have developed inde-pendently in distantly related species of moths that are pro-tected from bats in different ways This suggests that the pre-

existing ear prompted the development of intraspecificacoustic communication in certain moths (Conner 1999Skals and Surlykke 1999)

Some moths have changed to diurnal life a secondaryadaptation perhaps in response to predation by bats Oftendiurnal moths are protected by toxins and warning colors likesome butterflies These day fliers include many tiger moths(Arctiidae) especially from the subfamily Ctenuchinae Onlyrelatively few Noctuidae are day fliers One example is the Aus-tralian whistling moth Hecatesia thyridion (Agaristinae)which is brightly patterned and probably toxic Male whistlingmoths produce sounds that are audible but most of the en-ergy is in the ultrasonic range where their hearing is best Theyuse sounds to defend their territories and to attract females(Surlykke and Fullard 1989) Some diurnal moths are silentand apparently their hearing has no function at all For ex-ample diurnal notodontid moths in the subfamily Dioptinaefrom Venezuela show varying degrees of auditory degenera-tion ranging from almost normal sensitivity in some speciesto very reduced sensitivity especially at ultrasonic frequenciesin other species (Fullard et al 1997) Similarly the diurnalgeometrid Archiearis parthenias is practically deaf to ultrasonicfrequencies (Surlykke et al 1998)

Sound as defenseMany arctiids possess tymbal organs located on the sides ofthe metathorax (Figure 5a Conner 1999) Special musclesbuckle the tymbal membrane generating one click or a burstof clicks per activation cycle (Figure 5b) Click amplitudes varyfrom about 50ndash90 dB SPL measured at 5 cm with maxi-mum sound energy falling between 30 and 80 kHz (Figure 5cFullard and Fenton 1977 Surlykke and Miller 1985) Flyingarctiids may click when they hear the biosonar signals ofbats Thresholds for clicking can be as low as 60ndash75 dB SPLfor simulated search-phase signals (Fullard 1979 Surlykke andMiller 1985) but considerably higher for short signals (about2 ms Fullard 1984b)

Some bats and insects share the same hibernacula andmarauding bats feed on hibernating insects Nymphalid but-terflies sense the vibrations in the substratum as the batcrawls toward it The torpid butterfly opens its wings in a char-acteristic manner which produces intense ultrasonic clicksfrom a special area of the wing membrane (Moslashhl and Miller1976) What purpose do the clicks serve There are threelikely functions of clicking sounds They could startle bats theycould interfere with the batsrsquo biosonar system or they couldwarn bats of a distasteful prey as many arctiid moths containtoxins in their body tissues or in special glands

Startle and interference The clicks of nymphalid but-terflies startle bats and thus provide a chance for the insect toescape However a bat quickly habituates to the sounds andeats these butterflies (Moslashhl and Miller 1976) For experi-enced bats clicks can act as a dinner bellArctiid clicks can star-tle inexperienced and naive bats (Eptesicus fuscus) but thesebats also habituate rapidly (Bates and Fenton 1990 Miller

July 2001 Vol 51 No 7 BioScience 577

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Figure 4 Male stridulatory organ used for the productionof intraspecific communication sounds by the noctuidmoth Rileyana fovea (formerly Thecophora fovea)Sound pulses with carrier frequencies of about 30 kHzare produced by scraping the file on the tarsus of the hindleg against the stridulatory swelling (fovea) on thehindwing Modified from Surlykke and Gogala 1986

1991) Thus clicks must be used sparingly to have survivalvalue as startle signals

The ultrasonic clicks of arctiids might disturb bat biosonarin two ways by simulating multiple targets (Fullard et al1979 1994) and by interfering with range determination(Miller 1991) The arctiid Cycnia tenera produces long trainsof clicks at high rates Fullard et al (1979 1994) hypothesizedthat clicks of C tenera could function as acoustical camou-flage by simulating multiple targets (false echoes) near themoth and thus jam a batrsquos (Eptesicus fuscus) biosonar Theybased their conclusion mainly on the ability of the moth totime its clicking to the terminal phase of the batrsquos signals Milleret al (forthcoming) tested this idea using bats (Pipistrellus pip-istrellus) trained to catch catapulted meal worms after whichnatural click sequences from the arctiid Phragmatobia fulig-inosa were played back during the batsrsquo terminal phase Thebats reacted by increasing the harmonic structure of their ter-minal signals but clicks did not influence the success rate of

prey capture The results suggest that the clicks produced byP fuliginosa do not interfere with the batsrsquo sonar system per-haps because the click rate is too low However in psy-chophysical experiments the clicks from P fuliginosa did in-terfere with the ability of bats (Eptesicus fuscus) to determinerange differences (Miller 1991) When clicks triggered bythe batsrsquo own signals fall repeatedly within a critical time win-dow of about 15 ms before an echo the batrsquos discriminationof range differences deteriorated by as much as 40-fold A sin-gle artificial click placed within the critical window inter-feres with range difference determination (Tougaard et alforthcoming) and with neural responses (Tougaard et al1998) In either case a bat would miss its target if clicks rep-resent false echoes from phantom objects or if they interferewith the batrsquos ranging mechanism

Warning sounds toxins and mimicry Several factspoint to the warning function of clicks as suggested by Dun-ning (1968) The Arctiidae (including the Ctenuchinae) aregenerally unpalatable and arctiids are the only noctuoidmoths that click in response to bat sonar sounds Arctiidclicks could warn the bat of a noxious prey Evidence sup-porting a warning function comes from studies in the labo-ratory and the field In experimental studies bats (Pipistrel-lus pipistrellus and Eptesicus fuscus) habituated to arctiid clickswhen given palatable rewards (Surlykke and Miller 1985Bates and Fenton 1990) However the same bats learned veryquickly to associate moth clicks with a distasteful rewardField studies indicated that bats (Lasiurus sp) foraging aroundstreet lights often aborted their attacks in the approach or ter-minal phase when the prey was the noisy arctiid mothHypoprepia fucosa (Acharya and Fenton 1992) Wild H fucosadid not take visible evasive action to attacking bats Batsavoided more than 90 of the moths released and droppedthe few they captured usually undamaged The bats showedno evidence of habituation although H fucosa were abundantcomposing more than 30 of the moth population Hy-poprepia fucosa has classic warning coloration and patterns as-sociated with toxic species Evidence favors the assumptionthat arctiid clicks are acoustical aposematic signals warningbats that the moths taste bad (Dunning and Kruumlger 1996)

Combining acoustic defenses The startle interferenceand warning hypotheses are not mutually exclusive In areaswhere arctiid moths are scarce the clicks may mostly startlebats Because bats quickly adapt to the clicks a warning func-tion is most likely in areas where arctiid moths are abundantWarning seems especially likely for toxic arctiids like Arctia cajawhich produce few but intense clicks in response to batlikesignals (Surlykke and Miller 1985) At least some species of arc-tiids begin clicking to the searching signals of aerial hawkingbats at distances of about 2ndash4 m (Surlykke and Miller 1985)At these distances the bat should be able to hear the clicks giv-ing an experienced predator ample time to avoid the dis-tasteful prey There is sufficient time for the bat to change itsbehavior even if the warning comes during the approach or

578 BioScience July 2001 Vol 51 No 7

Articles

Figure 5 Arctiid tymbal organ and clicks (a) The tymbalorgan on the lateral surface of the metathoracic segmentof the arctiid Phragmatobia fuliginosa (b) The tymbalorgan produces a burst of clicks each time it buckles (c)The power spectrum of the burst has a maximum atabout 80 kHz (a) Modified from Surlykke and Miller1985 (b) and (c) modified from Miller 1991

terminal phases of the batrsquos pursuit (Acharya and Fenton1992) Should the mothrsquos clicks arrive at the batrsquos ear just be-fore the echoes the batrsquos estimation of range to the preyblurs perhaps causing the bat to miss the target Moths us-ing long trains of click bursts could exploit this strategy Allthree possibilities startle interference and warning offerselective advantages for arctiid moths in addition to thoseprovided by changes in flight behavior

Potential countertactics for batsThe diet of many bats contains very few moths perhaps be-cause of their effective defenses However some barbastelle batsprey almost exclusively on tympanate moths and just how theydo this is not known (Sierro and Arlettaz 1997) Here wepresent some possible double-edged strategies that may ex-plain bat adaptations

Changing signals Echolocating bats announce their pres-ence to all potential prey equipped with auditory bat detec-tors and bats may use different acoustic strategies to reducetheir conspicuousness One strategy would be an adaptationthat moved frequencies of sonar signals out of the rangewhere tympanate insects are most sensitive (Dunning andKruumlger 1996) Some bats use very high frequencies whichmake them less audible to most noctuoid moths Howeversmall moths such as some geometrids (Surlykke and Filskov1997) the pyralid Galleria mellonella (Figure 2b right) andmany tropical noctuoids (Fullard 1988) are quite sensitive tohigh frequencies The attenuation of high frequencies re-duces the useful range of bat sonar so the advantage of thisstrategy may be limited If emission of high frequencies werea countermeasure against tympanate insects one would ex-pect to find bats exploiting this strategy in temperate regionswhere many moths do have poor sensitivity at high frequen-cies (Fullard 1988) The only temperate nongleaning batsthat use relatively high frequencies are small ones (eg Pip-istrellus spp) which detect small prey While the emission ofhigh frequencies may be a response to insect defenses it mayalso be a way to increase resolution and thus increase the abil-ity of bats to detect smaller insects (Surlykke et al 1993)

A second strategy would be for bats to emit very low fre-quencies which would make them less conspicuous to moths(Rydell and Arlettaz 1994) This strategy is employed mostlyby fast-flying bats that hunt aerial insects far from the groundand vegetation (Neuweiler 1989 Fenton 1990) Low fre-quencies increase the batsrsquo range but lower the resolution ofthe batsrsquo biosonar making only large insects detectable (Bar-clay 1986)

A third strategy would be an adaptation for bats to reducethe intensity of their signals Sound intensity is a measure ofsound energy and is proportional to the sound pressure(The dB scale is adapted such that any change in sound pres-sure and the corresponding change in sound intensity resultin the same change in dB value) The advantage would be thatthe sound intensity decreases with the square of the distancebut the echo intensity decreases with the fourth power of the

distance (Surlykke 1988) making the bat less detectable to thetympanate insect We do not know if any bats exploit this strat-egy but we know that all bats studied so far when gleaninguse low-intensity sounds if they emit any signals at all(Neuweiler 1989 Miller and Treat 1993 Faure and Barclay1994) For a gleaning bat the reduction of detection range isprobably not an important restriction because reducingsound intensity gives the additional advantage of reducing clut-ter echoes from the background (see Schnitzler and Kalko2001) In contrast field studies using techniques to calculatethe distance and direction to the bat indicate that at least somebats hunting aerial insects in the open emit intense signals withsource levels up to 125 dB SPL the highest levels yet measured(Jensen and Miller 1999) Also bats that display both glean-ing and aerial-hawking modes of foraging such as for in-stance Myotis evotis (Faure and Barclay 1994) and M septen-trionalis (Miller and Treat 1993) emit high intensities whenhunting flying insects

Finally shorter echolocation signals should be less con-spicuous to prey However shorter signals mean shorterechoes with less energy which are less conspicuous to the batstoo Also short search signals are recorded mainly from batsusing frequency-modulated calls and hunting close to clut-ter (Neuweiler 1989 Fenton 1990) Hencewe believe that shortcalls probably are not a countermeasure against insect hear-ing but rather an adaptation for reducing the overlap betweenechoes from clutter and those from prey

Listening to prey sounds The most effective way for abat to sneak close to tympanate prey is to cease echolocatingaltogether and detect prey using passive sensory cues If theinsects produce sound bats may find them using passivehearing Gleaning bats such as Plecotus auritus and Myotis evo-tis usually have large pinnae (Faure and Barclay 1994) Theyreact with very fast positive phonotaxis to insect-producedsounds such as the sound of wings fluttering or of an insectcrawling on a surface Some gleaning bats emit the full reper-toire of biosonar signals including the terminal phase(Schumm et al 1991) However gleaners generally stop call-ing before the attack and produce no terminal phase(Neuweiler 1989 Faure and Barclay 1994) Whether omissionof the terminal phase reduces the insectrsquos chance of escapingis difficult to say because tympanate insects probably detectecholocating bats long before the terminal phase (Roeder1967a Surlykke et al1999) However omitting the terminalphase may prevent last-chance escape maneuvers (Miller1984) On the other hand sedentary moths stay motionlessor freeze when hearing echolocation signals Turning off thesonar in the final phase may not be a countermeasure againsttympanate insects it may simply be that the bat does not needto continuously update the estimated position of a motion-less insect In contrast the prey of aerial hunters change po-sition continuously in three dimensions thus forcing the batto use its biosonar nearly to the moment of capture

It is difficult to determine if the acoustical adaptations ofbats are responses to constraints of the environment or to the

July 2001 Vol 51 No 7 BioScience 579

Articles

batsrsquo hunting strategies or are intended to overcome insect de-fenses In any case some bat echolocation signals are lessconspicuous to tympanate prey

Concluding remarksThe evolutionary arms race continues between bats and theirinsect prey and undiscovered strategies await to be revealedSome suspected strategies such as acoustical mimicry needto be documented by laboratory and field studies Experi-mental studies in the field can elucidate some questions aboutbat and insect interactions For example wild gleaning batshunting at familiar sites (Miller and Treat 1993 Faure and Bar-clay 1994) offer unique opportunities to test some hypothe-ses about echolocation behavior and the functions of clicksas interfering or warning signals Employing modern digitalsystems that can reproduce clicks and simulate insect echoeswill assist in such studies

Some questions will be difficult to answer An individualbat can modify at least some of its strategies through learn-ing whereas insect counterstrategies appear through theslower process of natural selection Does this mean insectstrategies lag behind those of their predators Perhaps not Thevariability of an individual insectrsquos antibat behaviors might bea response to the predatorrsquos ability to learn Perhaps theldquoevitabilityrdquo of the preyrsquos behavior (Roeder 1975) makeslearning by the predator less effective

AcknowledgmentsWe thank Raymond CoxOle Naeligsbye Larsen and our students(Vibeke Futtrup Marianne E Jensen Niels Skals) for com-ments on the manuscript We also appreciate the commentsof five anonymous reviewers Our research has been sup-ported by grants from the Danish Natural Sciences ResearchCouncil the Danish National Research Foundation and theCarlsberg Foundation

References citedAcharya L Fenton MB 1992 Echolocation behaviour of vespertilionid bats

(Lasiurus cinereus and Lasiurus borealis) attacking airborne targets in-cluding arctiid moths Canadian Journal of Zoology 70 1292ndash1298

Acharya L McNeil J 1998 Predation risk and mating behavior The re-sponses of moths to batlike ultrasound Behavioral Ecology 9 552ndash558

Ball EE Field LH 1981 Structure of the auditory system of the wetaHemideina crassidens (Blanchard1851) (Orthoptera Ensifera Gryl-lacridoidea Stenopelmantidae) 1 Morphology and histology Cell Tis-sue Res 217 321ndash343

Barclay RMR 1986 The echolocation calls of hoary (Lasiurus cinereus) andsilver-haired (Lasionycteris noctivagans) bats as adaptations for long-versus short-range foraging strategies and the consequences for prey se-lection Canadian Journal of Zoology 64 2700ndash2705

Bates DL Fenton MB 1990 Aposematism or startle Predators learn their re-sponses to the defenses of prey Canadian Journal of Zoology 68 49ndash52

Boyan GS Fullard JH 1986 Interneurones responding to sound in the to-bacco budworm moth Heliothis virescens (Noctuidae) Morphological andphysiological characteristics Journal of Comparative Physiology A Sen-sory Neural and Behavioral Physiology 158 391ndash404

Boyan GS Miller LA 1991 Parallel processing of afferent input by identi-fied interneurones in the auditory pathway of the noctuid moth Noctuapronuba (L) Journal of Comparative PhysiologyA Sensory Neural andBehavioral Physiology 168 727ndash738

Conner WE 1999ldquoUn chant drsquoappel amoureusrdquo Acoustic communicationin moths Journal of Experimental Biology 202 1711ndash1723

Cumming GS 1996 Mantis movements by night and the interactions of sym-patric bats and mantises Canadian Journal of Zoology 74 1771ndash1774

Dunning DC 1968 Warning sounds of moths ZTierpsychol 25 129ndash138Dunning DC Kruumlger M 1996 Predation upon moths by free-foraging Hip-

posideros caffer Journal of Mammalogy 77 708ndash715Eggers F 1919 Das thoracale bitympanale Organ einer Gruppe der Lepi-

doptera Heterocera Zool Jb (Anat) 41 273ndash376Faure PA Barclay RMR 1994 Substrate-gleaning versus aerial-hawking

Plasticity in the foraging and echolocation behaviour of the long-earedbat Myotis evotis Journal of Comparative PhysiologyA Sensory Neuraland Behavioral Physiology 174 651ndash660

Faure PA Hoy RR 2000 Neuroethology of the katydid T-cell II Responsesto acoustic playback of conspecific and predatory signals Journal ofExperimental Biology 203 3243ndash3254

Fenton MB1990 The foraging behaviour and ecology of animal-eating batsCanadian Journal of Zoology 68 411ndash422

Fenton MB Fullard JH 1981 Moth hearing and the feeding strategies of batsAmerican Scientist 69 266ndash275

Forrest TG Read MP Farris HE Hoy RR 1997 A tympanal hearing organin scarab beetles Journal of Experimental Biology 200 601ndash606

Fullard JH 1979 Behavioral analyses of auditory sensitivity in Cycnia ten-era Huumlbner (Lepidoptera Arctiidae) Journal of Comparative Physiol-ogy A Sensory Neural and Behavioral Physiology 129 79ndash83

mdashmdashmdash 1984a Acoustic relationships between tympanate moths and theHawaiian hoary bat (Lasiurus cinereus semotus) Journal of ComparativePhysiology ASensory Neuraland Behavioral Physiology 155 795ndash801

mdashmdashmdash 1984b Listening for bats Pulse repetition rate as a cue for a defen-sive behavior in Cycnia tenera (LepidopteraArctiidae)Journal of Com-parative Physiology A Sensory Neural and Behavioral Physiology 154249ndash252

mdashmdashmdash 1988 The tuning of moth ears Experientia 44 423ndash428mdashmdashmdash 1994Auditory changes in noctuid moths endemic to a bat-free niche

