interspecific responses to distress calls in bats (chiroptera: vespertilionidae): a function for...

ANIMAL BEHAVIOUR, 2004, 67, 1005e1014doi:10.1016/j.anbehav.2003.09.003

ARTICLES

Interspecific responses to distress calls in bats

(Chiroptera: Vespertilionidae): a function for

convergence in call design?

J . M. RUSS*, G. JONES†, I . J . MACKIE* & P. A. RACEY*

*Department of Zoology, University of Aberdeen

ySchool of Biological Sciences, University of Bristol

(Received 25 April 2003; initial acceptance 13 June 2003;

final acceptance 7 September 2003; MS. number: 7697)

Distress calls were recorded from three sympatric species of pipistrelle bat (Pipistrellus nathusii, P. pipistrellusand P. pygmaeus) in England and Northern Ireland. At foraging sites, we conducted playback experiments,consisting of experimental distress call sequences from each species and control sequences of randomnoise and sound recorded with no bats present. We measured response by simultaneously recordingultrasound during playbacks and counting the echolocation pulses above a predetermined thresholdwhich were then identified to species. All three species responded to each other’s calls. The number ofrecorded echolocation pulses of all species increased eight-fold, on average, during the playback of distresscall sequences compared with the playback of ultrasonic noise, and four-fold compared with the playbackof silence. In a separate playback experiment, the number of echolocation pulses of P. pygmaeus increased14-fold during the playback of distress calls of four endemic species of bat from Madagascar (Emballonuraatrata, Myotis goudoti, Miniopterus majori and M. manavi) compared with the playback of silence. Thisincreased response might have been caused by the high calling rates of the Malagasy species. Distress callsof P. nathusii, P. pipistrellus and P. pygmaeus were structurally convergent, consisting of a series ofdownward-sweeping, frequency-modulated elements of short duration and high intensity with a relativelystrong harmonic content. Selection may favour convergence in the structure of distress calls among batspecies, if attracting heterospecifics increases the chance of repelling predators by mobbing.

� 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Distress calls are vocalizations of animals in situations ofextreme distress. Such situations usually involve beingphysically constrained in some way, such as attacked bya predator (Hogstedt 1983; Davis 1991; Koenig et al.1991), caught in a trap (Avery et al. 1984; Russ et al. 1998)or held by an experimenter (e.g. Stefanski & Falls 1972a, b;Bremond & Aubin 1990).The distress calls of birds have been particularly well

described and a number of hypotheses have been putforward to explain their function. Distress calls may (1)startle a predator into releasing its prey or attract asecondary predator to scare off the original predator(Driver & Humphries 1969; Perrone 1980; Hogstedt1983; Conover 1994), (2) warn other individuals of the

Correspondence: J. M. Russ, Department of Zoology, University ofAberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, U.K. (email:[email protected]). G. Jones is at the School of Biological Sciences,University of Bristol, Woodland Road, Bristol BS8 1UG, U.K.

1000003e3472/03/$30.00/0 � 2004 The Association

presence of a predator (Inglis et al. 1982; Koenig et al.1991), (3) provide other individuals with informationabout a predator and thus reduce the chance of thoseindividuals falling prey to a predator in the future(Conover & Perito 1981; Conover 1987, 1994), (4) requestaid from kin or reciprocal altruists (Stefanski & Falls 1972a,b; Rohwer et al. 1976) or (5) attract other individuals thatwill mob a predator which may in turn facilitate thecaller’s escape (Inglis et al. 1982; Neudorf & Sealy 2002).Conover (1994) pointed out that these functions are notmutually exclusive and distress calls may have more thanone function.Few studies have investigated the distress calls of bats.

