Vocal tract filtering and sound radiation in a songbird
1 Department of Biology, Indiana University, Bloomington, Indiana, 47405,
USA
2 Behavioural Biology, Institute of Biology, Leiden University, PO Box 9516,
2300RA, Leiden, The Netherlands
3 School of Medicine, Indiana University, Bloomington, Indiana, 47405,
USA
* Author for correspondence (e-mail: bsnelson{at}uoneuro.uoregon.edu)
Accepted 10 November 2004
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: songbird, vocal production, directional sound radiation, vocal tract resonance, beak gape
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
In contrast with these theoretical predictions, experimental results
reported for the European blackbird (Turdus merula) suggested that
changes in beak gape might simply alter the amplitudes of sound frequencies
above 4 kHz (Fig. 1;
Larsen and Dabelsteen, 1990
).
These authors do not describe vocal tract resonances. Nevertheless, several
subsequent studies have reported results in which it remains unclear whether
birds vary beak gape as a mechanism for `tracking' fundamental frequency or as
a mechanism for controlling amplitude above
34 kHz
(Fig. 1B; e.g.
Goller et al., 2004
;
Nowicki, 1987
;
Podos et al., 2004
;
Suthers and Goller, 1997
;
Westneat et al., 1993
).
To distinguish between these two alternatives we replaced eastern towhee, Pipilo erythrophthalmus L., syringes with a small speaker and quantified how sound radiates as a function of: (1) sound frequency, (2) head and body orientation and (3) beak gape. We propose that small birds do not vary beak gape as a mechanism for `tracking' fundamental frequencies in vocalizations, but instead decrease beak gape as a mechanism for controlling the amplitudes of sound frequencies between approximately 4 and 7.5 kHz.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
Subjects were next mounted above the top of a 60 cm (0.96 cm diameter)
steel pole in a natural posture by clamping the upper half of each leg between
two small sheets of perforated aluminum (36cmx2.5 cmx0.8
mm, 127 1.1 mm diameter holes per cm2; Small Parts). Each subject's
head was then positioned as described below using a rigid steel wire
(50x1.2 mm diameter) glued to the mandible and to the top of the 60
cm pole. Mounted subjects were next positioned at least 60 cm from each wall
of a humidified 2.0x2.4x2.75 m sound-attenuating chamber
(Industrial Acoustics Company, Inc., Bronx, New York, USA) that was lined with
at least one layer of acoustic foam (classic 7.62 cm wedges; Sonex,
Minneapolis, Minnesota, USA) to absorb reflections that might otherwise occur
from the semi-reflective perforated steel walls of the chamber.
We generated and played frequency sweeps from the speaker, as opposed to noise or recorded vocalizations, to maximize signal to background noise ratios and to simplify spectral comparisons. Linear frequency sweeps (1 s, 0.511.0 kHz) were generated with 10 ms raised cosine onset and offset ramps using an array processor [AP2; TuckerDavis Technologies (TDT), Alachua, Florida, USA]. Sweeps were then played from the speaker using a digital to analog converter (DD1; TDT; 16 bit, 40 kHz) and attenuator (PA4; TDT;52 dB). Sweeps were recorded using a 1/2 inch microphone (4189; Brüel & Kjaer, Nærum, Denmark) mounted on the end of a threaded rod (90x0.95 cm) and positioned 90 cm from the opening of each subject's glottis (2671 preamplifier, WB 1372 power supply; Brüel & Kjaer; MP-1 preamplifier; Sound Devices, Reedsburg, Wisconsin, USA; 160 Hz6 dB octave1 high-pass filter with no gain; ULN-2 preamplifier; Metric Halo, Hopewell Junction, New York, USA; 66 dB gain). Recordings were digitized (DD1; TDT; 16 bits, 40 kHz, 15 kHz anti-alias filter) and saved to disk using an array processor (AP2; TDT). Spectra were generated using 1000 point (40 ms) Hanning windows that were overlapped (98%) and averaged over the duration of each stimulus (Igor Pro v4; Wavemetrics, Lake Oswego, Oregon, USA).
Sound radiation
To quantify how sound radiates as a function of beak gape we varied head
and body orientation in 9° increments over 360° around a single
vertical axis leading from the top of the pole on which subjects were mounted
to the opening of the glottis. Orientation was controlled using a stepper
motor (5x5x5 cm) mounted 60 cm below the subject's abdomen and on
the top of a tripod that was positioned near the floor and covered with
acoustic foam (7.62 cm wedges). Recordings were also obtained from two
subjects (390 and 430) with three beak gapes (2, 6 and 11 mm) after the
microphone was positioned at either a higher (+20°) or lower elevation
(20°) relative to where the microphone was normally positioned (see
below).
Beak gape
Frames (311x40 mm) made from of steel wire (1 mmdiameter) were
used to vary beak gape (i.e., the distance between the tips of the maxilla and
mandible; Fig. 2). A small
amount of heated glue was used to prevent the wire frame from moving as
subjects were rotated. Unless otherwise noted, the mandible was directed
towards the microphone and we varied only the vertical angle of the maxilla
(and head). One subject (430) had grown a small `hook' on the tip of his
maxilla and in this case the upper wire was placed just behind the hook and
measurements were obtained relative to the lower edge of the maxilla
immediately behind the hook. Measurements of beak gape were accurate to within
no more than ±0.2 mm although individual differences in beak size and
shape preclude precise comparisons between individuals.