Journal of Evolutionary Biology 7 435ndash445Fullard JH Fenton MB 1977 Acoustic behavioural analyses of the sounds

produced by some species of Nearctic Arctiidae (Lepidoptera)CanadianJournal of Zoology 55 1213ndash1224

Fullard JH Fenton MB Simmons JA 1979 Jamming bat echolocation Theclicks of arctiid moths Canadian Journal of Zoology 57 647ndash649

Fullard JH Simmons JA Saillant PA 1994 Jamming bat echolocation Thedogbane tiger moth Cycnia tenera times its clicks to the terminal attackcalls of the big brown bat Eptesicus fuscus Journal of Experimental Bi-ology 194 285ndash298

Fullard JH Dawson JW Otero LD Surlykke A1997 Bat-deafness in day-fly-ing moths (Lepidoptera Notodontidae Dioptinae) Journal of Com-parative Physiology A Sensory Neural and Behavioral Physiology 181277ndash483

Goumlpfert MC Wasserthal LT 1999 Auditory sensory cells in hawkmoths Iden-tification physiology and structure Journal of Experimental Biology 2021579ndash1587

Hoy RR 1992 The evolution of hearing in insects as an adaptation to pre-dation from batsPages 115ndash129 in Webster DB Fay RR Popper AN edsThe Evolutionary Biology of Hearing New York Springer-Verlag

Hoy RR Nolen T Brodfuehrer P 1989 The neuroethology of acoustic star-tle and escape in flying insects Journal of Experimental Biology 146287ndash306

Jensen ME Miller LA 1999 Echolocation signals of the bat Eptesicus serot-inus recorded using a vertical microphone array Effect of flight altitudeon searching signals Behavioral Ecology and Sociobiology 47 60ndash69

Kennel JV Eggers F 1933 Die abdominalen Tympanalorgane der Lepi-dopteren Zool Jb (Anat) 57 1ndash104

Lakes-Harlan R Heller K-G 1992 Ultrasound-sensitive ears in a parasitoidfly Naturwissenschaften 79 224ndash226

Larsen ON Kleindienst H-UMichelsen A1989 Biophysical aspects of soundreception Pages 364ndash390 in Huber F Moore TELoher W eds Cricket Be-havior and Neurobiology Ithaca (NY) Cornell University Press

580 BioScience July 2001 Vol 51 No 7

Articles

at about 10 times the distance over which bats can detectmoths (Surlykke et al 1999)

Many interneurons in the thoracic and cephalic ganglia ofnoctuids have been characterized (Roeder 1975 Boyan andFullard 1986) For example two identified neurons receive di-rect input from the A1 afferent in parallelbut they process tem-poral information differently (Boyan and Miller 1991) Synap-tic input to some motor neurons controlling the upndashdownmovement of the wings occurs only when the A2 sensory cellis activated (Madsen and Miller 1987) The role individual in-terneurons play in eliciting behavior is speculative principallybecause the responses of moths are exceedingly difficult tostudy under controlled conditions (Roeder 1967b)

Arctiid moths behave like noctuids but are more reluctantto do so In addition some arctiids produce ultrasonic click-ing sounds from tymbal organs when they hear bat signals orare touched (The clicks have various effects on bats as de-scribed below) Cycnia tenera starts clicking before it stops fly-ing in response to ultrasonic stimuli (Fullard 1979) Thethreshold for flight cessation is about 10ndash20 dB above that forclicking and repetition rates from 17ndash40 pulses per secondare best at eliciting clicking (Fullard 1984b) Also the rate ofmotor spikes to the tymbal muscles increases when the stim-ulus rate increases (Northcott and Fullard 1996) So both am-plitude and pulse repetition rate of the ultrasonic stimulus in-fluence behavioral responses from noctuid and arctiid moths

The Geometridae Pyralidae and Drepanidae have ultra-sound-sensitive ears on the first abdominal segment (Minetand Surlykke 2001) In the geometrids (Figure 2b left) thetympana are adjacent to the midline and point caudally (Fig-ure 2b middle) The tympana in pyralids point rostrally andhave a slight tilt ventrallyFour sensory (A) cells attach to eachtympanum The dynamic range for hearing in the geometridBiston betularia is about 50 dB because each cell covers asmaller range (10ndash15 dB) than the A cells in a noctuid ear Thefrequency range of hearing extends to at least 100 kHz in allspecies studied thus far (Figure 2b right B betularia Surlykkeand Filskov 1997) Some geometrids show flight cessation andother responses to ultrasound (Rydell et al 1997) Pyralid waxmoths respond to bat cries (Spangler and Takessian 1983) andGalleria mellonella shows a number of behavioral responseswhile in stationary flight the most noticeable of which isflight cessation (Skals and Surlykke 2000) Flight cessationwhich is the behavior with the highest threshold occurs at +20to +25 dB with respect to the threshold for the A1 cell (Fig-ure 2b right G mellonella) Actually avoidance behavior tobat echolocation is so powerful that some pyralid (and noc-tuid) moths abort sexually oriented flight to females broad-casting pheromones (Acharya and McNeil 1998)

The bat-detecting ear of some hawk moths (Figure 2cleft) consists of air-filled labial palps that transmit sound en-ergy to the pilifers located on either side of the proboscis(Figure 2c middle) Other hawk moths have scale plates onthe labial palps rather than air-filled palps Neurophysiolog-ical recordings from the labial nerve or from interneurons re-veal the auditory characteristics in both types of hawk moths

(Figure 2c right) They are most sensitive to frequencies be-tween 20 and 30 kHz with a threshold of 40ndash50 dB sound pres-sure level The dynamic range of the single auditory sensoryneuron in the pilifer is about 20 dB resembling that in the earof notodontid moths Hawk moths in tethered flight respondto ultrasound with changes in flight speed with nondirectionalturning and sometimes by emitting sound The behavioralthreshold is about 70 dB SPL or 20 dB above the sensorythreshold (Roeder et al 1970 Goumlpfert and Wasserthal 1999)

Green lacewings The ear of the green lacewing (Figure 2dleft) is located in a bulge near the base of the radial vein in eachforewing (Figure 2d middle) It is a true tympanal organwhich is mostly fluid filled and contains a small trachea It isthe smallest tympanal organ knownPerhaps only 6 of the 25sensory cells actually respond to ultrasound (see Miller 1984for a review) Like wax moths green lacewings in stationaryflight show a number of responses to lower intensity stimulibefore ceasing their flight (Miller 1975) Flight cessation (Fig-ure 2d right) occurs most reliably to ultrasonic signals broad-cast at rates of 1ndash50 pulses per second High stimulus repe-tition rates alone were ineffective in stopping the flight ofrestrained green lacewings

A more realistic picture of behavior emerged from studieson freely flying green lacewings and bats (Figure 3) Bat sig-nals at low repetition rates possibly combined with low in-tensities cause insects to fold their wings and passively diveThe green lacewing shows this nondirectional early-warningresponse to batsrsquo searching signals (Figure 3 between flashes2 and 3) The bat increases its call rate as it approaches a fallinginsect (Figure 3 flashes 3 to 4) Just before capturing its preythe bat increases its repetition rate to a maximum of about200 signals per second in the terminal phase for most bats (Fig-ure 3 flash 5) During the terminal phase the insect suddenlyflipped open its wings (Figure 3 flash 5 arrow) presumablyin response to the high repetition rate signals This last-chance response breaks the dive and foils the bat in this caseafter which the insect continues its dive (Figure 3 flash 6)Artificial bat signals mimicking the sequence shown in Fig-ure 3 evoke the same behavior (Miller and Olesen 1979) Byrepeating the experiments with deafened green lacewingswe showed that the selective advantage of reactors over non-reactors was 47 or about the same as that found for moths(see Miller 1982) Unidentified neurons in the prothoracic gan-glion respond to ultrasound but their role in eliciting behavioris unknown (Miller 1984)

Conclusions about insect behaviorsWe can draw some conclusions and make predictions basedon what we know about avoidance behaviors Looking at allthe behavioral response types for all the insects mentionedabove we find that the best frequency the frequency at whichneural or behavioral responses have the lowest thresholdlies between about 20 and 60 kHz with thresholds betweenabout 30 and 70 dB SPL The response latencies range from40ndash70 ms at +15 dB with respect to the behavioral threshold

July 2001 Vol 51 No 7 BioScience 575

Articles

Because the distance at which the insects respond to 40 kHzsounds varies from 65ndash37 m for bats using intense signalsthe insects have several tenths of a second to avoid even fast-flying bats (Surlykke 1988) The situation is somewhat differentfor whispering bats which use intensities of less than about75 dB SPL and hunt near vegetation Here the response dis-tances for flying insects are from 01ndash27 m depending on thehearing threshold However bats can detect a moth-sizedecho at about 06 m putting the less-sensitive insects in dan-ger Many of the insects mentioned above are open-air fliersand normally do not meet whispering bats

The tuning of neurons suspected to be involved in avoid-ance behavior in preadapted insects such as crickets grasshop-pers and preying mantids poorly match the behavioral tun-ing This discrepancy suggests that these auditory neurons havebeen molded into an antibat circuitry as a result of selectionpressure Behaviors such as turning in midflight or flightcessation have thresholds typically 20 dB higher than thosefor sensory neurons or interneurons (except premotor in-terneurons) in the same insects Consequently yet undis-covered behaviors to low stimulus intensities may provide ad-ditional survival advantage

Insect avoidance behaviors and their underlying mecha-nisms are undoubtedly complicated Take for example the vari-ability of responses The behaviors cannot be reliably predictedand the same individual may show different responses or noresponse at all to the same stimulus Roeder called this theldquoevitabilityrdquoof behavior which provides a survival advantageby making it difficult for the predator to predict what the preywill do The characteristic feature of evitability makes it dif-ficult to study but it seems to be present in the behavior and

physiology of some moths (Roeder 1975 Madsen and Miller1987) and green lacewings (Miller and Olesen 1979)Nevertheless the auditory and behavioral mechanismspresented here found in many families in several orders ofinsects give an overall picture of convergent evolution inresponse to bat predation

Insects living in bat-free environments

Spatial isolation Some moths escape from the risk of pre-dation by insectivorous bats simply by living in places whereno bats occur Bats are found on all continents except Antarc-tica and on the majority of islands but some remote islandsare free of bats for instance the Faroe Islands in the NorthAtlantic and the islands in French Polynesia

In general moth hearing sensitivity tends to reflect thecharacteristic frequencies and intensities of the local batfaunaHowever moths from the Faroes (Surlykke 1986) as wellas those from Tahiti (French Polynesia Fullard 1994) have re-tained auditory sensitivity in complete isolation from bats Iso-lated moths have thresholds at the best frequencies that arecomparable to the thresholds of moths sympatric with batsin similar habitats temperate or tropical Moths from HighArctic areas also show evasive maneuvers to ultrasound (Ry-dell et al 2000) The reason these moths have retained sen-sitive hearing which seems totally superfluous is not knownIt may simply be due to the slow regression of a character ifthere is no selection pressure against it In contrast a characterthat has adaptive value may spread through the populationafter only a few generations as shown by melanism in the pep-pered moth Biston betularia

576 BioScience July 2001 Vol 51 No 7

Articles

Figure 3 The behavioral responses of a green lacewing to a hunting pipistrelle bat The behavior was photographed in alarge flight cage using stroboscopic flashes at 70-ms intervals The biosonar signals that the bat emitted during the variousstages of hunting were simultaneously recorded The signals are schematic and only the intervals are accurately shownModified from Miller and Olesen 1979

Temporal isolation This is another strategy to avoidbats The Cuculliinae (Noctuidae) include moths that areactive in the winter Several species (eg Lithophane grotei andEupsilia vinulenta) were captured in Massachusetts in No-vember over a 3-week period when snow covered the groundand nightly bat censuses revealed none All captured mothshad functional ears tuned to bat sounds with thresholds as lowas their relatives flying in the summer (Surlykke and Treat1995) A study of hearing in winter-active geometrid mothsgave a similar result (Rydell et al 1997) Apparently noctur-nally active winter moths do not use their hearing even forintraspecific communication Isolated moths retain their ul-trasonic hearing which indicates that it is not very costly evo-lutionarily speaking to retain ears if they provide wintermoths with additional protection such as from the possibil-ity of occasionally overlapping with bats

The nocturnal noctuid moth Rileyana fovea (formerlyThecophora fovea) from Central Europe emerges in late Oc-tober to early November after bat activity has decreased Ri-leyana fovea communicates with ultrasound The males singin flight by scraping the file of the hind tarsus against the foveawhich is an inflated bubble on the hindwing supported by theheavily sclerotized radial vein (Figure 4) The intense sounds(80 dB at 1 m) have peak power around 30 kHz which wouldmake the moths very conspicuous to bats The moths are read-ily eaten by captive bats However by being active at a timeof the year with few bats R fovea can use ultrasound for in-traspecific communication Hence it seems that a completeconversion of hearing from a defensive context to a sexual onehas occurred secondarily in R fovea (Surlykke and Gogala1986) Ultrasound-producing organs have developed inde-pendently in distantly related species of moths that are pro-tected from bats in different ways This suggests that the pre-

existing ear prompted the development of intraspecificacoustic communication in certain moths (Conner 1999Skals and Surlykke 1999)

Some moths have changed to diurnal life a secondaryadaptation perhaps in response to predation by bats Oftendiurnal moths are protected by toxins and warning colors likesome butterflies These day fliers include many tiger moths(Arctiidae) especially from the subfamily Ctenuchinae Onlyrelatively few Noctuidae are day fliers One example is the Aus-tralian whistling moth Hecatesia thyridion (Agaristinae)which is brightly patterned and probably toxic Male whistlingmoths produce sounds that are audible but most of the en-ergy is in the ultrasonic range where their hearing is best Theyuse sounds to defend their territories and to attract females(Surlykke and Fullard 1989) Some diurnal moths are silentand apparently their hearing has no function at all For ex-ample diurnal notodontid moths in the subfamily Dioptinaefrom Venezuela show varying degrees of auditory degenera-tion ranging from almost normal sensitivity in some speciesto very reduced sensitivity especially at ultrasonic frequenciesin other species (Fullard et al 1997) Similarly the diurnalgeometrid Archiearis parthenias is practically deaf to ultrasonicfrequencies (Surlykke et al 1998)

Sound as defenseMany arctiids possess tymbal organs located on the sides ofthe metathorax (Figure 5a Conner 1999) Special musclesbuckle the tymbal membrane generating one click or a burstof clicks per activation cycle (Figure 5b) Click amplitudes varyfrom about 50ndash90 dB SPL measured at 5 cm with maxi-mum sound energy falling between 30 and 80 kHz (Figure 5cFullard and Fenton 1977 Surlykke and Miller 1985) Flyingarctiids may click when they hear the biosonar signals ofbats Thresholds for clicking can be as low as 60ndash75 dB SPLfor simulated search-phase signals (Fullard 1979 Surlykke andMiller 1985) but considerably higher for short signals (about2 ms Fullard 1984b)

Some bats and insects share the same hibernacula andmarauding bats feed on hibernating insects Nymphalid but-terflies sense the vibrations in the substratum as the batcrawls toward it The torpid butterfly opens its wings in a char-acteristic manner which produces intense ultrasonic clicksfrom a special area of the wing membrane (Moslashhl and Miller1976) What purpose do the clicks serve There are threelikely functions of clicking sounds They could startle bats theycould interfere with the batsrsquo biosonar system or they couldwarn bats of a distasteful prey as many arctiid moths containtoxins in their body tissues or in special glands

Startle and interference The clicks of nymphalid but-terflies startle bats and thus provide a chance for the insect toescape However a bat quickly habituates to the sounds andeats these butterflies (Moslashhl and Miller 1976) For experi-enced bats clicks can act as a dinner bellArctiid clicks can star-tle inexperienced and naive bats (Eptesicus fuscus) but thesebats also habituate rapidly (Bates and Fenton 1990 Miller

July 2001 Vol 51 No 7 BioScience 577

Articles

Figure 4 Male stridulatory organ used for the productionof intraspecific communication sounds by the noctuidmoth Rileyana fovea (formerly Thecophora fovea)Sound pulses with carrier frequencies of about 30 kHzare produced by scraping the file on the tarsus of the hindleg against the stridulatory swelling (fovea) on thehindwing Modified from Surlykke and Gogala 1986

1991) Thus clicks must be used sparingly to have survivalvalue as startle signals

The ultrasonic clicks of arctiids might disturb bat biosonarin two ways by simulating multiple targets (Fullard et al1979 1994) and by interfering with range determination(Miller 1991) The arctiid Cycnia tenera produces long trainsof clicks at high rates Fullard et al (1979 1994) hypothesizedthat clicks of C tenera could function as acoustical camou-flage by simulating multiple targets (false echoes) near themoth and thus jam a batrsquos (Eptesicus fuscus) biosonar Theybased their conclusion mainly on the ability of the moth totime its clicking to the terminal phase of the batrsquos signals Milleret al (forthcoming) tested this idea using bats (Pipistrellus pip-istrellus) trained to catch catapulted meal worms after whichnatural click sequences from the arctiid Phragmatobia fulig-inosa were played back during the batsrsquo terminal phase Thebats reacted by increasing the harmonic structure of their ter-minal signals but clicks did not influence the success rate of

prey capture The results suggest that the clicks produced byP fuliginosa do not interfere with the batsrsquo sonar system per-haps because the click rate is too low However in psy-chophysical experiments the clicks from P fuliginosa did in-terfere with the ability of bats (Eptesicus fuscus) to determinerange differences (Miller 1991) When clicks triggered bythe batsrsquo own signals fall repeatedly within a critical time win-dow of about 15 ms before an echo the batrsquos discriminationof range differences deteriorated by as much as 40-fold A sin-gle artificial click placed within the critical window inter-feres with range difference determination (Tougaard et alforthcoming) and with neural responses (Tougaard et al1998) In either case a bat would miss its target if clicks rep-resent false echoes from phantom objects or if they interferewith the batrsquos ranging mechanism

