Stereotypy and variability of social calls among clustering female big-footed myotis (Myotis macrodactylus)

2018·7.9 MB·

by  Xiao, Yan-Hong

ZOOLOGICAL RESEARCH
Stereotypy and variability of social calls among
clustering female big-footed myotis
(Myotis macrodactylus)
Yan-HongXiao1,LeiWang1,JosephR.Hoyt3,Ting-LeiJiang1,Ai-QingLin1,JiangFeng1,2,*
1JilinProvincialKeyLaboratoryofAnimalResourceConservationandUtilization,NortheastNormalUniversity,ChangchunJilin130117,China
2SchoolofAnimalScience&Technology,JilinAgriculturalUniversity,ChangchunJilin130118,China
3DepartmentofEcologyandEvolutionaryBiology,UniversityofCalifornia,SantaCruzCA95064,USA
ABSTRACT electrical, and acoustic signals. Of the communication
modalities, acoustic signals have the advantage of
Echolocating bats have developed advanced
broadcasting information for longer distances with less
auditory perception systems, predominantly using
interferencefromphysicalbarriers. Thisadvantagewaslikely
acoustic signaling to communicate with each other.
a driving force in the evolution of acoustic communication
They can emit a diverse range of social calls in in a wide range of taxa (Seyfarth et al., 2010; Wilkins et al.,
complexbehavioralcontexts. Thisstudyexaminedthe 2012). Acoustic communication fulfills an important function
vocalrepertoireoffivepregnantbig-footedmyotisbats in social interactions, especially for bats, who are among
the most diverse and gregarious of all mammals and live in
(Myotismacrodactylus). Intheprocessofclustering,
predominatelydarkenvironments(Kerth,2008). Theacoustic
thelastindividualtoreturntothecolony(LI)emitted
communication systems observed in echolocating bats are
socialcallsthatcorrelatedwithbehavior,asrecorded
extremelycomplexinthemammalianworldbecausetheycan
onaPC-baseddigitalrecorder. Theselastindividuals emit two kinds of calls: echolocation and social calls, which
could emit 10 simple monosyllabic and 27 complex servedifferentfunctions(Kanwal,2009,2012).Socialcallsare
multisyllabic types of calls, constituting four types of mainly used to transmit information under special behavioral
contexts.Manybatspeciesdemonstrateadiverserepertoireof
syllables. The social calls were composed of highly
socialcallsunderavarietyofbehavioralconditions(Bohnetal.,
stereotyped syllables, hierarchically organized by
2008;Clementetal.,2006;Gadziolaetal.,2012;Knörnschild
a common set of syllables. However, intra-specific et al., 2010; Ma et al., 2006). These characteristics of
variation was also found in the number of syllables, bats provide a unique opportunity for research on acoustic
syllableorderandpatternsofsyllablerepetitionacross communicationofanimalsociality.
callrenditions. Datawereobtainedtocharacterizethe The motivation-structure hypothesis states that social
call types are decided by the behavioral context of birds
significant individual differences that existed in the
and mammals (Kanwal, 2009; Morton, 1977). In bats, the
maximumfrequencyanddurationofcalls. Timetaken
behavioral settings of their vocalizations include aggressive
toreturntotheroostwasnegativelyassociatedwith
thediversityofsocialcalls. Ourfindingsindicatethat
variabilityinsocialcallsmaybeaneffectivestrategy
Received:25September2017;Accepted:11January2018
takenbyindividualsduringreintegrationintoclusters
Foundationitems:ThisresearchwassupportedbytheNationalNatural
offemaleM.macrodactylus.
ScienceFoundationofChina(31700319,31670390);theFundamental
Keywords: Socialcalls;Clustering;Big-footedmyotis Research Funds for the Central Universities (2412017QD026); U.S.
