J Comp Physiol A (2004) 190: 665–673

DOI 10.1007/s00359-004-0525-4

O R I GI N A L P A P E R

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

Ultrasonic singing by the blue-throated hummingbird: a comparison

between production and perception

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

Abstract Blue-throated hummingbirds produce elabo-

rate songs extending into the ultrasonic frequency range,
Introduction
up to 30 kHz. Ultrasonic song elements include har-
Hummingbirds (Trochilidae: Apodiformes) are not
monics and extensions of audible notes, non-harmonic
renowned for the splendor or complexity of their vocal-
components of audible syllables, and sounds produced
izations. Perhaps, however, this is an oversight reflecting
at frequencies above 20 kHz without corresponding
our sensory bias against the shrill and high-pitched
hearing range sound. To determine whether ultrasonic
sounds produced by many hummingbird species. Schu-
song elements function in intraspecific communication,
chmann (1999) noted that high frequencies are common
we tested the hearing range of male and female blue-
among hummingbirds and reported that the song of the
throated hummingbirds. We measured auditory thresh-
black jacobin (Florisuga fusca) may in fact contain
olds for tone pips ranging from 1 kHz to 50 kHz using
ultrasonic components. We have observed a South
auditory brainstem responses. Neither male nor female
American hummingbird perched in a singing posture
blue-throated hummingbirds appear to be able to hear
while fluttering its throat feathers without any audible
above 7 kHz. No auditory brainstem responses could be
sound, indicating the possibility of song frequencies
detected between 8 and 50 kHz at 90 dB. This high-
outside the range of human hearing (M.S. Ficken, per-
frequency cutoff is well within the range reported for
sonal observation). The blue-throated hummingbird
other species of birds. These results suggest that high-
(Lampornis clemenciae) also demonstrates unusual sing-
frequency song elements are not used in intraspecific
ing behaviors which are suggestive of the use of ultrasonic
communication. We propose that the restricted hum-
frequencies, and is notable for its large and complex vocal
mingbird hearing range may exemplify a phylogenetic
repertoire (Ficken et al. 2000). We decided to test whether
constraint.
this species emits ultrasounds, and if so, to determine the
hearing range of blue-throated hummingbirds.
Keywords Hearing Æ Hummingbird Æ Perception Æ
Avian species which echolocate and might be
Song Æ Ultrasound
expected to use ultrasound, such as the nocturnal oilbird
(Steatornis caripensis) and cave-dwelling swiftlets (genus
Collocalia), produce broadband echolocation clicks with
a maximum energy concentration below 8 kHz, well
within the sonic range (Pye 1980; Suthers and Hector
C. L. Pytte (&) 1982, 1985). Ultrasonic harmonics have recently been
Biology Department, Wesleyan University, described in the songs of the oscine rufous-faced warbler
Middletown, CT 06459, USA (Abroscopus albogularis) demonstrating that it is not
E-mail: cpytte@wesleyan.edu outside the capability of the syrinx to generate extremely
Fax: +1-860-6853785
high-frequency sounds (Narins et al. 2004). Humming-
M. S. Ficken birds, along with swifts, compose an independent order
Department of Biological Sciences,
University of Wisconsin-Milwaukee and UWM Field Station,
that is phylogenetically distant from the songbirds (os-
3095 Blue Goose Road, Saukville, WI 53080, USA cine passerines) and parrots (Psittaciformes) which have
largely dominated the study of avian sound production
A. Moiseff
Department of Physiology and Neurobiology,
and perception. Despite the wealth of knowledge of
University of Connecticut, 3107 Horsebarn Hill Road, hearing in other birds, hearing tests have not been pre-
Storrs, CT 06269, USA viously performed on any hummingbird species.
666
Blue-throated hummingbirds exhibit strong niche
specificity, inhabiting wooded riparian canyons in the
extreme southwestern United States and Mexico. In the
breeding season, males establish and defend territories
along streams. During this time, males produce two
predominant vocalizations: repetitions of acoustically
simple notes, ‘‘serial chips,’’ which apparently function in
long-distance territorial advertisement, and a structurally
and syntactically complex song which appears to attract
both males and females. Playback of male song results in
a significant number of approaches by males to the
playback speaker (Ficken et al. 2002). Attraction of
females 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 males
spend a much greater portion of time resting than sing-