Intraspecific responses to both caged individuals and toa loudspeaker emitting distress calls have been recordedfor the vespertilionid bats Myotis lucifugus (Fenton et al.1976; Avery et al. 1984) and Pipistrellus pygmaeus (Russet al. 1998). Russ et al. (1998) showed that P. pygmaeusrespond to the distress calls of unrelated conspecifics, thus

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ANIMAL BEHAVIOUR, 67, 61006

rejecting the hypothesis that distress calls request aid fromkin, and concluded that such calls probably function inattracting conspecifics that performmobbing behaviour asan antipredator response. Some authors have observedinterspecific responses to the distress calls of bats. Forexample, bat species of the same family respond to thereal or simulated distress calls of the phyllostomid bat,Artibeus jamaicensis (August 1979; Ryan et al. 1985), andTuttle (1976) found that the distress calls of small batsattract larger bats as well as those of the same size as thecaller. August (1979) suggested that responding to distresscalls may function in scaring a potential predator awayfrom a foraging site; it would benefit all bats that forage inthe area to respond, as there would be per capita reductionin the probability of being taken by a predator. Thisobservation has been frequently reported for bird species(e.g. Marler 1957; Hurd 1996).Among avian species, distress calls are notably similar in

structure (Hogstedt 1983; Jurisevic & Sanderson 1998),generally consisting of short, repeated bursts of soundcovering a wide range of frequencies, characteristics thatincrease the effective distance (Marten &Marler 1977) andlocalization of the call (Marler 1955; Knudsen 1980).Marler (1957) suggested that if distress calls effect a changein a predator, thereby deterring predation, and passerineswithin a particular area are threatened by the samepredators, then an evolutionary convergence in thestructure of distress calls would be expected. Morton(1977, 1982) proposed a set of motivation-structural rules,which govern the physical structure of acoustic commu-nication in birds and mammals and predict interspecificconvergence in call structure for acoustic signals of similarfunction. The rules predict that friendly or nonaggressivevocalizations are characterized by pure tones of high orlow frequency, whereas fear is expressed with increasinglyhigher frequency tonal sounds and aggression is expressedwith increasingly lower frequencies consisting of harsh orbroadband sound. Intermediate frequencies and band-widths indicate conflicting motivational levels. In addi-tion, a downward-modulated frequency sweep signalsslightly greater aggressiveness whereas an upward-modu-lated sweep signals less aggressiveness. Where fear orappeasement and aggression are interacting, such as whenan animal is in distress, signals should be broadband ornoisy and generally rise in frequency (kHz).We aimed to test the following hypotheses: (1) distress

calls of P. nathusii, P. pipistrellus and P. pygmaeus arestructurally similar; (2) distress call structure does not varybetween individuals; (3) P. nathusii, P. pipistrellus andP. pygmaeus respond to each other’s distress calls; and(4) pipistrelle bats are attracted to the distress calls ofgeographically isolated species.

METHODS

During AprileJune 2002, we caught female pipistrelle bats(Pipistrellus pipistrellus: Jones & Barratt 1999; P. pygmaeus:Jones & Barratt 1999; Anon. 2003; P. nathusii) in hand netsat maternity colonies in southwest England and NorthernIreland in areas in which they occur sympatrically. TwoP. nathusii and three P. pygmaeus roosts were located in Co.

Antrim, Northern Ireland and six P. pipistrellus and fourP. pygmaeus roosts were located in the counties of Avon,Somerset and Gloucestershire, England. We assignedcolonies to species by recording echolocation pulses ofemerging bats (e.g. Jones & van Parijs 1993; Vaughan et al.1997) and identified caught individuals by morphologicalmeasurements (Yalden 1985; Haussler et al. 1999; Senderet al. 2002; von Helversen & Holderied 2003). A total of 31P. nathusii, 40 P. pipistrellus and 64 P. pygmaeus were caughtunder licence from English Nature and The Environment& Heritage Service (Northern Ireland).

Distress Call Sequences and Sonagraphic Analysis

We recorded vocalizations via the high-frequency out-put of a Pettersson D-980 bat detector (PetterssonElektronik AB, Uppsala, Sweden) connected to a laptopcomputer incorporating a DAQCard-6062E high-speeddata acquisition card (National Instruments Corporation,Austin, Texas, U.S.A.). The frequency response of themicrophone was G5 dB between 20 and 120 kHz (D. A.Waters, unpublished data). Signals were acquired ata sample rate of 200 kHz and a sample size of 12 bitsand subsequently stored as a ‘wav’ (PCM) file using thesoftware program Avisoft-RECORDER (Avisoft, Berlin,Germany). To encourage calling, bats were held in thehand and their lower back was gently massaged. Thedistance between the bat and the microphone wasapproximately 0.5 m. Morphological measurements (fore-arm length, length of fifth digit, mass) were recorded withcallipers (G0.1 mm) and a Pesola spring balance (G0.1 g)and the individual was then released.