NationalScienceFoundation(NSF)(DEB-1115895);andtheNSFEast
INTRODUCTION
AsianPacificSummerInstituteProgramIIA-1415092
Animals have evolved a variety of communication systems *Correspondingauthor,E-mail:[email protected]
across all sensory modalities, such as visual, chemical, DOI:10.24272/j.issn.2095-8137.2018.026
114 SciencePress ZoologicalResearch39(2):114-122,2018
or warning, courtship, communication, distress, mother-infant MATERIALSANDMETHODS
recognition, and clustering behaviors. Intra-specific
Acquisitionandmaintenanceofanimals
communication under specific behavioral contexts usually
carries significant information about the signaler (Behr et The study was conducted from May to June 2010. Five
al., 2009; Behr & von Helversen, 2004; Knörnschild and pregnantM.macrodactylusindividualswererandomlychosen
von Helversen, 2008). Under some behaviors, intra-specific from90pregnantbatsinanaturalcaveinJilinProvince,China.
differences and elaborate sequences of acoustic signals are They were banded and roosted together as a colony in a
of importance, and contribute to accurate mother-infant and temperature- and humidity-controlled animal room (20 m×10
individual recognition within a colony. For instance, songs of m×4m)atNortheastNormalUniversityinChangchun, China.
free-tail bats contain multiple elements (e.g., syllables, notes Theday-nightcyclewascontrolledat12hdarkand12hlight.
and/or phrases) with highly structured, rather than random, They could fly freely within the animal facility and were given
arrangement. Males often modify types of calls through waterandmealwormsadlibitum.Beforetheexperiment,allfive
modulating the repeated syllables, which can differ among subjectswerehabituatedtohandlingandtothetestingcage.
individuals(Bohnetal.,2009). Clusteringbehaviorisanother
Acousticrecordings
important context in which bats emit social calls. Mammals
We recorded and analyzed the social calls and associated
living in low-temperature ambient environments often huddle
behaviorsofthecaptivebats.Tooptimizerecordingquality,the
togethertoreduceenergyconsumptionandpromotemember
fiveanimalswerehousedinasmalltestingcage(200cm×80
fitness (Gilbert et al., 2010). The central temperature of a
cm×100cm)inaroomlinedwithanechoicfoam,separatefrom
cluster is higher, and the central site is safer than the border
theanimalholdingroom.Toreduceenvironmentalinterference
position (Hatchwell et al., 2009). Thus, achieving the central
with the ultrasonic calls, environmental temperature and
position is often the objective of an individual within a cluster.
humidityoftheroomwerekeptconstant.
Acoustic signals containing characteristic information may
Vocalizationswererecordedusingtwoultrasoniccondenser
contribute to accurate recognition, which can help individuals
microphones (CM16, Avisoft Bioacoustics, Berlin, Germany)
saveenergyandtimeduringcontentionforthecentralcluster
connected to amplifiers and A/D converters (UltraSoundGate
site (Dugatkin and Earley, 2004). Although several studies
416 H). The microphone had a flat frequency response
have examined the clustering behavior of bat species (Kerth,
from 10–250 kHz. The gain of each microphone was
2008), there have been no studies on the diversity and
independently adjusted to optimize the signal-to-noise ratio
structuralcharacteristicsofacousticcommunicationthatoccur
of the recording. Acoustic signals were digitized at 375 kHz
duringtheclusteringofgregariousbats.