To test whether results might differ when the maxilla is held in place, and when the position of the mandible is varied, we replicated measurements obtained for subject BB after gluing the maxilla to the top inside edge of a steel wire loop (1x30 mm). We then varied only the orientation of the mandible while the orientation of the maxilla was held constant and directed towards the microphone.
Resonances
We estimated tracheal resonances by comparing recordings described above
with reference recordings that we obtained after mounting the speaker alone,
without the bird, above an identical 60 cm (0.96 cm diameter) steel pole using
a small amount of glue and a 2 cm steel wire (1 mm diameter). No tubes were
attached to the speaker and the speaker was positioned by itself close to
where the glottis was positioned in each mounted subject (90 cm or 15 cm from
the microphone). Reference spectra were obtained with the speaker port
directed towards the microphone, however spectra varied little as the speaker
was rotated (S.D.<2 dB, 110 kHz, 0360°).
We also obtained recordings at a distance of 15 cm from the glottis after laying each subject on a horizontal platform made from perforated aluminum (127 1.1 mm diameter holes per cm2). Recordings were obtained while gently stretching or shortening the trachea relative to what was deemed to be each trachea's natural length (i.e., the in vivo distance from the syrinx to where connective tissue was removed). Recordings were obtained from two subjects after removing either a 5 mm (subjects 430 and BB) or 8 mm (subject 430) segment from the trachea and re-inserting the speaker into the shortened trachea.
Controls
Recordings were terminated after 45 h and initial recordings were
repeated to ensure that no acoustical changes occurred within the vocal tract
during this period. In addition, recordings were obtained using a random
assortment of beak gapes (subject 358) or were obtained for odd valued beak
gapes (11 mm, 9 mm, etc.) before even valued beak gapes (10 mm, 8 mm, etc.,
subjects 390, 430 and BB). Visual inspection of the glottis indicated that no
obvious physical changes occurred during the recording period. The exposed
lower portion of the trachea dried slightly but could still be stretched and
longitudinally compressed at the end of the experiment.
To ensure that spectra generated from frequency sweeps were not biased, we occasionally recorded noise signals (WB 1314 noise generator; Brüel & Kjaer; 10 s, 0.411 kHz, 45 dB attenuation). In all cases, spectra obtained from frequency sweeps were similar to those obtained from smoothed recordings of noise signals (±1 dB).
To ensure that recordings were not biased due to microphone or subject locations within the acoustic chamber we obtained recordings at a distance of 90 cm from several wooden spheres (3.0, 2.5, 2.0 and 1.8 cm diameter) after inserting a silastic tube (4.5 cm long, 1.47 mm i.d., 1.96 mm o.d.) through the middle of each sphere. Spectra obtained as spheres were rotated (360°) did not vary when spheres were positioned in different locations within the chamber (±1 dB). Spectra for some orientations varied when spheres were placed next to a wall (within 20 cm, ±2 dB), however subjects and microphones were always positioned at least 60 cm from each wall.
Although the interface between the Teflon tube, speaker port and trachea was secured with a suture and a small amount of adhesive glue during each experiment, some sound may have radiated from this junction or from the exposed portion of the trachea. To assure that sound from these sources did not influence our recordings we obtained additional recordings after inserting a silastic plug (2x8 mm) into the glottis and clamping the beak in a closed position (0 mm, Fig. 3). We do not know how effective this plug was in attenuating sound, or if it caused sound to radiate from other locations (e.g. from the larynx or upper portion of the trachea). As a conservative precaution we excluded frequency bins in spectra above 10 kHz that sometimes fell below threshold levels that were obtained under these conditions. Substantial low frequency noise existed in the chamber and this required us also to exclude sound frequencies below 1 kHz.
|
|
|
|
|
Fundamental frequency was estimated using an autocorrelation algorithm (1.5
ms window), however harmonic amplitudes were measured from spectra that were
extracted from time-frequency spectrograms (44.1 or 48 kHz sampling rate, 34.8
ms Hanning window, 46.4 ms FFT frame, and 98% overlap between each successive
46.4 ms frame, 6.97e4 sframe rate; see
Nelson 2004 for further
details). Absolute amplitudes were calculated using 94 dB (relative 20 µPa)
calibration signals (see Nelson,
2000
). For clarity, however the amplitudes of second and third
harmonics were scaled relative to the amplitudes of fundamental frequencies.
Means and standard deviations were calculated for harmonics corresponding with
fundamental frequencies that fell within 100 Hz bins.
We do not attempt to provide a thorough description of how towhees vary
beak gape while vocalizing. As support for our hypotheses, however we analyzed
video recordings that were obtained previously of seven male Florida eastern
towhees and six male Indiana eastern towhees
(Nelson, 2000; B.S.N.,
unpublished). Three of the Florida birds were video taped from a distance of
23 m while they were held in a small cage (see above) using a Hi-8
video camera (ES6000; Canon, USA). Analog recordings were then transferred to
a digital video camera (TRV-900; Sony, USA) and then to a computer for
analysis (CatDV v3; Square Box Systems, Stratford-upon-Avon, UK; sampling rate
= 30 frames s1). Four free-ranging Florida towhees were
video taped outside of the cage from a distance of 45 m (ES6000; Canon
or TRV-900; Sony). All six Indiana birds were video taped from a distance of
23 m (TRV-900; Sony) while they were held in the cage. Recordings
obtained with the digital video camera were transferred directly to a
computer.