Sound intensity levels of eight bats of each species wereobtained with a Bruel & Kjaer 2209 sound pressure levelmeter (Bruel & Kjaer, Naerum, Denmark) and Bruel &Kjaer 4939 microphone (frequency response: G2 dB,4e100 kHz) connected to the high-speed data acquisitioncard. All intensity levels are based on peak-to-peak read-ings at a reference distance of 10 cm (Møhl 1988) and werecalculated with Avisoft-SASLAB Pro version 4.3 (Avisoft).

We selected distress call sequences of 45 individuals (15P. nathusii, 15 P. pipistrellus and 15 P. pygmaeus) foranalysis. We used calls with good signal to noise ratiosand avoided those with clipped waveforms and interfer-ence from background monitor ‘whine’ and the batteryDC converter. Ten calls were randomly selected from eachindividual and were analysed with Avisoft-SASLAB Proversion 4.3. In all instances a Fast Fourier Transform size of512 and a temporal overlap of 87.5% was used, givinga frequency resolution of 391 Hz and a reading accuracy of0.32 ms. All time (ms) and frequency (kHz) measurementswere obtained from the sonagram and included thenumber of elements (Elements), the frequency containingmaximum energy of each element (FmaxE), the start,centre and end frequencies of each element (Sfreq, Cfreqand Efreq, respectively), the duration of each element(Dur) and the interpulse interval from the start of oneelement to the start of the next element (IPI). Start andend frequencies were determined with an amplitudecriterion in SASLAB Pro. Centre frequency was calculatedas ðSfreq� EfreqÞ=2. The duty cycle index (pulses/s;

RUSS ET AL.: RESPONSES TO BAT DISTRESS CALLS 1007

Dcycle) was based on a randomly selected 10-s section ofeach recorded call sequence. Frequency measurementswere taken from the fundamental harmonic.

Response to Playback of Distress Calls

We selected the distress call sequences of nine individ-uals of each species (27 in total) as experimental sequencesfor playback experiments. We used Avisoft-SASLAB Pro toensure call sequences were of similar amplitude and toremove unwanted echolocation signals from the sequen-ces. Nine 2-min sequences were assembled, each consist-ing of three 15-s treatment sequences of bat distress calls(PNx, PPx, PYx where PNZ P. nathusii, PPZ P. pipistrellus,PYZ P. pygmaeus and x is an integer identifying theindividual) and two 15-s control sequences consisting ofsound recorded with no bats present (S) and randomlygenerated noise (R) each separated by 7.5 s of silence (I).Randomly generated noise consisted of pink noise(spectral frequency of 1/f ) plus randomly generated tonesbetween 10 Hz and 100 kHz which were subsequentlyrandomly shuffled and reversed. The overall intensity ofrandom noise was 118 dB SPL. Thus a typical 2-minsequence can be represented by I-PY1-I-S-I-PN5-I-PP9-I-R-I.Each distress call sequence of an individual bat was usedonly once over the nine 2-min sequences and on any onenight the order of control and experimental sequenceswithin each 2-min sequence was random, as was the orderof playback of the nine 2-min sequences.We carried out playback experiments during May and

June 2002 at foraging sites in the southwest of England inwhich at least two of the three species were known toforage (J. Russ, personal observation). Recorded calls werebroadcast through an ultrasound loudspeaker (S56, UltraSound Advice, London, U.K., frequency response:G3.5 dB, 20e120 kHz) via an amplifier (S55, Ultra SoundAdvice) using the output of the high-speed data acquisi-tion card. Playback of the nine 2-min control/experimen-tal sequences, which was carried out once each night,began approximately 1 h after dusk. The 2-min sequenceswere preceded and followed by 2-min of silence. Theexperiment was carried out over 26 nights. To obtaina level of activity of responding bats, we placed a micro-phone (D-980 bat detector) about 0.5 m from theloudspeaker and simultaneously recorded the echoloca-tion pulses of responding bats and the experimental andcontrol signals emitted by the loudspeaker. The gain of themicrophone was set to the same level each night, as wasthe gain of the amplifier. The intensity of playback calls(XG SE; P. nathusii: 119:4G0:4 dB SPL; P. pipistrellus:119:4G0:2 dB SPL; P. pygmaeus: 122:3G0:6 dB SPL; basedon a single call from 10 individuals of each species) wassimilar to that of live bats (see Results).We defined a positive response as an increase in the