Warning sounds toxins and mimicry Several factspoint to the warning function of clicks as suggested by Dun-ning (1968) The Arctiidae (including the Ctenuchinae) aregenerally unpalatable and arctiids are the only noctuoidmoths that click in response to bat sonar sounds Arctiidclicks could warn the bat of a noxious prey Evidence sup-porting a warning function comes from studies in the labo-ratory and the field In experimental studies bats (Pipistrel-lus pipistrellus and Eptesicus fuscus) habituated to arctiid clickswhen given palatable rewards (Surlykke and Miller 1985Bates and Fenton 1990) However the same bats learned veryquickly to associate moth clicks with a distasteful rewardField studies indicated that bats (Lasiurus sp) foraging aroundstreet lights often aborted their attacks in the approach or ter-minal phase when the prey was the noisy arctiid mothHypoprepia fucosa (Acharya and Fenton 1992) Wild H fucosadid not take visible evasive action to attacking bats Batsavoided more than 90 of the moths released and droppedthe few they captured usually undamaged The bats showedno evidence of habituation although H fucosa were abundantcomposing more than 30 of the moth population Hy-poprepia fucosa has classic warning coloration and patterns as-sociated with toxic species Evidence favors the assumptionthat arctiid clicks are acoustical aposematic signals warningbats that the moths taste bad (Dunning and Kruumlger 1996)

Combining acoustic defenses The startle interferenceand warning hypotheses are not mutually exclusive In areaswhere arctiid moths are scarce the clicks may mostly startlebats Because bats quickly adapt to the clicks a warning func-tion is most likely in areas where arctiid moths are abundantWarning seems especially likely for toxic arctiids like Arctia cajawhich produce few but intense clicks in response to batlikesignals (Surlykke and Miller 1985) At least some species of arc-tiids begin clicking to the searching signals of aerial hawkingbats at distances of about 2ndash4 m (Surlykke and Miller 1985)At these distances the bat should be able to hear the clicks giv-ing an experienced predator ample time to avoid the dis-tasteful prey There is sufficient time for the bat to change itsbehavior even if the warning comes during the approach or

578 BioScience July 2001 Vol 51 No 7

Articles

Figure 5 Arctiid tymbal organ and clicks (a) The tymbalorgan on the lateral surface of the metathoracic segmentof the arctiid Phragmatobia fuliginosa (b) The tymbalorgan produces a burst of clicks each time it buckles (c)The power spectrum of the burst has a maximum atabout 80 kHz (a) Modified from Surlykke and Miller1985 (b) and (c) modified from Miller 1991

terminal phases of the batrsquos pursuit (Acharya and Fenton1992) Should the mothrsquos clicks arrive at the batrsquos ear just be-fore the echoes the batrsquos estimation of range to the preyblurs perhaps causing the bat to miss the target Moths us-ing long trains of click bursts could exploit this strategy Allthree possibilities startle interference and warning offerselective advantages for arctiid moths in addition to thoseprovided by changes in flight behavior

Potential countertactics for batsThe diet of many bats contains very few moths perhaps be-cause of their effective defenses However some barbastelle batsprey almost exclusively on tympanate moths and just how theydo this is not known (Sierro and Arlettaz 1997) Here wepresent some possible double-edged strategies that may ex-plain bat adaptations

Changing signals Echolocating bats announce their pres-ence to all potential prey equipped with auditory bat detec-tors and bats may use different acoustic strategies to reducetheir conspicuousness One strategy would be an adaptationthat moved frequencies of sonar signals out of the rangewhere tympanate insects are most sensitive (Dunning andKruumlger 1996) Some bats use very high frequencies whichmake them less audible to most noctuoid moths Howeversmall moths such as some geometrids (Surlykke and Filskov1997) the pyralid Galleria mellonella (Figure 2b right) andmany tropical noctuoids (Fullard 1988) are quite sensitive tohigh frequencies The attenuation of high frequencies re-duces the useful range of bat sonar so the advantage of thisstrategy may be limited If emission of high frequencies werea countermeasure against tympanate insects one would ex-pect to find bats exploiting this strategy in temperate regionswhere many moths do have poor sensitivity at high frequen-cies (Fullard 1988) The only temperate nongleaning batsthat use relatively high frequencies are small ones (eg Pip-istrellus spp) which detect small prey While the emission ofhigh frequencies may be a response to insect defenses it mayalso be a way to increase resolution and thus increase the abil-ity of bats to detect smaller insects (Surlykke et al 1993)

A second strategy would be for bats to emit very low fre-quencies which would make them less conspicuous to moths(Rydell and Arlettaz 1994) This strategy is employed mostlyby fast-flying bats that hunt aerial insects far from the groundand vegetation (Neuweiler 1989 Fenton 1990) Low fre-quencies increase the batsrsquo range but lower the resolution ofthe batsrsquo biosonar making only large insects detectable (Bar-clay 1986)

A third strategy would be an adaptation for bats to reducethe intensity of their signals Sound intensity is a measure ofsound energy and is proportional to the sound pressure(The dB scale is adapted such that any change in sound pres-sure and the corresponding change in sound intensity resultin the same change in dB value) The advantage would be thatthe sound intensity decreases with the square of the distancebut the echo intensity decreases with the fourth power of the

distance (Surlykke 1988) making the bat less detectable to thetympanate insect We do not know if any bats exploit this strat-egy but we know that all bats studied so far when gleaninguse low-intensity sounds if they emit any signals at all(Neuweiler 1989 Miller and Treat 1993 Faure and Barclay1994) For a gleaning bat the reduction of detection range isprobably not an important restriction because reducingsound intensity gives the additional advantage of reducing clut-ter echoes from the background (see Schnitzler and Kalko2001) In contrast field studies using techniques to calculatethe distance and direction to the bat indicate that at least somebats hunting aerial insects in the open emit intense signals withsource levels up to 125 dB SPL the highest levels yet measured(Jensen and Miller 1999) Also bats that display both glean-ing and aerial-hawking modes of foraging such as for in-stance Myotis evotis (Faure and Barclay 1994) and M septen-trionalis (Miller and Treat 1993) emit high intensities whenhunting flying insects

Finally shorter echolocation signals should be less con-spicuous to prey However shorter signals mean shorterechoes with less energy which are less conspicuous to the batstoo Also short search signals are recorded mainly from batsusing frequency-modulated calls and hunting close to clut-ter (Neuweiler 1989 Fenton 1990) Hencewe believe that shortcalls probably are not a countermeasure against insect hear-ing but rather an adaptation for reducing the overlap betweenechoes from clutter and those from prey

Listening to prey sounds The most effective way for abat to sneak close to tympanate prey is to cease echolocatingaltogether and detect prey using passive sensory cues If theinsects produce sound bats may find them using passivehearing Gleaning bats such as Plecotus auritus and Myotis evo-tis usually have large pinnae (Faure and Barclay 1994) Theyreact with very fast positive phonotaxis to insect-producedsounds such as the sound of wings fluttering or of an insectcrawling on a surface Some gleaning bats emit the full reper-toire of biosonar signals including the terminal phase(Schumm et al 1991) However gleaners generally stop call-ing before the attack and produce no terminal phase(Neuweiler 1989 Faure and Barclay 1994) Whether omissionof the terminal phase reduces the insectrsquos chance of escapingis difficult to say because tympanate insects probably detectecholocating bats long before the terminal phase (Roeder1967a Surlykke et al1999) However omitting the terminalphase may prevent last-chance escape maneuvers (Miller1984) On the other hand sedentary moths stay motionlessor freeze when hearing echolocation signals Turning off thesonar in the final phase may not be a countermeasure againsttympanate insects it may simply be that the bat does not needto continuously update the estimated position of a motion-less insect In contrast the prey of aerial hunters change po-sition continuously in three dimensions thus forcing the batto use its biosonar nearly to the moment of capture

It is difficult to determine if the acoustical adaptations ofbats are responses to constraints of the environment or to the

July 2001 Vol 51 No 7 BioScience 579

Articles

batsrsquo hunting strategies or are intended to overcome insect de-fenses In any case some bat echolocation signals are lessconspicuous to tympanate prey

Concluding remarksThe evolutionary arms race continues between bats and theirinsect prey and undiscovered strategies await to be revealedSome suspected strategies such as acoustical mimicry needto be documented by laboratory and field studies Experi-mental studies in the field can elucidate some questions aboutbat and insect interactions For example wild gleaning batshunting at familiar sites (Miller and Treat 1993 Faure and Bar-clay 1994) offer unique opportunities to test some hypothe-ses about echolocation behavior and the functions of clicksas interfering or warning signals Employing modern digitalsystems that can reproduce clicks and simulate insect echoeswill assist in such studies

Some questions will be difficult to answer An individualbat can modify at least some of its strategies through learn-ing whereas insect counterstrategies appear through theslower process of natural selection Does this mean insectstrategies lag behind those of their predators Perhaps not Thevariability of an individual insectrsquos antibat behaviors might bea response to the predatorrsquos ability to learn Perhaps theldquoevitabilityrdquo of the preyrsquos behavior (Roeder 1975) makeslearning by the predator less effective

AcknowledgmentsWe thank Raymond CoxOle Naeligsbye Larsen and our students(Vibeke Futtrup Marianne E Jensen Niels Skals) for com-ments on the manuscript We also appreciate the commentsof five anonymous reviewers Our research has been sup-ported by grants from the Danish Natural Sciences ResearchCouncil the Danish National Research Foundation and theCarlsberg Foundation

References citedAcharya L Fenton MB 1992 Echolocation behaviour of vespertilionid bats

(Lasiurus cinereus and Lasiurus borealis) attacking airborne targets in-cluding arctiid moths Canadian Journal of Zoology 70 1292ndash1298

Acharya L McNeil J 1998 Predation risk and mating behavior The re-sponses of moths to batlike ultrasound Behavioral Ecology 9 552ndash558

Ball EE Field LH 1981 Structure of the auditory system of the wetaHemideina crassidens (Blanchard1851) (Orthoptera Ensifera Gryl-lacridoidea Stenopelmantidae) 1 Morphology and histology Cell Tis-sue Res 217 321ndash343

Barclay RMR 1986 The echolocation calls of hoary (Lasiurus cinereus) andsilver-haired (Lasionycteris noctivagans) bats as adaptations for long-versus short-range foraging strategies and the consequences for prey se-lection Canadian Journal of Zoology 64 2700ndash2705

Bates DL Fenton MB 1990 Aposematism or startle Predators learn their re-sponses to the defenses of prey Canadian Journal of Zoology 68 49ndash52

Boyan GS Fullard JH 1986 Interneurones responding to sound in the to-bacco budworm moth Heliothis virescens (Noctuidae) Morphological andphysiological characteristics Journal of Comparative Physiology A Sen-sory Neural and Behavioral Physiology 158 391ndash404

Boyan GS Miller LA 1991 Parallel processing of afferent input by identi-fied interneurones in the auditory pathway of the noctuid moth Noctuapronuba (L) Journal of Comparative PhysiologyA Sensory Neural andBehavioral Physiology 168 727ndash738

Conner WE 1999ldquoUn chant drsquoappel amoureusrdquo Acoustic communicationin moths Journal of Experimental Biology 202 1711ndash1723

Cumming GS 1996 Mantis movements by night and the interactions of sym-patric bats and mantises Canadian Journal of Zoology 74 1771ndash1774

Dunning DC 1968 Warning sounds of moths ZTierpsychol 25 129ndash138Dunning DC Kruumlger M 1996 Predation upon moths by free-foraging Hip-

posideros caffer Journal of Mammalogy 77 708ndash715Eggers F 1919 Das thoracale bitympanale Organ einer Gruppe der Lepi-

doptera Heterocera Zool Jb (Anat) 41 273ndash376Faure PA Barclay RMR 1994 Substrate-gleaning versus aerial-hawking

Plasticity in the foraging and echolocation behaviour of the long-earedbat Myotis evotis Journal of Comparative PhysiologyA Sensory Neuraland Behavioral Physiology 174 651ndash660

Faure PA Hoy RR 2000 Neuroethology of the katydid T-cell II Responsesto acoustic playback of conspecific and predatory signals Journal ofExperimental Biology 203 3243ndash3254

Fenton MB1990 The foraging behaviour and ecology of animal-eating batsCanadian Journal of Zoology 68 411ndash422

Fenton MB Fullard JH 1981 Moth hearing and the feeding strategies of batsAmerican Scientist 69 266ndash275

Forrest TG Read MP Farris HE Hoy RR 1997 A tympanal hearing organin scarab beetles Journal of Experimental Biology 200 601ndash606

Fullard JH 1979 Behavioral analyses of auditory sensitivity in Cycnia ten-era Huumlbner (Lepidoptera Arctiidae) Journal of Comparative Physiol-ogy A Sensory Neural and Behavioral Physiology 129 79ndash83

mdashmdashmdash 1984a Acoustic relationships between tympanate moths and theHawaiian hoary bat (Lasiurus cinereus semotus) Journal of ComparativePhysiology ASensory Neuraland Behavioral Physiology 155 795ndash801

mdashmdashmdash 1984b Listening for bats Pulse repetition rate as a cue for a defen-sive behavior in Cycnia tenera (LepidopteraArctiidae)Journal of Com-parative Physiology A Sensory Neural and Behavioral Physiology 154249ndash252

mdashmdashmdash 1988 The tuning of moth ears Experientia 44 423ndash428mdashmdashmdash 1994Auditory changes in noctuid moths endemic to a bat-free niche

Journal of Evolutionary Biology 7 435ndash445Fullard JH Fenton MB 1977 Acoustic behavioural analyses of the sounds

produced by some species of Nearctic Arctiidae (Lepidoptera)CanadianJournal of Zoology 55 1213ndash1224

Fullard JH Fenton MB Simmons JA 1979 Jamming bat echolocation Theclicks of arctiid moths Canadian Journal of Zoology 57 647ndash649

Fullard JH Simmons JA Saillant PA 1994 Jamming bat echolocation Thedogbane tiger moth Cycnia tenera times its clicks to the terminal attackcalls of the big brown bat Eptesicus fuscus Journal of Experimental Bi-ology 194 285ndash298

Fullard JH Dawson JW Otero LD Surlykke A1997 Bat-deafness in day-fly-ing moths (Lepidoptera Notodontidae Dioptinae) Journal of Com-parative Physiology A Sensory Neural and Behavioral Physiology 181277ndash483

Goumlpfert MC Wasserthal LT 1999 Auditory sensory cells in hawkmoths Iden-tification physiology and structure Journal of Experimental Biology 2021579ndash1587

Hoy RR 1992 The evolution of hearing in insects as an adaptation to pre-dation from batsPages 115ndash129 in Webster DB Fay RR Popper AN edsThe Evolutionary Biology of Hearing New York Springer-Verlag

Hoy RR Nolen T Brodfuehrer P 1989 The neuroethology of acoustic star-tle and escape in flying insects Journal of Experimental Biology 146287ndash306

Jensen ME Miller LA 1999 Echolocation signals of the bat Eptesicus serot-inus recorded using a vertical microphone array Effect of flight altitudeon searching signals Behavioral Ecology and Sociobiology 47 60ndash69

Kennel JV Eggers F 1933 Die abdominalen Tympanalorgane der Lepi-dopteren Zool Jb (Anat) 57 1ndash104

Lakes-Harlan R Heller K-G 1992 Ultrasound-sensitive ears in a parasitoidfly Naturwissenschaften 79 224ndash226

Larsen ON Kleindienst H-UMichelsen A1989 Biophysical aspects of soundreception Pages 364ndash390 in Huber F Moore TELoher W eds Cricket Be-havior and Neurobiology Ithaca (NY) Cornell University Press

580 BioScience July 2001 Vol 51 No 7

Articles

Because the distance at which the insects respond to 40 kHzsounds varies from 65ndash37 m for bats using intense signalsthe insects have several tenths of a second to avoid even fast-flying bats (Surlykke 1988) The situation is somewhat differentfor whispering bats which use intensities of less than about75 dB SPL and hunt near vegetation Here the response dis-tances for flying insects are from 01ndash27 m depending on thehearing threshold However bats can detect a moth-sizedecho at about 06 m putting the less-sensitive insects in dan-ger Many of the insects mentioned above are open-air fliersand normally do not meet whispering bats

The tuning of neurons suspected to be involved in avoid-ance behavior in preadapted insects such as crickets grasshop-pers and preying mantids poorly match the behavioral tun-ing This discrepancy suggests that these auditory neurons havebeen molded into an antibat circuitry as a result of selectionpressure Behaviors such as turning in midflight or flightcessation have thresholds typically 20 dB higher than thosefor sensory neurons or interneurons (except premotor in-terneurons) in the same insects Consequently yet undis-covered behaviors to low stimulus intensities may provide ad-ditional survival advantage

Insect avoidance behaviors and their underlying mecha-nisms are undoubtedly complicated Take for example the vari-ability of responses The behaviors cannot be reliably predictedand the same individual may show different responses or noresponse at all to the same stimulus Roeder called this theldquoevitabilityrdquoof behavior which provides a survival advantageby making it difficult for the predator to predict what the preywill do The characteristic feature of evitability makes it dif-ficult to study but it seems to be present in the behavior and

physiology of some moths (Roeder 1975 Madsen and Miller1987) and green lacewings (Miller and Olesen 1979)Nevertheless the auditory and behavioral mechanismspresented here found in many families in several orders ofinsects give an overall picture of convergent evolution inresponse to bat predation

Insects living in bat-free environments

Spatial isolation Some moths escape from the risk of pre-dation by insectivorous bats simply by living in places whereno bats occur Bats are found on all continents except Antarc-tica and on the majority of islands but some remote islandsare free of bats for instance the Faroe Islands in the NorthAtlantic and the islands in French Polynesia

In general moth hearing sensitivity tends to reflect thecharacteristic frequencies and intensities of the local batfaunaHowever moths from the Faroes (Surlykke 1986) as wellas those from Tahiti (French Polynesia Fullard 1994) have re-tained auditory sensitivity in complete isolation from bats Iso-lated moths have thresholds at the best frequencies that arecomparable to the thresholds of moths sympatric with batsin similar habitats temperate or tropical Moths from HighArctic areas also show evasive maneuvers to ultrasound (Ry-dell et al 2000) The reason these moths have retained sen-sitive hearing which seems totally superfluous is not knownIt may simply be due to the slow regression of a character ifthere is no selection pressure against it In contrast a characterthat has adaptive value may spread through the populationafter only a few generations as shown by melanism in the pep-pered moth Biston betularia

576 BioScience July 2001 Vol 51 No 7

Articles

Figure 3 The behavioral responses of a green lacewing to a hunting pipistrelle bat The behavior was photographed in alarge flight cage using stroboscopic flashes at 70-ms intervals The biosonar signals that the bat emitted during the variousstages of hunting were simultaneously recorded The signals are schematic and only the intervals are accurately shownModified from Miller and Olesen 1979