ing. Female attraction to male song seems to be related to
courtship behavior and the attraction of males appears to
occur in aggressive contexts (Ficken et al. 2002).
There are several aspects of the blue-throated hum-
mingbird’s singing behavior which are puzzling and
which led to our choice of this species for investigation of
ultrasound use. Selective pressures for effective mate
attraction would presumably result in song transmission
distance 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 extremely
low amplitude (<30 dB at 10 m), much less than that of
agonistic vocalizations or serial chips (Pytte et al. 2003).
To our ears, the song cannot be heard from more than a
few meters from the singing bird. In addition, rather than
avoiding high background noise, birds generally sing
within several meters of a stream and often perched right
above one. In such cases, the background noise entirely
obscures our detection of the song. Furthermore, males
have been observed to sing up to 10 min at a stretch in
the absence of other individuals in the vicinity, suggesting
that it may not function solely as a short range signal
although the song is also used in dual singing interactions
between a male and female perched a few centimeters
apart (Ficken et al. 2000). However, despite the low
signal-to-noise ratio during song production, we suspect
that localization of singing males is primarily based on
auditory cues. This has been supported by numerous
observations of females approaching singing males that
are perched in dense vegetation obscuring visual cues
(M.S. Ficken, personal observation), as well as playback
studies with a hidden speaker (Ficken et al. 2002).
The use of ultrasonic frequencies during singing
would essentially explain this perplexing singing behav-
ior—the production of a complex, low-amplitude song,
while visually obscured in a noisy environment. While
the sounds audible to humans are very low in amplitude,
perhaps ultrasonic frequencies carry the majority of the
sound energy.
High frequencies would increase the signal band-
width, facilitating sound localization (Park and Dooling
1991; Dooling 1992), and also provide an acoustic
channel, improving the signal to noise ratio for intra-
specific communication. Although high frequencies do
not transmit over long distances, ultrasonic singing
could enhance signal detection by making use of a fre-
quency channel that is relatively free from competition
from water noise and vocalizations of other birds,
thereby providing a valuable sound window for broad-
casting song.
Here, we present the results of ultrasonic recordings
of male song and of hearing tests in the male and female
blue-throated hummingbird using auditory brainstem
responses (ABRs) to pure tones to reveal their audible
frequency range.
Materials and methods
Ultrasonic production
Recordings
Recordings of sonic and ultrasonic vocalizations and
mechanical (wing and tail) noises were made using a
dual recording system to collect data in the hearing
range simultaneously with sound in the ultrasonic range.
We recorded with a Sony Walkman WM-D6C (flat
frequency response from 40 Hz to 15 kHz) and an
Audiotechnica AT877 microphone (flat response from
60 Hz to 14 kHz) as well as with another Sony Walk-
man WM-D6C connected to a Pettersson Ultrasound
Detector D230 (flat response from 10 to 120 kHz, fre-
quency division setting). Recordings were made onto
synchronized analog tapes which are archived at the
University of Wisconsin-Milwaukee Field Station.
Sound detected by the ultrasonic microphone was
transposed by a factor of 10 in the frequency domain
prior to recording on tape while the original amplitude
envelope and true time domain were maintained. The
recording input level on both recorders was adjusted to
ensure that artificial harmonics and other synthetic
acoustics were not produced.
Eleven songs were used in this study, recorded from
four individually identified males (4 songs from one
male, 3 from another, and 2 from two others). The songs
were selected from a larger sample of songs within a
singing bout. Males were identified by territory occu-
pancy as territories were linear and non-overlapping
(Williamson 2000, personal observation). Recordings
were made in a territory only once to provide additional
certainty of recording from a specific individual. We
recorded singing throughout the day during the breeding
season in August 2000 at the Southwestern Research
Station, Portal, Arizona.
Analysis
Ultrasonics are defined as sound frequencies above the
upper boundary of human hearing, generally considered
to be 20 kHz. Although our ‘‘hearing range’’ recordings
and ‘‘ultrasonic range’’ recordings overlap, we regard

