ORIGINAL PAPER

Carolyn L. Pytte Æ Millicent S. Ficken Æ Andrew Moiseff

Ultrasonic singing by the blue-throated hummingbird: a comparisonbetween production and perception

Received: 23 September 2003 / Revised: 18 March 2004 / Accepted: 9 April 2004 / Published online: 26 May 2004� Springer-Verlag 2004

Abstract Blue-throated hummingbirds produce elabo-rate songs extending into the ultrasonic frequency range,up to 30 kHz. Ultrasonic song elements include har-monics and extensions of audible notes, non-harmoniccomponents of audible syllables, and sounds producedat frequencies above 20 kHz without correspondinghearing range sound. To determine whether ultrasonicsong elements function in intraspecific communication,we tested the hearing range of male and female blue-throated hummingbirds. We measured auditory thresh-olds for tone pips ranging from 1 kHz to 50 kHz usingauditory brainstem responses. Neither male nor femaleblue-throated hummingbirds appear to be able to hearabove 7 kHz. No auditory brainstem responses could bedetected between 8 and 50 kHz at 90 dB. This high-frequency cutoff is well within the range reported forother species of birds. These results suggest that high-frequency song elements are not used in intraspecificcommunication. We propose that the restricted hum-mingbird hearing range may exemplify a phylogeneticconstraint.

Keywords Hearing Æ Hummingbird Æ Perception ÆSong Æ Ultrasound

Introduction

Hummingbirds (Trochilidae: Apodiformes) are notrenowned for the splendor or complexity of their vocal-izations. Perhaps, however, this is an oversight reflectingour sensory bias against the shrill and high-pitchedsounds produced by many hummingbird species. Schu-chmann (1999) noted that high frequencies are commonamong hummingbirds and reported that the song of theblack jacobin (Florisuga fusca) may in fact containultrasonic components. We have observed a SouthAmerican hummingbird perched in a singing posturewhile fluttering its throat feathers without any audiblesound, indicating the possibility of song frequenciesoutside the range of human hearing (M.S. Ficken, per-sonal observation). The blue-throated hummingbird(Lampornis clemenciae) also demonstrates unusual sing-ing behaviors which are suggestive of the use of ultrasonicfrequencies, and is notable for its large and complex vocalrepertoire (Ficken et al. 2000).We decided to test whetherthis species emits ultrasounds, and if so, to determine thehearing range of blue-throated hummingbirds.

Avian species which echolocate and might beexpected to use ultrasound, such as the nocturnal oilbird(Steatornis caripensis) and cave-dwelling swiftlets (genusCollocalia), produce broadband echolocation clicks witha maximum energy concentration below 8 kHz, wellwithin the sonic range (Pye 1980; Suthers and Hector1982, 1985). Ultrasonic harmonics have recently beendescribed in the songs of the oscine rufous-faced warbler(Abroscopus albogularis) demonstrating that it is notoutside the capability of the syrinx to generate extremelyhigh-frequency sounds (Narins et al. 2004). Humming-birds, along with swifts, compose an independent orderthat is phylogenetically distant from the songbirds (os-cine passerines) and parrots (Psittaciformes) which havelargely dominated the study of avian sound productionand perception. Despite the wealth of knowledge ofhearing in other birds, hearing tests have not been pre-viously performed on any hummingbird species.

C. L. Pytte (&)Biology Department, Wesleyan University,Middletown, CT 06459, USAE-mail: cpytte@wesleyan.eduFax: +1-860-6853785

M. S. FickenDepartment of Biological Sciences,University of Wisconsin-Milwaukee and UWM Field Station,3095 Blue Goose Road, Saukville, WI 53080, USA

A. MoiseffDepartment of Physiology and Neurobiology,University of Connecticut, 3107 Horsebarn Hill Road,Storrs, CT 06269, USA