Temporal isolation This is another strategy to avoidbats The Cuculliinae (Noctuidae) include moths that areactive in the winter Several species (eg Lithophane grotei andEupsilia vinulenta) were captured in Massachusetts in No-vember over a 3-week period when snow covered the groundand nightly bat censuses revealed none All captured mothshad functional ears tuned to bat sounds with thresholds as lowas their relatives flying in the summer (Surlykke and Treat1995) A study of hearing in winter-active geometrid mothsgave a similar result (Rydell et al 1997) Apparently noctur-nally active winter moths do not use their hearing even forintraspecific communication Isolated moths retain their ul-trasonic hearing which indicates that it is not very costly evo-lutionarily speaking to retain ears if they provide wintermoths with additional protection such as from the possibil-ity of occasionally overlapping with bats

The nocturnal noctuid moth Rileyana fovea (formerlyThecophora fovea) from Central Europe emerges in late Oc-tober to early November after bat activity has decreased Ri-leyana fovea communicates with ultrasound The males singin flight by scraping the file of the hind tarsus against the foveawhich is an inflated bubble on the hindwing supported by theheavily sclerotized radial vein (Figure 4) The intense sounds(80 dB at 1 m) have peak power around 30 kHz which wouldmake the moths very conspicuous to bats The moths are read-ily eaten by captive bats However by being active at a timeof the year with few bats R fovea can use ultrasound for in-traspecific communication Hence it seems that a completeconversion of hearing from a defensive context to a sexual onehas occurred secondarily in R fovea (Surlykke and Gogala1986) Ultrasound-producing organs have developed inde-pendently in distantly related species of moths that are pro-tected from bats in different ways This suggests that the pre-

existing ear prompted the development of intraspecificacoustic communication in certain moths (Conner 1999Skals and Surlykke 1999)

Some moths have changed to diurnal life a secondaryadaptation perhaps in response to predation by bats Oftendiurnal moths are protected by toxins and warning colors likesome butterflies These day fliers include many tiger moths(Arctiidae) especially from the subfamily Ctenuchinae Onlyrelatively few Noctuidae are day fliers One example is the Aus-tralian whistling moth Hecatesia thyridion (Agaristinae)which is brightly patterned and probably toxic Male whistlingmoths produce sounds that are audible but most of the en-ergy is in the ultrasonic range where their hearing is best Theyuse sounds to defend their territories and to attract females(Surlykke and Fullard 1989) Some diurnal moths are silentand apparently their hearing has no function at all For ex-ample diurnal notodontid moths in the subfamily Dioptinaefrom Venezuela show varying degrees of auditory degenera-tion ranging from almost normal sensitivity in some speciesto very reduced sensitivity especially at ultrasonic frequenciesin other species (Fullard et al 1997) Similarly the diurnalgeometrid Archiearis parthenias is practically deaf to ultrasonicfrequencies (Surlykke et al 1998)

Sound as defenseMany arctiids possess tymbal organs located on the sides ofthe metathorax (Figure 5a Conner 1999) Special musclesbuckle the tymbal membrane generating one click or a burstof clicks per activation cycle (Figure 5b) Click amplitudes varyfrom about 50ndash90 dB SPL measured at 5 cm with maxi-mum sound energy falling between 30 and 80 kHz (Figure 5cFullard and Fenton 1977 Surlykke and Miller 1985) Flyingarctiids may click when they hear the biosonar signals ofbats Thresholds for clicking can be as low as 60ndash75 dB SPLfor simulated search-phase signals (Fullard 1979 Surlykke andMiller 1985) but considerably higher for short signals (about2 ms Fullard 1984b)

Some bats and insects share the same hibernacula andmarauding bats feed on hibernating insects Nymphalid but-terflies sense the vibrations in the substratum as the batcrawls toward it The torpid butterfly opens its wings in a char-acteristic manner which produces intense ultrasonic clicksfrom a special area of the wing membrane (Moslashhl and Miller1976) What purpose do the clicks serve There are threelikely functions of clicking sounds They could startle bats theycould interfere with the batsrsquo biosonar system or they couldwarn bats of a distasteful prey as many arctiid moths containtoxins in their body tissues or in special glands

Startle and interference The clicks of nymphalid but-terflies startle bats and thus provide a chance for the insect toescape However a bat quickly habituates to the sounds andeats these butterflies (Moslashhl and Miller 1976) For experi-enced bats clicks can act as a dinner bellArctiid clicks can star-tle inexperienced and naive bats (Eptesicus fuscus) but thesebats also habituate rapidly (Bates and Fenton 1990 Miller

July 2001 Vol 51 No 7 BioScience 577

Articles

Figure 4 Male stridulatory organ used for the productionof intraspecific communication sounds by the noctuidmoth Rileyana fovea (formerly Thecophora fovea)Sound pulses with carrier frequencies of about 30 kHzare produced by scraping the file on the tarsus of the hindleg against the stridulatory swelling (fovea) on thehindwing Modified from Surlykke and Gogala 1986

1991) Thus clicks must be used sparingly to have survivalvalue as startle signals

The ultrasonic clicks of arctiids might disturb bat biosonarin two ways by simulating multiple targets (Fullard et al1979 1994) and by interfering with range determination(Miller 1991) The arctiid Cycnia tenera produces long trainsof clicks at high rates Fullard et al (1979 1994) hypothesizedthat clicks of C tenera could function as acoustical camou-flage by simulating multiple targets (false echoes) near themoth and thus jam a batrsquos (Eptesicus fuscus) biosonar Theybased their conclusion mainly on the ability of the moth totime its clicking to the terminal phase of the batrsquos signals Milleret al (forthcoming) tested this idea using bats (Pipistrellus pip-istrellus) trained to catch catapulted meal worms after whichnatural click sequences from the arctiid Phragmatobia fulig-inosa were played back during the batsrsquo terminal phase Thebats reacted by increasing the harmonic structure of their ter-minal signals but clicks did not influence the success rate of

prey capture The results suggest that the clicks produced byP fuliginosa do not interfere with the batsrsquo sonar system per-haps because the click rate is too low However in psy-chophysical experiments the clicks from P fuliginosa did in-terfere with the ability of bats (Eptesicus fuscus) to determinerange differences (Miller 1991) When clicks triggered bythe batsrsquo own signals fall repeatedly within a critical time win-dow of about 15 ms before an echo the batrsquos discriminationof range differences deteriorated by as much as 40-fold A sin-gle artificial click placed within the critical window inter-feres with range difference determination (Tougaard et alforthcoming) and with neural responses (Tougaard et al1998) In either case a bat would miss its target if clicks rep-resent false echoes from phantom objects or if they interferewith the batrsquos ranging mechanism

Warning sounds toxins and mimicry Several factspoint to the warning function of clicks as suggested by Dun-ning (1968) The Arctiidae (including the Ctenuchinae) aregenerally unpalatable and arctiids are the only noctuoidmoths that click in response to bat sonar sounds Arctiidclicks could warn the bat of a noxious prey Evidence sup-porting a warning function comes from studies in the labo-ratory and the field In experimental studies bats (Pipistrel-lus pipistrellus and Eptesicus fuscus) habituated to arctiid clickswhen given palatable rewards (Surlykke and Miller 1985Bates and Fenton 1990) However the same bats learned veryquickly to associate moth clicks with a distasteful rewardField studies indicated that bats (Lasiurus sp) foraging aroundstreet lights often aborted their attacks in the approach or ter-minal phase when the prey was the noisy arctiid mothHypoprepia fucosa (Acharya and Fenton 1992) Wild H fucosadid not take visible evasive action to attacking bats Batsavoided more than 90 of the moths released and droppedthe few they captured usually undamaged The bats showedno evidence of habituation although H fucosa were abundantcomposing more than 30 of the moth population Hy-poprepia fucosa has classic warning coloration and patterns as-sociated with toxic species Evidence favors the assumptionthat arctiid clicks are acoustical aposematic signals warningbats that the moths taste bad (Dunning and Kruumlger 1996)

Combining acoustic defenses The startle interferenceand warning hypotheses are not mutually exclusive In areaswhere arctiid moths are scarce the clicks may mostly startlebats Because bats quickly adapt to the clicks a warning func-tion is most likely in areas where arctiid moths are abundantWarning seems especially likely for toxic arctiids like Arctia cajawhich produce few but intense clicks in response to batlikesignals (Surlykke and Miller 1985) At least some species of arc-tiids begin clicking to the searching signals of aerial hawkingbats at distances of about 2ndash4 m (Surlykke and Miller 1985)At these distances the bat should be able to hear the clicks giv-ing an experienced predator ample time to avoid the dis-tasteful prey There is sufficient time for the bat to change itsbehavior even if the warning comes during the approach or

578 BioScience July 2001 Vol 51 No 7

Articles

Figure 5 Arctiid tymbal organ and clicks (a) The tymbalorgan on the lateral surface of the metathoracic segmentof the arctiid Phragmatobia fuliginosa (b) The tymbalorgan produces a burst of clicks each time it buckles (c)The power spectrum of the burst has a maximum atabout 80 kHz (a) Modified from Surlykke and Miller1985 (b) and (c) modified from Miller 1991

terminal phases of the batrsquos pursuit (Acharya and Fenton1992) Should the mothrsquos clicks arrive at the batrsquos ear just be-fore the echoes the batrsquos estimation of range to the preyblurs perhaps causing the bat to miss the target Moths us-ing long trains of click bursts could exploit this strategy Allthree possibilities startle interference and warning offerselective advantages for arctiid moths in addition to thoseprovided by changes in flight behavior

Potential countertactics for batsThe diet of many bats contains very few moths perhaps be-cause of their effective defenses However some barbastelle batsprey almost exclusively on tympanate moths and just how theydo this is not known (Sierro and Arlettaz 1997) Here wepresent some possible double-edged strategies that may ex-plain bat adaptations

Changing signals Echolocating bats announce their pres-ence to all potential prey equipped with auditory bat detec-tors and bats may use different acoustic strategies to reducetheir conspicuousness One strategy would be an adaptationthat moved frequencies of sonar signals out of the rangewhere tympanate insects are most sensitive (Dunning andKruumlger 1996) Some bats use very high frequencies whichmake them less audible to most noctuoid moths Howeversmall moths such as some geometrids (Surlykke and Filskov1997) the pyralid Galleria mellonella (Figure 2b right) andmany tropical noctuoids (Fullard 1988) are quite sensitive tohigh frequencies The attenuation of high frequencies re-duces the useful range of bat sonar so the advantage of thisstrategy may be limited If emission of high frequencies werea countermeasure against tympanate insects one would ex-pect to find bats exploiting this strategy in temperate regionswhere many moths do have poor sensitivity at high frequen-cies (Fullard 1988) The only temperate nongleaning batsthat use relatively high frequencies are small ones (eg Pip-istrellus spp) which detect small prey While the emission ofhigh frequencies may be a response to insect defenses it mayalso be a way to increase resolution and thus increase the abil-ity of bats to detect smaller insects (Surlykke et al 1993)

A second strategy would be for bats to emit very low fre-quencies which would make them less conspicuous to moths(Rydell and Arlettaz 1994) This strategy is employed mostlyby fast-flying bats that hunt aerial insects far from the groundand vegetation (Neuweiler 1989 Fenton 1990) Low fre-quencies increase the batsrsquo range but lower the resolution ofthe batsrsquo biosonar making only large insects detectable (Bar-clay 1986)

A third strategy would be an adaptation for bats to reducethe intensity of their signals Sound intensity is a measure ofsound energy and is proportional to the sound pressure(The dB scale is adapted such that any change in sound pres-sure and the corresponding change in sound intensity resultin the same change in dB value) The advantage would be thatthe sound intensity decreases with the square of the distancebut the echo intensity decreases with the fourth power of the

distance (Surlykke 1988) making the bat less detectable to thetympanate insect We do not know if any bats exploit this strat-egy but we know that all bats studied so far when gleaninguse low-intensity sounds if they emit any signals at all(Neuweiler 1989 Miller and Treat 1993 Faure and Barclay1994) For a gleaning bat the reduction of detection range isprobably not an important restriction because reducingsound intensity gives the additional advantage of reducing clut-ter echoes from the background (see Schnitzler and Kalko2001) In contrast field studies using techniques to calculatethe distance and direction to the bat indicate that at least somebats hunting aerial insects in the open emit intense signals withsource levels up to 125 dB SPL the highest levels yet measured(Jensen and Miller 1999) Also bats that display both glean-ing and aerial-hawking modes of foraging such as for in-stance Myotis evotis (Faure and Barclay 1994) and M septen-trionalis (Miller and Treat 1993) emit high intensities whenhunting flying insects

Finally shorter echolocation signals should be less con-spicuous to prey However shorter signals mean shorterechoes with less energy which are less conspicuous to the batstoo Also short search signals are recorded mainly from batsusing frequency-modulated calls and hunting close to clut-ter (Neuweiler 1989 Fenton 1990) Hencewe believe that shortcalls probably are not a countermeasure against insect hear-ing but rather an adaptation for reducing the overlap betweenechoes from clutter and those from prey

Listening to prey sounds The most effective way for abat to sneak close to tympanate prey is to cease echolocatingaltogether and detect prey using passive sensory cues If theinsects produce sound bats may find them using passivehearing Gleaning bats such as Plecotus auritus and Myotis evo-tis usually have large pinnae (Faure and Barclay 1994) Theyreact with very fast positive phonotaxis to insect-producedsounds such as the sound of wings fluttering or of an insectcrawling on a surface Some gleaning bats emit the full reper-toire of biosonar signals including the terminal phase(Schumm et al 1991) However gleaners generally stop call-ing before the attack and produce no terminal phase(Neuweiler 1989 Faure and Barclay 1994) Whether omissionof the terminal phase reduces the insectrsquos chance of escapingis difficult to say because tympanate insects probably detectecholocating bats long before the terminal phase (Roeder1967a Surlykke et al1999) However omitting the terminalphase may prevent last-chance escape maneuvers (Miller1984) On the other hand sedentary moths stay motionlessor freeze when hearing echolocation signals Turning off thesonar in the final phase may not be a countermeasure againsttympanate insects it may simply be that the bat does not needto continuously update the estimated position of a motion-less insect In contrast the prey of aerial hunters change po-sition continuously in three dimensions thus forcing the batto use its biosonar nearly to the moment of capture

It is difficult to determine if the acoustical adaptations ofbats are responses to constraints of the environment or to the

July 2001 Vol 51 No 7 BioScience 579

Articles

batsrsquo hunting strategies or are intended to overcome insect de-fenses In any case some bat echolocation signals are lessconspicuous to tympanate prey

Concluding remarksThe evolutionary arms race continues between bats and theirinsect prey and undiscovered strategies await to be revealedSome suspected strategies such as acoustical mimicry needto be documented by laboratory and field studies Experi-mental studies in the field can elucidate some questions aboutbat and insect interactions For example wild gleaning batshunting at familiar sites (Miller and Treat 1993 Faure and Bar-clay 1994) offer unique opportunities to test some hypothe-ses about echolocation behavior and the functions of clicksas interfering or warning signals Employing modern digitalsystems that can reproduce clicks and simulate insect echoeswill assist in such studies

Some questions will be difficult to answer An individualbat can modify at least some of its strategies through learn-ing whereas insect counterstrategies appear through theslower process of natural selection Does this mean insectstrategies lag behind those of their predators Perhaps not Thevariability of an individual insectrsquos antibat behaviors might bea response to the predatorrsquos ability to learn Perhaps theldquoevitabilityrdquo of the preyrsquos behavior (Roeder 1975) makeslearning by the predator less effective

AcknowledgmentsWe thank Raymond CoxOle Naeligsbye Larsen and our students(Vibeke Futtrup Marianne E Jensen Niels Skals) for com-ments on the manuscript We also appreciate the commentsof five anonymous reviewers Our research has been sup-ported by grants from the Danish Natural Sciences ResearchCouncil the Danish National Research Foundation and theCarlsberg Foundation

References citedAcharya L Fenton MB 1992 Echolocation behaviour of vespertilionid bats

(Lasiurus cinereus and Lasiurus borealis) attacking airborne targets in-cluding arctiid moths Canadian Journal of Zoology 70 1292ndash1298

Acharya L McNeil J 1998 Predation risk and mating behavior The re-sponses of moths to batlike ultrasound Behavioral Ecology 9 552ndash558

Ball EE Field LH 1981 Structure of the auditory system of the wetaHemideina crassidens (Blanchard1851) (Orthoptera Ensifera Gryl-lacridoidea Stenopelmantidae) 1 Morphology and histology Cell Tis-sue Res 217 321ndash343

Barclay RMR 1986 The echolocation calls of hoary (Lasiurus cinereus) andsilver-haired (Lasionycteris noctivagans) bats as adaptations for long-versus short-range foraging strategies and the consequences for prey se-lection Canadian Journal of Zoology 64 2700ndash2705

Bates DL Fenton MB 1990 Aposematism or startle Predators learn their re-sponses to the defenses of prey Canadian Journal of Zoology 68 49ndash52

Boyan GS Fullard JH 1986 Interneurones responding to sound in the to-bacco budworm moth Heliothis virescens (Noctuidae) Morphological andphysiological characteristics Journal of Comparative Physiology A Sen-sory Neural and Behavioral Physiology 158 391ndash404

Boyan GS Miller LA 1991 Parallel processing of afferent input by identi-fied interneurones in the auditory pathway of the noctuid moth Noctuapronuba (L) Journal of Comparative PhysiologyA Sensory Neural andBehavioral Physiology 168 727ndash738

Conner WE 1999ldquoUn chant drsquoappel amoureusrdquo Acoustic communicationin moths Journal of Experimental Biology 202 1711ndash1723

Cumming GS 1996 Mantis movements by night and the interactions of sym-patric bats and mantises Canadian Journal of Zoology 74 1771ndash1774

Dunning DC 1968 Warning sounds of moths ZTierpsychol 25 129ndash138Dunning DC Kruumlger M 1996 Predation upon moths by free-foraging Hip-

posideros caffer Journal of Mammalogy 77 708ndash715Eggers F 1919 Das thoracale bitympanale Organ einer Gruppe der Lepi-

doptera Heterocera Zool Jb (Anat) 41 273ndash376Faure PA Barclay RMR 1994 Substrate-gleaning versus aerial-hawking