with16-bitdepth,andmonitoredinrealtimewithRECORDER
Big-footed myotis, Myotis macrodactylus, belongs to the
software. Weusedtwoinfraredsurveillancecameras(Pensee,
subgenus Leuconoë of the genus Myotis (Yangochiroptera,
PIS-322EG) to simultaneously record the behavior of all
Vespertilionidae). Sexual segregation in colonies is known
animals. We defined the last animal to join the group (LI) as
to occur in many bat species, with separate clustering of
the last individual moving toward the cluster and displaying
females during the summer pupping season (Bradbury,
“approaching”behavior(Kobayasietal.,2012). Inmostcases,
1977; McCracken and Wilkinson, 2000). Females rear their
the LI was observed as roosting last within a cluster. Most
young communally with the formation of maternity colonies,
recordings occurred during the clustering process after bats
whereas males are solitary or form small bachelor groups
had eaten (Figure 1). The characteristics of their social calls
(Senior et al., 2005). The clustering of pregnant bats is a
and the time they took to join the cluster were analyzed
cooperativebehaviorthatpermitsindividualsinvolvedinsocial
using Avisoft-SasLab Pro software, Version 5.1.20 (Avisoft
thermoregulation to minimize heat loss and thereby lower
Bioacoustics, Berlin, Germany). Time here was defined as
their energy expenditure, and may allow them to reallocate
consumedtime(CT).Thestudywasconductedfor38dfrom
the saved energy to other functions such as growth and
2100h–0100heachnight.
reproduction(Gilbertetal.,2010). Thus, theclustercenteris
the optimal position for pregnant bats, and may assist better
Analysisofvocalizations
fetal development. According to our observations, the last
We examined the social call sequences of the LI using
individuals (LI) returning to a group will usually try to enter
nomenclature similar to Kanwal et al. (1994) and Bohn et al.
the central position of the cluster. Approaching behaviors
(2008),withasyllableconsideredthesmallestacousticunitof
are always accompanied by social calls produced by the LI
avocalizationdefinedasonecontinuousemissionsurrounded
until physical contact with the other bats. Thus, we assumed
by background noise, and a call considered the simplest
that the social calls emitted by the LI attempting to enter the
emission pattern of a vocalization used for communication
clustercenterarerelatedtothisspecialbehavior.Wetherefore
consisting of one or more elements (syllables). Vocalizations
examinedtwoquestions: (1)Arethesesocialcallsassociated
were semi-automatically analyzed using Avisoft-SasLab Pro
with successful entrance into the center of the cluster? (2)
software (Version 5.1.20 Avisoft Bioacoustics). Syllable start
Does the variety or structure of the social calls influence this
and end times were automatically detected using a standard
behavior? Werecordedandanalyzedthesocialcallsemitted
threshold level (5%) and hold time (2 ms), and manually
byM.macrodactylusunderthisbehavioralcontext.
adjusted when necessary. Signals were high-pass filtered
ZoologicalResearch39(2):114-122,2018 115
200 cm
A B
80 cm Bats
1
Mic-1
2
Video-2
Video-1 LI
Colony bats
Quick movement
UltraSoundGate 3 Slow movement
Mic-2
Figure1Schematicshowingthecageset-upforsimultaneousaudioandvideorecordingsofcaptiveM.macrodactylus
A:Testingwasconductedinawiremeshcage(200cm×80cm×100cm). Twoultrasonicmicrophones(UltraSoundGateCM16)wereplacedoutsidethecage
andpointedatthecenteroftheceilingofthecage,whichwasabout50cmabovethetipofthemicrophone.Twovideomonitorswereusedtomonitorandrecord
behaviors. B:Clusterofbats(illustratedassolidcircles)andapproachingbat(dottedcircle),bothinabottom-upview. Thesketch,takenfromasequenceof
videoframes,showstheLIapproachingthecolonyafterforaging.
at 1 kHz and the amplitude of each pulse was normalized Statisticalanalyses
to 0.75 V (Bohn et al., 2008; Gadziola et al., 2012; Kanwal Call parameters were checked for normality using the
et al., 1994). As a result, social call sequences were of Kolmogorov-Smirnov test. Since all call parameters were
similar amplitude and unwanted echolocation signals were normallydistributed,differencesincallcharacteristicsbetween
removed. Foranalyses, werandomlyselectedthreecallsper individuals were compared using one-way ANOVA, followed
call type from all individuals that were of sufficient quality for by Tukey multiple-comparison tests. Discriminant function
measurementsandsyllableidentification.Thesocialcallswere analysis (DFA) was used to determine to which individual
automatically analyzed with the Avisoft-SasLab Pro software certain social calls should belong. We examined the general
(Version 5.1.20 Avisoft Bioacoustics). Spectral and temporal relationshipsbetweenthevariablesacrossalltheLIs,including
analyseswereobtainedfromthespectrogramandoscillogram call variants and CTs, by performing Spearman correlations.