number of recorded echolocation pulses during theplayback of experimental sound indicating that (1) therewere more bats within the vicinity of the loudspeaker, (2)a bat was approaching the loudspeaker and thereforeincreasing its repetition rate and/or (3) an individual hadoriented itself towards the loudspeaker. From the record-ings made during playback, we identified responding bats

to species based on their echolocation signals (Jones & vanParijs 1993; Vaughan et al. 1997) and counted separateecholocation pulses occurring above a predeterminedintensity threshold level during playback of experimentaland control sequences to obtain an index of bat activity.Echolocation pulses occurring during the 7.5 s of gapsilence (I) were ignored.We performed an additional playback experiment, using

the equipment and methods outlined above but withdistress calls obtained in 1999 from four endemic speciesof bats from Madagascar (Emballonura atrata, Myotisgoudoti, Miniopterus majori and M. manavi). As only shortcall sequences were recorded in the field, consisting ofa maximum of three calls from each individual, we loopedcalls to create longer sequences for playback, whichtherefore had high calling rates. Sequences consisting offour 30-s sequences of experimental sound (distress calls)and one 30-s sequence of control sound (recorded with nobats present) were played back with a 1-min intervalbetween experimental or control periods. Experimentalsound consisted of a single multicomponent distress callrepeated for 30 s. Playbacks were performed at 14 foragingsites on different nights. Only data for respondingP. pygmaeus are presented, as there were insufficient datafor P. nathusii or P. pipistrellus.During both playback experiments, we looked out for

potential predators but none were noted.

Statistical Analysis

Analysis of variances (ANOVAs) and multivariate anal-yses of variance (MANOVAs), with ‘individual’ nestedwithin ‘species’ were conducted to determine intra- andinterspecific differences in the structure of distress calls.Multivariate discriminant analyses were carried out on themeasured parameters: the first analysis classified individ-uals to species and three further analyses classified calls toindividual. We carried out three separate repeated meas-ures ANOVAs for each responding species, with night asthe repeated measure, to establish differences in theresponse of bats to the different playback stimuli. Analyseswere carried out with Minitab v13 statistical software.Means are givenG SE.

RESULTS

Of the 135 bats caught, 97% of P. nathusii, 50% ofP. pipistrellus and 95% of P. pygmaeus gave distress callswhile physically restrained. Distress calls of all specieswere of similar structure and consisted of a high-intensity,downward frequency-modulated sweep of short durationusually repeated in rapid succession with a strong har-monic content (Fig. 1).

Inter- and Intraspecific Differences in Call Structure

There were significant differences in the number ofelements within each call and the frequencies and durationof individual elements between species (Table 1). Distresscalls of P. pygmaeus contained more components than calls


Figure 1. Sonagrams, oscillograms and power spectra of typical single element and multiple element distress calls from (a) P. nathusii,

(b) P. pipistrellus and (c) P. pygmaeus.

of either P. nathusii or P. pipistrellus. Individual distress callelements were longer with longer interpulse intervals for P.nathusii. Start and end frequencies of individual callcomponents for P. pygmaeus were significantly higher thanthose of P. nathusii which were significantly higher thanthose of P. pipistrellus. However, the centre frequency andthe frequency containing maximum energy were signifi-cantly higher only for P. pygmaeus. There was a significantdifference in duty cycle index between species (F2;44 ¼ 4:21,P!0:05) with post hoc tests revealing that it wassignificantly higher in P. pygmaeus than in P. pipistrellus

and P. nathusii. Themean call intensity was similar for eachspecies (P. nathusii: 118:7G1:0 dB SPL; P. pipistrellus:118:3G1:1 dB SPL; P. pygmaeus: 117:9G0:4 dB SPL).

