Adaptive echolocation behavior in bats for the analysis of auditory scenes

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1 9 The Journl of Experimentl Biology, 9- Pulished y The Compny of Biologists 9 doi:./je.7 Adptive eholotion ehvior in ts for the nlysis of uditory senes Chen Chiu*, Wei Xin nd Cynthi F. Moss Deprtment of Psyhology, Neurosiene nd Cognitive Siene Progrm, University of Mrylnd, College Prk, MD 7, USA *Author for orrespondene (e-mil: hiu@umd.edu) Aepted Ferury 9 SUMMARY Eholoting ts emit sonr pulses nd listen to returning ehoes to proe their surroundings. Bts dpt their eholotion ll design to ope with dynmi hnges in the ousti environment, inluding hitt hnge or the presene of nery onspeifis/heterospeifis. Seven pirs of ig rown ts, Eptesius fusus, were tested in this study to exmine how they djusted their eholotion lls when flying nd ompeting with onspeifi for food. Results showed tht differenes in five ll prmeters, strt/end frequenies, durtion, ndwidth nd sweep rte, signifintly inresed in the two-t ondition ompred with the seline dt. In ddition, the mgnitude of spetrl seprtion of lls ws negtively orrelted with the seline ll design differenes in individul ts. Bts with smll seline ll frequeny differenes showed lrger inreses in ll frequeny seprtion when pired thn those with lrge seline ll frequeny differenes, suggesting tht ts tively hnge their sonr ll struture if pre-existing differenes in ll design re smll. Cll design djustments were lso influened y physil sping etween two ts. Clls of pired ts exhiited the lrgest design seprtions when inter-t distne ws shorter thn. m, nd the seprtion deresed s the sping inresed. All individuls modified t lest one seline ll prmeter in response to the presene of nother onspeifi. We propose tht dissimilrity etween the time frequeny fetures of sonr lls produed y different ts ids eh individul in segregting ehoes of its own sonr voliztions from the ousti signls of neighoring ts. Key words: ts, eholotion, dptive vol ehvior, flexiility, ll design, uditory sene nlysis, onspeifis. INTRODUCTION Auditory sene nlysis is the proess tht llows listeners to segment, integrte nd segregte sounds in omplex ousti environment into meningful strems (Bregmn, 99; Hulse, ). For exmple, when sentene spoken y one person, together with kground noise from the environment, rrives t listener s er, the listener must proess the ousti signls, integrte meningful segments nd seprte these sounds from kground noise. The ility to nlyze uditory senes is exhiited y humns nd other niml speies, suh s irds nd frogs, whih rely hevily on ousti ommunition (Hulse, ). Bregmn provides numerous exmples demonstrting tht humn listener n seprte nd identify uditory ojets y listening to differenes in the pith, timre, melody nd temporl pttern of sound sequene (Bregmn, 99). Auditory signls tht fll in different frequeny nds, for exmple, n provide ue for humn listener to segregte sounds into seprte uditory strems. A listener tends to segregte ousti signls with lrge frequeny differenes into seprte uditory strems, nd to group those with smll differenes in frequeny into the sme uditory strem (Crlyon, ; Drwins, 997; Moore nd Gokel, ). Spetrl or temporl ues used y humn listeners n e pplied to the understnding of uditory sene nlysis in niml models s well. Previous studies hve demonstrted tht frequeny seprtions nd differenes in temporl ptterns of ousti stimuli re importnt ftors tht ffet uditory strem segregtion in fish, nurns nd irds. Goldfish n segregte two sequenes of pulses ording to the differenes in repetition rtes nd spetrl fetures (Fy, 99; Fy, ). Seprtion in spetrl fetures of voliztions nd ll timing re ruil ftors tht ffet ousti ehvior in frogs (Frris et l., ; Greenfield nd Rnd, ; Nrins, 99; Shwrtz, 99) nd irds (Hulse et l., 997; Wisniewsky nd Hulse, 997). It is prtiulrly importnt for eholoting ts to pereive nd interpret uditory senes, euse they generte sonr pulses nd listen to the fetures of ehoes refleted from ojets to pereive their surroundings. Their ility to orient, pture prey nd void ostles ll depend on orretly grouping nd segregting ehoes from sonr trgets in omplex environment nd on differentiting their own lls/ehoes from those produed y other ts in their surroundings. Bkground noise nd lls/ehoes from other nimls my influene t s pereption of uditory ojets. Pst studies hve reported tht ts modify the spetrl temporl fetures of their voliztions in response to the presene of onspeifis. Field reordings hve shown tht ts flying in groups produe lls with different frequenies nd/or temporl ptterns thn those flying lone (Orist, 99; Ulnovsky et l., ). A plyk experiment showed tht Tdrid rsiliensis rised the end frequeny of the frequeny modulted (FM) sweep in response to plyk jmming signls, whose frequenies were equl to the verge end frequenies of this speies sonr lls (Gillm et l., 7). It hs een hypothesized tht the t modifies its ll design in order to void interferene from the voliztions of onspeifis nd improve loliztion of uditory ojets. Most studies of eholotion ehvior in the presene of onspeifis hve een onduted in the field nd lk reords of the -D positions of the ts nd ll design hnges in identified individuls. Differenes in ll design mesured in most previous studies ould hve een evoked y the presene of onspeifis ut

2 Vol djustment in eholoting ts 9 ould lso hve een pre-existing inter-individul differenes prior to the introdution of onspeifis. Only one study so fr hs demonstrted shift of the t s ll frequeny in response to the rodst of jmming signls in unidentified ts in the field (Gillm et l., 7). We pired ts in lrge flight room, presented single prey item nd reorded eh t s eholotion lls efore (seline) nd during (two-t) piring. Reordings from ultrsound-sensitive mirophones nd high-speed stereo video enled us to trk voliztions nd flight trjetories in individul ts. We hypothesize tht ts djust fetures of their eholotion lls when flying in the sme ir spe in order to nlyze uditory senes nd void signl jmming. This leds us to predit tht the mount of ll modifition my e relted to the similrity in seline ll design of individul ts, the reltive position etween pired ts nd the timing of suessive voliztions. We report here the first detiled study to ddress hnges in sonr ll design of identified free-flying eholoting ts in response to volizing onspeifis. Results