with a Fast Fourier Transform (FFT) length of 512 points We used a simple linear regression analysis to assess the
(87.5% overlap), which allowed for a frequency resolution of statistical significance of call variation as a predictor of
732 Hz and temporal resolution of 0.171 ms. We measured individual recognition of CT in the process of approaching
the following parameters for each social call (Figure 2): total clusters. All statistical analyses were performed using SPSS
durationofcall(totdur),minimum(fmin)andmaximum(fmax) 15.0 statistical software (SPSS Inc., Chicago, IL, USA). The
frequencies of call, and mean frequency of highest energy alpha level was set to 0.05 and data were presented as
(freq). This was done by measuring the peak frequency of means±SD.
each component (and then calculating average); number of
RESULTS
componentstocall(nocomp);andnumberofdifferentsyllables
(Difptype) in each call (Russ et al., 2004; Russo & Jones, Acousticstructureofcalls
1999). Ifmorethanoneharmonicwaspresent, valuesofthe A total of 885 call sequences were analyzed from five
first(fundamental)harmonicweretaken. Additionally,weused individuals when the LI approached the cluster. We
oscillogramsandspectrogramstoidentifysyllableswithincalls. distinguished a total of four syllable types, which could be
Wealsoexaminedthecompositionofeachcallintermsofthe combinedtoform10simplemonosyllabiccallsand27complex
total number of each syllable type and the proportion of calls multisyllabic calls. The four syllable types and their 37
with syllables. Finally, for each call recorded, we assigned a combinationsareoutlinedinFigure3andFigure4: downward
callvariantandcalltypebasedonitssequenceofsyllables. frequency-modulatedsyllable(DFM;Figure3A),shortquasi-V
116 www.zoores.ac.cn
175
150
125
100
75
50
25
0.02 0.04 0.06
Time (s)
Figure2Spectrograms(center)ofsocialcallsofMyotismacrodactylusshowingthechangeoffrequencywithtime
Oscillogram(top)givesthechangeofamplitudewithtime. Meanfrequencies(leftpartofspectrum)aretheaverageamplitudeofdifferentfrequenciesofthe
measuredtimewindow.Parametersevaluatedinthisstudyareshown.
Time (s)
Figure3Echolocationpulse(FM)andsimplesyllables
Oscillogram(top)ofthesyllable(s)withthecorrespondingspectrogram(bottom). Syllablesare: A,downwardfrequency-modulatedsyllable(DFM);B,short
quasi-Vfrequency-modulatedsyllable(VFM);C,archedfrequency-modulatedsyllable(AFM);D,sinusoidalfrequency-modulatedsyllable(SFM).
frequency-modulated syllable (VFM; Figure 3B), arched we performed a DFA using four spectrotemporal and two
frequency-modulatedsyllable(AFM;Figure3C)andsinusoidal syllable parameters (Table 1). This analysis resulted in two
frequency-modulatedsyllable(SFM;Figure3D).Inthesyllable canonical functions with eigenvalues greater than 1, which
sequence (Figure 5), social calls started with DFM syllables, togetherexplained90.1%ofthevariationinthecallsfromthe
which, in turn, usually gave way to VFM syllables. The VFM five bats (Figure 6). Subsequent univariate ANOVA showed
syllableswerefollowedbySFMsyllables,usuallyattheendof that the first and second canonical functions could be used
acall.TheAFMsyllableswereonlyinterjacentinthesequence to differentiate between social calls of individual bats (PC1:
and only made transition with DFM syllables. Typically, SFM F =36.6, P<0.001; PC2: F =13.4, P<0.001). Maximum
4,67 4,67
syllableshadalongerduration(10.4±2.8ms)thanthatofthe frequency and duration were the most distinctive features of
othersyllabletypes(DFM,1.6±0.7ms;VFM,4.2±0.8ms;AFM, these calls, indicating different acoustic repertoires. These
3.5±0.8ms). analyses suggested that social calls from different individuals
shouldbedistinguishablebyconspecifics.