Plasticity in the foraging and echolocation behaviour of the long-earedbat Myotis evotis Journal of Comparative PhysiologyA Sensory Neuraland Behavioral Physiology 174 651ndash660

Faure PA Hoy RR 2000 Neuroethology of the katydid T-cell II Responsesto acoustic playback of conspecific and predatory signals Journal ofExperimental Biology 203 3243ndash3254

Fenton MB1990 The foraging behaviour and ecology of animal-eating batsCanadian Journal of Zoology 68 411ndash422

Fenton MB Fullard JH 1981 Moth hearing and the feeding strategies of batsAmerican Scientist 69 266ndash275

Forrest TG Read MP Farris HE Hoy RR 1997 A tympanal hearing organin scarab beetles Journal of Experimental Biology 200 601ndash606

Fullard JH 1979 Behavioral analyses of auditory sensitivity in Cycnia ten-era Huumlbner (Lepidoptera Arctiidae) Journal of Comparative Physiol-ogy A Sensory Neural and Behavioral Physiology 129 79ndash83

mdashmdashmdash 1984a Acoustic relationships between tympanate moths and theHawaiian hoary bat (Lasiurus cinereus semotus) Journal of ComparativePhysiology ASensory Neuraland Behavioral Physiology 155 795ndash801

mdashmdashmdash 1984b Listening for bats Pulse repetition rate as a cue for a defen-sive behavior in Cycnia tenera (LepidopteraArctiidae)Journal of Com-parative Physiology A Sensory Neural and Behavioral Physiology 154249ndash252

mdashmdashmdash 1988 The tuning of moth ears Experientia 44 423ndash428mdashmdashmdash 1994Auditory changes in noctuid moths endemic to a bat-free niche

Journal of Evolutionary Biology 7 435ndash445Fullard JH Fenton MB 1977 Acoustic behavioural analyses of the sounds

produced by some species of Nearctic Arctiidae (Lepidoptera)CanadianJournal of Zoology 55 1213ndash1224

Fullard JH Fenton MB Simmons JA 1979 Jamming bat echolocation Theclicks of arctiid moths Canadian Journal of Zoology 57 647ndash649

Fullard JH Simmons JA Saillant PA 1994 Jamming bat echolocation Thedogbane tiger moth Cycnia tenera times its clicks to the terminal attackcalls of the big brown bat Eptesicus fuscus Journal of Experimental Bi-ology 194 285ndash298

Fullard JH Dawson JW Otero LD Surlykke A1997 Bat-deafness in day-fly-ing moths (Lepidoptera Notodontidae Dioptinae) Journal of Com-parative Physiology A Sensory Neural and Behavioral Physiology 181277ndash483

Goumlpfert MC Wasserthal LT 1999 Auditory sensory cells in hawkmoths Iden-tification physiology and structure Journal of Experimental Biology 2021579ndash1587

Hoy RR 1992 The evolution of hearing in insects as an adaptation to pre-dation from batsPages 115ndash129 in Webster DB Fay RR Popper AN edsThe Evolutionary Biology of Hearing New York Springer-Verlag

Hoy RR Nolen T Brodfuehrer P 1989 The neuroethology of acoustic star-tle and escape in flying insects Journal of Experimental Biology 146287ndash306

Jensen ME Miller LA 1999 Echolocation signals of the bat Eptesicus serot-inus recorded using a vertical microphone array Effect of flight altitudeon searching signals Behavioral Ecology and Sociobiology 47 60ndash69

Kennel JV Eggers F 1933 Die abdominalen Tympanalorgane der Lepi-dopteren Zool Jb (Anat) 57 1ndash104

Lakes-Harlan R Heller K-G 1992 Ultrasound-sensitive ears in a parasitoidfly Naturwissenschaften 79 224ndash226

Larsen ON Kleindienst H-UMichelsen A1989 Biophysical aspects of soundreception Pages 364ndash390 in Huber F Moore TELoher W eds Cricket Be-havior and Neurobiology Ithaca (NY) Cornell University Press

580 BioScience July 2001 Vol 51 No 7

Articles

Temporal isolation This is another strategy to avoidbats The Cuculliinae (Noctuidae) include moths that areactive in the winter Several species (eg Lithophane grotei andEupsilia vinulenta) were captured in Massachusetts in No-vember over a 3-week period when snow covered the groundand nightly bat censuses revealed none All captured mothshad functional ears tuned to bat sounds with thresholds as lowas their relatives flying in the summer (Surlykke and Treat1995) A study of hearing in winter-active geometrid mothsgave a similar result (Rydell et al 1997) Apparently noctur-nally active winter moths do not use their hearing even forintraspecific communication Isolated moths retain their ul-trasonic hearing which indicates that it is not very costly evo-lutionarily speaking to retain ears if they provide wintermoths with additional protection such as from the possibil-ity of occasionally overlapping with bats

The nocturnal noctuid moth Rileyana fovea (formerlyThecophora fovea) from Central Europe emerges in late Oc-tober to early November after bat activity has decreased Ri-leyana fovea communicates with ultrasound The males singin flight by scraping the file of the hind tarsus against the foveawhich is an inflated bubble on the hindwing supported by theheavily sclerotized radial vein (Figure 4) The intense sounds(80 dB at 1 m) have peak power around 30 kHz which wouldmake the moths very conspicuous to bats The moths are read-ily eaten by captive bats However by being active at a timeof the year with few bats R fovea can use ultrasound for in-traspecific communication Hence it seems that a completeconversion of hearing from a defensive context to a sexual onehas occurred secondarily in R fovea (Surlykke and Gogala1986) Ultrasound-producing organs have developed inde-pendently in distantly related species of moths that are pro-tected from bats in different ways This suggests that the pre-

existing ear prompted the development of intraspecificacoustic communication in certain moths (Conner 1999Skals and Surlykke 1999)

Some moths have changed to diurnal life a secondaryadaptation perhaps in response to predation by bats Oftendiurnal moths are protected by toxins and warning colors likesome butterflies These day fliers include many tiger moths(Arctiidae) especially from the subfamily Ctenuchinae Onlyrelatively few Noctuidae are day fliers One example is the Aus-tralian whistling moth Hecatesia thyridion (Agaristinae)which is brightly patterned and probably toxic Male whistlingmoths produce sounds that are audible but most of the en-ergy is in the ultrasonic range where their hearing is best Theyuse sounds to defend their territories and to attract females(Surlykke and Fullard 1989) Some diurnal moths are silentand apparently their hearing has no function at all For ex-ample diurnal notodontid moths in the subfamily Dioptinaefrom Venezuela show varying degrees of auditory degenera-tion ranging from almost normal sensitivity in some speciesto very reduced sensitivity especially at ultrasonic frequenciesin other species (Fullard et al 1997) Similarly the diurnalgeometrid Archiearis parthenias is practically deaf to ultrasonicfrequencies (Surlykke et al 1998)

Sound as defenseMany arctiids possess tymbal organs located on the sides ofthe metathorax (Figure 5a Conner 1999) Special musclesbuckle the tymbal membrane generating one click or a burstof clicks per activation cycle (Figure 5b) Click amplitudes varyfrom about 50ndash90 dB SPL measured at 5 cm with maxi-mum sound energy falling between 30 and 80 kHz (Figure 5cFullard and Fenton 1977 Surlykke and Miller 1985) Flyingarctiids may click when they hear the biosonar signals ofbats Thresholds for clicking can be as low as 60ndash75 dB SPLfor simulated search-phase signals (Fullard 1979 Surlykke andMiller 1985) but considerably higher for short signals (about2 ms Fullard 1984b)

Some bats and insects share the same hibernacula andmarauding bats feed on hibernating insects Nymphalid but-terflies sense the vibrations in the substratum as the batcrawls toward it The torpid butterfly opens its wings in a char-acteristic manner which produces intense ultrasonic clicksfrom a special area of the wing membrane (Moslashhl and Miller1976) What purpose do the clicks serve There are threelikely functions of clicking sounds They could startle bats theycould interfere with the batsrsquo biosonar system or they couldwarn bats of a distasteful prey as many arctiid moths containtoxins in their body tissues or in special glands

Startle and interference The clicks of nymphalid but-terflies startle bats and thus provide a chance for the insect toescape However a bat quickly habituates to the sounds andeats these butterflies (Moslashhl and Miller 1976) For experi-enced bats clicks can act as a dinner bellArctiid clicks can star-tle inexperienced and naive bats (Eptesicus fuscus) but thesebats also habituate rapidly (Bates and Fenton 1990 Miller

July 2001 Vol 51 No 7 BioScience 577

Articles

Figure 4 Male stridulatory organ used for the productionof intraspecific communication sounds by the noctuidmoth Rileyana fovea (formerly Thecophora fovea)Sound pulses with carrier frequencies of about 30 kHzare produced by scraping the file on the tarsus of the hindleg against the stridulatory swelling (fovea) on thehindwing Modified from Surlykke and Gogala 1986

1991) Thus clicks must be used sparingly to have survivalvalue as startle signals

The ultrasonic clicks of arctiids might disturb bat biosonarin two ways by simulating multiple targets (Fullard et al1979 1994) and by interfering with range determination(Miller 1991) The arctiid Cycnia tenera produces long trainsof clicks at high rates Fullard et al (1979 1994) hypothesizedthat clicks of C tenera could function as acoustical camou-flage by simulating multiple targets (false echoes) near themoth and thus jam a batrsquos (Eptesicus fuscus) biosonar Theybased their conclusion mainly on the ability of the moth totime its clicking to the terminal phase of the batrsquos signals Milleret al (forthcoming) tested this idea using bats (Pipistrellus pip-istrellus) trained to catch catapulted meal worms after whichnatural click sequences from the arctiid Phragmatobia fulig-inosa were played back during the batsrsquo terminal phase Thebats reacted by increasing the harmonic structure of their ter-minal signals but clicks did not influence the success rate of

prey capture The results suggest that the clicks produced byP fuliginosa do not interfere with the batsrsquo sonar system per-haps because the click rate is too low However in psy-chophysical experiments the clicks from P fuliginosa did in-terfere with the ability of bats (Eptesicus fuscus) to determinerange differences (Miller 1991) When clicks triggered bythe batsrsquo own signals fall repeatedly within a critical time win-dow of about 15 ms before an echo the batrsquos discriminationof range differences deteriorated by as much as 40-fold A sin-gle artificial click placed within the critical window inter-feres with range difference determination (Tougaard et alforthcoming) and with neural responses (Tougaard et al1998) In either case a bat would miss its target if clicks rep-resent false echoes from phantom objects or if they interferewith the batrsquos ranging mechanism

Warning sounds toxins and mimicry Several factspoint to the warning function of clicks as suggested by Dun-ning (1968) The Arctiidae (including the Ctenuchinae) aregenerally unpalatable and arctiids are the only noctuoidmoths that click in response to bat sonar sounds Arctiidclicks could warn the bat of a noxious prey Evidence sup-porting a warning function comes from studies in the labo-ratory and the field In experimental studies bats (Pipistrel-lus pipistrellus and Eptesicus fuscus) habituated to arctiid clickswhen given palatable rewards (Surlykke and Miller 1985Bates and Fenton 1990) However the same bats learned veryquickly to associate moth clicks with a distasteful rewardField studies indicated that bats (Lasiurus sp) foraging aroundstreet lights often aborted their attacks in the approach or ter-minal phase when the prey was the noisy arctiid mothHypoprepia fucosa (Acharya and Fenton 1992) Wild H fucosadid not take visible evasive action to attacking bats Batsavoided more than 90 of the moths released and droppedthe few they captured usually undamaged The bats showedno evidence of habituation although H fucosa were abundantcomposing more than 30 of the moth population Hy-poprepia fucosa has classic warning coloration and patterns as-sociated with toxic species Evidence favors the assumptionthat arctiid clicks are acoustical aposematic signals warningbats that the moths taste bad (Dunning and Kruumlger 1996)

Combining acoustic defenses The startle interferenceand warning hypotheses are not mutually exclusive In areaswhere arctiid moths are scarce the clicks may mostly startlebats Because bats quickly adapt to the clicks a warning func-tion is most likely in areas where arctiid moths are abundantWarning seems especially likely for toxic arctiids like Arctia cajawhich produce few but intense clicks in response to batlikesignals (Surlykke and Miller 1985) At least some species of arc-tiids begin clicking to the searching signals of aerial hawkingbats at distances of about 2ndash4 m (Surlykke and Miller 1985)At these distances the bat should be able to hear the clicks giv-ing an experienced predator ample time to avoid the dis-tasteful prey There is sufficient time for the bat to change itsbehavior even if the warning comes during the approach or

578 BioScience July 2001 Vol 51 No 7

Articles

Figure 5 Arctiid tymbal organ and clicks (a) The tymbalorgan on the lateral surface of the metathoracic segmentof the arctiid Phragmatobia fuliginosa (b) The tymbalorgan produces a burst of clicks each time it buckles (c)The power spectrum of the burst has a maximum atabout 80 kHz (a) Modified from Surlykke and Miller1985 (b) and (c) modified from Miller 1991

terminal phases of the batrsquos pursuit (Acharya and Fenton1992) Should the mothrsquos clicks arrive at the batrsquos ear just be-fore the echoes the batrsquos estimation of range to the preyblurs perhaps causing the bat to miss the target Moths us-ing long trains of click bursts could exploit this strategy Allthree possibilities startle interference and warning offerselective advantages for arctiid moths in addition to thoseprovided by changes in flight behavior

Potential countertactics for batsThe diet of many bats contains very few moths perhaps be-cause of their effective defenses However some barbastelle batsprey almost exclusively on tympanate moths and just how theydo this is not known (Sierro and Arlettaz 1997) Here wepresent some possible double-edged strategies that may ex-plain bat adaptations

Changing signals Echolocating bats announce their pres-ence to all potential prey equipped with auditory bat detec-tors and bats may use different acoustic strategies to reducetheir conspicuousness One strategy would be an adaptationthat moved frequencies of sonar signals out of the rangewhere tympanate insects are most sensitive (Dunning andKruumlger 1996) Some bats use very high frequencies whichmake them less audible to most noctuoid moths Howeversmall moths such as some geometrids (Surlykke and Filskov1997) the pyralid Galleria mellonella (Figure 2b right) andmany tropical noctuoids (Fullard 1988) are quite sensitive tohigh frequencies The attenuation of high frequencies re-duces the useful range of bat sonar so the advantage of thisstrategy may be limited If emission of high frequencies werea countermeasure against tympanate insects one would ex-pect to find bats exploiting this strategy in temperate regionswhere many moths do have poor sensitivity at high frequen-cies (Fullard 1988) The only temperate nongleaning batsthat use relatively high frequencies are small ones (eg Pip-istrellus spp) which detect small prey While the emission ofhigh frequencies may be a response to insect defenses it mayalso be a way to increase resolution and thus increase the abil-ity of bats to detect smaller insects (Surlykke et al 1993)

A second strategy would be for bats to emit very low fre-quencies which would make them less conspicuous to moths(Rydell and Arlettaz 1994) This strategy is employed mostlyby fast-flying bats that hunt aerial insects far from the groundand vegetation (Neuweiler 1989 Fenton 1990) Low fre-quencies increase the batsrsquo range but lower the resolution ofthe batsrsquo biosonar making only large insects detectable (Bar-clay 1986)

A third strategy would be an adaptation for bats to reducethe intensity of their signals Sound intensity is a measure ofsound energy and is proportional to the sound pressure(The dB scale is adapted such that any change in sound pres-sure and the corresponding change in sound intensity resultin the same change in dB value) The advantage would be thatthe sound intensity decreases with the square of the distancebut the echo intensity decreases with the fourth power of the

distance (Surlykke 1988) making the bat less detectable to thetympanate insect We do not know if any bats exploit this strat-egy but we know that all bats studied so far when gleaninguse low-intensity sounds if they emit any signals at all(Neuweiler 1989 Miller and Treat 1993 Faure and Barclay1994) For a gleaning bat the reduction of detection range isprobably not an important restriction because reducingsound intensity gives the additional advantage of reducing clut-ter echoes from the background (see Schnitzler and Kalko2001) In contrast field studies using techniques to calculatethe distance and direction to the bat indicate that at least somebats hunting aerial insects in the open emit intense signals withsource levels up to 125 dB SPL the highest levels yet measured(Jensen and Miller 1999) Also bats that display both glean-ing and aerial-hawking modes of foraging such as for in-stance Myotis evotis (Faure and Barclay 1994) and M septen-trionalis (Miller and Treat 1993) emit high intensities whenhunting flying insects

Finally shorter echolocation signals should be less con-spicuous to prey However shorter signals mean shorterechoes with less energy which are less conspicuous to the batstoo Also short search signals are recorded mainly from batsusing frequency-modulated calls and hunting close to clut-ter (Neuweiler 1989 Fenton 1990) Hencewe believe that shortcalls probably are not a countermeasure against insect hear-ing but rather an adaptation for reducing the overlap betweenechoes from clutter and those from prey

Listening to prey sounds The most effective way for abat to sneak close to tympanate prey is to cease echolocatingaltogether and detect prey using passive sensory cues If theinsects produce sound bats may find them using passivehearing Gleaning bats such as Plecotus auritus and Myotis evo-tis usually have large pinnae (Faure and Barclay 1994) Theyreact with very fast positive phonotaxis to insect-producedsounds such as the sound of wings fluttering or of an insectcrawling on a surface Some gleaning bats emit the full reper-toire of biosonar signals including the terminal phase(Schumm et al 1991) However gleaners generally stop call-ing before the attack and produce no terminal phase(Neuweiler 1989 Faure and Barclay 1994) Whether omissionof the terminal phase reduces the insectrsquos chance of escapingis difficult to say because tympanate insects probably detectecholocating bats long before the terminal phase (Roeder1967a Surlykke et al1999) However omitting the terminalphase may prevent last-chance escape maneuvers (Miller1984) On the other hand sedentary moths stay motionlessor freeze when hearing echolocation signals Turning off thesonar in the final phase may not be a countermeasure againsttympanate insects it may simply be that the bat does not needto continuously update the estimated position of a motion-less insect In contrast the prey of aerial hunters change po-sition continuously in three dimensions thus forcing the batto use its biosonar nearly to the moment of capture

It is difficult to determine if the acoustical adaptations ofbats are responses to constraints of the environment or to the