ultrasonic frequencies as only those above 20 kHz.
Spectrographs of the hearing range and ultrasonic range
recordings 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 that
is identical to that of the hearing range signal, and a
frequency axis that is a multiple of 10 times that of the
hearing range spectrographs. Thus, using the 0- to 16-
kHz setting, the frequency range of ultrasound spec-
trographs is 10–160 kHz. Hearing range and ultrasonic
range recordings were aligned temporally and analyzed
using Raven (Beta 1, 2002 Cornell Laboratory of
Ornithology), Sound Analysis 3.19 (Tchernichovski
et al. 2000) and Avisoft (4.2, Specht). Power spectra
were produced with Avisoft using the hamming func-
tion, a bandwidth of 2.2 Hz, resolution of 1.3 Hz, and
smoothing over 41.7 Hz. Peak detection of the power
spectra 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 the
song that are not simply extensions or harmonics of
hearing range sounds, we identified sounds that met
these criteria: (1) ultrasonic elements which did not also
contain energy in the hearing range and (2) ultrasonic
components which differed in acoustic structure from
simultaneous hearing range sound. In addition, we
noted song elements in the hearing range that did not
contain ultrasonic components.
Perception
Subjects
Adult male and female blue-throated hummingbirds
(n=4 males, 2 females) were mist-netted in southeastern
Arizona and transported to Wesleyan University where
they were housed until completion of the hearing tests.
The birds were housed in individual 0.5-m3 mesh cages
in a communal room and kept in visual isolation in
order to minimize stress. Blue-throated males are highly
territorial during the breeding season and display
aggressive behaviors to males within view. The birds
were able to interact vocally. Throughout the period of
captivity, the birds were maintained on photo period
and temperature conditions matched to those of their
capture location. They were provided with commercially
prepared hummingbird food (Nekton, Nektar-plus)
made fresh daily. Mean (±SE) bird weights were
8.15±0.14 (males) and 6.05±0.05 (females).
ABR recording
The birds were anesthetized with an intramuscular
injection of 24 lg g)1 xylazine and 12 lg g)1 ketamine.
667
Supplemental doses were not necessary. Feathers were
removed from the crown of the head and bilaterally
caudal to the external auditory meatus. Electrodes (400-
lm steel wire) were inserted subcutaneously at the apex
(positive), caudal to the right ear (negative), and caudal
to the left ear (ground), and held in place with tissue
adhesive. All tests were conducted within a sound-
attenuating, anechoic room. The bird was wrapped
loosely in a cloth surrounded by a heating pad. Body
temperature was maintained at 37°C. The bird was
placed with both ears equidistant to the speaker, with
the external ear canals 30 mm from the speaker and the
beak 90° to the flat surface of the speaker, centered
approximately at the speaker midline.
Custom designed software (by A.M.) interfaced with
a sine wave generator (AG-7001C Audio Generator,
frequency range 10 Hz–1 MHz, distortion <0.1% at
500 Hz–100 kHz; EZ-Digital) controlled the generation
of 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, flat
frequency response between 1 kHz and 110 kHz; Tucker
Davis Technologies, Gainesville, Fla., USA). Responses
were band-pass filtered (10–3 kHz) and passed through
a 60-Hz notch filter before amplifying. Amplifier gain
was calibrated using a voltage calibrator (2010 Omnical
Voltage Calibrator, World Precision Instruments). Re-
sponses were viewed in real-time on a digital oscillo-
scope (Tektronix 2230) and, simultaneously, 40-ms
epochs were digitized (25-kHz sample rate) for averag-
ing. Electronic delays were employed so that response
sampling began 4.5 ms before the onset of the sound
stimulus as recorded at the bird’s ears. Averages from 50
stimulus presentations were viewed on a monitor and
stored for offline analysis. At the end of the recording
session, the birds were given a 0.6 lg g)1 intramuscular
injection of yohimbine and placed under a heat lamp
until they fully recovered from anesthesia.
Stimuli
The hummingbirds were tested for ABR thresholds
using tone pips between 1 kHz and 50 kHz, 8 ms in
duration including 1 ms rise and fall, presented with a
750-ms interstimulus interval. Frequencies were pre-
sented in an arbitrary order at 0.5- or 1-kHz increments
between 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, stimulus
intensity was varied by 10-dB steps until near threshold,
and by 3-dB steps surrounding threshold until the ABR
threshold was identified. Stimulus intensity ranged from