Beak gape was measured from video frames using custom computer procedures
(Igor Pro v4) and was defined as the distance between the tips of the maxilla
and mandible. Raw measurements of beak gape were obtained by placing cursors
on these tips and by calculating the linear distance between the cursors
(within each 720x480 point video frame). Raw measurements were then
converted into measurements of beak gape (mm) using a reference defined as the
distance from the anterior end of the nares to the tip of the maxilla
(Podos et al., 2004). The
conversion was made using a scaling factor that was calculated as the ratio
between the raw distance from the anterior end of the nares to the tip of the
maxilla (within the 720x480 point video frame matrix) and the same
distance that was measured using calipers from real birds (see below). When
possible, scaling factors (1.72.3) were obtained during vocalizations
but were often obtained from previous or subsequent frames. Reference
distances were always obtained when the head was perpendicular to the camera.
Reference distances could not be obtained from video taped subjects. As a
consequence, we used mean values calculated from birds within each population
(reference distance = 10.5±0.1 mean ± S.D.,
N=3 for FL subjects, 9.8±0.1, N=15 for IN subjects).
Overall measurement accuracy depended on the quality of our recordings but is
not believed to have exceeded ±1.5 mm.
Many factors limited the number of measurements that could be obtained
(Florida: 362 frames from 50 calls, N=18, 6, 6 calls in the cage; 9,
6, 4, 1 calls outside of the cage; Indiana: 854 frames from 97 calls,
N=53, 15, 13, 10, 5, 1). For example, in addition to limitations
described by Podos et al.
(2004), we could not obtain
measurements when the tips of the beak were hidden by the cage. To ensure that
intermediate beak gapes and midrange sound frequencies were not under-sampled
we excluded calls in which we could not obtain three consecutive measurements.
In addition, we excluded calls if these three consecutive measurements did not
encompass the loudest part of each call.
Measurements of peak frequency that are presented together with
measurements of beak gape were obtained from 3.33 ms audio segments (sampling
rate = 48 kHz), corresponding with extracted video frames. Measurements of
peak frequency within each 3.33 ms audio segment were calculated using a
previously described autocorrelation algorithm
(Nelson, 2004; measurements
correspond well with measurements obtained from spectra, 1600 point FFT).
Audio recordings were obtained using each video camera's built-in microphone.
Measurements obtained from these recordings did not vary when compared with
recordings obtained simultaneously from a distance of 100 cm (see above).
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Towhee tracheas are 45 mm long and
1 mm in diameter. Resonances
observed correspond well with odd numbered quarter wavelength resonances near
2 and 5.5 kHz that are predicted for a stopped tube of this length near 1.88
kHz and 5.67 kHz (Fig. 4).
Resonance frequencies remained relatively constant even as the trachea was
stretched or compressed so as to slightly increase or decrease the distance
between exposed cartilaginous rings (Fig.
4B). Resonances changed slightly when the trachea was shortened 5
or 8 mm. In particular, the resonance peak that we observed near 2 kHz when
the trachea was at a normal length both decreased in magnitude and was shifted
to a slightly higher frequency under these experimental conditions
(Fig. 4C).
Beak gape
Changes in beak gape did not substantially shift the resonance frequency of
the vocal tract. Instead, changes in beak gape seem to amplify or attenuate
sound frequencies between 4 and 7.5 kHz depending on which beak gape is
chosen as a reference (Fig.
5A). To assess the frequencies over which changes in beak gape had
the greatest effect we calculated standard deviation (S.D.) across
spectra that are plotted in Fig.
5A (Fig. 5B).
Calculations of S.D. are minimally dependent on which beak gape is
chosen as a reference and again suggest that changes in amplitude will occur
between
4 and 7.5 kHz with smaller changes in amplitude occurring between
7.5 and 10 kHz.
Decreases in beak gape sometimes amplified sound frequencies between
3.5 and 5.5 kHz at the position of the microphone (subjects 430 and BB).
This increase in amplitude should be viewed with caution, however, since the
relative differences that are evident in
Fig. 5A are dependent on the 11
mm gape reference spectrum that was used to derive each additional spectrum.
Indeed, these relative differences vary by a small amount when we choose a
different reference beak gape. Nevertheless, relative differences between
3.5 and 5.5 kHz that are evident in spectra shown in
Fig. 5A are also evident in raw
spectra (see Fig. 3). As a
consequence, it remains possible that a decrease in beak gape might sometimes
amplify sound frequencies between
3.5 and 5.5 kHz (primarily near
4
kHz).
Spectral peaks shift in frequency between 4 and 5.5 kHz as beak gape
varies (Fig. 5A). Again,
however these relative differences change when we choose a different reference
beak gape. In addition, shifts in these spectral peaks may occur, in part, due
to small changes in head diameter or vertical changes in head orientation that
occurred as beak gape was varied. Thus, shifts in spectral peaks that are
evident between
4 and 5.5 kHz in Figs
5 and
6 should be viewed with
caution.
Increasing beak gape by repositioning the mandible, as opposed to the
maxilla, did not substantially alter results below 5 kHz
(Fig. 6). Sound levels
increased above
5 kHz when the upper mandible was held in a constant
position, although much of this increase can be attributed to differences in
head diameter or differences in vertical head orientation and not beak
gape.
Amplitude levels varied considerably with beak gape near 6.5 kHz in all
subjects and amplitude, at the position of the microphone, increased linearly
with beak gape at this frequency (Fig.
7). These results suggest that relatively small changes in beak
gape will result in relatively large changes in amplitude above 4 kHz as
long as birds to not open their beaks beyond
5 mm (when amplitude is
viewed on a logarithmic scale, dB). Conversely, sound frequencies above
4
kHz will attenuate the least when birds increase beak gape beyond
5 mm.