J Comp Physiol A (2004) 190: 665–673DOI 10.1007/s00359-004-0525-4

Blue-throated hummingbirds exhibit strong nichespecificity, inhabiting wooded riparian canyons in theextreme southwestern United States and Mexico. In thebreeding season, males establish and defend territoriesalong streams. During this time, males produce twopredominant vocalizations: repetitions of acousticallysimple notes, ‘‘serial chips,’’ which apparently function inlong-distance territorial advertisement, and a structurallyand syntactically complex song which appears to attractboth males and females. Playback of male song results ina significant number of approaches by males to theplayback speaker (Ficken et al. 2002). Attraction offemales to singing males has been observed with regu-larity in the field, whereas females have never been ob-served to approach silent males despite the fact that malesspend a much greater portion of time resting than sing-ing. Female attraction to male song seems to be related tocourtship behavior and the attraction of males appears tooccur in aggressive contexts (Ficken et al. 2002).

There are several aspects of the blue-throated hum-mingbird’s singing behavior which are puzzling andwhich led to our choice of this species for investigation ofultrasound use. Selective pressures for effective mateattraction would presumably result in song transmissiondistance at least to the territory boundary (approxi-mately 15 m, based on our observations of territory size).However, blue-throated song is produced at an extremelylow amplitude (<30 dB at 10 m), much less than that ofagonistic vocalizations or serial chips (Pytte et al. 2003).To our ears, the song cannot be heard from more than afew meters from the singing bird. In addition, rather thanavoiding high background noise, birds generally singwithin several meters of a stream and often perched rightabove one. In such cases, the background noise entirelyobscures our detection of the song. Furthermore, maleshave been observed to sing up to 10 min at a stretch inthe absence of other individuals in the vicinity, suggestingthat it may not function solely as a short range signalalthough the song is also used in dual singing interactionsbetween a male and female perched a few centimetersapart (Ficken et al. 2000). However, despite the lowsignal-to-noise ratio during song production, we suspectthat localization of singing males is primarily based onauditory cues. This has been supported by numerousobservations of females approaching singing males thatare perched in dense vegetation obscuring visual cues(M.S. Ficken, personal observation), as well as playbackstudies with a hidden speaker (Ficken et al. 2002).

The use of ultrasonic frequencies during singingwould essentially explain this perplexing singing behav-ior—the production of a complex, low-amplitude song,while visually obscured in a noisy environment. Whilethe sounds audible to humans are very low in amplitude,perhaps ultrasonic frequencies carry the majority of thesound energy.

High frequencies would increase the signal band-width, facilitating sound localization (Park and Dooling1991; Dooling 1992), and also provide an acousticchannel, improving the signal to noise ratio for intra-

specific communication. Although high frequencies donot transmit over long distances, ultrasonic singingcould enhance signal detection by making use of a fre-quency channel that is relatively free from competitionfrom water noise and vocalizations of other birds,thereby providing a valuable sound window for broad-casting song.

Here, we present the results of ultrasonic recordingsof male song and of hearing tests in the male and femaleblue-throated hummingbird using auditory brainstemresponses (ABRs) to pure tones to reveal their audiblefrequency range.

Materials and methods

Ultrasonic production

Recordings

Recordings of sonic and ultrasonic vocalizations andmechanical (wing and tail) noises were made using adual recording system to collect data in the hearingrange simultaneously with sound in the ultrasonic range.We recorded with a Sony Walkman WM-D6C (flatfrequency response from 40 Hz to 15 kHz) and anAudiotechnica AT877 microphone (flat response from60 Hz to 14 kHz) as well as with another Sony Walk-man WM-D6C connected to a Pettersson UltrasoundDetector D230 (flat response from 10 to 120 kHz, fre-quency division setting). Recordings were made ontosynchronized analog tapes which are archived at theUniversity of Wisconsin-Milwaukee Field Station.Sound detected by the ultrasonic microphone wastransposed by a factor of 10 in the frequency domainprior to recording on tape while the original amplitudeenvelope and true time domain were maintained. Therecording input level on both recorders was adjusted toensure that artificial harmonics and other syntheticacoustics were not produced.

Eleven songs were used in this study, recorded fromfour individually identified males (4 songs from onemale, 3 from another, and 2 from two others). The songswere selected from a larger sample of songs within asinging bout. Males were identified by territory occu-pancy as territories were linear and non-overlapping(Williamson 2000, personal observation). Recordingswere made in a territory only once to provide additionalcertainty of recording from a specific individual. Werecorded singing throughout the day during the breedingseason in August 2000 at the Southwestern ResearchStation, Portal, Arizona.