of this study extend our understnding of the eholoting t s tive vol ontrol in the nlysis of uditory senes. MATERIALS AND METHODS Animls We studied the vol ehvior of eight ig rown ts, Eptesius fusus Beuvois, nd dt from seven pirs re reported in the present study. Bts were olleted from different regions in Mrylnd (olletion permit #SCO ) nd kept in ptivity t the University of Mrylnd, College Prk, MD, USA. The niml housing fility mintined reltively stle temperture ( C) nd humidity ( %). The light/drk yle in the room ws reversed y h to ensure tht ts were t their most tive periods during the ehviorl experiment. The mss of eh t ws etween nd g, typil of n dult ig rown t. All niml re nd experimentl proedures were pproved y the Institutionl Animl Cre nd Use Committee t the University of Mrylnd, College Prk, MD, USA. Experimentl setup All eight ts were first trined to fly nd pture tethered melworm Tenerio molitor Linneus in lrge nehoi flight room (7.m) (L W H) equipped with synhronized udio nd high-speed stereo video equipment. After eh t rehed the suess pture rte of %, we egn to reord its eholotion lls nd flight pths. During dt reording, only long-wvelength lighting (> nm) ws ville, preventing the t from using visul ues to lolize the trget nd onspeifis (Hope nd Bhtngr, 979). Bts were tested in two experimentl onditions, seline nd twot onditions, with trils per dy in eh ondition. Bseline dt were reorded when t flew nd ptured tethered melworm lone in the room. Two-t dt were olleted when pired ts flew nd ompeted to pture single tethered melworm. Pired ts were relesed simultneously from the sme spot in the flight room nd the relesing spot ws lwys the sme in seline nd two-t onditions. Bseline nd two-t dt were reorded on different test dys. Ten trils per dy over four test dys were reorded in the seline ondition, yielding t lest seline trils for eh t. Fifteen trils per dy over minimum of three test dys, yielding t lest two-t trils per t pir, were reorded in the two-t ondition fter ompletely finishing olleting seline dt. Between nd trils per individul/pir with high-qulity udio nd video reordings from eh ondition were seleted for further nlysis. Dt reordings Audio dt were reorded with three ultrsound-sensitive mirophones (UltrSound Advie, London, UK) on the floor, nd video dt were reorded with two high-speed digitl video mers (Kodk MotionCorder Anlyzer, Model, frmess ; Sn Diego, CA, USA) mounted in two djent orners of the flight room, permitting the -D reonstrution of the t s flight pth. The frequeny response of ll three mirophones ws flt within ± db for frequenies etween 9 khz. The sensitivity dropped y db for frequenies etween 9 nd khz. An eight seond irulting uffer of udio nd video reordings ws end-triggered synhronously y the investigtor when the t mde ontt with the tethered worm in eh tril. The udio nd video dt from eh tril were nlyzed off-line using two ustom MATLAB progrms (Mthworks, Ntik, MA, USA) (see elow). Dt nlysis A ustom MATLAB progrm ws used to nlyze udio dt, nd five prmeters were pplied to hrterize the ll design of n FM sonr voliztion. These five prmeters re durtion (ms), ndwidth (khz), strt nd end frequenies of the FM sweep (khz) nd sweep rte (khzms ), ll tken from the fundmentl. Sweep rte is lulted y dividing ndwidth y durtion nd desries the slope of the FM ll. Dt nlysis of video reordings ws omplished y digitizing the position of eh t nd mirophone nd reonstruting the -D flight pth vi nother ustom MATLAB progrm. Dt nlysis for udio reording in the two-t ondition ws different from the one-t ondition, euse the ultrsoundsensitive mirophones on the floor reorded the voliztions from oth ts, nd it ws neessry to ssoite given eholotion ll with the individul t tht produed it. For the two-t ondition, we first visully inspeted ll eholotion lls in the three udio reording hnnels, nd ssigned lls mnully to eh t ording to differenes in signture using the sme ustom MATLAB progrm employed to nlyze the seline udio dt. Eh ll s onset times in two different mirophones were mrked in order to lulte the tul udio dely (Fig.). Beuse the mirophones were positioned t different lotions in the room, ll tht ws produed y t would reh these mirophones t different times. The tul udio dely of one ll refers to the differene of the reorded signl s onset time etween two mirophones. The position of these two mirophones nd pired ts were lredy estlished y video dt nlysis. The estimted udio dely ws omputed y mesuring the distne of eh t to the mirophones nd estimting the ousti signl trvel time differenes of the lls t eh of these mirophones. When we ssigned given ll to the volizing individul, we onfirmed tht the tul nd estimted udio delys were the sme. Therefore, y ompring the vlues of tul nd estimted udio dely, we ould unmiguously ssoite eh eholotion ll to the t tht volized. Detiled nlysis methods re reported in Chiu et l. (Chiu et l., ). RESULTS Cll design modifitions y one t to inrese the differenes etween its voliztions nd those of onspeifis flying in proximity ould serve s strtegy to void signl jmming. Sequentil lls mde y different ts in pir were nlyzed to determine if the fetures of one t s voliztions re influened y losely timed lls of nother onspeifi. In the present study we investigted possile ftors driving ll modifitions, inluding

3 9 C. Chiu, W. Xin nd C. F. Moss t = d. Mirophone Bt vol time Mirophone T T seline differenes in ll design nd sptil seprtion etween ts. Seprtion in ll design during piring (two-t ondition) ws lso ompred with ll design differenes etween the two ts efore piring (seline ondition) to determine if the signl seprtion in the two-t ondition ws the onsequene of nother t s presene. Anlysis of seline dt reveled tht some ts hve more similr ll designs when they flew lone; therefore, we studied whether or not the similrity in seline ll design ould predit ll djustments when individuls were pired. The effet of inter-t sping on sonr ll djustments is lso exmined in this study. Anlysis of sequentil lls produed y pired ts The most ommon flight ehvior of pired ts in this study ws following flight, whih is defined s one t flying ehind the other t nd oth ts heding towrd similr diretion (the ngle etween pired ts hedings is ute). Aout % of the time in this study one t followed the other one, % of the time two ts flew towrd eh other nd nother % of the time ts flew