It should be noted, however that increases in amplitude that occur with beak
gapes larger than 5 mm may, in some cases, be lost if subjects are not
oriented towards a receiver (or have their heads directed upwards) since
vocalizations also become more directional as beak gape increases (see
below).
Sound radiation
Sound radiation patterns were relatively simple and, in all cases,
consisted of a single amplitude decrement near ±130°
(Fig. 8). The width (in
degrees) of this amplitude decrement increased with sound frequency and seems
to explain decreases in amplitude that were observed across all directions.
Differences in radiation patterns are difficult to summarize both as a
function of beak gape and sound frequency. As a consequence, we summarize how
sound radiates as a function of these two factors using calculations of
S.D. (calculated across 360°, N=40, 9°
increments). S.D. increased positively with sound frequency and
beak gape, although relatively large increases in S.D. occurred
between 3 and 3.5 kHz and again near
7 kHz
(Fig. 9). S.D.
calculations increased over relatively high sound frequencies after we lowered
the elevation of the microphone (20°) but decreased after we
increased the elevation of the microphone (+20°;
Fig. 10).
|
|
|
Individual differences
The shapes of the filter functions that we observed above 4 kHz varied
between subjects (Fig. 5). We
do not know if these differences represent physical differences that exist in
living subjects or whether these differences might simply represent
differences in how subjects were prepared and mounted before recordings were
obtained. In either case, however, the differences that we observed might
represent variation that occurs naturally as subjects change the configuration
of their vocal tract or overall posture. Some of the differences that are
evident in Figs 5 and
6 can also be attributed to
individual differences in reference spectra (i.e., spectra obtained with
11 mm beak gapes).
Calculations of directivity (S.D.) exceeded 3 dB near 3.5
kHz in subjects 358 and BB but exceeded
3 dB near 3 kHz in subjects 390
and 430 (Fig. 9). These
differences may again correspond with differences in how subjects were
prepared and mounted before recordings were obtained. Nevertheless, these
differences might also be explained by differences in body size since
directionality is presumed to depend, in part, on body size. Subjects 358 and
BB, for example, weighed only 34 and 36 g while subjects 390 and 430 weighed
56 and 54 g. Our sample size does not allow us to establish a clear
relationship between directionality and body weight. Nevertheless, our results
are consistent with the hypothesis that sound radiates from larger subjects in
a more directional manner. Wild-caught towhees in Indiana weigh 3950 g
(43.5±2.7 g, mean ± S.D., N=20) and thus our
results are likely to span differences in directionality that might occur
within this population due to typical differences in body size.
Harmonic amplitude and beak movements
Second harmonics in Florida `tow-hee' calls, on average, have relatively
low amplitudes between 4 and 8 kHz (<30 dB;
Fig. 11A). Harmonic amplitudes
are highly variable although much of this variation can likely be attributed
to variation in subject orientation (Fig.
9).
|
Towhees in both Indiana and Florida tend to produce low sound frequencies
(<3.54 kHz) with small beak gapes (<
4 mm), but produce
higher sound frequencies with large gapes (>4 mm) or a wide range of beak
gapes (010 mm;Figs 11B
and 12). In most cases,
subjects produced high frequencies (>
4 kHz) with a small beak gape
(<
4 mm) as calls were ending. Relatively few measurements were
obtained for intermediate beak gapes (
4 mm) and midrange sound
frequencies (
3.54.0 kHz) even though calls were not analyzed if
beak gapes corresponding with these midrange frequencies could not be
measured.
|
Subjects often increased beak gape (to 0.52.0 mm) shortly
before (12 frames) producing the relatively loud sinusoidal frequency
`sweep' that characterizes this call. This increase in beak gape corresponds
with a low-level, rapidly modulated, sound that is often emitted prior to call
onset (within
25 ms, not illustrated). In addition, one subject tended to
maintain a relatively large beak gape (
5 mm) throughout the recording
period. Nevertheless, all subjects began producing the `sweep' with a small
beak gape (<
1 mm) even if this required a brief (12 frames),
presumably rapid, decrease in beak gape (not illustrated). `Tow-hee' calls are
highly variable in acoustic structure
(Nelson, 2000
) and it should
be noted that low frequency Indiana calls (<
3 kHz) and high frequency
(>
4 kHz) Florida calls may be underrepresented in our sample.
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Vocal tract resonances
Audibility functions obtained for numerous avian species demonstrate that
birds are most sensitive to sound frequencies near 3 kHz
(Dooling et al., 2000). Many
songbirds and nonpasserines alike often produce strong frequency components in
vocalizations near 3 kHz and may do so in order to increase efficacy of
communication over distance (e.g. Wiley
and Richards, 1978
; Wright et
al., 2003
). Our results suggest that tracheal resonances, and
perhaps vocal tract resonances as a whole, function to emphasize sound
frequencies near 2 and 5.5 kHz as opposed to near
3 kHz. Thus, vocal
tract resonances might function to increase the distance over which modulated
vocalizations spanning
1.5 to 7.5 kHz can be used as effective
communication signals. Towhees and other songbirds, for example, often
modulate their vocalizations over a relatively wide range of sound frequencies
(see below, Wiley and Richards,
1982
) and vocal tract resonances (near 2 and 5.5 kHz) may function
to increase the distance over which these modulated vocalizations can be
detected and discriminated (Lohr et al.,
2003
).
The towhee's trachea is 45 mm long and odd numbered, quarter length,
resonances predicted near 1.88 kHz and 5.67 kHz correspond well with
resonances in our recordings. It remains possible that songbirds are able to
alter these resonances by changing the configuration of the larynx.