Individualacousticaldifferences
Toestablish whetherthesocial calls were individual-specific,
ZoologicalResearch39(2):114-122,2018 117
Figure4Spectrogramsandoscillogramsofmulti-elementsocialcallsfromfemaleMyotismacrodactylus
B
D
Start A End
C
Figure5Modelofcallsbasedontransitionsyllables
Arrowsrepresenttransitionsfromonesyllabletothenext. Arrowthicknessincreaseswithtransitionfrequenciesthatdeviatefromtheexpectedbymorethan
10%,30%,or50%.Dottedlinesrepresenttheendofacall.SeeFigure4forexamplesofeachcall.
118 www.zoores.ac.cn
Table1SocialcallparametersfromMyotismacrodactylusfemales
Bat Call(n) Variants totdur(ms) freq(kHz) fmax(kHz) fmin(kHz) Pulses(per0.1s) Difptype
1 33(3) 4 46.6±10.5b 49.4±5.2a 100.4±6.7a 23.6±3.1b 5.5±1.2a 1.0±0.0a
2 51(4) 7 37.8±7.9a 49.6±9.3a 99.1±8.5a 25.5±3.6a 4.9±0.8a 1.4±0.6b
3 120(5) 12 51.1±15.3bc 39.8±4.3c 78.4±8.1d 18.0±3.1e 7.4±2.3c 1.1±0.2a
4 297(11) 20 52.0±14.1c 46.2±5.2b 93.1±9.6b 20.6±2.9c 7.2±2.1c 1.2±0.4a
5 384(15) 29 49.7±10.6bc 45.8±4.6b 87.0±7.5c 19.2±2.8d 6.5±1.5b 1.4±0.7b
F 14.94* 50.59* 105.43* 79.39* 26.37* 18.37*
“n”isthetotalnumberoftimesthebatwasLI,restrictinganalysistothreecallspercalltype.Sameletter(a,b,c,d,e)indicatesnotsignificantly
differentfromeachother(Tukeymultiple-comparisontest).*:P<0.001.
Figure6Distributionofsocialcallsfromfivefemales(markedbydifferentsymbols)onfirsttwocanonicalaxes
Function1wasmostcorrelatedwithmaximumfrequencyandfunction2wasmostcorrelatedwithduration.Largecirclesencloseareaswith75%probabilityof
includingcallsfromeachbat.
Callvariantsandclustersuccess waspositivelycorrelatedwithclusteringefficiency.
The clustering success of females was measured as the
DISCUSSION
time taken to join a cluster (CT). We correlated the CT
with the number of call variants emitted during one complete Intra-species variability of LI calls was found in the number
processofreturningtothecolony. Becausecallvariantswere of syllables, syllable order and syllable repetition across
most influenced by type and number of syllables, a negative call renditions. These data confirmed that differences in
correlation between the call variants of the LI and cluster social calls existed between M. macrodactylus individuals
success was derived (Figure 7). Clustering success tended during the process of approaching the colony. Our results
toincreasewiththetotalnumberofcallvariantsproduced.The further confirmed the hypothesis that social call richness
numberofsocialcallsforthefiveindividualsvariedfrom4to29 was significantly negatively correlated with time taken for the
duringtheentireresearchsession. Wefoundthatcalldiversity successfulreunionofM.macrodactylusfemalesinacluster.