wy from eh other (Chiu et l., ). Individul ts usully showed differenes in ll design nd these differenes my e used to void ll interferene from neighoring onspeifis. Fig. shows the flight trjetories, reltive positions nd ll design mesurements of eh t in pir from two seleted trils. One t ws following nother t in the first exmple nd grdully shortened its distne to the other niml (Fig. A,B). The seprtion in strt frequeny etween the sonr lls of pired ts inresed s the inter-t distne deresed. Smll seprtions were oserved in their sonr ll end frequenies, nd hnges in the inter-t sping did not pper relted to these seprtions. These two ts mintined smll seprtion in ll durtion nd sweep rte ut the seprtion lso did not hnge with inter-t sping. Bts in the seond exmple were flying lmost in prllel t the eginning of the t = d. Fig.. Illustrtion of ssignment of eholotion lls to individul ts. The sound speed is. m s ; T nd T is the onset time of reorded lls t mirophone nd, respetively; t nd t is the signl trvel time from the t to mirophones nd, respetively, whih re estimted from video reordings; d nd d is the distne etween t nd mirophone nd, respetively. Atul udio dely is lulted from udio reordings nd is equl to T T. Estimted udio dely is lulted from video reordings nd is equl to t t. Vlues of rel udio dely nd estimted udio dely re the sme if one ll ws orretly ssigned to the volizing t. segment nd susequently one t fell ehind the other t efore their flight pths diverged (Fig. C,D). These two ts mintined smll mount of seprtion in ll frequeny s they flew in lose proximity. Seprtion in ll durtion ws similr to tht in the first exmple ut seprtions in ll sweep rte were smller thn those in exmple No.. This exmple does not show ny systemti inrese in ll design seprtion with deresing inter-t distne ut ll the dt presented ome from distnes of less thn m. The exmples ove suggest tht differenes in ll design etween two ts sometimes ourred only in short period of time when the ts flew lose together. Bt eholotion lls my lso exhiit ontext-speifi hnges; therefore, we exmined the ll design differenes etween two onseutive voliztions produed y different ts in pirs. Fig. shows two sequenes of lls with vrious strt frequenies from two different ts in pir. Two onseutive voliztions, produed y the sme t, were exluded from this nlysis euse the min fous here is to determine the differenes in ll design etween pired ts in response to the other t s lls. Therefore, the sequentil ll nlysis exmple in Fig. only inludes the solute differenes etween the following pirs of lls: A B, B A, A B nd B A. If the intervl etween two onseutive voliztions from different ts ws greter thn ms or one t produed voliztion efore or while it herd nother t s voliztion, these dt were exluded from this nlysis. The time intervl of ms ws hosen euse the sound propgtion distne in this time period is out 7m, whih is lmost the length of the flight room (speed of sound is.ms t C). High repetition rte feeding uzzes, whih re used y ts in the terminl phse of prey pture, were lso exluded from this nlysis, euse the vol djustment during this period of time is relted to the presene of prey rther thn onspeifis. We omputed the solute differenes etween two sequentil voliztions in lls produed y different ts ross trils nd found tht seprtions in eh ll prmeter were ll signifintly lrger thn zero nd lso signifintly greter thn ll design seprtion prior to piring (one smple t-test, P<.). Histogrms of seprtion in eh ll prmeter in the two-t ondition nd their seline seprtions re shown in Fig.. Nerly 9% of voliztions exeed the seline seprtions in durtion nd sweep rte when two ts flew together wheres over % of voliztions in the two-t ondition show seprtions in strt/end frequenies nd ndwidth greter thn seline dt. Overll, pired ts inresed their ll design seprtion when flying together ompred with their seline differenes in ll design. Similrity in seline ll design Individul ts in this study showed different mounts of seprtion in their seline ll design, nd the similrity etween the ll design of pired ts influened how eh t djusted its lls. The mgnitude of ll design djustment represents the inrese in ll design seprtions etween pired ts from the seline to twot ondition. It is lulted y sutrting the differene etween the mens of the seline ll fetures of pired ts from the differene etween fetures of two sequentil lls produed y different nimls in the two-t ondition. Three (pirs, nd ) out of seven t pirs showed lrge seline seprtion in strt/end frequenies nd ndwidth, nd four others (pirs,, nd 7) showed smll seline seprtions. A negtive orreltion ws found etween the seline seprtion of spetrl ll fetures nd the mgnitude of ll design djustment under pired onditions (Fig.A C). Fig.A C show tht the t pirs with the most similr seline ll frequenies (strt/end) nd ndwidth inresed their

4 Vol djustment in eholoting ts 9. z (m) Inter-t distne (m) Frequeny (khz) A B Durtion (ms) Sweep rte (khz ms ).7.7 y (m) x (m). z (m) C.. D Time (s) y (m) x (m)..... Fig.. Two exmples show the reltive position of pired ts nd the design of their voliztions. The -D flight pths of eh t in (A) exmple No. nd (B) exmple No.. Arrows in the strting points of eh flight urve mrked the flight diretion of eh t. Flight trjetories of eh t were mrked y different olors (lue nd red). One t flew ehind the other t nd followed the leding t s flight trjetory in exmple No.. Two ts flew lmost prllel in the eginning of exmple No.. The numer eside eh flight pth is the tril time nd mthed the x-xis in pnel (B) nd (D), respetively. Eh sterisk nd open irle represents one voliztion from t A (sterisks) nd t B (open irles). The inter-t distne nd ll design of t A nd t B re shown in (B) exmple No. nd (D) exmple No.. The sterisks represent voliztions from t A nd the open irles represent voliztions from t B. From the upper to lower pnels re inter-t distne, strt/end frequenies (those two urves with higher vlues re strt frequenies nd the other two re end frequenies), durtion nd sweep rte. differenes in these prmeters when they flew together, nd the mgnitude of ll djustment vried with seline ll similrity. Chnges in ll durtion nd sweep rte in the two-t ondition were not predited y seline seprtion of these two ll prmeters (Fig. D,E). Similrity in seline ll frequeny ws lso relted to how the t djusted its ll frequeny in response