30 dB to a maximum of 90 dB and was monitored with
a calibrated microphone located midway between the
speaker and the bird’s head, positioned so that it did not
block the sound path to the ears. Stimulus intensity in
the audio range (<15 kHz) was confirmed in the free
668
field using a sound pressure level meter (Bruel and Kjaer
2226) placed at the position of the bird’s ear by
recording SPLs directly using the same tones presented
as stimuli. Ultrasonic sound intensities were determined
by measuring the voltage output of the ultrasonic
microphone on an oscilloscope and calculating dB re.
20 lPa.
ABR analysis
Evoked potential peaks were identified visually in the
recording trace by two observers. The lowest intensity at
which a response was present was determined to be the
response threshold (as in Boettcher et al. 1993; Brittan-
Powell and Dooling 2002). The ABR was identified as a
peak above baseline followed by a trough below the
baseline waveform. We did not attempt to identify
multiple successive peaks since a single, broad peak is
characteristic of long duration stimuli such as those
used. The neural generators of the ABR wave are un-
known for hummingbirds. Peak latencies and ampli-
tudes were not measured since our objective was to
identify the presence or absence of a response in order to
generate a threshold audiogram.
Results
Ultrasonic production
Blue-throated hummingbirds produce ultrasonic sounds
vocally 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 stereotyped
across tail shuffling episodes. Wing noises are similarly
broadband short duration clicks, although interpulse
intervals are not stereotyped. Tail shuffling appears to be
a ritualized behavior and occurs in the context of close
range agonistic encounters, usually produced by a ter-
ritory resident when confronted by an intruding hum-
mingbird. Wing sounds are produced in this context as
well, and were also observed after agonistic encounters
while apparently guarding a food source.
A detailed description of the sonic song elements has
previously been reported (Ficken et al. 2000). As in the
sonic range, ultrasonic frequencies contain acoustically
differentiated syllables composed primarily of broad-
band transients, clicks, and trills. Song organization is
based on five different sets of syllable clusters or song
‘‘units’’ A–E (Fig. 1). Within a unit, syllables are entirely
stereotyped in acoustic structure and order. The
sequence of units comprising a song may vary in number
and order; however, the variation follows specific
sequencing rules (Ficken et al. 2000). As has been
reported 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 elements
are high-frequency extensions of broadband transients
and clicks notes. As these elements are not acoustically
differentiated in the ultrasonic range, there is no com-
pelling reason to suggest that these categories of sounds
may contain additional information not provided within
the sonic range. Instead, we were interested in ultrasonic
elements which did not also contain energy in the
hearing range, as well as ultrasonic components of notes
which differed in acoustic structure from simultaneous
hearing range sound. Several ultrasonic elements meet
these 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-ms
peak beginning approximately 1.5 ms after stimulus
arrival at the ears, followed by a 1.5-ms depression be-
fore returning to baseline. As is characteristic of the
ABR across vertebrates, decreased stimulus intensity
resulted in decreased peak amplitude and increased
response latency (Fig. 2) (Corwin et al. 1982).
Hearing range
Most importantly for our purposes, we conclude that
neither male nor female blue-throated hummingbirds
hear high frequencies between 8 and 50 kHz (at 90 dB),
as determined by ABR. We tested tones at 1- to 5-kHz
intervals 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 Pye
1974). Instead, the highest frequency at which a
threshold response was noted was 7 kHz for both males
and females (Fig. 3a). None of the birds exhibited a
response to an 8-kHz tone, and no intervals between 7
and 8 kHz were tested.
Females demonstrated a range of best hearing for
frequencies 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 a
threshold response within 20 dB of the peak hearing
sensitivity. The mean female hearing threshold
increases 16 dB between 2.5 and 3.0 kHz. Males
showed best hearing for frequencies between 1.0 and
3.5 kHz, with peak sensitivity at 2.5 kHz. The mean
male hearing threshold increases by 9 dB between 2.5
and 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 hearing
threshold at 2.0 kHz, however, the differences are not
 669