The frequency containing maximum energy for eachseparate element within a distress call increased with timeacross elements for each species (Fig. 2a), from 21:2G0:6 kHz (first element) to 27:9G2:0 kHz (seventh ele-ment) for P. nathusii (regression: F1;94 ¼ 7:52, R2 ¼ 0:321,P!0:0001, FmaxE ¼ 1:35!Elementþ 18:61), from21:3G0:9 kHz (first element) to 21:7G0:8 kHz (seventhelement) for P. pipistrellus (regression: F1;80 ¼ 45:41, R2 ¼


Table 1. Distress call parameters of P. nathusii, P. pipistrellus and P. pygmaeus

Parametery P. nathusii P. pipistrellus P. pygmaeus

Species

F2,405

Individual

Call VCEF42,405 VCEz

Elements 3.51G0.14 3.61G0.17 4.93G0.29x 17.36* 3.36* 0.62 0.38FmaxE 22.2G0.3 22.2G0.4 28.2G0.5x 115.99* 14.33* 0.54 0.46Cfreq 21.6G0.3 20.5G0.4 26.7G0.5x 147.54* 12.71* 0.41 0.59Efreq 19.7G0.3x 17.80G0.4x 23.0G0.5x 148.94* 12.37* 0.57 0.43Sfreq 27.6G0.4x 25.7G0.8x 32.5G0.6x 54.05* 7.90* 0.54 0.46IPI 8.43G0.38x 7.47G0.28 7.40G0.17 15.38* 10.24* 0.53 0.47Dur 4.36G0.23x 2.40G0.11 2.09G0.10 151.73* 17.62* 0.19 0.81Dcycle 14.30G1.46 13.76G3.10 25.38G4.35x d d d

Data are means and standard errors of mean values (based on number of elements) of 10 calls from 15 bats of each species (N ¼ 150). F valuesare nested ANOVAs on each parameter. *P !0:001.yParameters are defined in the Methods.zVCE is the added variance component estimate, showing the proportion of added variance explained by the differences between individuals,and between calls within individuals.xSignificant difference between values for the other two species.

0:064, P!0:01, FmaxE ¼ 0:321!Elementþ 20:18) andfrom 26:7G1:2 kHz (first element) to 39:4G5:6 kHz(13th element) for P. pygmaeus (regression: F1;140 ¼ 67:25,R2 ¼ 0:321, P!0:0001, FmaxE ¼ 0:95!Elementþ 24:98).However, although the result for P. pipistrellus is significant,the precision of the analysis tool (frequency resolu-tion = 390 Hz) is coarser than the average difference of theextreme data points.For all species, the duration of each individual element

generally increased and then decreased across elements,with the longest duration for P. nathusii and P. pipistrellusbeing the fourth element (4:94G0:60 ms and 2:88G0:34 ms, respectively) and the longest duration forP. pygmaeus being the fifth element (2:48G0:35ms;Fig. 2b).

A MANOVA with ‘individual’ nested within ‘species’including all call parameters measured showed thatdistress calls differed significantly between individuals(Wilk’s l ¼ 0:009, P!0:001) and between species(Wilk’s l ¼ 0:116, P!0:001). Added variance compo-nent estimates for each parameter (Table 1) showedthat, on average, over all the parameters, 49% of thecall variation was explained by differences betweenindividuals and 51% by differences between calls. Alinear discriminant analysis on all the parametersmeasured (Elements, Sfreq, Cfreq, Efreq, FmaxE, Dur,IPI) classified 78.2% of P. nathusii calls correctly, 87.7%of calls of P. pipistrellus correctly and 62.3% of calls ofP. pygmaeus correctly. Discriminant analyses classified36.9% of calls to the correct individual for P. nathusii,

0 1 2 3 4 5 6 7 8 9 10 11 12 130

1

2

3

4

5

6(b)

P. nathusiiP. pipistrellusP. pygmaeus

Du

rati

on (

ms)

Element

20

30

40

50(a)

Fmax

E (k

Hz)

Figure 2. Variation in (a) the frequency containing maximum energy (FmaxE) and (b) duration between separate elements of the distress calls

of P. nathusii, P. pipistrellus and P. pygmaeus. Error bars represent SEs.