to nery onspeifis. We lulted the proportion of one t s voliztions with higher strt/end frequenies thn the other t in pir, nd seleted the proportion elonging to the individul with higher seline ll frequeny to plot s funtion of the seline frequeny seprtion (Fig. ). A positive orreltion etween these two mesurements mens tht the individul with the higher strt frequeny mintined this higher frequeny in the two-t ondition for those t pirs with greter strt frequeny seprtions in the seline ondition. The sme reltionship lso pplies to ll end frequeny. Therefore, whether the t lled t higher frequeny thn the other t in the two-t ondition or not depended on seline ll frequeny design. Sptil seprtion Cll design differenes of suessive lls produed y different ts were signifintly ffeted y the sptil seprtion of pired nimls [one-wy nlysis of vrine (ANOVA), P<. for ll five prmeters]. The Sheffé test ws used for post-ho omprisons to determine whih inter-t sping influened vol djustment of ts. The lrgest seprtions in strt nd end frequenies, durtion nd ndwidth ourred when the inter-t distne ws shorter thn.m (Fig.7). When the inter-t distne ws etween. nd m, Strt frequeny (khz) 7 A A B A B.... Time (s) Fig.. Shemti representtion of sequentil ll nlysis. Eh point represents the strt frequeny of one voliztion, nd different letters men lls mde y different ts. For exmple, A is the first ll t A produed nd B is the third ll t B generted. The x-xis is the time nd y-xis is the strt frequeny of lls. Curves etween two lls represent two onseutive voliztions produed y different ts nd solute differenes etween these two sequentil lls re used to represent seprtion in pired ts ll design. Two onseutive lls, whih were not onneted y urves, were not inluded in dt nlysis euse they were produed y the sme individul. B B A

5 9 C. Chiu, W. Xin nd C. F. Moss A.% D.9% Fig.. Distriution of ll design seprtion etween two sequentil lls produed y different ts when they flew together. The thik lk line in eh histogrm indites the seline seprtion, whih is the differene in ll design etween two ts when they eh flew lone. The perentges mrk the proportion of lls tht exeed the seline seprtion. Cll prmeters nlyzed here re (A) strt frequeny, (B) end frequeny, (C) ndwidth, (D) durtion nd (E) sweep rte. Numer of lls 7 Strt frequeny seprtion (khz) B.9% Durtion seprtion (ms) E.7% End frequeny seprtion (khz) C 9.% Sweep rte seprtion (khz ms ) Bndwidth seprtion (khz) the sweep rte differene etween pired ts ws the gretest. The seprtion in ll design generlly deresed s the inter-t distne inresed. Differenes in ll ll design when inter-t distne ws shorter thn. m ws lwys signifintly greter thn those when inter-t distne ws longer thn m. All differenes in ll prmeters, lthough influened y sptil seprtion etween pired ts, were still lrger thn the seline seprtion. Temporl seprtion of suessive lls Temporl seprtion in sonr lls ould lso e ftor ffeting the eholotion ll design djustments of pired ts. Bts dynmilly vried the intervl etween suessive lls nd timed their sonr voliztions to void overlp with the other t s lls. In this study, only 9.% of lls produed y pired ts overlpped for ny portion of the signl durtion. The effet of temporl seprtion etween suessive lls produed y different ts ws exmined y ompring the ll design seprtion of pired ts s funtion of the time window seprting their lls. We divided suessive lls into two groups; one with short time window ( ms) seprting the signls of the two ts nd one with longer time window (>ms) seprting the signls of the two ts. As the reltive position of the ts nd mirophones ws reorded in this study, we were le to lulte eh t s voliztion time nd the time this ll rrived t the other t s ers. Therefore, the temporl seprtion of lls produed y two ts is defined here y the intervl etween the time when the ll of one niml rehed the ers of the other (listening) niml nd the time when the listening niml produed its next ll. We pplied n independent smple t-test to exmine whether the time window seprting the sequentil lls of the two ts influened design djustments in the fetures of lls. When the time window etween the ll reeived y one t nd its next sonr ll ws less thn ms, the mgnitude of seprtion etween ll fetures ws signifintly greter thn when this time window ws greter thn ms (for ll five prmeters, P<.). Anlysis of glol ll djustments y individul ts Sequentil ll nlysis revels the dynmi nd short-term ll design hnges in pired ts. Here we exmine differenes in voliztions etween seline nd two-t onditions in eh t in pir to determine the generl pttern of ll struture djustments in individul ts. Diretion nd mgnitude of ll feture djustments ross t pirs Cll design in the two-t ondition minus tht in the seline ondition represented the mounts of hnge from the seline

6 Vol djustment in eholoting ts 97 Mgnitude of strt frequeny djustment (khz) Mgnitude of end frequeny djustment (khz) Mgnitude of ndwidth djustment (khz) A Person s r=.9** y=.77x+.9, R =.** 7 Bseline strt frequeny seprtion (khz) B 7 Person s r=.9** y=.x+.7, R =.9** Bseline end frequeny seprtion (khz) C 7 Person s r=.* y=.9x+.7, R =.7* Bseline ndwidth seprtion (khz) Mgnitude of durtion djustment (ms) Mgnitude of sweep rte djustment (khz ms ).... D Person s r=. y=.x+., R = Bseline durtion seprtion (ms) E 7 Person s r=.9 y=.x+7., R =..... Bseline sweep rte seprtion (khz ms ) Fig.. The orreltion etween eh pir s seline seprtion nd the mgnitude of djustment from seline to two-t ondition in (A) strt frequeny, (B) end frequeny, (C) ndwidth, (D) durtion nd (E) sweep rte. *Mens P<. nd ** mens P<.. Eh dt point represents one t pir nd the numer next to eh point refers to different t pirs. Only spetrl prmeters, strt/end frequenies nd ndwidth, show signifint negtive orreltion. ondition, nd ll ts modified t lest one ll prmeter when pired with nother t (Fig. ). Cll design hnges in different pirs nlyzed y one-smple t-tests reveled signifint derese in strt frequeny nd ndwidth in ll individuls, exept one t in pir. This prtiulr individul in pir only modified its sweep rte when pired with nother t ut the other individul in pir modified its strt frequeny, ndwidth nd sweep rte. No onsistent hnge pttern ws oserved in the diretion of sonr ll end frequeny, durtion nd sweep rte ut most ts mde either spetrl or temporl djustments in their ll designs when pired with nother