Analysis

Ultrasonics are defined as sound frequencies above theupper boundary of human hearing, generally consideredto be 20 kHz. Although our ‘‘hearing range’’ recordingsand ‘‘ultrasonic range’’ recordings overlap, we regard

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ultrasonic frequencies as only those above 20 kHz.Spectrographs of the hearing range and ultrasonic rangerecordings were printed using a Kay Elemetrics Sona-Graph (7800, 16-kHz scale, 300-Hz bandwidth). Spec-trographs of the ultrasonic signal display a time axis thatis identical to that of the hearing range signal, and afrequency axis that is a multiple of 10 times that of thehearing range spectrographs. Thus, using the 0- to 16-kHz setting, the frequency range of ultrasound spec-trographs is 10–160 kHz. Hearing range and ultrasonicrange recordings were aligned temporally and analyzedusing Raven (Beta 1, 2002 Cornell Laboratory ofOrnithology), Sound Analysis 3.19 (Tchernichovskiet al. 2000) and Avisoft (4.2, Specht). Power spectrawere produced with Avisoft using the hamming func-tion, a bandwidth of 2.2 Hz, resolution of 1.3 Hz, andsmoothing over 41.7 Hz. Peak detection of the powerspectra were determined using )10 dB from the maxi-mum peak amplitude and a hysteresis value of 10 dB.The frequencies of maximum energy (peak power)throughout the song were identified using Sound Anal-ysis.

In order to examine ultrasonic components of thesong that are not simply extensions or harmonics ofhearing range sounds, we identified sounds that metthese criteria: (1) ultrasonic elements which did not alsocontain energy in the hearing range and (2) ultrasoniccomponents which differed in acoustic structure fromsimultaneous hearing range sound. In addition, wenoted song elements in the hearing range that did notcontain ultrasonic components.

Perception

Subjects

Adult male and female blue-throated hummingbirds(n=4 males, 2 females) were mist-netted in southeasternArizona and transported to Wesleyan University wherethey were housed until completion of the hearing tests.The birds were housed in individual 0.5-m3 mesh cagesin a communal room and kept in visual isolation inorder to minimize stress. Blue-throated males are highlyterritorial during the breeding season and displayaggressive behaviors to males within view. The birdswere able to interact vocally. Throughout the period ofcaptivity, the birds were maintained on photo periodand temperature conditions matched to those of theircapture location. They were provided with commerciallyprepared hummingbird food (Nekton, Nektar-plus)made fresh daily. Mean (±SE) bird weights were8.15±0.14 (males) and 6.05±0.05 (females).

ABR recording

The birds were anesthetized with an intramuscularinjection of 24 lg g)1 xylazine and 12 lg g)1 ketamine.

Supplemental doses were not necessary. Feathers wereremoved from the crown of the head and bilaterallycaudal to the external auditory meatus. Electrodes (400-lm steel wire) were inserted subcutaneously at the apex(positive), caudal to the right ear (negative), and caudalto the left ear (ground), and held in place with tissueadhesive. All tests were conducted within a sound-attenuating, anechoic room. The bird was wrappedloosely in a cloth surrounded by a heating pad. Bodytemperature was maintained at 37�C. The bird wasplaced with both ears equidistant to the speaker, withthe external ear canals 30 mm from the speaker and thebeak 90� to the flat surface of the speaker, centeredapproximately at the speaker midline.

