Report Social Calls Predict Foraging Success in Big Brown Bats

Institute for Systems Research, University of Maryland,College Park, MD 20742, USASummaryAnimals foraging in the dark are engaged simultaneously inprey pursuit, collision avoidance, and interactions with con-specifics, makingefficient nonvisual communication essen-tial. A variety of birds and mammals emit food-associatedcalls that inform, attract, or repel conspecifics (e.g., [1]).Big brown bats (Eptesicus fuscus) are insectivorous aerialhawkers that may forage near conspecifics and are knownto emit social calls (e.g., [2–5]). Calls recorded in a foragingsetting might attract (e.g., [6]) or repel [7] conspecifics andcoulddenoteterritorialityor foodclaiming.Here,weprovideevidence that the ‘‘frequency-modulated bout’’ (FMB), a so-cial call emitted only by male bats (exclusively in a foragingcontext)[5],isusedtoclaimfoodandisindividuallydistinct.Bats were studied individually and in pairs in a flight roomequipped with synchronized high-speed stereo video andaudio recording equipment while sex and experience witha foraging task were experimentally manipulated. Malebats emitting the FMB showed greater success in capturingprey. Following FMB emission, interbat distance, divergingflight,andtheotherbat’sdistancetothepreyeachincreased.These findings highlight the importance and utility of vocalcommunication for a nocturnal animal mediating interac-tions with conspecifics in a fast-paced foraging setting.Results and DiscussionWe flew male and female big brown bats (Eptesicus fuscus)alone and in pairs in the presence of a tethered prey item andwithone,both,orneitherbathavingexperiencewiththisnovelforaging task. Synchronized high-speed video and audio re-cordings were acquired and digitally stored, allowing for care-ful analysis of call features and reconstruction of bat 3D flightpathsandpositions.Weexaminedbats’behaviorsurroundingthe frequency-modulated bout (FMB): a sequence of three tofour calls that are longer in duration and lower in frequencythan typical big brown bat echolocation pulses ([5]; Figure 1).In total, we recorded 186 FMBs from at least six individuals.Several lines of evidence indicate that FMBs are individuallydistinct and serve a food-defense function in male bats.FMBs Are Individually Distinct and Only Produced byMalesOf the 186 FMBs recorded, we successfully identified whichbats emitted 90% of the calls. Six individuals flying in 17–57paired trials each emitted at least two FMBs (range per bat:2–65).CallparametersforeachbatarelistedinTableS1(avail-able online), and spectrograms are presented in Figure 1and Figure S1. Results from a discriminant function analysis(DFA; quadratic, assuming unequal covariances) using startfrequency, end frequency, midfrequency (frequency midwaybetween start and end time), duration, and interpulse interval(IPI: time from the end of one pulse to the start of the next)revealedthat96.4%ofFMBswerecorrectlyassignedtothein-dividual emitting the call (Figure 2), compared with a chancelevel of 25%. Correct classification for individual bats variedfrom93.9%to100%,and98.2%ofthevariationwasexplainedby the first two canonical dimensions. Much of the variation isaccounted for by midfrequency and duration (Table S2). Inadditiontoservingafood-defensefunction,thesecallsappearto provide information about the individual.FMBs Are Produced Only When at Least One SkilledForager Is PresentWe never recorded FMBs when only two naive foragers werepresent (n = 181 trials), and FMBs were much more prevalent(80 of 152 trials) when two experienced bats were competingfor the prey item than when only one skilled forager was pre-sent (11 of 170 trials). We considered trials with only naivebats to be a nonforaging context because neither bat wasable to obtain the prey item, whereas trials with at least oneskilledbat wereconsidered to be aforaging context. Althoughcommunicative calls can serve to convey information aboutfoodand/or increase theforaging-related behavior of other in-dividuals(e.g.,rhesusmacaques[Macacamulatta][8];domes-tic chickens [Gallus gallus domesticus][9]; chimpanzees [Pantroglodytes][10]; bonobos [Pan paniscus][11]; marmosets[Callithrix geoffroyi][12]) or coordinate foraging among groupmembers(e.g.,Phyllostomus hastatus[6]),ourresultsindicatethe opposite function of FMBs. The bats from which we re-cordedFMBswerecompetingforasinglepreyitem,thusmak-ing it much more likely that this social call serves to defend orclaim food rather than to attract other bats to a feeding area.FMB Emission Repels Conspecifics from Caller and FoodFollowing FMB emission, bats alter their flight configurationsandincrease their distance from one another, andthe noncall-ing bat increases its distance from the prey item,as describedbelow.FMB Emissions Influence Flight TrajectoriesBats changed their flight configurations (see ExperimentalProcedures for details) following FMB emission significantlymore often than expected by chance. Specifically, for two-thirds of the FMB emissions with corresponding 3D positiondata available, flight configurations changed between the500 ms before and the 500 ms after FMB emission. Whenexamining data for each bat emitting multiple FMBs over thecourse of all trials, flight configuration changed during morethan half of the recordings containing an FMB (range:54.5%–93.8%). For comparison, we examined changes inflight behavior in 12 time segments from non-FMB-emittingfemale-female pairs and found that flight behavior changedin 50% of segments. When the identities of the FMB emitter