Fig. 1 Blue-throated
hummingbird song. Song of a
male blue-throated
hummingbird recorded at the
Southwestern Research Station
during the breeding season
showing the five component
song units A–E. An example
sound element that is produced
solely within the ultrasonic
range is indicated with (1). An
example of a syllable composed
of differing acoustic
morphologies in the ultrasonic
and sonic ranges is noted with
(2). Examples of other song
element types are broadband
transient notes which extend
from the sonic into the
ultrasonic range (3), syllables
produced within the hearing
range with a possible ultrasonic
harmonic (4), and syllables
produced entirely within the
hearing range (5)

significant (Mann Whitney U, P>0.05, Fig. 3a). The
mean of males and females combined reveals a range of
best hearing between 1.0 and 3.5 kHz, a peak in sensi-
tivity at 2.5 kHz, and an increase in threshold of
approximately 11 dB between 2.5 and 3.0 kHz (Fig. 3b).
just outside the upper boundary of the range of best
hearing (Fig. 5). Furthermore, we find that the peak
sensitivity frequencies of 2.0 and 2.5 kHz do not corre-
spond to any distinctive acoustic elements of the song
(Fig. 5).

Comparison of hearing range and song vocalizations

The frequencies of peak hearing sensitivity (2.0 and
2.5 kHz) do not correspond to a peak in the concen-
tration of energy in the song (Fig. 4). Amplitude peaks
in the song power spectrum occur at 3.3, 5.8, 6.9 and
8.6 kHz. Of the frequencies produced below 10 kHz,
only 25% of the sound energy falls between 1.0 and
3.5 kHz, within the range of best hearing. Interestingly,
the majority of the peak frequency trace (frequency of
maximum power at any given time) occurs at 4.0 kHz,
Discussion
Production
The blue-throated hummingbird’s song differs from
typical oscine songs in that it is atonal and composed
primarily of broadband transients, fricative sound
bursts, and click-note trills (Ficken et al. 2000). It is also
unusual in its wide frequency range, extending from
1.8 kHz to approximately 30 kHz. The ultrasonic
670
Fig. 2 Example of an ABR waveform. The top trace is a typical
ABR, produced by a male in response to a 2-kHz tone presented at
87 dB SPL. Subsequent traces show decreasing peak amplitude and
increased response latency correlated with decreasing stimulus
intensity. Sound reaches the bird’s ear at time 4.5 ms (arrow)
(>20 kHz) components of the song include continuous
extensions of hearing range sound, harmonics of hearing
range elements, non-harmonic sounds which are pro-
duced in concert with sonic elements, and also elements
that are produced without corresponding sonic sound.
High frequencies are not a necessary correlate of
sound production by blue-throated hummingbirds as
territorial advertisement serial chips do not contain
frequencies above 7 kHz (Ficken et al. 2002). It is
unlikely that the distinctive acoustic structure of the
song is the result of the small size of the sound pro-
ducing apparatus since smaller hummingbird species
produce whistles, frequency modulations, and tonal
sounds (reviewed by Kroodsma et al. 1996; Ornelas et al.
2002). Furthermore, we could not detect any ultrasonic
sounds produced by hummingbirds smaller than the
blue-throated, including the black-chinned (Archilochus
alexandri), Anna’s (Calypte anna) and broad-tailed
(Selasphorus platycercus) hummingbirds. The magnifi-
cent hummingbird (Eugenes fulgens) and white-eared
hummingbird (Hylocharis leucotis) songs have elements
that extend above 15 kHz but these components are a
continuation of sonic elements and thus not as intriguing
as the ultrasonic sounds of the blue-throated hum-
mingbird’s song.
Perception
The primary goal of the hearing tests was to identify the
high end of the hearing range in order to establish
whether or not blue-throated hummingbirds can hear
Fig. 3 a, b Audiograms. a Mean (±SE) threshold ABRs for males
and females at each frequency. b The combined (mean±SE) male
and female audiogram. All subjects were tested up to 50 kHz. No
responses to pure tone stimuli were obtained above 7 kHz at up to
90-dB stimulus intensity, the maximum intensity that we could
present
the ultrasonic sounds that they produce. Second, we
sought to determine the frequency of peak hearing sen-
sitivity and compare this with acoustic features of the
song. The results of ABR tests indicate that neither male
nor female blue-throated hummingbirds hear ultrasonic
frequencies. Rather, they have a maximum audible fre-
quency of 7 kHz at 90 dB. Blue-throated hummingbirds
hear best between 1.0 and 3.0 or 3.5 kHz with a peak in
sensitivity at 2.0–2.5 kHz (females and males, respec-
tively).
A correlation between the frequency of peak hearing
sensitivity and specific spectral features of song has been
demonstrated in passerines and also psittacines (Dooling
et 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 sensitivity
do not correspond to frequencies of increased amplitude
(Fig. 4) nor to any distinctive acoustic elements of the
song (Fig. 5). Furthermore, much of the maximum
power lies just outside the upper boundary of best
hearing (at 4.0 kHz) rather than within the 1.0–3.5 kHz
best hearing range (Fig. 5). The significance of this for
signal processing, if any, is unknown. In addition, there
 671

Fig. 4 Power spectrum of song.