individul. Five individuls did not show signifint inrese in the end frequeny of their voliztions when pired, nd oth ts in pirs nd did not hnge the end frequeny of their lls. When one individul in pir shifted its ll design, the other t did not lwys modify its ll design in the opposite diretion. Most ts djusted their strt frequeny nd ndwidth in the two-t ondition, nd end frequeny ws the ll prmeter tht exhiited the fewest hnges. Cll djustment depends on pulse intervl Cll design djustment y n individul t vried with the rte t whih it produed sonr lls. The mgnitude of ll design djustment refers to the solute differene etween eh individul t s ll design in seline nd two-t onditions nd it is plotted s funtion of pulse intervls in Fig.9. Pulse intervls were divided into five time ins of ms intervls. Pulse intervls elow ms were exluded from this nlysis to eliminte feeding uzzes. Differenes in mgnitude of ll djustment were signifintly influened y pulse intervl (one-wy ANOVA, P<. for ll five prmeters). The Sheffé test ws used for post-ho omprisons to determine whether ll prmeter djustments differed ross pulse intervl ins. The mgnitude of strt/end frequenies, ndwidth nd sweep rte djustment deresed s pulse intervls inresed, nd the mgnitude of durtion djustment showed the reversed trend. When pulse intervls were less thn ms, the mgnitude of strt frequeny nd ndwidth djustment ws the lrgest. Big rown ts showed the lrgest hnge in ll sweep

7 9 C. Chiu, W. Xin nd C. F. Moss Proportion of lls with higher frequeny thn the previous ll (%) End frequeny Person s r=.* y=.x+., R =.* Strt frequeny Person s r=.77* y=.x+., R =.* Bseline frequeny seprtion (khz) Fig.. The orreltion etween strt/end frequenies seprtion nd proportion of lls with higher strt/end frequenies thn the preeding ll. The losed irles represent strt frequeny nd the open irles represent end frequeny in eh t pir. The t with higher strt frequeny tended to keep higher frequeny thn the other t in the pir when the strt frequeny seprtion is lrge for this pir. End frequeny shows similr trend to strt frequeny. rte from seline produing sounds with intervls etween nd ms. The mgnitude of sweep rte djustment deresed for longer pulse intervls. DISCUSSION Humns nd other nimls n distinguish nd mke sense of uditory strems from omplex ousti senes (Bregmn, 99; Hulse, ). This study explores how the eholoting t orients in drk flight room in the presene of nother individul whose sonr signls re similr to its own. Results show tht ts modified their ll design signifintly in the two-t ondition, nd pired ts enlrged the differenes etween the time frequeny strutures of their voliztions. These differenes in ll design were ffeted y the sptil seprtion etween pired ts nd y the similrity in seline ll design of individul ts. Distint spetrl fetures or temporl ptterns n help ts integrte nd segregte uditory strems in omplex environment (Moss nd Surlykke, ). The results of this study suggest possile ousti ues, rising from ll design differenes, whih ould llow eholoting ts to segregte ehoes from their own sonr voliztions from the sonr signls of nery onspeifis. Rule one for signl modifition: individul signture nd similrity in ll design Signls with individul signture hve een disovered in tive sensing nimls nd one possile dvntge of these personl signls is for nimls to segregte their signls from those of onspeifis. Wve-type wekly eletri fish produe n individul-speifi eletri orgn dishrge (EOD) frequeny nd re ple of disriminting signls generted y different individuls (MGregor Strt frequeny seprtion (khz) A, Durtion seprtion (ms)..... D, End frequeny seprtion (khz) Bndwidth seprtion (khz) B C,,,, Inter-t distne (m) Sweep rte seprtion (khz ms ) E, Inter-t distne (m) Fig. 7. The men omprison of eh ll design seprtion etween two onseutive lls t different inter-t distne y one-wy nlysis of vrine (ANOVA). Error rs indite stndrd error of men. Different letters men tht there is signifint differene etween these two vlues. The dotted line in eh pnel shows the seline seprtion. Cll designs re mesured y five prmeters: (A) strt frequeny, (B) end frequeny, (C) ndwidth, (D) durtion nd (E) sweep rte. d

8 Vol djustment in eholoting ts 99 A. D Strt frequeny (khz) B Durtion (ms)..... E End frequeny (khz) Sweep rte (khz ms ) Bndwidth (khz) C Pir Pir Pir Pir Bt pirs Pir Pir Pir 7 Pir Pir Pir Pir Pir Pir Pir 7 Bt pirs Fig.. The mount of devition from seline dt in the two-t ondition for eh t in eh pir. White nd gry rs indite dt from different ts in pir. Five ll prmeters were presented here: (A) strt frequeny, (B) end frequeny, (C) ndwidth, (D) durtion nd (E) sweep rte. All devited mounts re either signifintly lrger or smller thn zero, exept those mrked with The x-xis shows t pirs nd these t pir numers orrespond to those shown in Fig.. Error rs represent stndrd error of the men. nd Westy, 99). Adult femle ts n identify their own pups when mny other pups re lling in the kground simultneously. Eh pup produes isoltion lls with spetrl nd temporl fetures distint from others, nd femle ts my use individulspeifi isoltion lls to help identify their own offspring (Blome, 99; Gelfnd nd MCrken, 9; Knörnshild et l., 7). A psyhoousti experiment shows tht femle greter sper-nosed ts, Phyllostomus hsttus, re ple of disriminting speifi pup s isoltion lls from others (Bohn et l., 7). Not only do pups show individul signtures in their isoltion lls ut so lso do dult ts. Inter-individul differenes in ll design hve een oserved in severl t speies (Siemers et l., ; Siemers nd Kerth, ). Eholotion lls of E. fusus show individul identity, ge nd group vrition (Msters et l., 99), nd femle ts of this speies reognize the gender of other ts y listening to their voliztions (Kzil et l., ). Other t speies, suh s Molossus molossus, Myotis luifugus, Nytieius unus nd Otomops mrtiensseni, lso produe distint eholotion lls for those individuls from different groups (Fenton et l., ; Kössl et l., 999; Mor et l., ; Perl nd Fenton, 99). Previous studies hve demonstrted tht onspeifi ts often produe lls with different design fetures, nd ts re ple of disriminting ll design differenes t the individul level. Differenes in these individul-speifi lls my e enough for the uditory system to segregte different ousti soures. The orreltion etween the similrity in ll fetures of ts flying lone