Alternatively, tracheal resonances may remain relatively stable
(Daley and Goller, 2004
).
Beak gape
Our results suggest that sound frequencies between 4 and 7.5 kHz will
be attenuated whenever towhees reduce the gape of their beak. This result is
inconsistent with the hypothesis that variation in beak gape functions to
shift the resonance frequency of the vocal tract since resonances that can be
attributed to the trachea did not shift upwards or downwards in frequency as
we varied beak gape. In particular, we did not observe shifts in resonance
frequency that were predicted to occur over relatively low sound frequencies
(<
3.5 kHz, e.g. Hoese et al.,
2000
; Podos et al.,
2004
). Nevertheless, our data are consistent with spectral changes
that were observed in the European blackbird
(Larsen and Dabelsteen, 1990
)
and with results that have been reported for living subjects. For example,
spectral changes in the songs of several species that were reported by Nowicki
(1987
) and Hoese et al.
(2000
) appear to occur
primarily above
3.5 kHz. Similarly, spectral changes reported by Goller
et al. (2004
) in zebra
finches, Taeniopygia guttata, occur primarily over relatively high
sound frequencies. Suthers and Goller
(1997
) also demonstrated that
harmonics of fundamentals below
3.5 kHz tend to be suppressed when
northern cardinals, Cardinalis cardinalis, sing songs with relatively
small beak gapes.
Podos et al. (2004) used
linear regression to describe correlations between fundamental frequency and
beak gape movements in several of Darwin's finches under the assumption that
monotonic (or linear) changes in beak gape might be used to `track'
fundamental frequency (Fig.
1A).Nevertheless, many of these species appear to use either a
relatively small beak gape (<
5 mm) when producing relatively low
fundamental frequencies (<
3.5 kHz) or employ a relative large beak
gape (>
5 mm) when producing high fundamental frequencies (>
3.5
kHz; Podos et al., 2004
). As a
consequence, intermediate gapes might occur during transitions between these
two ends and birds may simply strive to use a large beak gape when producing
sound frequencies above
3.5 kHz and strive to use a relatively small beak
gape when producing sound frequencies below
3.5 kHz.
We suggest that a decrease in beak gape functions to attenuate the second
resonance peak that we observed near 5.5 kHz in all subjects (Figs
1 and
4). Indeed, resonance peaks
shown in Fig. 4 were obtained
from subjects with a 5 mm beak gape and this resonance peak increases in both
width and amplitude as beak gape increases beyond 5 mm (i.e.,
4 dB at 11
mm).Subjects may therefore reduce beak gape as a mechanism for decreasing
harmonic energy near this resonance frequency (
5.5 kHz). As an example, a
similar resonance peak and abnormally large beak gape might, in part, explain
the example of vocal tract filtering that was described in the canary,
Serinus canaria, by Hoese et al.
(2000
see
Fig. 7).
Fletcher and Tarnopolsky
(1999) used cylindrical and
conical models to estimate the effects of beak gape on radiated sound. Our
results are consistent with these models since high sound frequencies tend to
radiate more efficiently as beak gape is increased. Moreover, while transfer
functions shown in Figs 5 and
6 suggest that a decrease in
beak gape might function to attenuate sound frequencies between
4 and 7.5
kHz, increases in beak gape may alternatively amplify these same sound
frequencies. For example, resonances within the oral cavity between
4 and
7.5 kHz may combine with resonances near 5.5 kHz that can be attributed to the
trachea. Indeed, low-level spectral ripples in our recordings might also be
attributed to resonances within the oral cavity
(Fletcher and Tarnopolsky,
1999
). Finally, and under these latter conditions, it seems
possible that songbirds might be able to slightly raise or lower the
frequencies that are amplified or attenuated in vocalizations as subjects open
and close their beaks. For example, it seems possible that songbirds might be
able to modify the overall length and volume of the oral cavity through
laryngeal movements and possibly raise or lower the lowest resonance frequency
of the oral cavity.
Sound radiation
Directional sound radiation patterns were relatively simple and resemble
those reported for the European blackbird
(Larsen and Dabelsteen, 1990).
As a consequence, we summarize our results using calculations of standard
deviation (S.D.). Calculations of S.D. differ from
Direction Indices that have been used to summarize directivity patterns in
other studies (e.g. Fletcher and
Tarnopolsky, 1999
). Nevertheless, variation in radiated amplitude
is accurately characterized by this calculation and calculations of
S.D. can be used to assess how changes in orientation might
influence estimates of source amplitude that receivers must make in the
absence of reverberations or other cues that might directly indicate a
signaler's orientation (e.g. visual cues).
Calculations of S.D. increased between 3 and 3.5 kHz and again
near 7 kHz. We do not know what produces these increases in directionality
although an increase near 3.5 kHz can be attributed to head size (1.5 to
2 cm diameter), which is roughly equal to wavelength divided by 2
. Indeed,
increases in directionality near
3.5 kHz are consistent with calculations
of S.D. that we obtained after rotating several wooden spheres with
variable diameters around in the same horizontal plane (see Materials and
methods, results not illustrated). Directionality is also likely to vary with
body orientation and, potentially, with body size (see Results).
These data are consistent with results reported by Larsen and Dabelsteen
(1990) and are also consistent
with theoretical predictions (Fletcher and
Tarnopolsky, 1999
). Measurements of directionality that have been
obtained from living birds are also consistent with our results
(Brumm, 2002
;
Nelson, 2000
;
Witkin, 1977
). Interestingly,
Witkin (1977
) observed a small
decrease in chickadee `B' note amplitudes that were produced with sound
frequencies just above 5 kHz and we also observed a slight decrease in
directionality near 5 kHz.