Power spectrum of a single song
(units A–E). The box encloses
the mean frequency range of
best hearing for males and
females combined (1–3.5 kHz).
The shaded bar indicates the
sound energy between 2 and
2.5 kHz, the frequencies of
peak sensitivity in females and
males, respectively. Arrows
point to peaks in power at 3.3,
5.8, 6.9, and 8.6 kHz

Fig. 5 Peak frequency trace.

The frequency of maximum
energy at any given time
throughout a single song is
outlined in red. The horizontal
line indicates 4 kHz which
traces the majority of the
maximum sound energy

are no known calls in the repertoires of either adults or
juveniles that contain substantial energy below 3.5 kHz
(Ficken et al. 2002). In fact, most of the sound energy of
agonistic calls, alarm calls, serial chips, fledgling calls, as
well as female song, is concentrated well above 3.5 kHz,
and in the case of serial chips is entirely contained near
the outer extent of the hearing range, between 6 and
7 kHz. Perhaps a more consistent account of the fre-
quency of peak sensitivity and range of best hearing in
the blue-throated hummingbird is that these character-
istics have not been shaped entirely by pressures of
communication.
Evolution of hummingbird hearing
Two explanations are commonly proposed to explain
characteristics of hearing: (1) behavioral adaptations,
for example, sound localization, predator detection, or
intraspecific communication; and (2) phylogenetic and
developmental constraints on head and auditory struc-
ture morphologies. The latter explanation is supported
by numerous examples in mammals in which the
peripheral auditory system appears to have evolved
largely independent of behavioral factors (Plassman and
Brändle 1992). Similarly, it appears that in the blue-
throated hummingbird, neither the maximal audible
frequency nor the peak sensitivity frequency correspond
to 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 maximum
audible frequency (7.5 kHz) than passerines (9.7 kHz),
and both groups have a lower high-frequency cutoff
than owls (11.2 kHz). Non-passerines have the lowest
peak frequency sensitivity (2.1 kHz), followed by owls
(2.7 kHz), then passerines (2.9 kHz). These data are the
means of two species of Strigiformes (barn owl and great
horned owls), eight species of other nonpasserines, and
13 species of passerines (reviewed by Dooling 1992).
Ignoring the adaptive specializations of the owls for
nocturnal prey capture, characteristics of hummingbird
672
hearing are nearly identical to the mean of the other
nonpasserines that have been tested.
Nonpasserines, including Apodiformes, are thought
to evolutionarily pre-date passerines. Therefore, the
curtailed frequency range of hummingbird hearing
compared to their vocal production may represent a
phylogenetic constraint. Such constraints are generally
due to limitations of the cochlear and middle ear
structures, peripheral transduction, or central auditory
processing (Sachs et al. 1978). High frequency process-
ing in birds begins in the basal region of the basilar
papilla. The barn owl, which has the highest audible
frequency, also has the longest basilar papilla described
in birds, about 11 mm (reviewed by Carr 1992). Perhaps
the length of the basilar papilla in the hummingbird is
constrained by small head side, thus prohibiting high-
frequency hearing in small birds.
Similarly, peak sensitivity is determined by the
dimensions of a few middle ear structures which, in turn,
are stringently coupled to phylogenetic and develop-
mental factors. A shift in peak sensitivity toward lower
frequencies can be achieved by increasing the middle ear
volume, however this is largely constrained by overall
head size. A shift in the peak sensitivity range to higher
frequencies 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 behavioral
selective pressure; instead, behaviorally adaptive pres-
sures more often expand or shift the overall range of
hearing, without altering peak sensitivity (Plassman and
Brändle 1992). Our data are consistent with this idea in
that peak sensitivity in the blue-throated hummingbird
does not correspond to any notable vocal attributes and is
the 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 audiograms
are not necessarily consistent with absolute auditory
sensitivity and may underestimate the perceived sound
level thresholds (Borg and Engstrom 1983; Mann et al.
2001; Stapells and Oates 1997; Wenstrup 1984). Specif-
ically in birds, ABR-generated audiograms reflect the
bandwidth and shape of the behavioral audiogram,
including the frequencies of peak sensitivity (mallard
duck, Anas platyrhynchos, Dmitrieva and Gottlieb 1992;