Custom designed software (by A.M.) interfaced witha sine wave generator (AG-7001C Audio Generator,frequency range 10 Hz–1 MHz, distortion <0.1% at500 Hz–100 kHz; EZ-Digital) controlled the generationof stimuli, timing of presentation, and ABR acquisition.Stimuli were output through an electrostatic driver(ED1; Tucker Davis Technologies, Gainesville, Fla.,USA) connected to an electrostatic speaker (ES-1, flatfrequency response between 1 kHz and 110 kHz; TuckerDavis Technologies, Gainesville, Fla., USA). Responseswere band-pass filtered (10–3 kHz) and passed througha 60-Hz notch filter before amplifying. Amplifier gainwas calibrated using a voltage calibrator (2010 OmnicalVoltage Calibrator, World Precision Instruments). Re-sponses were viewed in real-time on a digital oscillo-scope (Tektronix 2230) and, simultaneously, 40-msepochs were digitized (25-kHz sample rate) for averag-ing. Electronic delays were employed so that responsesampling began 4.5 ms before the onset of the soundstimulus as recorded at the bird’s ears. Averages from 50stimulus presentations were viewed on a monitor andstored for offline analysis. At the end of the recordingsession, the birds were given a 0.6 lg g)1 intramuscularinjection of yohimbine and placed under a heat lampuntil they fully recovered from anesthesia.

Stimuli

The hummingbirds were tested for ABR thresholdsusing tone pips between 1 kHz and 50 kHz, 8 ms induration including 1 ms rise and fall, presented with a750-ms interstimulus interval. Frequencies were pre-sented in an arbitrary order at 0.5- or 1-kHz incrementsbetween 1 and 10 kHz, at 12 kHz, and at 5-kHz incre-ments from 15 to 50 kHz. All measurements are pre-sented in dB re. 20 lPa. At each frequency, stimulusintensity was varied by 10-dB steps until near threshold,and by 3-dB steps surrounding threshold until the ABRthreshold was identified. Stimulus intensity ranged from30 dB to a maximum of 90 dB and was monitored witha calibrated microphone located midway between thespeaker and the bird’s head, positioned so that it did notblock the sound path to the ears. Stimulus intensity inthe audio range (<15 kHz) was confirmed in the free

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field using a sound pressure level meter (Bruel and Kjaer2226) placed at the position of the bird’s ear byrecording SPLs directly using the same tones presentedas stimuli. Ultrasonic sound intensities were determinedby measuring the voltage output of the ultrasonicmicrophone on an oscilloscope and calculating dB re.20 lPa.

ABR analysis

Evoked potential peaks were identified visually in therecording trace by two observers. The lowest intensity atwhich a response was present was determined to be theresponse threshold (as in Boettcher et al. 1993; Brittan-Powell and Dooling 2002). The ABR was identified as apeak above baseline followed by a trough below thebaseline waveform. We did not attempt to identifymultiple successive peaks since a single, broad peak ischaracteristic of long duration stimuli such as thoseused. The neural generators of the ABR wave are un-known for hummingbirds. Peak latencies and ampli-tudes were not measured since our objective was toidentify the presence or absence of a response in order togenerate a threshold audiogram.

Results

Ultrasonic production

Blue-throated hummingbirds produce ultrasonic soundsvocally during singing as well as mechanically by shuf-fling tail and wing feathers while perched. Sound pro-duced while tail shuffling is composed of transient clicks(15–30 kHz). Interpulse intervals are highly stereotypedacross tail shuffling episodes. Wing noises are similarlybroadband short duration clicks, although interpulseintervals are not stereotyped. Tail shuffling appears to bea ritualized behavior and occurs in the context of closerange agonistic encounters, usually produced by a ter-ritory resident when confronted by an intruding hum-mingbird. Wing sounds are produced in this context aswell, and were also observed after agonistic encounterswhile apparently guarding a food source.

A detailed description of the sonic song elements haspreviously been reported (Ficken et al. 2000). As in thesonic range, ultrasonic frequencies contain acousticallydifferentiated syllables composed primarily of broad-band transients, clicks, and trills. Song organization isbased on five different sets of syllable clusters or song‘‘units’’ A–E (Fig. 1). Within a unit, syllables are entirelystereotyped in acoustic structure and order. Thesequence of units comprising a song may vary in numberand order; however, the variation follows specificsequencing rules (Ficken et al. 2000). As has beenreported for sounds in the hearing range (Ficken et al.2000), ultrasonic elements are stereotyped within indi-viduals and between individuals in a population.