43.1% of calls to the correct individual for P. pipistrellus and40.6% of calls to the correct individual for P. pygmaeus.

Relation Between Morphological andAcoustic Parameters

There were no significant correlations between any ofthe measured acoustic and morphological parameters forP. nathusii. However, there were significant negativecorrelations between mass and acoustic parameters forP. pipistrellus and between forearm and fifth digit lengthand acoustic parameters for P. pygmaeus (Table 2).

Responses to Playback Experiments

Bats at foraging sites responded almost immediately tothe playback of distress calls by swooping down towardsthe loudspeaker or appearing to deviate slightly from theiroriginal flight path.Significantly more echolocation pulses of P. nathusii,

P. pipistrellus and P. pygmaeus were recorded during play-back of distress calls (all species) than during playback ofcontrol sound (repeated measures ANOVA: F4;29 ¼ 6:597,P!0:001; F4;29 ¼ 9:426, P!0:0001; F4;29 ¼ 25:060, P!0:0001, respectively; Fig. 3aec). However, in all cases,there were no differences in the number of echolocationpulses recorded during playback of distress calls (allspecies) between species. For responding P. nathusii therewas a 15-fold increase in the mean number of echoloca-tion pulses recorded during the playback of distress calls(experimental) compared with the playback of randomultrasound (control) and a seven-fold increase comparedwith the playback of silence (control; Fisher’s PLSD posthoc test). Similarly, for responding P. pipistrellus there wasa five-fold and three-fold increase, respectively, and forresponding P. pygmaeus there was a four-fold and two-foldincrease, respectively (Fisher’s PLSD post hoc test). Overall,this amounted to an eight-fold increase compared with theplayback of ultrasound and a four-fold increase comparedwith the playback of silence. Significantlymore P. pygmaeusecholocation pulses were recorded during playback ofsilence than during the playback of random noise (Fisher’sPLSD post hoc test).

There was an overall mean 14-fold increase in thenumber of echolocation pulses of P. pygmaeus recordedduring the playback of distress calls of bats fromMadagascar compared to playback of silence (repeatedmeasures ANOVA: F4;3 ¼ 312:238, P!0:0001; Fig. 4). Thenumber of echolocation pulses differed between nights(repeated measures ANOVA: F4;42 ¼ 77:339, P!0:0001).There was also an interaction effect between night andplayback sequence (experimental/control; repeated mea-sures ANOVA: F56;42 ¼ 50:828, P!0:0001).

DISCUSSION

Distress calls are a type of assembly call that causedispersed receivers to move towards an isolated sender(Bradbury & Vehrencamp 1998). Call design for distressshould, therefore, be optimized for localization. Thedistress calls of P. nathusii, P. pipistrellus and P. pygmaeusconsisted of a series of downward-sweeping, frequency-modulated elements of short duration and high intensitywith a relatively strong harmonic content. In addition,elements within calls increased, then decreased in dura-tion and increased in frequency with time. To estimatea signaller’s location, a receiver must estimate its directionand range. One way to enhance localization (direction) ofan acoustic signal in the presence of scattering orturbulence is to include highly repetitive amplitude andfrequency modulation (Wiley & Richards 1982). This issupported by the many studies that have reported thatbirds are able to locate broadband signals easier than puretones (e.g. Shalter & Schleidt 1977; Knudsen & Konishi1979). A receiver may judge a signaller’s range by usingcues from processes of attenuation and degradation(Griffin & Hopkins 1974; Wiley & Richards 1978). Theuse of reverberations for estimating range is easiest if thesignal includes a variety of repetition rates of a givenfrequency (Wiley & Richards 1982). These structuralmodifications are clearly present in the distress calls ofthe pipistrelle species we studied.