Beak gape and sound radiation
Acoustic output above 4 kHz is determined both by orientation and beak
gape. As a consequence, it is interesting to consider how these two factors
might be related. For example, increases in directionality that occur with
beak gape might, in part, explain why relatively high sound frequencies
radiate more efficiently as beak gape increases. Nevertheless, the beak
functions to attenuate sound frequencies only between
4 and 7.5 kHz and
attenuation that occurs as a function of beak gape occurs independently of
head and body orientation. As such, additional factors such as resonances
within the oral cavity that may be controlled by impedance changes near the
beak are certain to eclipse increases in output that may be due to increased
directionality. Similarly, it seems likely that directionality depends
primarily on relationships between head size, body size and sound
wavelength.
Harmonic amplitude and beak movements
Towhees, as well as other species, tend to produce high sound frequencies
(>4 kHz) with a large beak gape (>
4 mm). This trend can be
explained by our data since high sound frequencies would be strongly
attenuated if birds were to produce them with a small beak gape
(Fig. 5). Conversely, the
amplitudes of fundamental frequencies in vocalizations might not be strongly
altered if birds were to maintain a relatively large beak gape (>
5 mm)
over the entire duration of a vocalization (especially below
4 kHz;
although see Goller et al.,
2004
). Why then do towhees and other species produce relatively
low sound frequencies (<
4 kHz) with a small beak gape?
One possible explanation is that these species produce relatively low sound
frequencies (<4 kHz) with a small beak gape as a mechanism for
attenuating harmonics with frequencies between
4 and 8 kHz that are
generated when birds produce fundamental frequencies between
2 and 4 kHz.
Indeed, harmonics with frequencies between
4 and 8 kHz might be
especially strong (loud) if birds did not produce fundamental frequencies
between
2 and 4 kHz with a small beak gape since sound (harmonic)
frequencies between
4 and 8 kHz resonate within the trachea.
Changes in beak gape do not strongly influence low sound frequencies
(<3.5 kHz), or midrange sound frequencies between
3.5 and 4 kHz,
and towhees tend to produce midrange frequencies with an intermediate beak
gape (
45 mm). We suggest that midrange sound frequencies are
produced with intermediate beak gapes simply because subjects must, at some
frequency, transition between vocalizing with a small and large beak gape (or
vice versa). That is, if towhees strive to use a relatively small
beak gape when producing sound frequencies below
3.5 kHz and strive to
use a large beak gape when producing sound frequencies above
3.5 kHz,
then intermediate values will occur naturally during transitions between these
two `extremes'. Thus, while intermediate beak gapes are commonly observed as
vocalizations sweep upwards or downwards through midrange sound frequencies
near
3.5 kHz (e.g. Fig.
12), intermediate beak gapes seem to be observed less frequently
when louder or longer sounds are produced in vocalizations with sound
frequencies below and above
3.5 kHz (e.g.
Podos et al., 2004
).
Implications for communication
Our results suggest that beak gape movements are unlikely to `track' a wide
range of fundamental frequencies in vocalizations in a linear manner
(Fig. 1A). Birds clearly vary
beak gape while vocalizing and thus our results lead to a slightly different
question: why might songbirds benefit from an ability to control the
amplitudes of sound frequencies between 4 and 7.5 kHz?
Changes in beak gape may function to produce species-specific or
individual-specific spectral cues. In fact, many songbirds produce frequency
components in their vocalizations that exceed 4 kHz and the amplitudes of
these modulations are likely to be strongly influenced by changes in beak
gape. Nevertheless, changes in beak gape do not strongly influence sound
frequencies below
4 kHz. In addition, changes in orientation may confound
spectral cues that occur above
4 kHz. As a consequence, changes in beak
gape are likely to have additional functions.
Some songbirds have been found to react strongly when played songs with
`pure-tone' syllables (Bremond,
1976; Falls, 1963
;
Nowicki et al., 1989
;
Strote and Nowicki, 1996
).
Harmonics with frequencies above
7 kHz attenuate rapidly over distance
(Nelson, 2003
;
Wiley and Richards, 1982
) and
may not be easily detected over relatively long distances
(Dooling et al., 2000
). Such
harmonics may therefore rarely be audible when birds produce fundamentals
above
3.5 kHz(harmonics >7 kHz) in vocalizations. Harmonics may also
be inaudible when birds produce lower frequency fundamentals between
2
and 4 kHz with a small beak gape since sound frequencies (harmonics) between
4 and 8 kHz are strongly attenuated by the beak.
Towhees rapidly modulate their calls (e.g.
Nelson, 2004) and often
modulate syllables within their songs even more strongly. Towhees do not
therefore seem to vary beak gape as a mechanism for producing pure-tone sounds
since these modulations result in `rough' sounding syllables. Furthermore,
while songbirds commonly produce pure-tones in their vocalizations, there are
no clear reasons to suspect that a decrease in `tonality' is the only factor
that influences how receivers react when harmonics are experimentally added to
vocalizations (Bremond, 1976
;
Falls, 1963
;
Nowicki et al., 1989
;
Strote and Nowicki, 1996
).
Towhees seem to discriminate and modulate sound frequencies above and below
3.5 kHz differently (Nelson,
2002
; Nelson,
2004
; Nelson and Suthers,
2004
). In addition: (1) sound frequencies above and below
3.5
kHz often propagate differently over distance (e.g.