All song units contain syllables that include ultra-sonic components, some of which appear to be har-monics of sonic fundamentals. Other ultrasonic elementsare high-frequency extensions of broadband transientsand clicks notes. As these elements are not acousticallydifferentiated in the ultrasonic range, there is no com-pelling reason to suggest that these categories of soundsmay contain additional information not provided withinthe sonic range. Instead, we were interested in ultrasonicelements which did not also contain energy in thehearing range, as well as ultrasonic components of noteswhich differed in acoustic structure from simultaneoushearing range sound. Several ultrasonic elements meetthese criteria (Fig. 1).

Perception

ABRs

ABR waveforms consisted of a single broad peak con-tained within 4 ms after the sound reached the bird’s ear.A typical ABR to an 87-dB stimulus exhibits a 1-mspeak beginning approximately 1.5 ms after stimulusarrival at the ears, followed by a 1.5-ms depression be-fore returning to baseline. As is characteristic of theABR across vertebrates, decreased stimulus intensityresulted in decreased peak amplitude and increasedresponse latency (Fig. 2) (Corwin et al. 1982).

Hearing range

Most importantly for our purposes, we conclude thatneither male nor female blue-throated hummingbirdshear high frequencies between 8 and 50 kHz (at 90 dB),as determined by ABR. We tested tones at 1- to 5-kHzintervals throughout this range in search of discontinu-ous sensitivity or a sensitivity window as has been re-ported in some rodent species (review in Sales and Pye1974). Instead, the highest frequency at which athreshold response was noted was 7 kHz for both malesand females (Fig. 3a). None of the birds exhibited aresponse to an 8-kHz tone, and no intervals between 7and 8 kHz were tested.

Females demonstrated a range of best hearing forfrequencies between 1 and 3 kHz and a peak in sensi-tivity at 2.0 kHz. The range of best hearing is arbi-trarily defined here as the frequencies eliciting athreshold response within 20 dB of the peak hearingsensitivity. The mean female hearing thresholdincreases 16 dB between 2.5 and 3.0 kHz. Malesshowed best hearing for frequencies between 1.0 and3.5 kHz, with peak sensitivity at 2.5 kHz. The meanmale hearing threshold increases by 9 dB between 2.5and 3.0 kHz.

The overall response curve of the males is not sig-nificantly different from that of the females (ANCOVA,P>0.05). Females appear to have a lower hearingthreshold at 2.0 kHz, however, the differences are not

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significant (Mann Whitney U, P>0.05, Fig. 3a). Themean of males and females combined reveals a range ofbest hearing between 1.0 and 3.5 kHz, a peak in sensi-tivity at 2.5 kHz, and an increase in threshold ofapproximately 11 dB between 2.5 and 3.0 kHz (Fig. 3b).

Comparison of hearing range and song vocalizations

The frequencies of peak hearing sensitivity (2.0 and2.5 kHz) do not correspond to a peak in the concen-tration of energy in the song (Fig. 4). Amplitude peaksin the song power spectrum occur at 3.3, 5.8, 6.9 and8.6 kHz. Of the frequencies produced below 10 kHz,only 25% of the sound energy falls between 1.0 and3.5 kHz, within the range of best hearing. Interestingly,the majority of the peak frequency trace (frequency ofmaximum power at any given time) occurs at 4.0 kHz,

just outside the upper boundary of the range of besthearing (Fig. 5). Furthermore, we find that the peaksensitivity frequencies of 2.0 and 2.5 kHz do not corre-spond to any distinctive acoustic elements of the song(Fig. 5).

Discussion

Production

The blue-throated hummingbird’s song differs fromtypical oscine songs in that it is atonal and composedprimarily of broadband transients, fricative soundbursts, and click-note trills (Ficken et al. 2000). It is alsounusual in its wide frequency range, extending from1.8 kHz to approximately 30 kHz. The ultrasonic

Fig. 1 Blue-throatedhummingbird song. Song of amale blue-throatedhummingbird recorded at theSouthwestern Research Stationduring the breeding seasonshowing the five componentsong units A–E. An examplesound element that is producedsolely within the ultrasonicrange is indicated with (1). Anexample of a syllable composedof differing acousticmorphologies in the ultrasonicand sonic ranges is noted with(2). Examples of other songelement types are broadbandtransient notes which extendfrom the sonic into theultrasonic range (3), syllablesproduced within the hearingrange with a possible ultrasonicharmonic (4), and syllablesproduced entirely within thehearing range (5)

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(>20 kHz) components of the song include continuousextensions of hearing range sound, harmonics of hearingrange elements, non-harmonic sounds which are pro-duced in concert with sonic elements, and also elementsthat are produced without corresponding sonic sound.