ZoologicalResearch39(2):114-122,2018 119
y=113.2−1.8x
R2=0.982, P<0.001
30
Figure7RelationshipbetweencallvariantsandtimetakentojoinaclusterinMyotismacrodactylus
Solidlinedepictslinearregression.
The LI can emit 10 simple monosyllabic and 27 complex inter-individual differences in calls, with males able to emit
multisyllabic call types composed of four syllable types. diverse courtship calls, and differences in individual calls
In previous studies, simple monosyllabic calls have been most evident in regard to maximum frequency and duration.
recorded in Myotis species at maternity roosts before bats Higher diversity in the community may contribute to species
leave and after they arrive (Pfalzer & Kusch, 2003), and identification in bats. In our study, individuals emitting low
usually begin with downward frequency-modulated signals. diversity calls required more time to join the group, and
In mammals, repeated calls in communication signals can occasionally could not attain the central position. The border
indicateageneralcodingrule(Fischeretal.,2001;Schehkaet temperatureofagroupislowerthanthatofthecentralposition,
al.,2007). However, complexmultisyllabiccallsinPipistrellus so bats need more energy consumption for thermogenesis.
pipistrellus constitute different syllables, which may attract Therefore, the LI must repeatedly communicate with others
conspecifics and thereby help to deter predators (Budenz et when returning to the colony to obtain maximum benefit. To
al., 2009). We found that complex multisyllabic calls were reduce the time taken for the recognition process, social
emitted by M. macrodactylus females returning to the colony; behaviormaydrivethediversityofindividualcalls.
furthermore,thediversityofcallswasaffectedbysyllabletype Wealsofoundthatthesamecallswereemittedbydifferent
and unique syllable types led to specific calls. New evidence individuals; these calls may function as identification signals
has suggested that Megaderma lyra can regularly modify the among members of a colony and have a universal meaning.
structure of their calls, including the number and repetition of However,variationinthenumberandtypeofsyllablesmaybe
syllables,accordingtocompetingstrength(Bastian&Schmidt, due to specific information conveyed by individuals. Huddling
2008), and signalers may convey their own properties in togetherinaroostislikelyathermoregulatorystrategyusedby
acousticsignals(JanßenandSchmidt,2009). M.macrodactylustoconserveenergyandincreasesurvivalor
ThesequencesofpulsesinM.macrodactylus femalecalls fitness. In this study, five individuals were randomly selected
demonstrated a stable pattern. The social calls always from 90 females, with no significant differences in forearm
beganwithadownwardfrequency-modulatedcomponentand length or body size impacting the results. Each of the five
were followed with one or two other sub-syllables; by adding bats could potentially be the LI, but the time spent alone
syllablesortypesofsyllablesbasedonthisrule, callvariants by each bat was negatively correlated to their call diversity.
wereincreased. Similardescriptionsofcallswithhighdiversity Under natural circumstances, calls may be relevant to status
have been found in studies on Saccopteryx bilineata (Behr & identification. The clustering of numerous individuals would
vonHelversen,2004),Tadaridabrasiliensis(Bohnetal.,2009) make diverse calls more identifiable by others. In this study,
and Pipistrellus nathusii (Russ and Racey, 2007; Jahelková individuals that emitted multiple social calls may be more
et al., 2008) courtship songs. These studies noted large easily identified and accepted by others, such that individual
120 www.zoores.ac.cn
calls may evolve towards complexity under natural selection. Fischer J, Hammerschmidt K, Cheney DL, Seyfarth RM. 2001. Acoustic
This article suggests a role for the sophisticated acoustic featuresoffemalechacmababoonbarks.Ethology,107(1):33–54.
communicationabilitydeveloped bybats. Furtherresearchis
Gadziola MA, Grimsley JMS, Faure PA, Wenstrup JJ. 2012. Social
neededtoelucidatetheprocessofidentificationthroughsocial
vocalizationsofbigbrownbatsvarywithbehavioralcontext.PLoSOne,7(9):
calls,whichcanbeconductedthroughmultiplemethodsandis
e44550.
affectedbybehavioralcontext.