High-frequency sounds are more directional (Kinsler &Frey 1962) and have high attenuation with distance thanlow-frequency sounds (Morton1975; Surlykke1988;Romer& Lewald 1992). Consequently, distress calls should beoptimized for long-distance communication and be of low

Table 2. Spearman rank correlations between morphological parameters and acoustic parameters of pipistrelle distress calls

P. pipistrellus P. pygmaeus All species

Element FmaxE Efreq Element FmaxE Efreq Element FmaxE Efreq

Forearm (mm)r �0.100 0.251 0.173 �0.543 �0.135 �0.054 �0.250 �0.382 �0.126P 0.733 0.387 0.555 !0.05 0.632 0.848 0.102 !0.05 0.415

Mass (g)r 0.083 �0.668 �0.652 �0.355 �0.530 �0.484 �0.317 �0.577 �0.378P 0.808 !0.05 !0.05 0.213 0.051 0.079 !0.05 !0.01 !0.05

Fifth digit (mm)r �0.145 0.023 �0.145 �0.649 �0.791 �0.767 �0.345 �0.485 �0.335P 0.621 0.939 0.620 !0.05 !0.01 !0.01 !0.05 !0.01 !0.05


SRSRSR

(c)

No.

of

ech

oloc

atio

n p

uls

es (

lg)

Silence Random noise P. nathusii P. pipistrellus P. pygmaeus

R

S

SRSRSR

Control/Treatment

(b)

SR

SRSR

(a)

0.01

0.1

1

10

0.1

1

10

100

0.01

0.1

1

10

Figure 3. Responses, in termsof the number of recorded echolocationpulses, of (a) P. nathusii, (b) P. pipistrellus and (c) P. pygmaeus to playbackofeachother’s distress calls, playbackof control soundandplaybackof silence. R indicates a significantdifference compared to theplaybackof control

sound and S indicates a significant difference compared to the playback of silence based on Fisher’s PLSD post hoc tests. Error bars represent SEs.

frequency. The distress signals of pipistrelle bats in thepresent study ranged from about 17 kHz to about 33 kHz(primarily ultrasonic components, O20 kHz). In birds, apositive correlation exists between sound frequency andbody size (mass and length; e.g. Wallschlager 1980;Bowman 1983; Ryan & Brenowitz 1985; Jurisevic &Sanderson1998;Neudorf& Sealy 2002),which is attributedto thicker syringeal membranes in larger species. In echo-locating bats, there is also a correlation between the domi-nant frequency of echolocation signals and body mass,with smaller bats producing echolocation calls of higherfrequency than larger bats (Jones 1999). We found a nega-tive correlation between morphological measurementsand the dominant frequencies in distress calls within thethree species of pipistrelle bats studied and there was also

a similar trend between species. Therefore, in much thesame way as in birds, the size of the vocal cords in bats (andindeed all mammals) dictates the range of frequencies thata bat can produce. Pipistrelle bats produce echolocationpulses in the range of 40e100 kHz with dominant frequen-cies occurring at around 40 kHz (P. nathusii), 46 kHz(P. pipistrellus) and 55 kHz (P. pygmaeus) (Jones & van Parijs1993; Vaughan et al 1997). Presumably, therefore, thedominant frequency of distress calls is at the lower endof the bat’s frequency range and represents an adaptationto maximize long-distance communication in thesespecies.Our results support our first hypothesis that distress

calls of the three species studied are structurally similar.They also support Morton’s (1977, 1982) proposals that


distress signals should be broadband or noisy in structureand show an overall rise in frequency. Structural similar-ities can also be seen in the distress calls of the bats fromMadagascar used in our playback experiments (Fig. 5).August (1985) observed similarities between the distress

Silence EA MG MMJ MMN0.1

1

10

100

No.

of

ech

oloc

atio

n p

uls

es (

lg)

Control/Treatment

Figure 4. Responses, in terms of the number of recorded echolo-

cation pulses, of P. pygmaeus to the playback of the distress calls offour endemic species of bat from Madagascar (EA: Emballonura

atrata; MG: Myotis goudoti; MMJ: Miniopterus majori and MMN:

Miniopterus manavi) and silence. Error bars represent SEs.

calls of A. jamaicensis and P. hastatus and Fenton et al.(1976) commented on similarities between distress calls inM. lucifugus and E. fuscus. Several authors have demon-strated convergence in distress call structure for birds(Marler 1955; Jurisevic & Sanderson 1998; Neudorf &Sealy 2002).