Bengalese finch, Lonchura striata domestica, Woolley
and Rubel 1999; budgerigar, Melopsitt undulatus, Brit-
tan-Powell et al. 2002). However, Brittan-Powell and
Dooling (2002) report that in budgerigars, the ABR-
generated audiogram is 30 dB higher than the behav-
iorally generated audiogram. Thus, it is not unlikely that
the hearing threshold levels may be lower in blue-
throated hummingbirds than demonstrated by the ABR
and 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 at
2.0 and 2.5 kHz, and would not necessarily result in the
inclusion of ultrasonic frequencies. Furthermore, in
generating behavioral audibility curves, the high fre-
quency cutoff is defined as the highest frequency a bird
can hear at a sound pressure level of 60 dB SPL
(Dooling 1980). Because we used a 90-dB stimulus to
determine audibility thresholds using the ABR, we have
somewhat compensated for the differences between the
two methods. The ABR is not limited by ultrasonic
frequencies per se, as it has been shown to successfully
identify hearing ranges that extend up to 80 kHz in
clupeiform fishes (Mann et al. 2001).
Why ultrasound production?
Thus far, we cannot provide an adaptive explanation for
the production of ultrasonic vocalizations, which
apparently do not function in intraspecific communica-
tion. Blue-throated hummingbirds often alternate sing-
ing with catching small flying insects. Perhaps the
ultrasonic clicks produced during singing flushes insects
from vegetation, or triggers erratic insect flight patterns,
thereby increasing visual salience for the hummingbird.
However, we have not observed any such effect of
singing on insects. Furthermore, vocal click sounds that
are produced by blue-throated hummingbirds while
actually chasing flying insects are audible and do not
contain ultrasonic components (unpublished data). We
also believe it is unlikely that ultrasound in blue-
throated song repels small rodents that prey on nestling
hummingbirds. Male blue-throated hummingbirds do
not guard nests and females have not been observed to
sing near nests (Johnsgard 1983). Blue-throated hum-
mingbirds have been observed to compete with the lesser
long-nosed bat (Leptonycteris curasoae) and the Mexi-
can long-tongued bat (Choeronycteris mexicana) at
agave plants in early mornings and evenings (Summer
Bennett, personal communication). These are times of
peak song production and thus ultrasonic sounds could
signal to bats a site of high resource competition.
However, even though ultrasonic elements might in fact
be detected by bats, there is no evidence that this
interaction may have provided selective pressure to the
structure of blue-throated song.
The high frequency cutoff in birds is usually related to
the highest frequency in the species’ song, and the
hearing sensitivity in many species is correlated with
their spectral output (reviewed by Dooling 1982).
However, this is not an absolute association. As dem-
onstrated by Konishi (1971), the frequency range of
audition does not always match the frequency range of
vocalizations. In fact, Woolley and Rubel (1999) dem-
onstrate that Bengalese finches may attend only to the
fundamental or low dominant frequencies in song
(<3 kHz) in order to maintain complete song structure
across a frequency range of up to 10 kHz. Although it is

more intuitive to dismiss the sound categories of ultra-
sonic harmonics and ultrasonic extensions of sonic
sounds as epiphenomenal, ultrasonic sounds that are
structurally independent, non-harmonic elements of
hearing range sounds may nonetheless also be epiphe-
nomenal artifacts generated by the syrinx or upper vocal
structures during sound production.
It must be considered that ultrasound may indeed be
produced and perceived by other hummingbird species
not yet tested. However, the production of ultrasonic
frequencies by blue-throated hummingbirds does not
appear to function in intraspecific communication and a
likely adaptive explanation for this phenomenon has yet
to be identified.
Acknowledgements We thank the Southwestern Research Station
for housing the hummingbirds. Elizabeth Sandlin provided the use
of mist nets and training in hummingbird capture. All animal care
and methods complied with the regulations of the Institutional
Animal Care and Use Committees of the affiliated universities, the
Arizona Game and Fish Department, the Connecticut Department
of Environmental Protection—Wildlife Division, and the US Fish
and Wildlife Service, as well as the Principles of Animal Care of the
National Institutes of Health. This research was funded by NSF
SGER 0077980.
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