July 2001 Vol 51 No 7 BioScience 579

Articles

batsrsquo hunting strategies or are intended to overcome insect de-fenses In any case some bat echolocation signals are lessconspicuous to tympanate prey

Concluding remarksThe evolutionary arms race continues between bats and theirinsect prey and undiscovered strategies await to be revealedSome suspected strategies such as acoustical mimicry needto be documented by laboratory and field studies Experi-mental studies in the field can elucidate some questions aboutbat and insect interactions For example wild gleaning batshunting at familiar sites (Miller and Treat 1993 Faure and Bar-clay 1994) offer unique opportunities to test some hypothe-ses about echolocation behavior and the functions of clicksas interfering or warning signals Employing modern digitalsystems that can reproduce clicks and simulate insect echoeswill assist in such studies

Some questions will be difficult to answer An individualbat can modify at least some of its strategies through learn-ing whereas insect counterstrategies appear through theslower process of natural selection Does this mean insectstrategies lag behind those of their predators Perhaps not Thevariability of an individual insectrsquos antibat behaviors might bea response to the predatorrsquos ability to learn Perhaps theldquoevitabilityrdquo of the preyrsquos behavior (Roeder 1975) makeslearning by the predator less effective

AcknowledgmentsWe thank Raymond CoxOle Naeligsbye Larsen and our students(Vibeke Futtrup Marianne E Jensen Niels Skals) for com-ments on the manuscript We also appreciate the commentsof five anonymous reviewers Our research has been sup-ported by grants from the Danish Natural Sciences ResearchCouncil the Danish National Research Foundation and theCarlsberg Foundation

References citedAcharya L Fenton MB 1992 Echolocation behaviour of vespertilionid bats

(Lasiurus cinereus and Lasiurus borealis) attacking airborne targets in-cluding arctiid moths Canadian Journal of Zoology 70 1292ndash1298

Acharya L McNeil J 1998 Predation risk and mating behavior The re-sponses of moths to batlike ultrasound Behavioral Ecology 9 552ndash558

Ball EE Field LH 1981 Structure of the auditory system of the wetaHemideina crassidens (Blanchard1851) (Orthoptera Ensifera Gryl-lacridoidea Stenopelmantidae) 1 Morphology and histology Cell Tis-sue Res 217 321ndash343

Barclay RMR 1986 The echolocation calls of hoary (Lasiurus cinereus) andsilver-haired (Lasionycteris noctivagans) bats as adaptations for long-versus short-range foraging strategies and the consequences for prey se-lection Canadian Journal of Zoology 64 2700ndash2705

Bates DL Fenton MB 1990 Aposematism or startle Predators learn their re-sponses to the defenses of prey Canadian Journal of Zoology 68 49ndash52

Boyan GS Fullard JH 1986 Interneurones responding to sound in the to-bacco budworm moth Heliothis virescens (Noctuidae) Morphological andphysiological characteristics Journal of Comparative Physiology A Sen-sory Neural and Behavioral Physiology 158 391ndash404

Boyan GS Miller LA 1991 Parallel processing of afferent input by identi-fied interneurones in the auditory pathway of the noctuid moth Noctuapronuba (L) Journal of Comparative PhysiologyA Sensory Neural andBehavioral Physiology 168 727ndash738

Conner WE 1999ldquoUn chant drsquoappel amoureusrdquo Acoustic communicationin moths Journal of Experimental Biology 202 1711ndash1723

Cumming GS 1996 Mantis movements by night and the interactions of sym-patric bats and mantises Canadian Journal of Zoology 74 1771ndash1774

Dunning DC 1968 Warning sounds of moths ZTierpsychol 25 129ndash138Dunning DC Kruumlger M 1996 Predation upon moths by free-foraging Hip-

posideros caffer Journal of Mammalogy 77 708ndash715Eggers F 1919 Das thoracale bitympanale Organ einer Gruppe der Lepi-

doptera Heterocera Zool Jb (Anat) 41 273ndash376Faure PA Barclay RMR 1994 Substrate-gleaning versus aerial-hawking

Plasticity in the foraging and echolocation behaviour of the long-earedbat Myotis evotis Journal of Comparative PhysiologyA Sensory Neuraland Behavioral Physiology 174 651ndash660

Faure PA Hoy RR 2000 Neuroethology of the katydid T-cell II Responsesto acoustic playback of conspecific and predatory signals Journal ofExperimental Biology 203 3243ndash3254

Fenton MB1990 The foraging behaviour and ecology of animal-eating batsCanadian Journal of Zoology 68 411ndash422

Fenton MB Fullard JH 1981 Moth hearing and the feeding strategies of batsAmerican Scientist 69 266ndash275

Forrest TG Read MP Farris HE Hoy RR 1997 A tympanal hearing organin scarab beetles Journal of Experimental Biology 200 601ndash606

Fullard JH 1979 Behavioral analyses of auditory sensitivity in Cycnia ten-era Huumlbner (Lepidoptera Arctiidae) Journal of Comparative Physiol-ogy A Sensory Neural and Behavioral Physiology 129 79ndash83

mdashmdashmdash 1984a Acoustic relationships between tympanate moths and theHawaiian hoary bat (Lasiurus cinereus semotus) Journal of ComparativePhysiology ASensory Neuraland Behavioral Physiology 155 795ndash801

mdashmdashmdash 1984b Listening for bats Pulse repetition rate as a cue for a defen-sive behavior in Cycnia tenera (LepidopteraArctiidae)Journal of Com-parative Physiology A Sensory Neural and Behavioral Physiology 154249ndash252

mdashmdashmdash 1988 The tuning of moth ears Experientia 44 423ndash428mdashmdashmdash 1994Auditory changes in noctuid moths endemic to a bat-free niche

Journal of Evolutionary Biology 7 435ndash445Fullard JH Fenton MB 1977 Acoustic behavioural analyses of the sounds

produced by some species of Nearctic Arctiidae (Lepidoptera)CanadianJournal of Zoology 55 1213ndash1224

Fullard JH Fenton MB Simmons JA 1979 Jamming bat echolocation Theclicks of arctiid moths Canadian Journal of Zoology 57 647ndash649

Fullard JH Simmons JA Saillant PA 1994 Jamming bat echolocation Thedogbane tiger moth Cycnia tenera times its clicks to the terminal attackcalls of the big brown bat Eptesicus fuscus Journal of Experimental Bi-ology 194 285ndash298

Fullard JH Dawson JW Otero LD Surlykke A1997 Bat-deafness in day-fly-ing moths (Lepidoptera Notodontidae Dioptinae) Journal of Com-parative Physiology A Sensory Neural and Behavioral Physiology 181277ndash483

Goumlpfert MC Wasserthal LT 1999 Auditory sensory cells in hawkmoths Iden-tification physiology and structure Journal of Experimental Biology 2021579ndash1587

Hoy RR 1992 The evolution of hearing in insects as an adaptation to pre-dation from batsPages 115ndash129 in Webster DB Fay RR Popper AN edsThe Evolutionary Biology of Hearing New York Springer-Verlag

Hoy RR Nolen T Brodfuehrer P 1989 The neuroethology of acoustic star-tle and escape in flying insects Journal of Experimental Biology 146287ndash306

Jensen ME Miller LA 1999 Echolocation signals of the bat Eptesicus serot-inus recorded using a vertical microphone array Effect of flight altitudeon searching signals Behavioral Ecology and Sociobiology 47 60ndash69

Kennel JV Eggers F 1933 Die abdominalen Tympanalorgane der Lepi-dopteren Zool Jb (Anat) 57 1ndash104

Lakes-Harlan R Heller K-G 1992 Ultrasound-sensitive ears in a parasitoidfly Naturwissenschaften 79 224ndash226

Larsen ON Kleindienst H-UMichelsen A1989 Biophysical aspects of soundreception Pages 364ndash390 in Huber F Moore TELoher W eds Cricket Be-havior and Neurobiology Ithaca (NY) Cornell University Press

580 BioScience July 2001 Vol 51 No 7

Articles

1991) Thus clicks must be used sparingly to have survivalvalue as startle signals

The ultrasonic clicks of arctiids might disturb bat biosonarin two ways by simulating multiple targets (Fullard et al1979 1994) and by interfering with range determination(Miller 1991) The arctiid Cycnia tenera produces long trainsof clicks at high rates Fullard et al (1979 1994) hypothesizedthat clicks of C tenera could function as acoustical camou-flage by simulating multiple targets (false echoes) near themoth and thus jam a batrsquos (Eptesicus fuscus) biosonar Theybased their conclusion mainly on the ability of the moth totime its clicking to the terminal phase of the batrsquos signals Milleret al (forthcoming) tested this idea using bats (Pipistrellus pip-istrellus) trained to catch catapulted meal worms after whichnatural click sequences from the arctiid Phragmatobia fulig-inosa were played back during the batsrsquo terminal phase Thebats reacted by increasing the harmonic structure of their ter-minal signals but clicks did not influence the success rate of

prey capture The results suggest that the clicks produced byP fuliginosa do not interfere with the batsrsquo sonar system per-haps because the click rate is too low However in psy-chophysical experiments the clicks from P fuliginosa did in-terfere with the ability of bats (Eptesicus fuscus) to determinerange differences (Miller 1991) When clicks triggered bythe batsrsquo own signals fall repeatedly within a critical time win-dow of about 15 ms before an echo the batrsquos discriminationof range differences deteriorated by as much as 40-fold A sin-gle artificial click placed within the critical window inter-feres with range difference determination (Tougaard et alforthcoming) and with neural responses (Tougaard et al1998) In either case a bat would miss its target if clicks rep-resent false echoes from phantom objects or if they interferewith the batrsquos ranging mechanism

Warning sounds toxins and mimicry Several factspoint to the warning function of clicks as suggested by Dun-ning (1968) The Arctiidae (including the Ctenuchinae) aregenerally unpalatable and arctiids are the only noctuoidmoths that click in response to bat sonar sounds Arctiidclicks could warn the bat of a noxious prey Evidence sup-porting a warning function comes from studies in the labo-ratory and the field In experimental studies bats (Pipistrel-lus pipistrellus and Eptesicus fuscus) habituated to arctiid clickswhen given palatable rewards (Surlykke and Miller 1985Bates and Fenton 1990) However the same bats learned veryquickly to associate moth clicks with a distasteful rewardField studies indicated that bats (Lasiurus sp) foraging aroundstreet lights often aborted their attacks in the approach or ter-minal phase when the prey was the noisy arctiid mothHypoprepia fucosa (Acharya and Fenton 1992) Wild H fucosadid not take visible evasive action to attacking bats Batsavoided more than 90 of the moths released and droppedthe few they captured usually undamaged The bats showedno evidence of habituation although H fucosa were abundantcomposing more than 30 of the moth population Hy-poprepia fucosa has classic warning coloration and patterns as-sociated with toxic species Evidence favors the assumptionthat arctiid clicks are acoustical aposematic signals warningbats that the moths taste bad (Dunning and Kruumlger 1996)

Combining acoustic defenses The startle interferenceand warning hypotheses are not mutually exclusive In areaswhere arctiid moths are scarce the clicks may mostly startlebats Because bats quickly adapt to the clicks a warning func-tion is most likely in areas where arctiid moths are abundantWarning seems especially likely for toxic arctiids like Arctia cajawhich produce few but intense clicks in response to batlikesignals (Surlykke and Miller 1985) At least some species of arc-tiids begin clicking to the searching signals of aerial hawkingbats at distances of about 2ndash4 m (Surlykke and Miller 1985)At these distances the bat should be able to hear the clicks giv-ing an experienced predator ample time to avoid the dis-tasteful prey There is sufficient time for the bat to change itsbehavior even if the warning comes during the approach or

578 BioScience July 2001 Vol 51 No 7

Articles

Figure 5 Arctiid tymbal organ and clicks (a) The tymbalorgan on the lateral surface of the metathoracic segmentof the arctiid Phragmatobia fuliginosa (b) The tymbalorgan produces a burst of clicks each time it buckles (c)The power spectrum of the burst has a maximum atabout 80 kHz (a) Modified from Surlykke and Miller1985 (b) and (c) modified from Miller 1991

terminal phases of the batrsquos pursuit (Acharya and Fenton1992) Should the mothrsquos clicks arrive at the batrsquos ear just be-fore the echoes the batrsquos estimation of range to the preyblurs perhaps causing the bat to miss the target Moths us-ing long trains of click bursts could exploit this strategy Allthree possibilities startle interference and warning offerselective advantages for arctiid moths in addition to thoseprovided by changes in flight behavior

Potential countertactics for batsThe diet of many bats contains very few moths perhaps be-cause of their effective defenses However some barbastelle batsprey almost exclusively on tympanate moths and just how theydo this is not known (Sierro and Arlettaz 1997) Here wepresent some possible double-edged strategies that may ex-plain bat adaptations

Changing signals Echolocating bats announce their pres-ence to all potential prey equipped with auditory bat detec-tors and bats may use different acoustic strategies to reducetheir conspicuousness One strategy would be an adaptationthat moved frequencies of sonar signals out of the rangewhere tympanate insects are most sensitive (Dunning andKruumlger 1996) Some bats use very high frequencies whichmake them less audible to most noctuoid moths Howeversmall moths such as some geometrids (Surlykke and Filskov1997) the pyralid Galleria mellonella (Figure 2b right) andmany tropical noctuoids (Fullard 1988) are quite sensitive tohigh frequencies The attenuation of high frequencies re-duces the useful range of bat sonar so the advantage of thisstrategy may be limited If emission of high frequencies werea countermeasure against tympanate insects one would ex-pect to find bats exploiting this strategy in temperate regionswhere many moths do have poor sensitivity at high frequen-cies (Fullard 1988) The only temperate nongleaning batsthat use relatively high frequencies are small ones (eg Pip-istrellus spp) which detect small prey While the emission ofhigh frequencies may be a response to insect defenses it mayalso be a way to increase resolution and thus increase the abil-ity of bats to detect smaller insects (Surlykke et al 1993)

A second strategy would be for bats to emit very low fre-quencies which would make them less conspicuous to moths(Rydell and Arlettaz 1994) This strategy is employed mostlyby fast-flying bats that hunt aerial insects far from the groundand vegetation (Neuweiler 1989 Fenton 1990) Low fre-quencies increase the batsrsquo range but lower the resolution ofthe batsrsquo biosonar making only large insects detectable (Bar-clay 1986)

A third strategy would be an adaptation for bats to reducethe intensity of their signals Sound intensity is a measure ofsound energy and is proportional to the sound pressure(The dB scale is adapted such that any change in sound pres-sure and the corresponding change in sound intensity resultin the same change in dB value) The advantage would be thatthe sound intensity decreases with the square of the distancebut the echo intensity decreases with the fourth power of the

distance (Surlykke 1988) making the bat less detectable to thetympanate insect We do not know if any bats exploit this strat-egy but we know that all bats studied so far when gleaninguse low-intensity sounds if they emit any signals at all(Neuweiler 1989 Miller and Treat 1993 Faure and Barclay1994) For a gleaning bat the reduction of detection range isprobably not an important restriction because reducingsound intensity gives the additional advantage of reducing clut-ter echoes from the background (see Schnitzler and Kalko2001) In contrast field studies using techniques to calculatethe distance and direction to the bat indicate that at least somebats hunting aerial insects in the open emit intense signals withsource levels up to 125 dB SPL the highest levels yet measured(Jensen and Miller 1999) Also bats that display both glean-ing and aerial-hawking modes of foraging such as for in-stance Myotis evotis (Faure and Barclay 1994) and M septen-trionalis (Miller and Treat 1993) emit high intensities whenhunting flying insects

Finally shorter echolocation signals should be less con-spicuous to prey However shorter signals mean shorterechoes with less energy which are less conspicuous to the batstoo Also short search signals are recorded mainly from batsusing frequency-modulated calls and hunting close to clut-ter (Neuweiler 1989 Fenton 1990) Hencewe believe that shortcalls probably are not a countermeasure against insect hear-ing but rather an adaptation for reducing the overlap betweenechoes from clutter and those from prey

Listening to prey sounds The most effective way for abat to sneak close to tympanate prey is to cease echolocatingaltogether and detect prey using passive sensory cues If theinsects produce sound bats may find them using passivehearing Gleaning bats such as Plecotus auritus and Myotis evo-tis usually have large pinnae (Faure and Barclay 1994) Theyreact with very fast positive phonotaxis to insect-producedsounds such as the sound of wings fluttering or of an insectcrawling on a surface Some gleaning bats emit the full reper-toire of biosonar signals including the terminal phase(Schumm et al 1991) However gleaners generally stop call-ing before the attack and produce no terminal phase(Neuweiler 1989 Faure and Barclay 1994) Whether omissionof the terminal phase reduces the insectrsquos chance of escapingis difficult to say because tympanate insects probably detectecholocating bats long before the terminal phase (Roeder1967a Surlykke et al1999) However omitting the terminalphase may prevent last-chance escape maneuvers (Miller1984) On the other hand sedentary moths stay motionlessor freeze when hearing echolocation signals Turning off thesonar in the final phase may not be a countermeasure againsttympanate insects it may simply be that the bat does not needto continuously update the estimated position of a motion-less insect In contrast the prey of aerial hunters change po-sition continuously in three dimensions thus forcing the batto use its biosonar nearly to the moment of capture

It is difficult to determine if the acoustical adaptations ofbats are responses to constraints of the environment or to the

July 2001 Vol 51 No 7 BioScience 579

Articles

batsrsquo hunting strategies or are intended to overcome insect de-fenses In any case some bat echolocation signals are lessconspicuous to tympanate prey

Concluding remarksThe evolutionary arms race continues between bats and theirinsect prey and undiscovered strategies await to be revealedSome suspected strategies such as acoustical mimicry needto be documented by laboratory and field studies Experi-mental studies in the field can elucidate some questions aboutbat and insect interactions For example wild gleaning batshunting at familiar sites (Miller and Treat 1993 Faure and Bar-clay 1994) offer unique opportunities to test some hypothe-ses about echolocation behavior and the functions of clicksas interfering or warning signals Employing modern digitalsystems that can reproduce clicks and simulate insect echoeswill assist in such studies

Some questions will be difficult to answer An individualbat can modify at least some of its strategies through learn-ing whereas insect counterstrategies appear through theslower process of natural selection Does this mean insectstrategies lag behind those of their predators Perhaps not Thevariability of an individual insectrsquos antibat behaviors might bea response to the predatorrsquos ability to learn Perhaps theldquoevitabilityrdquo of the preyrsquos behavior (Roeder 1975) makeslearning by the predator less effective