9 C. Chiu, W. Xin nd C. F. Moss Mgnitude of strt frequeny djustment (khz) 9 A Mgnitude of durtion djustment (ms).... D, Fig. 9. The mgnitude of ll design djustment from seline to two-t ondition s funtion of pulse intervls. Error ts indite stndrd error of men nd different letters men tht there is signifint differene etween these two vlues. The x-xis is the pulse intervl of individul ts nd the y-xis is the mgnitude of djustment for five ll prmeters: (A) strt frequeny, (B) end frequeny, (C) ndwidth, (D) durtion nd (E) sweep rte. Mgnitude of end frequeny djustment (khz) Mgnitude of ndwidth djustment (khz) B C, + Pulse intervl (ms) Mgnitude of sweep rte djustment (khz ms ) E + Pulse intervl (ms) nd the mgnitude of hnge when pired indites tht eholoting ts n use personl signls to void ll jmming from onspeifis, s long s the differenes in these individul-speifi signls re disriminle. In this study, eh individul in pir inresed differenes in lling frequenies or ndwidth if seline voliztions showed similr spetrl fetures to the t it ws pired with. Pired ts, whose lls lredy showed onsiderle design feture seprtion in the seline ondition, did not inrese their differenes in strt/end frequenies nd ndwidth. For those pirs with less similr seline lling frequenies, the t with the higher frequeny voliztions tended to mintin higher lling frequenies. The estimted mount of seprtion required for pired ts to distinguish their own lls/ehoes from those of onspeifi n e inferred from this study. The men seprtions in ll design of pired ts when flying together were. khz for strt frequeny,.khz for end frequeny,.ms for durtion,.khz for ndwidth nd.khzms for sweep rte. These men vlues provide n estimte of disriminle spetrl nd temporl feture seprtions in ll design of pired ig rown ts. Two pipistrelle ts, Pipistrellus pipistrellus nd Pipistrellus pygmeus, produe lls with pek frequenies of nd khz, respetively. Their ll design hnged when they flew with onspeifis ut their lls remined the sme when flying with heterospeifis (Brtonik et l., 7). The uthors of this previous study suggested tht ll differene etween these two pipistrelle speies, whih is khz, is enough to void jmming mong heterospeifis. Seprtion of khz in the pek frequenies of pipistrelle ts is etween the men strt frequeny (. khz) nd end frequeny (. khz) seprtion in the present study. The onstnt frequeny omponent of lesser mouse-tiled t s (Rhinopom hrdwikei) eholotion lls tend to fll into one of three different frequeny nds (,., khz) when they fly in group (Hersetzer, 9). This result suggests tht. khz seprtion in ll frequeny is enough for R. hrdwikei to disriminte differenes etween its own eholotion ll nd the lls of onspeifis. These findings suggest referene for onduting further psyhoousti experiments on the t s ility to disriminte signls with different time frequeny strutures. Rule two for signl modifition: sptil seprtion We nlyzed in detil vol hnges the t mde in response to the presene of nother t t prtiulr sptil seprtion, euse reording nd nlysis methods permitted us to ssoite eh ll with n identified individul nd its -D position with respet to the niml. Short-term hnges in voliztions n e deteted y sequentil ll nlysis, s one t my enlrge differenes etween its lls nd those of the other t for short period of time when ll interferene is lrge. We disovered tht seprtion in ll design is dependent on the inter-t distne. Strt/end frequenies, durtion nd ndwidth of the FM sweep showed the lrgest differenes etween pired ts when the inter-t distne ws shorter thn

10 Vol djustment in eholoting ts. m. The mgnitude of ll interferene eme high when pired ts flew lose to eh other nd one t in pir sometimes stopped volizing for more thn. s, possily to void signl jmming from onspeifis. Silene hs een oserved in pired eholoting ts ompeting for single food item, nd it hs een hypothesized tht silene is strtegy used y ts to void ll interferene (Chiu et l., ). When oth ts volized t short inter-t distnes, the seprtion of their ll fetures inresed s well. Our dt suggest tht ts inresed their ll feture seprtions to void interferene used y nother t nery, nd greter inter-t distnes ould help ts resolve the prolem of onspeifi sonr interferene. Other niml speies hve een found to mintin sptil seprtion mong individuls when ommuniting in omplex ousti environments, potentilly to void ll interferene. For exmple, mle frogs typilly mintin minimum distne in horus (Gerhrdt nd Huer, ). Rule three for ll modifition: temporl seprtion of suessive lls In this study, only osionlly did voliztions of pired ts overlp in time. Insted, there were temporl gps etween the lls of individul ts, nd the intervls etween lls vried over the ourse of eh tril. Two ird speies, the red-eyed vireo (Vireo oliveus) nd the lest flyther (Empidonx minimus), modify temporl ptterns of their songs to void signl overlp (Fiken et l., 97). Mle singing nightingles (Lusini megrhynhos) sing preferentilly during the silent windows etween heterospeifi songs in order to trnsmit their songs more effiiently (Brumn, ). The otton-top tmrins (Sguinus oedipus) n djust their volizing time to fll into the silent windows etween white noises (Egnor et l., 7). The tropil frog, Eleutherodtylus oqui, lso djusts the timing of its mting lls to fll in gps etween the voliztions of neighoring frogs (Nrins, 99; Zelik nd Nrins, 9). The eholoting t ould pply the sme priniple y listening to the other t s voliztions to selet its ll timing, nd when intervls etween the lls of pired ts re short enough to rete interferene, this my drive further djustments to sonr signl design. Support for this omes from our present finding tht the lrgest ll design seprtions ourred when one t volized less thn ms fter the other t s voliztions. The inreses in ll design differenes for losely timed lls imply tht the ig rown t tively ontrols timing nd ll fetures to void ll interferene from onspeifis. As elorted elow, ehviorl studies of eho rnging y eholotion in ts hve reported tht interfering signls disrupt distne disrimintion, nd the ousti feture nd temporl seprtion etween jmming signls nd ehoes ffets the mgnitude of interferene (Msters nd Rver 99; Møhl nd Surlykke 99; Roverud, 99; Roverud nd Grinnell, 9; Roverud nd Grinnell, 9). Glol signl djustments in the presene of onspeifis Big rown ts hnged fetures of their eholotion lls when flying with onspeifis. The question of whether the oserved