GilbertC,McCaffertyD,LeMahoY,MartretteJM,GiroudS,BlancS,Ancel
Our results indicated that the social calls emitted by
A.2010.Oneforallandallforone: theenergeticbenefitsofhuddlingin
clusteringM.macrodactylusfemalesalwaysexhibitedastable
endotherms.BiologicalReviews,85(3):545–569.
structureanddiversity. Furthermore, differencesinsocialcall
variabilitybetweenM.macrodactylus femaleswasfound, and HatchwellBJ,SharpSP,SimeoniM,McGowanA.2009.Factorsinfluencing
individuals emitting more complex social calls took less time overnight loss of body mass in the communal roosts of a social bird.
to rejoin the cluster. However, further work is needed to FunctionalEcology,23(2):367–372.
investigatethespecificfunctionofthisdiversityinsocialcalls. Jahelková H, Horácˇek I, Bartonicˇka T. 2008. The advertisement song of
Pipistrellus nathusii (Chiroptera, Vespertilionidae): a complex message
COMPETINGINTERESTS
containingacousticsignaturesofindividuals.ActaChiropterologica, 10(1):
Theauthorsdeclarethattheyhavenocompetinginterests. 103–126.
JanßenS,SchmidtS.2009.Evidenceforaperceptionofprosodiccuesin
AUTHORS’CONTRIBUTIONS
batcommunication:contactcallclassificationbyMegadermalyra.Journalof
Y.H.X. and L.W. completed the experiments in lab, and supervised the ComparativePhysiologyA,195(7):663–672.
analyses, anddraftedthemanuscript. L.W.andJ.F.conceivedthestudy KanwalJS,MatsumuraS,OhlemillerK,SugaN.1994.Analysisofacoustic
anddesignedthestudy.L.W.,T.L.J.andA.Q.L.participatedinthefieldwork. elementsandsyntaxincommunicationsoundsemittedbymustachedbats.
Y.H.X.andJ.R.H.revisedthemanuscript.Allauthorsreadandapprovedthe TheJournaloftheAcousticalSocietyofAmerica,96(3):1229–1254.
finalmanuscript. Kanwal JS. 2009. Audiovocal communication in bats. In: Squire L R.
EncyclopediaofNeuroscience.Oxford,UK:AcademicPress,681–690.
REFERENCES
KanwalJS.2012.Right–leftasymmetryinthecorticalprocessingofsounds
Bastian A, Schmidt S. 2008. Affect cues in vocalizations of the bat, for social communication vs. navigation in mustached bats. European
Megadermalyra,duringagonisticinteractions.TheJournaloftheAcoustical JournalofNeuroscience,35(2):257–270.
SocietyofAmerica,124(1):598–608. KerthG.2008.Causesandconsequencesofsocialityinbats.BioScience,
BehrO,vonHelversenO.2004.Batserenades-complexcourtshipsongs 58(8):737–746.
of the Sac-winged bat (Saccopteryx bilineata). Behavioral Ecology and Knörnschild M, von Helversen O. 2008. Nonmutual vocal mother-pup
Sociobiology,56(2):106–115. recognition in the greater sac-winged bat. Animal Behaviour, 76(3):
BehrO,KnörnschildM,vonHelversenO.2009.Territorialcounter-singingin 1001–1009.
malesac-wingedbats(Saccopteryxbilineata): low-frequencysongstrigger KnörnschildM,GlöcknerV,vonHelversenO.2010.Thevocalrepertoireof
astrongerresponse.BehavioralEcologyandSociobiology,63(3):433–442. twosympatricspeciesofnectar-feedingbats(GlossophagasoricinaandG.