However, we also observed differences in measuredparameters between species. Interspecific differences incall structure could theoretically be attributed to distresscalls playing a role in species recognition, a commonfeature of many vocal signals. For example, Barlow & Jones(1997) found significant structural differences in theadvertisement calls of two cryptic species of pipistrelle.However, calls used in mate choice are expected to bespecies specific to allow mate recognition (Marler 1967;Bradbury 1977)whereas it would seem that distress calls aredesigned to elicit interspecific responses and we failed tofind differences in responses between species. It is possible,therefore, that differences in distress call structure betweenspecies may arise from morphological differences. We alsorejected our second hypothesis that distress calls do notdiffer structurally between individuals, although classifica-tion based on discriminant analyses was relatively weak.

Our results support our third hypothesis that P. nathusii,P. pipistrellus and P. pygmaeus respond to each other’s calls.August (1979) reported similar findings with A. jamaicensisand P. hastatus and hypothesized that it would benefitdifferent species of bat to respond if they shared the sameforaging site and therefore the same predators, as is widely

Figure 5. Sonagrams, oscillograms and power spectra of typical distress calls of (a) Emballonura atrata, (b) Myotis goudoti, (c) Miniopterusmajori and (d) Miniopterus manavi.


reported for bird studies (Marler 1967, 1969; Stefanski &Falls 1972a). Aubin & Bremond (1989) and Aubin (1990)suggested that, for birds, these reactions may be a result ofacoustic similarities between vocalizations of differentspecies and similarities in the process of recognition of thesignal sent. Marler (1957) suggested that if mobbing calls(distress calls) effect a change in a predator, therebydeterring predation, and passerines within a particulararea are menaced by the same predators, then anevolutionary convergence in the structure of mobbingcalls would be expected. Support for our fourth hypoth-esis, that pipistrelle bats are attracted to the distress calls ofgeographically isolated species probably not sharing thesame predators, would suggest that it is likely that conver-gence in signal design and therefore interspecific responseis more likely to be primarily related to structural-motivation rules and the optimization of distress callsfor localization.Driver & Humphries (1969) suggested that distress calls

in birds may startle a predator into releasing its prey. Ourresults suggest that it is unlikely that pipistrelle distresscalls are designed to startle avian predators, as the overallminimum frequency in the bats’ calls is about 17 kHz.Jurisevic & Sanderson (2000) have shown that Australianraptors have a hearing range extending from lowfrequencies (0.25 kHz or less) to around 10 kHz, withmost raptors unresponsive to sounds above 12 kHz, andbarn owls, Tyto alba, have a high-frequency cutoff at about12.5 kHz (Dooling 1982). However, felids and somemustelids have both been known to prey on batsopportunistically and both have hearing ranges wellabove 17 kHz (e.g. Felis catus: 45e64000 kHz; Mustelaputorius furo: 16e44000 Hz: Fay 1988).Hogstedt (1983) and Koenig et al. (1991) hypothesized

that distress calls may attract another predator which mayscare off the attacking predator. In our playback experi-ments totalling almost 4 h of continual distress callplayback, we saw no potential predator at any of theforaging sites. However, further work examining theresponse of such predators to the playback of distresscalls is required. Russ et al. (1998) rejected the hypothesisthat distress calls function to increase the fitness of kin byshowing that bats from different colonies (and thusunrelated individuals) responded to each other’s distresscalls and concluded that distress calls probably function inattracting conspecifics which perform mobbing behaviouras an antipredator response. It is likely that distress callselicit help, therefore, from reciprocal altruists, which isfacilitated by the fact that pipistrelle bats form stablesocial groups. We have extended Russ et al.’s (1998) studyby demonstrating that three congeners respond to eachother’s calls and that one of these species, P. pygmaeus,responds to calls of bats endemic to a different geo-graphical area and from different genera.

Acknowledgments

J.M.R. was supported by a Royal Society Research Grantand a Leverhulme Trust Research Grant F/00152/D toP.A.R. We are grateful to M. B. Fenton, B. Siemers and an

anonymous referee for helpful comments on the manu-script. We thank the Avon, Somerset and Wiltshire BatGroups for their assistance in locating maternity roosts,Bristol Water for permission to work on their land, MarkBriffa for statistical advice and Raimund Specht forsoftware support.

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