Nelson, 2003
;
Wiley and Richards, 1982
); (2)
several songbirds produce these two frequency ranges using separate sides of
their bipartite syrinx (e.g. Suthers,
1999
; Suthers and Goller,
1997
; Suthers et al.,
2004
); and (3) female canaries prefer rapid trills that span these
same two sound frequency ranges (Vallet et
al., 1998
). Resonances that we attribute to the trachea would also
seem to emphasize sound frequencies to each side of
3.5 kHz. Wetherefore
propose that towhees vary beak gape as a mechanism for excluding and/or
concentrating energy within at least two distinct sound frequency channels and
that songbirds may, in general, often produce narrow-band or pure-tone sounds
when they achieve this goal.
More specifically, because changes in beak gape alter only the amplitudes
of sound frequencies above 3.54.0 kHz, we propose that towhees
vary beak gape as a mechanism for preserving the fine (sinusoidal) amplitude
envelopes that are imposed upon `tow-hee' calls by modulations occurring at a
rate of
500 Hz (Nelson,
2004
, acoustical changes not illustrated). In addition, we propose
that songbirds may, in general, vary beak gape as a mechanism for attenuating
harmonics above
4 kHz so that temporal patterns over these same sound
frequencies are not degraded by the harmonics of preceding or subsequent notes
(or syllables) that are produced with lower frequencies (<
4 kHz;
Fig. 13). Indeed, harmonics
between
4 and 7.5 kHz depicted in
Fig. 13A might degrade
temporal patterns over these high sound frequencies similarly to the way that
environmental reverberations are thought to degrade vocalizations (e.g.
Dabelsteen et al., 1993
;
Wiley and Richards, 1982
).
Unlike environmental reflections, however, harmonics that are associated with,
but not correlated with, preceding or subsequent low frequency components
(
2-4 kHz; Fig. 13A) are
unlikely to be suppressed by acoustical interactions by neural mechanisms
(e.g. Dent and Dooling,
2003a
,b
).
We do not present a natural example of degradation that might be attributed to
an abnormally large beak gape. Nevertheless, a clear illustration of this
effect was presented by Hoese et al.
(2000
) in their
fig. 7, in which normal
temporal patterns across notes with frequencies above
4 kHz are clearly
degraded by abnormal harmonics near the same frequency (
4 kHz, presumably
caused by the addition of weights to the beak).
|
Whether weakly filtered harmonics would normally be strong enough to
degrade fine or course temporal patterns in vocalizations remains unclear.
Nevertheless, changes in amplitude that can be attributed to changes in
subject orientation and beak gape occur primarily above 4 kHz and these
changes may help to explain why towhees use attenuation (amplitude) as a
distance cue only when listening to sound frequencies below
3.5 kHz
(Nelson, 2002
). The reason
being that attenuation could not function as a reliable distance cue if
signalers were able to vary beak gape or orientation and alter what otherwise
seems to be a reliable relationship between distance and attenuation (where
attenuation is proportional to distance and equal to source amplitude minus
incident amplitude). These results do not explain why towhees sometimes
vocalize with a small beak gape (although see
Goller et al., 2004
), but do
suggest that towhees may pay attention to different dynamic variables when
hearing sound frequencies below or above
3.5 kHz.
How towhees vary beak gape while singing is not expected to differ markedly
from other songbird species (e.g. Hoese et
al., 2000; Podos et al.,
2004
; Westneat et al.,
1993
). Indeed preliminary analyses suggest that introductory
syllables in towhee songs with sound frequencies below
3.54.0 kHz
are produced with a relatively small beak gape (04 mm) while sound
frequencies between
4 and 7.5 kHz are produced with a relatively wide
range of beak gapes (011 mm). In addition, while it seems possible that
songbirds might be able to slightly raise or lower the frequencies of
resonances that are associated with the oral cavity (see above), there are no
clear reasons to presume that different sounds or vocalization types will
resonate differently within the vocal tract (e.g. synthetic frequency sweeps,
calls or songs).
In conclusion, we propose that songbirds vary beak gape as a mechanism for
excluding and/or concentrating energy within at least two distinct sound
frequency `channels', where a channel is defined as the proportion of a
frequency spectrum that is used for a specific purpose. We further propose
that achieving this goal avoids degrading temporal patterns and that
narrow-band sounds are produced in vocalizations when songbirds achieve this
more ostensible goal. We do not quantify the dynamics with which towhees vary
beak gape when producing rapid trills in songs. Nevertheless, prior results
(Hoese et al., 2000) suggest
that towhees may need to rapidly modulate the gapes of their beaks in order to
maintain temporal clarity across notes that are produced with frequencies
above
3.54.0 kHz.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Bremond, J. C. (1976). Specific recognition of the song of Bonelli's warbler. Behaviour 58, 99-116.
Brumm, H. (2002). Sound radiation patterns in Nightingale (Luscinia megarhynchos) songs. J. Ornithol. 143,468 -471.[CrossRef]
Dabelsteen, T., Larsen, O. N. and Pedersen, S. B. (1993). Habitat-induced degradation of sound signals: quantifying the effects of communication sounds and bird location on blurr ratio, excess attenuation, and signal-to-noise ratio in blackbird song. J. Acoust. Soc. Am. 93,2206 -2220.