High frequencies are not a necessary correlate ofsound production by blue-throated hummingbirds asterritorial advertisement serial chips do not containfrequencies above 7 kHz (Ficken et al. 2002). It isunlikely that the distinctive acoustic structure of thesong is the result of the small size of the sound pro-ducing apparatus since smaller hummingbird speciesproduce whistles, frequency modulations, and tonalsounds (reviewed by Kroodsma et al. 1996; Ornelas et al.2002). Furthermore, we could not detect any ultrasonicsounds produced by hummingbirds smaller than theblue-throated, including the black-chinned (Archilochusalexandri), Anna’s (Calypte anna) and broad-tailed(Selasphorus platycercus) hummingbirds. The magnifi-cent hummingbird (Eugenes fulgens) and white-earedhummingbird (Hylocharis leucotis) songs have elementsthat extend above 15 kHz but these components are acontinuation of sonic elements and thus not as intriguingas the ultrasonic sounds of the blue-throated hum-mingbird’s song.

Perception

The primary goal of the hearing tests was to identify thehigh end of the hearing range in order to establishwhether or not blue-throated hummingbirds can hear

the ultrasonic sounds that they produce. Second, wesought to determine the frequency of peak hearing sen-sitivity and compare this with acoustic features of thesong. The results of ABR tests indicate that neither malenor female blue-throated hummingbirds hear ultrasonicfrequencies. Rather, they have a maximum audible fre-quency of 7 kHz at 90 dB. Blue-throated hummingbirdshear best between 1.0 and 3.0 or 3.5 kHz with a peak insensitivity at 2.0–2.5 kHz (females and males, respec-tively).

A correlation between the frequency of peak hearingsensitivity and specific spectral features of song has beendemonstrated in passerines and also psittacines (Doolinget al. 1971; Konishi 1971; Dooling and Saunders 1975).We find that the frequency range of best hearing over-laps the largest peak in the power spectrum of the blue-throated song. However, the peaks in hearing sensitivitydo not correspond to frequencies of increased amplitude(Fig. 4) nor to any distinctive acoustic elements of thesong (Fig. 5). Furthermore, much of the maximumpower lies just outside the upper boundary of besthearing (at 4.0 kHz) rather than within the 1.0–3.5 kHzbest hearing range (Fig. 5). The significance of this forsignal processing, if any, is unknown. In addition, there

Fig. 2 Example of an ABR waveform. The top trace is a typicalABR, produced by a male in response to a 2-kHz tone presented at87 dB SPL. Subsequent traces show decreasing peak amplitude andincreased response latency correlated with decreasing stimulusintensity. Sound reaches the bird’s ear at time 4.5 ms (arrow)

Fig. 3 a, b Audiograms. a Mean (±SE) threshold ABRs for malesand females at each frequency. b The combined (mean±SE) maleand female audiogram. All subjects were tested up to 50 kHz. Noresponses to pure tone stimuli were obtained above 7 kHz at up to90-dB stimulus intensity, the maximum intensity that we couldpresent

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are no known calls in the repertoires of either adults orjuveniles that contain substantial energy below 3.5 kHz(Ficken et al. 2002). In fact, most of the sound energy ofagonistic calls, alarm calls, serial chips, fledgling calls, aswell as female song, is concentrated well above 3.5 kHz,and in the case of serial chips is entirely contained nearthe outer extent of the hearing range, between 6 and7 kHz. Perhaps a more consistent account of the fre-quency of peak sensitivity and range of best hearing inthe blue-throated hummingbird is that these character-istics have not been shaped entirely by pressures ofcommunication.