differenes in ll fetures re the result of tive jmming voidne or simply due to individul-speifi ll design n e resolved here y ompring lls in the two-t ondition with seline voliztion dt. In our study, most individuls flying in pirs showed signifint hnges in eh ll prmeter ompred with the lls produed in seline reordings when eh flew lone, suggesting tht the presene of the onspeifi eliited vol djustments. Cll design seprtion ws ffeted y the sptil distne etween pired ts nd seline similrity in ll design, whih further suggests tht the t tively djusts its ll design to void signl interferene from onspeifis. Severl t speies, inluding R. hrdwikei, Blntiopteryx plit, T. rsiliensis nd Tdrid teniotis, hve een reported to djust their ll frequenies when flying in groups (Brtonik et l., 7; Hersetzer, 9; Iánez et l., ; Rtliffe et l., ; Ulnovsky et l., ). Some t speies modified temporl fetures rther thn spetrl fetures of their voliztions to void ll interferene from onspeifis (Orist, 99). Ulnovsky et l. (Ulnovsky et l. ) nd Gillm et l. (Gillm et l., 7) hve reported end frequeny djustments in voliztions of two t speies, T. rsiliensis nd T. teniotis, when flying with onspeifis. Although ig rown ts, E. fusus, in the present study lso showed ll modifition in end frequeny, djustments in strt frequeny were lrger thn end frequeny. This finding is onsistent with nother study tht reported lrger ll frequeny seprtion in strt frequeny thn in end frequeny in E. fusus nd Lsiurus inerus ut not in Lsiurus orelis nd Euderm multum (Orist, 99). Previous nd present reserh findings suggest tht inter-speifi vrition exists in ll modifition of eholoting ts. Reserh on other niml speies hs lso reported modifition in spetrl nd temporl fetures in the presene of onspeifis. Wve-type eletri fish, whih lso rely on tive sensing for orienttion, shift their EOD frequenies to void signl jmming with onspeifis (Bullok et l., 97; Wtne nd Tked, 9). Pulse-type eletri fish inrese or derese the dishrge rte of their eletri orgn to void signl overlp with nother fish (Heiligenerg, 99). Similr temporl nd spetrl modifitions in signls used s strtegy to void signl interferene hve lso een reported in other nimls, whih do not rely on tive sensing (Egnor et l., 7; Frris et l., ; Fiken et l., 97; Greenfield nd Rnd, ; Serrno nd Terhune, ). Animls dopt different strtegies to hieve seprtion in signls nd void jmming. Previous reports on eletri fish hve desried how two fish djust their EODs to inrese differenes etween their signls. For exmple, wve-type eletri fish modify their EOD frequenies, nd the one with the higher frequeny inreses its frequeny nd the other shifts its frequeny in the opposite diretion (Bullok et l., 97; Wtne nd Tked, 9). No similr rule hs een reported so fr out how two or more ts djust their ll design to reh suffiient seprtion to minimize interferene from the signls of onspeifis. Pst reserh hs reported n overll upwrd shift or downwrd shift in ll frequenies of severl t speies in response to neighoring onspeifis (Hersetzer, 9; Iánez et l., ; Kössl et l., 999; Miller nd Degn, 9; Rtliffe et l., ; Surlykke nd Moss, ). Gry s-winged ts, B. plit, shifted their pek frequenies slightly upwrd when flying in groups (Iánez et l., ) nd T. rsiliensis shifted their end frequenies upwrd when plyk t lls were rodst (Gillm et l., 7). Btes et l. reported tht the ig rown t, performing in two-lterntive fored-hoie detetion tsk, shifted lling frequenies upwrd when lower jmming frequenies were rodst nd shifted lls downwrd when higher jmming frequenies were rodst (Btes et l., ). By ontrst, the present study reports n overll downwrd shift in strt frequeny nd ndwidth of the ig rown ts voliztions when they flew in pirs, exept one individul in pir mintined the sme seline strt frequeny nd ndwidth. No ler modifition pttern ws found in three other ll prmeters, end frequeny, durtion nd sweep rte. Although no ler overll vol djustment pttern ws found when ompring

11 C. Chiu, W. Xin nd C. F. Moss eh individul s ll design hnges in seline nd two-t onditions, pired ts were still le to estlish lrge enough seprtion of its signls from nother t to void interferene y dynmilly hnging ll struture. The ft tht pired ig rown ts did not ollide with eh other or show ny sign of disorienttion demonstrtes tht this speies employs suessful strtegies to void signl jmming from onspeifis. The overll strt frequeny drop ould e the onsequene of deteting nery ojet (nother flying t in this se) t lose distne, s ts using FM signls tend to employ lower strt frequeny nd shorter ndwidth lls when pprohing trget (Shnitzler et l., ; Simmons et l., 979). A possile explntion is tht the t my deliertely lower its ll intensity to void ll interferene when flying with onspeifis nd therefore our reording devies did not reeive the high frequeny prts of lls due to the exess ttenution of high frequeny sounds (Lwrene nd Simmons, 9). Cll intensity derese due to the presene of onspeifis ould e nother vol djustment strtegy the t uses to void signl jmming. A lirted mesurement of the t s ll intensity is required in the future to onfirm whether ts derese their ll intensity to void signl jmming. Eholoting ts generte pulses with short intervls when ttempting to pture their prey or pprohing ostles nd produe sonr pulses with low repetition rte when serhing for trgets or orienting in spe. It hs een inferred tht ts use high repetition rte lls to quire preise informtion from trgets nd use low repetition rte lls when no trget of interest is shown in the viinity (Shnitzler nd Klko, ). Big rown ts in this study inresed the mgnitude of djustment in strt/end frequenies, ndwidth nd sweep rte when pulse intervls deresed, whih suggests tht the t modifies fetures of its sonr lls the most when it needs to strem detiled informtion from trget ehoes t short distne. Auditory strem segregtion Gestlt psyhologists suggest tht severl priniples, suh s similrity, proximity nd losure, influene humn visul pereption. For instne, humns tend to group visul ojets together ording to similr hrteristis, suh s olor or shpe. Bregmn suggests tht the sme priniples n e pplied to uditory sene nlysis (Bregmn, 99). The priniple of similrity enles the uditory system to segregte nd integrte omplex sound ptterns. Eholoting ts my pply these priniples to distinguish its own emissions/ehoes from those of others nd to trk ehoes