Daley, M. and Goller, F. (2004). Tracheal length changes during zebra finch song and their possible role in upper vocal tract filtering. J. Neurobiol. 59,319 -330.[CrossRef][Medline]
Dent, M. L. and Dooling, R. (2003a). Investigations of the precedence effect in budgerigars: effect of stimulus type, intensity, duration, and location. J. Acoust. Soc. Am. 113,2146 -2158.[CrossRef][Medline]
Dent, M. L. and Dooling, R. (2003b). Investigations of the precedence effect in budgerigars: the perceived location of auditory images. J. Acoust. Soc. Am. 113,2159 -2169.[CrossRef][Medline]
Dooling, R. J., Lohr, B. and Dent, M. L. (2000). Hearing in birds and reptiles. In Comparative Hearing in Birds and Reptiles, vol. 13 (ed. R. J. Dooling, R. R. Fay and A. N. Popper). New York: Springer-Verlag.
Falls, J. B. (1963). Properties of bird song eliciting responses from territorial males. Proc Int. Ornith. Congr. 13,259 -271.
Fletcher, N. H. and Tarnopolsky, A. (1999). Acoustics of the avian vocal tract. J. Acoust. Soc. Am. 105,35 -49.[CrossRef]
Goller, F., Mallinckrodt, M. J. and Torti, S. D. (2004). Beak gape dynamics during song in the zebra finch. J. Neurobiol. 59,289 -303.[CrossRef][Medline]
Hoese, W. J., Podos, J., Boetticher, N. C. and Nowicki, S.
(2000). Vocal tract function in birdsong production; experimental
manipulation of beak movements. J. Exp. Biol.
203,1845
-1855.
Larsen, O. N. and Dabelsteen, T. (1990). Directionality of blackbird vocalization, implications for vocal communication and its further study. Ornis Scandinavica 21, 37-45.
Lohr, B., Wright, T. F. and Dooling, R. J. (2003). Detection and discrimination of natural call in masking noise by birds: estimating the active space of a signal. Anim. Behav. 65,763 -777.[CrossRef]
Nelson, B. S. (2000). Avian dependence on sound-pressure level as an auditory distance cue. Anim. Behav. 59,57 -67.[CrossRef][Medline]
Nelson, B. S. (2002). Duplex auditory distance assessment in a small passerine bird (Pipilo erythrophthalmus). Behav. Ecol. Sociobiol. 53, 42-50.[CrossRef]
Nelson, B. S. (2003). Reliability of sound attenuation in Florida scrub habitat and behavioral implications. J. Acoust. Soc. Am. 113,2900 -2910.
Nelson, B. S. (2004). Dynamics of frequency and amplitude modulations in vocalizations produced by eastern towhees, Pipilo erythrophthalmus. J. Acoust. Soc. Am. 115,1333 -1344.[CrossRef][Medline]
Nelson, B. S. and Suthers, R. A. (2004). Sound
localization in a small passerine bird: discrimination of azimuth as a
function of head orientation and sound frequency. J. Exp.
Biol. 207,4121
-4133.
Nowicki, S. (1987). Vocal tract resonances in oscine bird song production: evidence from birdsongs in a helium atmosphere. Nature 325,53 -55.[CrossRef][Medline]
Nowicki, S. and Marler, P. (1988). How do birds sing? Music Percept. 5,53 -55.
Nowicki, S., Mitani, J., Nelson, D. A. and Marler, P. (1989). The communicative significance of tonality in birdsong: responses to songs produced in helium. Bioacoustics 2, 35-46.
Podos, J., Southall, J. A. and Rossi-Santos, M. R.
(2004). Vocal mechanics in Darwin's finches: correlation of beak
gape and song frequency. J. Exp. Biol.
207,607
-619.
Strote, J. and Nowicki, S. (1996). Responses to songs with altered tonal quality by adult song sparrows (Melospiza melodia). Behaviour 133,161 -172.
Suthers, R. A. (1999). The motor basis of vocal performance in songbirds. In The Design of Animal Communication (ed. M. D. Hauser and M. Konishi), pp.37 -62. Cambridge, USA: MIT press.
Suthers, R. A. and Goller, F. (1997). Motor correlates of vocal diversity in songbirds Vol. 14. In Current Ornithology, vol. 14 (ed. V. J. Nolan, E. Ketterson and C. Thompson), pp. 235-288. New York: Plenum Press.
Suthers, R. A., Vallet, E., Tanvez, A. and Kreutzer, M. (2004). Bilateral song production in domestic canaries. J. Neurobiol. 60,381 -393.[CrossRef][Medline]
Vallet, E., Beme, I. and Kreutzer, M. (1998). Two-note syllables in canary song elicit high levels of sexual display. Anim. Behav. 55,291 -297.[Medline]
Westneat, M. W., Long, J. H. J., Hoese, W. and Nowicki, S.
(1993). Kinematics of birdsong: functional correlations of
cranial movements and acoustic features in sparrows. J. Exp.
Biol. 182,147
-171.
Wiley, R. H. and Richards, D. G. (1978). Physical constraints on acoustic communication in the atmosphere: implications for the evolution of animal vocalizations. Behav. Ecol. Sociobiol. 3,69 -94.
Wiley, R. H. and Richards, D. G. (1982). Adaptations for acoustic communication in birds: sound transmission and signal detection. In Acoustic Communication in Birds (ed. D. E. Kroodsma and E. H. Miller), pp. 132-163. New York: Academic Press.
Witkin, S. R. (1977). The importance of directional sound radiation in avian vocalization. Condor 79,490 -493.
Wright, T. F., Cortopassi, K. A., Bradbury, J. W. and Dooling, R. (2003). Hearing and vocalizations in the orange-fronted conure. J. Comp. Psychol. 117, 87-95.[CrossRef][Medline]