Evolution of hummingbird hearing

Two explanations are commonly proposed to explaincharacteristics of hearing: (1) behavioral adaptations,for example, sound localization, predator detection, orintraspecific communication; and (2) phylogenetic anddevelopmental constraints on head and auditory struc-

ture morphologies. The latter explanation is supportedby numerous examples in mammals in which theperipheral auditory system appears to have evolvedlargely independent of behavioral factors (Plassman andBrandle 1992). Similarly, it appears that in the blue-throated hummingbird, neither the maximal audiblefrequency nor the peak sensitivity frequency correspondto any obvious behaviorally adaptive correlates.

A comparison of behaviorally determined audio-grams among three groups of birds indicates that non-passerines (excluding owls) have a lower maximumaudible frequency (7.5 kHz) than passerines (9.7 kHz),and both groups have a lower high-frequency cutoffthan owls (11.2 kHz). Non-passerines have the lowestpeak frequency sensitivity (2.1 kHz), followed by owls(2.7 kHz), then passerines (2.9 kHz). These data are themeans of two species of Strigiformes (barn owl and greathorned owls), eight species of other nonpasserines, and13 species of passerines (reviewed by Dooling 1992).Ignoring the adaptive specializations of the owls fornocturnal prey capture, characteristics of hummingbird

Fig. 4 Power spectrum of song.Power spectrum of a single song(units A–E). The box enclosesthe mean frequency range ofbest hearing for males andfemales combined (1–3.5 kHz).The shaded bar indicates thesound energy between 2 and2.5 kHz, the frequencies ofpeak sensitivity in females andmales, respectively. Arrowspoint to peaks in power at 3.3,5.8, 6.9, and 8.6 kHz

Fig. 5 Peak frequency trace.The frequency of maximumenergy at any given timethroughout a single song isoutlined in red. The horizontalline indicates 4 kHz whichtraces the majority of themaximum sound energy

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hearing are nearly identical to the mean of the othernonpasserines that have been tested.

Nonpasserines, including Apodiformes, are thoughtto evolutionarily pre-date passerines. Therefore, thecurtailed frequency range of hummingbird hearingcompared to their vocal production may represent aphylogenetic constraint. Such constraints are generallydue to limitations of the cochlear and middle earstructures, peripheral transduction, or central auditoryprocessing (Sachs et al. 1978). High frequency process-ing in birds begins in the basal region of the basilarpapilla. The barn owl, which has the highest audiblefrequency, also has the longest basilar papilla describedin birds, about 11 mm (reviewed by Carr 1992). Perhapsthe length of the basilar papilla in the hummingbird isconstrained by small head side, thus prohibiting high-frequency hearing in small birds.

Similarly, peak sensitivity is determined by thedimensions of a few middle ear structures which, in turn,are stringently coupled to phylogenetic and develop-mental factors. A shift in peak sensitivity toward lowerfrequencies can be achieved by increasing the middle earvolume, however this is largely constrained by overallhead size. A shift in the peak sensitivity range to higherfrequencies can occur by thickening the basilar mem-brane in the cochlea (Neuweiler et al. 1980). However,peak sensitivity is not likely to be subject to behavioralselective pressure; instead, behaviorally adaptive pres-sures more often expand or shift the overall range ofhearing, without altering peak sensitivity (Plassman andBrandle 1992). Our data are consistent with this idea inthat peak sensitivity in the blue-throated hummingbirddoes not correspond to any notable vocal attributes and isthe same as that of other non-passerines, excluding owls.

Methodological constraints

It must also be considered that while frequency-depen-dent ABRs correspond well with the shape of behav-iorally generated audiogram curves, ABR audiogramsare not necessarily consistent with absolute auditorysensitivity and may underestimate the perceived soundlevel thresholds (Borg and Engstrom 1983; Mann et al.2001; Stapells and Oates 1997; Wenstrup 1984). Specif-ically in birds, ABR-generated audiograms reflect thebandwidth and shape of the behavioral audiogram,including the frequencies of peak sensitivity (mallardduck, Anas platyrhynchos, Dmitrieva and Gottlieb 1992;Bengalese finch, Lonchura striata domestica, Woolleyand Rubel 1999; budgerigar, Melopsitt undulatus, Brit-tan-Powell et al. 2002). However, Brittan-Powell andDooling (2002) report that in budgerigars, the ABR-generated audiogram is 30 dB higher than the behav-iorally generated audiogram. Thus, it is not unlikely thatthe hearing threshold levels may be lower in blue-throated hummingbirds than demonstrated by the ABRand frequencies higher than 7 kHz may in fact be per-ceived. However, shifting the absolute sensitivity level by