BohnKM,Schmidt-FrenchB,MaST,PollakGD.2008.Syllableacoustics, commissarisi).ActaChiropterologica,12(1):205–215.
temporal patterns, and call composition vary with behavioral context in Kobayasi KI, Hiryu S, Shimozawa R, Riquimaroux H. 2012. Vocalization
Mexicanfree-tailedbats.TheJournaloftheAcousticalSocietyofAmerica, ofecholocation-likepulsesforinterindividualinteractioninhorseshoebats
124(3):1838–1848. (Rhinolophus ferrumequinum). The Journal of the Acoustical Society of
BohnKM,Schmidt-FrenchB,SchwartzC,SmothermanM,PollakGD.2009. America,132(5):EL417–EL422.
Versatilityandstereotypyoffree-tailedbatsongs.PLoSOne,4(8):e6746. Ma J, Kobayasi K, Zhang SY, Metzner W. 2006. Vocal communication
BradburyJW.1977.Socialorganizationandcommunication.In:WimsattWA. in adult greater horseshoe bats, Rhinolophus ferrumequinum. Journal of
BiologyofBats.NewYork:AcademicPress,2–72. ComparativePhysiologyA,192(5):535–550.
BudenzT,HeibS,KuschJ.2009.Functionsofbatsocialcalls:theinfluence McCrackenGF,WilkinsonGS.2000.Batmatingsystems.In:CrichtonEG,
oflocalabundance,interspecificinteractionsandseasonontheproductionof Krutzsch PH. Reproductive Biology of Bats. New York: Academic Press,
pipistrelle(Pipistrelluspipistrellus)typeDsocialcalls.ActaChiropterologica, 321–362.
11(1):173–182. Morton ES. 1977. On the occurrence and significance of
ClementMJ,DietzN,GuptaP,KanwalJS.2006.Audiovocalcommunication motivation-structuralrulesinsomebirdandmammalsounds.TheAmerican
andsocialbehaviorinmustachedbats.In:KanwalJS,EhretE.Behaviorand Naturalist,111(981):855–869.
Neurodynamics for Auditory Communication. Cambridge, UK: Cambridge Pfalzer G, Kusch J. 2003. Structure and variability of bat social calls:
UniversityPress. implications for specificity and individual recognition. Journal of Zoology,
DugatkinLA,EarleyRL.2004.Individualrecognition,dominancehierarchies 261(1):21–33.
andwinnerandlosereffects.ProceedingsoftheRoyalSocietyB:Biological Russ JM, Jones G, Mackie IJ, Racey PA. 2004. Interspecific responses
Sciences,271(1547):1537–1540. to distress calls in bats (Chiroptera: Vespertilionidae): a function for
ZoologicalResearch39(2):114-122,2018 121
convergenceincalldesign?AnimalBehaviour,67(6):1005–1014. SeniorP,ButlinRK,AltringhamJD.2005.Sexandsegregationintemperate
Russ JM, Racey PA. 2007. Species-specificity and individual variation in bats.ProceedingsoftheRoyalSocietyB:BiologicalSciences,272(1580):
the song of male Nathusius’ pipistrelles (Pipistrellus nathusii). Behavioral 2467–2473.
EcologyandSociobiology,61(5):669–677. Seyfarth RM, Cheney DL, Bergman T, Fischer J, Zuberbühler K,
RussoD,JonesG.1999.ThesocialcallsofKuhl’spipistrellesPipistrellus HammerschmidtK.2010.Thecentralimportanceofinformationinstudies
kuhlii (Kuhl, 1819): structure and variation (Chiroptera: Vespertilionidae). ofanimalcommunication.AnimalBehaviour,80(1):3–8.
JournalofZoology,249(4):476–481. WilkinsMR,SeddonN,SafranRJ.2012.Evolutionarydivergenceinacoustic
Schehka S, Esser KH, Zimmermann E. 2007. Acoustical expression of signals: causesandconsequences.TrendsinEcology&Evolution,28(3):
arousalinconflictsituationsintreeshrews(Tupaiabelangeri).Journalof 156–166.
ComparativePhysiologyA,193(8):845–852.
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