AcknowledgmentsWe thank Raymond CoxOle Naeligsbye Larsen and our students(Vibeke Futtrup Marianne E Jensen Niels Skals) for com-ments on the manuscript We also appreciate the commentsof five anonymous reviewers Our research has been sup-ported by grants from the Danish Natural Sciences ResearchCouncil the Danish National Research Foundation and theCarlsberg Foundation

References citedAcharya L Fenton MB 1992 Echolocation behaviour of vespertilionid bats

(Lasiurus cinereus and Lasiurus borealis) attacking airborne targets in-cluding arctiid moths Canadian Journal of Zoology 70 1292ndash1298

Acharya L McNeil J 1998 Predation risk and mating behavior The re-sponses of moths to batlike ultrasound Behavioral Ecology 9 552ndash558

Ball EE Field LH 1981 Structure of the auditory system of the wetaHemideina crassidens (Blanchard1851) (Orthoptera Ensifera Gryl-lacridoidea Stenopelmantidae) 1 Morphology and histology Cell Tis-sue Res 217 321ndash343

Barclay RMR 1986 The echolocation calls of hoary (Lasiurus cinereus) andsilver-haired (Lasionycteris noctivagans) bats as adaptations for long-versus short-range foraging strategies and the consequences for prey se-lection Canadian Journal of Zoology 64 2700ndash2705

Bates DL Fenton MB 1990 Aposematism or startle Predators learn their re-sponses to the defenses of prey Canadian Journal of Zoology 68 49ndash52

Boyan GS Fullard JH 1986 Interneurones responding to sound in the to-bacco budworm moth Heliothis virescens (Noctuidae) Morphological andphysiological characteristics Journal of Comparative Physiology A Sen-sory Neural and Behavioral Physiology 158 391ndash404

Boyan GS Miller LA 1991 Parallel processing of afferent input by identi-fied interneurones in the auditory pathway of the noctuid moth Noctuapronuba (L) Journal of Comparative PhysiologyA Sensory Neural andBehavioral Physiology 168 727ndash738

Conner WE 1999ldquoUn chant drsquoappel amoureusrdquo Acoustic communicationin moths Journal of Experimental Biology 202 1711ndash1723

Cumming GS 1996 Mantis movements by night and the interactions of sym-patric bats and mantises Canadian Journal of Zoology 74 1771ndash1774

Dunning DC 1968 Warning sounds of moths ZTierpsychol 25 129ndash138Dunning DC Kruumlger M 1996 Predation upon moths by free-foraging Hip-

posideros caffer Journal of Mammalogy 77 708ndash715Eggers F 1919 Das thoracale bitympanale Organ einer Gruppe der Lepi-

doptera Heterocera Zool Jb (Anat) 41 273ndash376Faure PA Barclay RMR 1994 Substrate-gleaning versus aerial-hawking

Plasticity in the foraging and echolocation behaviour of the long-earedbat Myotis evotis Journal of Comparative PhysiologyA Sensory Neuraland Behavioral Physiology 174 651ndash660

Faure PA Hoy RR 2000 Neuroethology of the katydid T-cell II Responsesto acoustic playback of conspecific and predatory signals Journal ofExperimental Biology 203 3243ndash3254

Fenton MB1990 The foraging behaviour and ecology of animal-eating batsCanadian Journal of Zoology 68 411ndash422

Fenton MB Fullard JH 1981 Moth hearing and the feeding strategies of batsAmerican Scientist 69 266ndash275

Forrest TG Read MP Farris HE Hoy RR 1997 A tympanal hearing organin scarab beetles Journal of Experimental Biology 200 601ndash606

Fullard JH 1979 Behavioral analyses of auditory sensitivity in Cycnia ten-era Huumlbner (Lepidoptera Arctiidae) Journal of Comparative Physiol-ogy A Sensory Neural and Behavioral Physiology 129 79ndash83

mdashmdashmdash 1984a Acoustic relationships between tympanate moths and theHawaiian hoary bat (Lasiurus cinereus semotus) Journal of ComparativePhysiology ASensory Neuraland Behavioral Physiology 155 795ndash801

mdashmdashmdash 1984b Listening for bats Pulse repetition rate as a cue for a defen-sive behavior in Cycnia tenera (LepidopteraArctiidae)Journal of Com-parative Physiology A Sensory Neural and Behavioral Physiology 154249ndash252

mdashmdashmdash 1988 The tuning of moth ears Experientia 44 423ndash428mdashmdashmdash 1994Auditory changes in noctuid moths endemic to a bat-free niche

Journal of Evolutionary Biology 7 435ndash445Fullard JH Fenton MB 1977 Acoustic behavioural analyses of the sounds

produced by some species of Nearctic Arctiidae (Lepidoptera)CanadianJournal of Zoology 55 1213ndash1224

Fullard JH Fenton MB Simmons JA 1979 Jamming bat echolocation Theclicks of arctiid moths Canadian Journal of Zoology 57 647ndash649

Fullard JH Simmons JA Saillant PA 1994 Jamming bat echolocation Thedogbane tiger moth Cycnia tenera times its clicks to the terminal attackcalls of the big brown bat Eptesicus fuscus Journal of Experimental Bi-ology 194 285ndash298

Fullard JH Dawson JW Otero LD Surlykke A1997 Bat-deafness in day-fly-ing moths (Lepidoptera Notodontidae Dioptinae) Journal of Com-parative Physiology A Sensory Neural and Behavioral Physiology 181277ndash483

Goumlpfert MC Wasserthal LT 1999 Auditory sensory cells in hawkmoths Iden-tification physiology and structure Journal of Experimental Biology 2021579ndash1587

Hoy RR 1992 The evolution of hearing in insects as an adaptation to pre-dation from batsPages 115ndash129 in Webster DB Fay RR Popper AN edsThe Evolutionary Biology of Hearing New York Springer-Verlag

Hoy RR Nolen T Brodfuehrer P 1989 The neuroethology of acoustic star-tle and escape in flying insects Journal of Experimental Biology 146287ndash306

Jensen ME Miller LA 1999 Echolocation signals of the bat Eptesicus serot-inus recorded using a vertical microphone array Effect of flight altitudeon searching signals Behavioral Ecology and Sociobiology 47 60ndash69

Kennel JV Eggers F 1933 Die abdominalen Tympanalorgane der Lepi-dopteren Zool Jb (Anat) 57 1ndash104

Lakes-Harlan R Heller K-G 1992 Ultrasound-sensitive ears in a parasitoidfly Naturwissenschaften 79 224ndash226

Larsen ON Kleindienst H-UMichelsen A1989 Biophysical aspects of soundreception Pages 364ndash390 in Huber F Moore TELoher W eds Cricket Be-havior and Neurobiology Ithaca (NY) Cornell University Press

580 BioScience July 2001 Vol 51 No 7

Articles

terminal phases of the batrsquos pursuit (Acharya and Fenton1992) Should the mothrsquos clicks arrive at the batrsquos ear just be-fore the echoes the batrsquos estimation of range to the preyblurs perhaps causing the bat to miss the target Moths us-ing long trains of click bursts could exploit this strategy Allthree possibilities startle interference and warning offerselective advantages for arctiid moths in addition to thoseprovided by changes in flight behavior

Potential countertactics for batsThe diet of many bats contains very few moths perhaps be-cause of their effective defenses However some barbastelle batsprey almost exclusively on tympanate moths and just how theydo this is not known (Sierro and Arlettaz 1997) Here wepresent some possible double-edged strategies that may ex-plain bat adaptations

Changing signals Echolocating bats announce their pres-ence to all potential prey equipped with auditory bat detec-tors and bats may use different acoustic strategies to reducetheir conspicuousness One strategy would be an adaptationthat moved frequencies of sonar signals out of the rangewhere tympanate insects are most sensitive (Dunning andKruumlger 1996) Some bats use very high frequencies whichmake them less audible to most noctuoid moths Howeversmall moths such as some geometrids (Surlykke and Filskov1997) the pyralid Galleria mellonella (Figure 2b right) andmany tropical noctuoids (Fullard 1988) are quite sensitive tohigh frequencies The attenuation of high frequencies re-duces the useful range of bat sonar so the advantage of thisstrategy may be limited If emission of high frequencies werea countermeasure against tympanate insects one would ex-pect to find bats exploiting this strategy in temperate regionswhere many moths do have poor sensitivity at high frequen-cies (Fullard 1988) The only temperate nongleaning batsthat use relatively high frequencies are small ones (eg Pip-istrellus spp) which detect small prey While the emission ofhigh frequencies may be a response to insect defenses it mayalso be a way to increase resolution and thus increase the abil-ity of bats to detect smaller insects (Surlykke et al 1993)

A second strategy would be for bats to emit very low fre-quencies which would make them less conspicuous to moths(Rydell and Arlettaz 1994) This strategy is employed mostlyby fast-flying bats that hunt aerial insects far from the groundand vegetation (Neuweiler 1989 Fenton 1990) Low fre-quencies increase the batsrsquo range but lower the resolution ofthe batsrsquo biosonar making only large insects detectable (Bar-clay 1986)

A third strategy would be an adaptation for bats to reducethe intensity of their signals Sound intensity is a measure ofsound energy and is proportional to the sound pressure(The dB scale is adapted such that any change in sound pres-sure and the corresponding change in sound intensity resultin the same change in dB value) The advantage would be thatthe sound intensity decreases with the square of the distancebut the echo intensity decreases with the fourth power of the

distance (Surlykke 1988) making the bat less detectable to thetympanate insect We do not know if any bats exploit this strat-egy but we know that all bats studied so far when gleaninguse low-intensity sounds if they emit any signals at all(Neuweiler 1989 Miller and Treat 1993 Faure and Barclay1994) For a gleaning bat the reduction of detection range isprobably not an important restriction because reducingsound intensity gives the additional advantage of reducing clut-ter echoes from the background (see Schnitzler and Kalko2001) In contrast field studies using techniques to calculatethe distance and direction to the bat indicate that at least somebats hunting aerial insects in the open emit intense signals withsource levels up to 125 dB SPL the highest levels yet measured(Jensen and Miller 1999) Also bats that display both glean-ing and aerial-hawking modes of foraging such as for in-stance Myotis evotis (Faure and Barclay 1994) and M septen-trionalis (Miller and Treat 1993) emit high intensities whenhunting flying insects

Finally shorter echolocation signals should be less con-spicuous to prey However shorter signals mean shorterechoes with less energy which are less conspicuous to the batstoo Also short search signals are recorded mainly from batsusing frequency-modulated calls and hunting close to clut-ter (Neuweiler 1989 Fenton 1990) Hencewe believe that shortcalls probably are not a countermeasure against insect hear-ing but rather an adaptation for reducing the overlap betweenechoes from clutter and those from prey

Listening to prey sounds The most effective way for abat to sneak close to tympanate prey is to cease echolocatingaltogether and detect prey using passive sensory cues If theinsects produce sound bats may find them using passivehearing Gleaning bats such as Plecotus auritus and Myotis evo-tis usually have large pinnae (Faure and Barclay 1994) Theyreact with very fast positive phonotaxis to insect-producedsounds such as the sound of wings fluttering or of an insectcrawling on a surface Some gleaning bats emit the full reper-toire of biosonar signals including the terminal phase(Schumm et al 1991) However gleaners generally stop call-ing before the attack and produce no terminal phase(Neuweiler 1989 Faure and Barclay 1994) Whether omissionof the terminal phase reduces the insectrsquos chance of escapingis difficult to say because tympanate insects probably detectecholocating bats long before the terminal phase (Roeder1967a Surlykke et al1999) However omitting the terminalphase may prevent last-chance escape maneuvers (Miller1984) On the other hand sedentary moths stay motionlessor freeze when hearing echolocation signals Turning off thesonar in the final phase may not be a countermeasure againsttympanate insects it may simply be that the bat does not needto continuously update the estimated position of a motion-less insect In contrast the prey of aerial hunters change po-sition continuously in three dimensions thus forcing the batto use its biosonar nearly to the moment of capture

It is difficult to determine if the acoustical adaptations ofbats are responses to constraints of the environment or to the

July 2001 Vol 51 No 7 BioScience 579

Articles

batsrsquo hunting strategies or are intended to overcome insect de-fenses In any case some bat echolocation signals are lessconspicuous to tympanate prey

Concluding remarksThe evolutionary arms race continues between bats and theirinsect prey and undiscovered strategies await to be revealedSome suspected strategies such as acoustical mimicry needto be documented by laboratory and field studies Experi-mental studies in the field can elucidate some questions aboutbat and insect interactions For example wild gleaning batshunting at familiar sites (Miller and Treat 1993 Faure and Bar-clay 1994) offer unique opportunities to test some hypothe-ses about echolocation behavior and the functions of clicksas interfering or warning signals Employing modern digitalsystems that can reproduce clicks and simulate insect echoeswill assist in such studies

Some questions will be difficult to answer An individualbat can modify at least some of its strategies through learn-ing whereas insect counterstrategies appear through theslower process of natural selection Does this mean insectstrategies lag behind those of their predators Perhaps not Thevariability of an individual insectrsquos antibat behaviors might bea response to the predatorrsquos ability to learn Perhaps theldquoevitabilityrdquo of the preyrsquos behavior (Roeder 1975) makeslearning by the predator less effective

AcknowledgmentsWe thank Raymond CoxOle Naeligsbye Larsen and our students(Vibeke Futtrup Marianne E Jensen Niels Skals) for com-ments on the manuscript We also appreciate the commentsof five anonymous reviewers Our research has been sup-ported by grants from the Danish Natural Sciences ResearchCouncil the Danish National Research Foundation and theCarlsberg Foundation

References citedAcharya L Fenton MB 1992 Echolocation behaviour of vespertilionid bats

(Lasiurus cinereus and Lasiurus borealis) attacking airborne targets in-cluding arctiid moths Canadian Journal of Zoology 70 1292ndash1298

Acharya L McNeil J 1998 Predation risk and mating behavior The re-sponses of moths to batlike ultrasound Behavioral Ecology 9 552ndash558

Ball EE Field LH 1981 Structure of the auditory system of the wetaHemideina crassidens (Blanchard1851) (Orthoptera Ensifera Gryl-lacridoidea Stenopelmantidae) 1 Morphology and histology Cell Tis-sue Res 217 321ndash343

Barclay RMR 1986 The echolocation calls of hoary (Lasiurus cinereus) andsilver-haired (Lasionycteris noctivagans) bats as adaptations for long-versus short-range foraging strategies and the consequences for prey se-lection Canadian Journal of Zoology 64 2700ndash2705

Bates DL Fenton MB 1990 Aposematism or startle Predators learn their re-sponses to the defenses of prey Canadian Journal of Zoology 68 49ndash52

Boyan GS Fullard JH 1986 Interneurones responding to sound in the to-bacco budworm moth Heliothis virescens (Noctuidae) Morphological andphysiological characteristics Journal of Comparative Physiology A Sen-sory Neural and Behavioral Physiology 158 391ndash404

Boyan GS Miller LA 1991 Parallel processing of afferent input by identi-fied interneurones in the auditory pathway of the noctuid moth Noctuapronuba (L) Journal of Comparative PhysiologyA Sensory Neural andBehavioral Physiology 168 727ndash738

Conner WE 1999ldquoUn chant drsquoappel amoureusrdquo Acoustic communicationin moths Journal of Experimental Biology 202 1711ndash1723

Cumming GS 1996 Mantis movements by night and the interactions of sym-patric bats and mantises Canadian Journal of Zoology 74 1771ndash1774

Dunning DC 1968 Warning sounds of moths ZTierpsychol 25 129ndash138Dunning DC Kruumlger M 1996 Predation upon moths by free-foraging Hip-

posideros caffer Journal of Mammalogy 77 708ndash715Eggers F 1919 Das thoracale bitympanale Organ einer Gruppe der Lepi-

doptera Heterocera Zool Jb (Anat) 41 273ndash376Faure PA Barclay RMR 1994 Substrate-gleaning versus aerial-hawking

Plasticity in the foraging and echolocation behaviour of the long-earedbat Myotis evotis Journal of Comparative PhysiologyA Sensory Neuraland Behavioral Physiology 174 651ndash660

Faure PA Hoy RR 2000 Neuroethology of the katydid T-cell II Responsesto acoustic playback of conspecific and predatory signals Journal ofExperimental Biology 203 3243ndash3254

Fenton MB1990 The foraging behaviour and ecology of animal-eating batsCanadian Journal of Zoology 68 411ndash422

Fenton MB Fullard JH 1981 Moth hearing and the feeding strategies of batsAmerican Scientist 69 266ndash275

Forrest TG Read MP Farris HE Hoy RR 1997 A tympanal hearing organin scarab beetles Journal of Experimental Biology 200 601ndash606

Fullard JH 1979 Behavioral analyses of auditory sensitivity in Cycnia ten-era Huumlbner (Lepidoptera Arctiidae) Journal of Comparative Physiol-ogy A Sensory Neural and Behavioral Physiology 129 79ndash83

mdashmdashmdash 1984a Acoustic relationships between tympanate moths and theHawaiian hoary bat (Lasiurus cinereus semotus) Journal of ComparativePhysiology ASensory Neuraland Behavioral Physiology 155 795ndash801

mdashmdashmdash 1984b Listening for bats Pulse repetition rate as a cue for a defen-sive behavior in Cycnia tenera (LepidopteraArctiidae)Journal of Com-parative Physiology A Sensory Neural and Behavioral Physiology 154249ndash252

mdashmdashmdash 1988 The tuning of moth ears Experientia 44 423ndash428mdashmdashmdash 1994Auditory changes in noctuid moths endemic to a bat-free niche

Journal of Evolutionary Biology 7 435ndash445Fullard JH Fenton MB 1977 Acoustic behavioural analyses of the sounds

produced by some species of Nearctic Arctiidae (Lepidoptera)CanadianJournal of Zoology 55 1213ndash1224

Fullard JH Fenton MB Simmons JA 1979 Jamming bat echolocation Theclicks of arctiid moths Canadian Journal of Zoology 57 647ndash649

Fullard JH Simmons JA Saillant PA 1994 Jamming bat echolocation Thedogbane tiger moth Cycnia tenera times its clicks to the terminal attackcalls of the big brown bat Eptesicus fuscus Journal of Experimental Bi-ology 194 285ndash298