from moving trget in omplex ousti environment (Moss nd Surlykke, ). Inrese in ll design seprtion when flying with nother t provides demonstrtion tht the t my use the priniple of similrity in ll design to integrte its own signls/ehoes nd segregte them from onspeifi s signls/ehoes. Sweep rte seprtion inresed in the two-t ondition, suggesting tht the ig rown t hnged the slope of its FM sweep to mximize differenes from lls of onspeifis. Consistent with this suggestion re the results of psyhophysil experiments on trget rnging y eholoting ts. In one suh experiment, the ig rown t s rnge disrimintion performne deteriorted when phntom trget eho of the t s own ll ws repled y signls of other ts with different ll designs (Mster nd Rver, 99). In follow-up study, they found tht FM sweep urvture hnges in sonr signls ompromised the t s rnging ility (Msters nd Rver, ). As noted ove, interferene signls n lso ffet sonr rnging y ts. Msters nd Rver (Msters nd Rver, 99) report tht interferene signls degrded trget rnge disrimintion performne of the ig rown t, nd the mgnitude of interferene depended on the similrity etween trget ehoes nd interferene signls. Another study in P. pipistrellus reported tht liks from rtiid moth speies did not ffet the t s rnge disrimintion ility when rodst rndomly with respet to eho rrivl times (Surlykke nd Miller, 9). However, the ig rown t s rnge disrimintion performne deteriorted only when the lik of ruy tiger moth (Phrgmtoi fuliginos) ws rodst within. ms efore the eho return (Miller, 99), in time window when the lik my hve served s forwrd msker of the eho plyk stimulus (Moss nd Shnitzer, 99). Results from these studies suggest tht lls shring similr time frequeny struture disrupt the t s rnging ility the most. Therefore, minimizing the similrity in ll design from onspeifis seems to e suessful strtegy for the t to void sonr jmming from the signls of nery onspeifis. Two jmming voidne strtegies: vol djustment nd silene Reent reserh hs unovered tht pired ig rown ts tend to ese volizing t short inter-t distnes (Chiu et l., ). The present study on the sme speies with n identil experimentl setup revels tht ig rown ts lso tend to djust their voliztions in order to inrese ll design seprtions. Both studies demonstrted tht similrity in ll design nd sping etween pired ts re two importnt ftors to ffet the ig rown ts employment of silene nd vol djustment strtegies. These two ftors lso influene the interferene level of voliztions from onspeifis; therefore, silene nd/or ll design djustment pper to funtion to minimize signl interferene from onspeifis. An eholoting t shows signs of disorienttion when its hering is disrupted (Griffin, 9) ut it voids ollisions with nother flying niml when it goes silent (Chiu et l., ). A silent t n still listen to environmentl sounds, inluding the lls nd ehoes of onspeifis in the viinity, nd pssive loliztion of these sound soures presumly guides its orienttion in the environment. The listener needs to e lose to the volizing niml in order to use the other s voliztion for orienttion (Ku, ; Xito nd Roitlt, 99). As the volizing t n fly unexpetedly out of er shot of the pssively listening t, n eholoting t risks disorienttion when it shuts off its eholotion. Mny onditions would therefore fvor t s vol djustment strtegy over silene strtegy. However, the t my enounter diffiulties finding trnsmission hnnel tht is free from overlp with other individuls when employing vol djustment strtegy for jmming voidne, prtiulrly when it exits/enters its roost with mny dozens of onspeifis. Under suh onditions, vol djustment my prove of little use nd other strtegies would e needed. Silene is one potentil strtegy for t to employ when mny onspeifis re flying in lose proximity. Detiling the ftors tht drive silent nd vol djustment ehviors in eholoting ts is sujet for future reserh. As strting hypothesis, we propose tht silene is strtegy the ig rown t employs primrily to void potentilly disling interferene under onditions when its loliztion ury requirements re not high, e.g. voiding ostles. In this ontext, it is importnt to note tht the ig rown t lwys produes sonr lls s it prepres to interept prey, when the timing of voliztions nd returning ehoes is used for preise trget loliztion (Chiu et l., ). Vol djustment, s reported in the present study, my e used when it is diffiult for the t to use the signls of

12 Vol djustment in eholoting ts onspeifi or loliztion ury requirements re high, e.g. during prey pture. Conlusions The ig rown t (E. fusus) enounters nd interts with onspeifis frequently in nture (Simmons et l., ). Flying with other ts does not disrupt the ility of E. fusus to use eholotion for sptil orienttion, inditing tht this t speies must employ strtegies to ope with possile signl interferene from onspeifis. Results reported in this study show inreses in sonr signl ll design seprtion of E. fusus flying in pirs, nd the mgnitude of signl hnges depends on the seline similrity etween ll fetures of individul ts flying lone. These dt re onsistent with the hypothesis tht the ig rown t utilizes ll design modifitions to void ll interferene from neighoring onspeifis. We propose tht dissimilrity in time frequeny signl struture enles the ig rown t to segregte uditory strems of its lls nd ehoes from those of neighoring onspeifis. We thnk Amy Perez nd Kri Tither for help with the experiment nd dt nlysis. We would lso like to thnk two nonymous reviewers for their vlule omments. This reserh ws funded y NSF grnt IBN-97, NIH grnts R-MH nd R-EB7 to C.F.M. nd the Willim Hodos disserttion fellowship nd Ann G. Wiley disserttion fellowship to C.C. Deposited in PMC for relese fter months. REFERENCES Blome, J. P. (99). Vol reognition of pups y mother Mexin free-tiled ts, Tdrid rsiliensis mexin. Anim. Behv. 9, 9-9. Brtonik, T., Rehák, Z. nd Gisler, J. (7). Cn pipistrelles, Pipistrellus pipistrellus (Shreer, 77) nd Pipistrellus pygmeus (Leh, ), forging in group, hnge prmeters of their signls? J. Zool. Lond. 7, 9-. Btes, M. E., Stmper, S. A. nd Simmons, J. A. (). Jmming voidne response of ig rown ts in trget detetion. J. Exp. Biol., -. Bohn, K. M., Wilkinson, G. S. nd Moss, C. F. (7). Disrimintion of infnt isoltion lls y femle greter sper-nosed ts, Phyllostomus hsttus. Anim. Behv. 7, -. Bregmn, A. S. (99). 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