30 dB would not alter the steep drop in hearing sensi-tivity between 5 and 7 kHz nor the peak sensitivities at2.0 and 2.5 kHz, and would not necessarily result in theinclusion of ultrasonic frequencies. Furthermore, ingenerating behavioral audibility curves, the high fre-quency cutoff is defined as the highest frequency a birdcan hear at a sound pressure level of 60 dB SPL(Dooling 1980). Because we used a 90-dB stimulus todetermine audibility thresholds using the ABR, we havesomewhat compensated for the differences between thetwo methods. The ABR is not limited by ultrasonicfrequencies per se, as it has been shown to successfullyidentify hearing ranges that extend up to 80 kHz inclupeiform fishes (Mann et al. 2001).

Why ultrasound production?

Thus far, we cannot provide an adaptive explanation forthe production of ultrasonic vocalizations, whichapparently do not function in intraspecific communica-tion. Blue-throated hummingbirds often alternate sing-ing with catching small flying insects. Perhaps theultrasonic clicks produced during singing flushes insectsfrom vegetation, or triggers erratic insect flight patterns,thereby increasing visual salience for the hummingbird.However, we have not observed any such effect ofsinging on insects. Furthermore, vocal click sounds thatare produced by blue-throated hummingbirds whileactually chasing flying insects are audible and do notcontain ultrasonic components (unpublished data). Wealso believe it is unlikely that ultrasound in blue-throated song repels small rodents that prey on nestlinghummingbirds. Male blue-throated hummingbirds donot guard nests and females have not been observed tosing near nests (Johnsgard 1983). Blue-throated hum-mingbirds have been observed to compete with the lesserlong-nosed bat (Leptonycteris curasoae) and the Mexi-can long-tongued bat (Choeronycteris mexicana) atagave plants in early mornings and evenings (SummerBennett, personal communication). These are times ofpeak song production and thus ultrasonic sounds couldsignal to bats a site of high resource competition.However, even though ultrasonic elements might in factbe detected by bats, there is no evidence that thisinteraction may have provided selective pressure to thestructure of blue-throated song.

The high frequency cutoff in birds is usually related tothe highest frequency in the species’ song, and thehearing sensitivity in many species is correlated withtheir spectral output (reviewed by Dooling 1982).However, this is not an absolute association. As dem-onstrated by Konishi (1971), the frequency range ofaudition does not always match the frequency range ofvocalizations. In fact, Woolley and Rubel (1999) dem-onstrate that Bengalese finches may attend only to thefundamental or low dominant frequencies in song(<3 kHz) in order to maintain complete song structureacross a frequency range of up to 10 kHz. Although it is

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more intuitive to dismiss the sound categories of ultra-sonic harmonics and ultrasonic extensions of sonicsounds as epiphenomenal, ultrasonic sounds that arestructurally independent, non-harmonic elements ofhearing range sounds may nonetheless also be epiphe-nomenal artifacts generated by the syrinx or upper vocalstructures during sound production.

It must be considered that ultrasound may indeed beproduced and perceived by other hummingbird speciesnot yet tested. However, the production of ultrasonicfrequencies by blue-throated hummingbirds does notappear to function in intraspecific communication and alikely adaptive explanation for this phenomenon has yetto be identified.

Acknowledgements We thank the Southwestern Research Stationfor housing the hummingbirds. Elizabeth Sandlin provided the useof mist nets and training in hummingbird capture. All animal careand methods complied with the regulations of the InstitutionalAnimal Care and Use Committees of the affiliated universities, theArizona Game and Fish Department, the Connecticut Departmentof Environmental Protection—Wildlife Division, and the US Fishand Wildlife Service, as well as the Principles of Animal Care of theNational Institutes of Health. This research was funded by NSFSGER 0077980.

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