Fullard JH Dawson JW Otero LD Surlykke A1997 Bat-deafness in day-fly-ing moths (Lepidoptera Notodontidae Dioptinae) Journal of Com-parative Physiology A Sensory Neural and Behavioral Physiology 181277ndash483

Goumlpfert MC Wasserthal LT 1999 Auditory sensory cells in hawkmoths Iden-tification physiology and structure Journal of Experimental Biology 2021579ndash1587

Hoy RR 1992 The evolution of hearing in insects as an adaptation to pre-dation from batsPages 115ndash129 in Webster DB Fay RR Popper AN edsThe Evolutionary Biology of Hearing New York Springer-Verlag

Hoy RR Nolen T Brodfuehrer P 1989 The neuroethology of acoustic star-tle and escape in flying insects Journal of Experimental Biology 146287ndash306

Jensen ME Miller LA 1999 Echolocation signals of the bat Eptesicus serot-inus recorded using a vertical microphone array Effect of flight altitudeon searching signals Behavioral Ecology and Sociobiology 47 60ndash69

Kennel JV Eggers F 1933 Die abdominalen Tympanalorgane der Lepi-dopteren Zool Jb (Anat) 57 1ndash104

Lakes-Harlan R Heller K-G 1992 Ultrasound-sensitive ears in a parasitoidfly Naturwissenschaften 79 224ndash226

Larsen ON Kleindienst H-UMichelsen A1989 Biophysical aspects of soundreception Pages 364ndash390 in Huber F Moore TELoher W eds Cricket Be-havior and Neurobiology Ithaca (NY) Cornell University Press

580 BioScience July 2001 Vol 51 No 7

Articles

batsrsquo hunting strategies or are intended to overcome insect de-fenses In any case some bat echolocation signals are lessconspicuous to tympanate prey

Concluding remarksThe evolutionary arms race continues between bats and theirinsect prey and undiscovered strategies await to be revealedSome suspected strategies such as acoustical mimicry needto be documented by laboratory and field studies Experi-mental studies in the field can elucidate some questions aboutbat and insect interactions For example wild gleaning batshunting at familiar sites (Miller and Treat 1993 Faure and Bar-clay 1994) offer unique opportunities to test some hypothe-ses about echolocation behavior and the functions of clicksas interfering or warning signals Employing modern digitalsystems that can reproduce clicks and simulate insect echoeswill assist in such studies

Some questions will be difficult to answer An individualbat can modify at least some of its strategies through learn-ing whereas insect counterstrategies appear through theslower process of natural selection Does this mean insectstrategies lag behind those of their predators Perhaps not Thevariability of an individual insectrsquos antibat behaviors might bea response to the predatorrsquos ability to learn Perhaps theldquoevitabilityrdquo of the preyrsquos behavior (Roeder 1975) makeslearning by the predator less effective

AcknowledgmentsWe thank Raymond CoxOle Naeligsbye Larsen and our students(Vibeke Futtrup Marianne E Jensen Niels Skals) for com-ments on the manuscript We also appreciate the commentsof five anonymous reviewers Our research has been sup-ported by grants from the Danish Natural Sciences ResearchCouncil the Danish National Research Foundation and theCarlsberg Foundation

References citedAcharya L Fenton MB 1992 Echolocation behaviour of vespertilionid bats

(Lasiurus cinereus and Lasiurus borealis) attacking airborne targets in-cluding arctiid moths Canadian Journal of Zoology 70 1292ndash1298

Acharya L McNeil J 1998 Predation risk and mating behavior The re-sponses of moths to batlike ultrasound Behavioral Ecology 9 552ndash558

Ball EE Field LH 1981 Structure of the auditory system of the wetaHemideina crassidens (Blanchard1851) (Orthoptera Ensifera Gryl-lacridoidea Stenopelmantidae) 1 Morphology and histology Cell Tis-sue Res 217 321ndash343

Barclay RMR 1986 The echolocation calls of hoary (Lasiurus cinereus) andsilver-haired (Lasionycteris noctivagans) bats as adaptations for long-versus short-range foraging strategies and the consequences for prey se-lection Canadian Journal of Zoology 64 2700ndash2705

Bates DL Fenton MB 1990 Aposematism or startle Predators learn their re-sponses to the defenses of prey Canadian Journal of Zoology 68 49ndash52

Boyan GS Fullard JH 1986 Interneurones responding to sound in the to-bacco budworm moth Heliothis virescens (Noctuidae) Morphological andphysiological characteristics Journal of Comparative Physiology A Sen-sory Neural and Behavioral Physiology 158 391ndash404

Boyan GS Miller LA 1991 Parallel processing of afferent input by identi-fied interneurones in the auditory pathway of the noctuid moth Noctuapronuba (L) Journal of Comparative PhysiologyA Sensory Neural andBehavioral Physiology 168 727ndash738

Conner WE 1999ldquoUn chant drsquoappel amoureusrdquo Acoustic communicationin moths Journal of Experimental Biology 202 1711ndash1723

Cumming GS 1996 Mantis movements by night and the interactions of sym-patric bats and mantises Canadian Journal of Zoology 74 1771ndash1774

Dunning DC 1968 Warning sounds of moths ZTierpsychol 25 129ndash138Dunning DC Kruumlger M 1996 Predation upon moths by free-foraging Hip-

posideros caffer Journal of Mammalogy 77 708ndash715Eggers F 1919 Das thoracale bitympanale Organ einer Gruppe der Lepi-

doptera Heterocera Zool Jb (Anat) 41 273ndash376Faure PA Barclay RMR 1994 Substrate-gleaning versus aerial-hawking

Plasticity in the foraging and echolocation behaviour of the long-earedbat Myotis evotis Journal of Comparative PhysiologyA Sensory Neuraland Behavioral Physiology 174 651ndash660

Faure PA Hoy RR 2000 Neuroethology of the katydid T-cell II Responsesto acoustic playback of conspecific and predatory signals Journal ofExperimental Biology 203 3243ndash3254

Fenton MB1990 The foraging behaviour and ecology of animal-eating batsCanadian Journal of Zoology 68 411ndash422

Fenton MB Fullard JH 1981 Moth hearing and the feeding strategies of batsAmerican Scientist 69 266ndash275

Forrest TG Read MP Farris HE Hoy RR 1997 A tympanal hearing organin scarab beetles Journal of Experimental Biology 200 601ndash606

Fullard JH 1979 Behavioral analyses of auditory sensitivity in Cycnia ten-era Huumlbner (Lepidoptera Arctiidae) Journal of Comparative Physiol-ogy A Sensory Neural and Behavioral Physiology 129 79ndash83

mdashmdashmdash 1984a Acoustic relationships between tympanate moths and theHawaiian hoary bat (Lasiurus cinereus semotus) Journal of ComparativePhysiology ASensory Neuraland Behavioral Physiology 155 795ndash801

mdashmdashmdash 1984b Listening for bats Pulse repetition rate as a cue for a defen-sive behavior in Cycnia tenera (LepidopteraArctiidae)Journal of Com-parative Physiology A Sensory Neural and Behavioral Physiology 154249ndash252

mdashmdashmdash 1988 The tuning of moth ears Experientia 44 423ndash428mdashmdashmdash 1994Auditory changes in noctuid moths endemic to a bat-free niche

Journal of Evolutionary Biology 7 435ndash445Fullard JH Fenton MB 1977 Acoustic behavioural analyses of the sounds

produced by some species of Nearctic Arctiidae (Lepidoptera)CanadianJournal of Zoology 55 1213ndash1224

Fullard JH Fenton MB Simmons JA 1979 Jamming bat echolocation Theclicks of arctiid moths Canadian Journal of Zoology 57 647ndash649

Fullard JH Simmons JA Saillant PA 1994 Jamming bat echolocation Thedogbane tiger moth Cycnia tenera times its clicks to the terminal attackcalls of the big brown bat Eptesicus fuscus Journal of Experimental Bi-ology 194 285ndash298

Fullard JH Dawson JW Otero LD Surlykke A1997 Bat-deafness in day-fly-ing moths (Lepidoptera Notodontidae Dioptinae) Journal of Com-parative Physiology A Sensory Neural and Behavioral Physiology 181277ndash483

Goumlpfert MC Wasserthal LT 1999 Auditory sensory cells in hawkmoths Iden-tification physiology and structure Journal of Experimental Biology 2021579ndash1587

Hoy RR 1992 The evolution of hearing in insects as an adaptation to pre-dation from batsPages 115ndash129 in Webster DB Fay RR Popper AN edsThe Evolutionary Biology of Hearing New York Springer-Verlag

Hoy RR Nolen T Brodfuehrer P 1989 The neuroethology of acoustic star-tle and escape in flying insects Journal of Experimental Biology 146287ndash306

Jensen ME Miller LA 1999 Echolocation signals of the bat Eptesicus serot-inus recorded using a vertical microphone array Effect of flight altitudeon searching signals Behavioral Ecology and Sociobiology 47 60ndash69

Kennel JV Eggers F 1933 Die abdominalen Tympanalorgane der Lepi-dopteren Zool Jb (Anat) 57 1ndash104

Lakes-Harlan R Heller K-G 1992 Ultrasound-sensitive ears in a parasitoidfly Naturwissenschaften 79 224ndash226

Larsen ON Kleindienst H-UMichelsen A1989 Biophysical aspects of soundreception Pages 364ndash390 in Huber F Moore TELoher W eds Cricket Be-havior and Neurobiology Ithaca (NY) Cornell University Press

580 BioScience July 2001 Vol 51 No 7

Articles

Madsen BM Miller LA 1987 Auditory input to motor neurons of the dor-sal longitudinal flight muscles in a noctuid moth (Barathra brassica L)Journal of Comparative Physiology A Sensory Neural and BehavioralPhysiology 160 23ndash31

Mason AC Forrest TG Hoy RR 1998 Hearing in mole crickets (OrthopteraGryllotalpidae) at sonic and ultrasonic frequencies Journal of Experi-mental Biology 201 1967ndash1979

Miller LA 1975 The behaviour of flying green lacewings Chrysopa carneain the presence of ultrasound Journal of Insect Physiology 21 205ndash219

mdashmdashmdash 1982 The orientation and evasive behavior of insects to bat criesPages 393ndash405 in Addink ADF Spronk N eds Exogenous and Endoge-nous Influences on Metabolic and Neural Control Oxford (UK) Perg-amon

mdashmdashmdash 1984 Hearing in green lacewings and their responses to the cries ofbats Pages 134ndash149 in Canard M Seacutemeacuteria Y eds Biology of Chrysopi-dae The Hague Dr W Junk Publishers

mdashmdashmdash 1991 Arctiid moth clicks can degrade the accuracy of range differ-ence discrimination in echolocating big brown bats Eptesicus fuscusJournal of Comparative Physiology A Sensory Neural and BehavioralPhysiology 168 571ndash579

Miller LA Olesen J 1979 Avoidance behavior in green lacewings I Behav-ior of free flying green lacewings to hunting bats and ultrasound Jour-nal of Comparative Physiology A Sensory Neural and Behavioral Phys-iology 131 113ndash120

Miller LA Treat AE 1993 Field recording of echolocation and social signalsfrom the gleaning bat Myotis septentrionalis Bioacoustics 5 67ndash87

Miller LA Futtrup V Dunning DC Forthcoming How extrinsic sounds in-terfere with bat biosonar In Thomas JA Moss CF Vater M eds Echolo-cation in Bats and Dolphins Chicago University of Chicago Press

Minet J Surlykke A 2002 Sound producing and auditory organs Chap 11in Kristensen NP ed Lepidoptera Moths and Butterflies Vol 2 Mor-phology and Physiology Handbook of ZoologyHandbuch der Zoolo-gie IV 35 Berlin Walter de Gruyter

Moslashhl B Miller LA 1976 Ultrasonic clicks produced by the peacock butter-fly A possible bat-repellent mechanism Journal of Experimental Biol-ogy 64 639ndash644

Neuweiler G 1989 Foraging ecology and audition in echolocating batsTrends in Ecology and Evolution 4 160ndash166

Northcott MA Fullard JH 1996 The closed-loop nature of the tymbal re-sponse in the dogbane tiger moth Cycnia tenera (LepidopteraArctiidae)Brain Behavior and Evolution 48 130ndash136

Popov AV Shuvalov VF 1977 Phonotactic behaviour of crickets Journal ofComparative Physiology A Sensory Neural and Behavioral Physiology119 111ndash126

Popov AV Michelsen ALewis B1994 Changes in the mechanics of the cricketear during the early days of adult life Journal of Comparative Physiol-ogy A Sensory Neural and Behavioral Physiology 175 165ndash170

Robert D 1989 The auditory behaviour of flying locusts Journal of Exper-imental Biology 147 279ndash301

Robert D Amoroso J Hoy RR 1992 The evolutionary convergence of hear-ing in a parasitoid fly and its cricket host Science 258 1135ndash1137

Roeder KD 1964 Aspects of the noctuid tympanic nerve response havingsignificance in the avoidance of bats Journal of Insect Physiology 10529ndash546

mdashmdashmdash 1967a Nerve Cells and Insect Behavior Rev ed Cambridge (MA)Harvard University Press

mdashmdashmdash 1967b Turning tendency of moths exposed to ultrasound while instationary flight Journal of Insect Physiology 13 873ndash888

mdashmdashmdash 1975 Neural factors and evitability in insect behavior Journal of Ex-perimental Zoology 194 75ndash88

Roeder KD Treat AE Vande Berg JS 1970 Distal lobe of the pilifer An ul-trasonic receptor in Choerocampine hawkmoths Science 170 1098ndash1099

Roumlmer H Marquart V Hardt M 1988 Organization of a sensory neuropilein the auditory pathway of two groups of Orthoptera Journal of Com-parative Neurology 275 201ndash215

Rydell J Arlettaz R 1994 Low-frequency echolocation enables the batTadarida teniotis to feed on tympanate insects Proceedings of the RoyalSociety of London B 257 175ndash178

Rydell J Skals N Surlykke A Svensson M 1997 Hearing and bat defence ingeometrid winter moths Proceedings of the Royal Society of London B264 83ndash88

Rydell J Roininen H Philip KW 2000 Persistence of bat defence reactionsin high Arctic moths (Lepidoptera)Proceedings of the Royal Society ofLondon B 267 553ndash557

Schnitzler H-U Kalko EKV 2001 Echolocation by insect-eating bats Bio-Science 51 557ndash569

Schumm A Krull D Neuweiler G 1991 Echolocation in the notch-eared batMyotis emarginatus Behavioral Ecology and Sociobiology 28 255ndash261

Schwabe J 1906 Beitrage zur Morphologie und Histologie der tympanalenSinnesapparate der Orthopteren Zool Jb (Anat) 20 no 50 1ndash154

Sierro AArlettaz R 1997 Barbastelle bats (Barbestella spp) specialize in thepredation of moths Implications for foraging tactics and conservationActa Ecologica 18 91ndash106

Skals N Surlykke A 1999 Sound production by abdominal tymbal organsin two moth species The Green Silver-line and the Scarce Silver-line (Noc-tuoidea NolidaeChloephorinae) Journal of Experimental Biology 2022937ndash2949

mdashmdashmdash 2000 Hearing and evasive behaviour in the greater wax moth Gal-leria mellonella (Pyralidae) Physiological Entomology 251 354ndash362

Spangler HG Takessian A 1983 Sound perception by two species of waxmoths (Lepidoptera Pyralidae)Annals of the Entomological Society ofAmerica 76 94ndash97

Surlykke A 1986 Moth hearing on the Faeroe Islands an area without batsPhysiological Entomology 11 221ndash225

mdashmdashmdash 1988 Interaction between echolocating bats and their prey Pages551ndash566 in Nachtigall PE Moore PWB eds Animal Sonar Processes andPerformance New York Plenum Press

Surlykke A Filskov M 1997 Hearing in geometrid moths Naturwis-senschaften 84 356ndash359

Surlykke A Fullard JH 1989 Hearing of the Australian whistling mothHecatesia thyridion Naturwissenschaften 76 132ndash134

Surlykke A Gogala M 1986 Stridulation and hearing in the noctuid mothThecophora fovea (Tr) Journal of Comparative Physiology A SensoryNeural and Behavioral Physiology 159 267ndash273

Surlykke A Miller LA 1985 The influence of arctiid moth clicks on bat echolo-cation Jamming or warning Journal of Comparative Physiology ASensory Neural and Behavioral Physiology 156 831ndash843

Surlykke A Treat AE 1995 Hearing in winter moths Naturwissenschaften82 382ndash384

Surlykke A Miller LA Moslashhl B Andersen BB Christensen-Dalsgaard J Joslashr-gensen MB 1993 Echolocation in two very small bats from ThailandCraseonycteris thonglongyai and Myotis siligorensis Behavioral EcologySociobiology 33 1ndash12

Surlykke A Skals N Rydell J Svensson M 1998 Sonic hearing in a diurnalgeometrid moth Archiearis parthenias temporally isolated from batsNaturwissenschaften 85 36ndash37

Surlykke A Filskov M Fullard JH Forrest E 1999 Auditory relationships tosize in noctuid moths Bigger is better Naturwissenschaften 86 238ndash241

Tougaard J Casseday JH Covey E 1998 Arctiid moths and bat echolocationBroad-band clicks interfere with neural responses to auditory stimuli inthe nuclei of the lateral lemniscus of the big brown bat Journal of Com-parative Physiology A Sensory Neural and Behavioral Physiology 182203ndash215

Tougaard J Miller LA Simmons JA Forthcoming The role of arctiid mothclicks in defense against echolocating bats Interference with temporal pro-cessing In Thomas JA Moss CF Vater M eds Echolocation in Bats andDolphins Chicago University of Chicago Press

Yack JE Fullard JH 2000 Ultrasonic hearing in nocturnal butterflies Nature403 265ndash266

Yager DD 1999 Structure developmentand evolution of insect auditory sys-tems Microscopy Research and Technique 47 380ndash400

Yager DD Hoy RR 1986 The cyclopean ear A new sense for the praying man-tis Science 231 727ndash729

Yager DD Cook AP Pearson DL Spangler HG 2000 A comparative studyof ultrasound-triggered behaviour in tiger beetles (Cicindelidae) Jour-nal of Zoology London 251 355ndash368

July 2001 Vol 51 No 7 BioScience 581

Articles