Mechanisms of frequency and amplitude modulation in ring dove song
1 Behavioural Biology, Institute of Evolutionary and Ecological Sciences,
Leiden University, PO Box 9516, 2300 RA Leiden, The Netherlands
2 School of Medicine, Department of Biology and Program for Neuroscience,
Jordan Hall, Indiana University, Bloomington, IN 47405, USA
* Author for correspondence (e-mail: gabecker{at}indiana.edu)
Accepted 6 March 2003
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Summary |
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Key words: birdsong, phonation, amplitude modulation, frequency, air sac pressure, non-songbird, Streptopelia risoria, ring dove.
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Introduction |
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Songbirds as a group are widely considered to have a higher level of vocal
virtuosity and complexity than non-songbirds. This difference is attributed to
the more complex syringeal musculature of songbirds
(Gaunt, 1983). The involvement
of different peripheral systems in the modulation of phonation has been
relatively well-studied experimentally in a number of different songbird
species (e.g. Rüppell,
1933
; Suthers et al.,
1994
; Goller and Suthers,
1996
; Fee et al.,
1998
; Hoese et al.,
2000
; Larsen and Goller,
2002
). Studies on modulation in non-songbirds, however, are almost
non-existent, although the gating of phonation and sound generation as such
have received considerable attention (e.g.
Youngren et al., 1974
;
Lockner and Murrish, 1975
;
Nottebohm, 1976
;
Gaunt et al., 1977
;
Brackenbury, 1980
;
Suthers and Hector, 1985
;
Goller and Larsen, 1997a
;
Larsen and Goller, 2002
). A
better understanding of the differences in constraints and possibilities in
phonatory control mechanisms of songbirds and non-songbirds could provide an
insight into the factors underlying the disparity in song complexity between
these two groups. Mechanisms of sound modulation in non-songbirds are also
interesting in their own right, since about half of all bird species are
non-songbirds and vocal communication in these taxa seems to be no less
important than in songbirds.
In the current study, we investigate the mechanism by which ring doves,
Streptopelia risoria, produce frequency and amplitude modulation in
their vocalizations. This non-songbird is particularly interesting because its
vocal behaviour has been studied in a variety of contexts, including
reproduction (e.g. Lehrman,
1965), development (Nottebohm
and Nottebohm, 1971
), genetics
(Lade and Thorpe, 1964
),
neuroendocrinology (e.g. Cheng et al.,
1998
), behavioural ecology (e.g.
de Kort and ten Cate, 2001
)
and perception (Beckers et al., in
press
). Moreover, studies by Gaunt et al.
(1982
) on the mechanism of
phonation and sound modulation in ring doves provide a basis for further
study.
Ring doves are the domesticated form of the African collared-dove
Streptopelia roseogrisea. The vocalizations of domestic and wild
forms are not different (Goodwin,
1983; Slabbekoorn et al.,
1999
), and they are considered to be the same species
(Baptista et al., 1997
). Ring
dove advertisement vocalizations (`perch coos') have been described as
relatively simple and stereotypic coos
(Nottebohm and Nottebohm,
1971
; Slabbekoorn et al.,
1999
) that do not vary appreciably between birds
(Goodwin, 1983
). The
development of normal coo vocalizations does not depend on learning
(Nottebohm and Nottebohm,
1971
), and their acoustic structure has been studied in detail by
Gaunt et al. (1982
) and
Slabbekoorn et al. (1999
).
Ring dove coos consist of two sound elements (hereafter referred to as
e1 and e2), separated by a silent pause (p),
composed of a fundamental frequency (f0) without overtones
(Fig. 1A). The first part of
e2 is amplitude modulated [and is therefore considered a separate
note by Miller and Miller
(1958
)], which gives rise to a
trill-like, rolling quality. Gaunt et al.
(1982
) and Miller and Miller
(1958
) report that there is
little frequency modulation, although frequency varies slightly in the last
part of e2. Slabbekoorn et al.
(1999
) did not give any
specifics on frequency-modulation patterns but report that the frequency
varies, on average, from 388 Hz to 822 Hz within coos.
|
To identify physiological correlates of phonation and modulation, Gaunt et
al. (1982) recorded coo
vocalizations, together with concurrent air pressure variation in the trachea
and posterior thoracic air sac (PTAS; = caudal thoracic air sac), and
electromyograms (EMGs) of syringeal and abdominal muscles. From this, they
concluded the following: (1) syringeal muscles act to set the syrinx in
vocalizing position but they are probably not important for modulation; (2)
the overall two-element coo pattern is generated by airflow from two large
peaks of air sac pressure, caused by activity of abdominal muscles, and (3)
the trill-type amplitude modulation is due to pulsatile activity of the
abdominal muscles, which cause an oscillation in driving air sac pressure. In
addition, Gaunt et al. (1982
)
recognized a second, subtle type of amplitude modulation, which they explained
by a muffler action of lateral tympaniform membranes (LTMs) and small
differences in the vibration frequencies of median tympaniform membranes
(MTMs). However, this explanation is probably incorrect, since Goller and
Larsen (1997a
) showed that the
LTMs rather than the MTMs are the sound source in domesticated rock pigeons
(Columba livia), a species that is closely related to ring doves
(Johnson et al., 2001
) and has
a very similar syringeal anatomy.
The experiments reported here were designed to examine the physiological
events responsible for the trill-type amplitude modulation, a common
phenomenon in dove vocalizations, and to examine the mechanism of frequency
modulation. Frequency modulation, although limited
(Miller and Miller, 1958;
Gaunt et al., 1982
), is also
present in many other dove species. Even small differences in frequency have
been shown to have communicative meaning in Eurasian collared-doves
(Streptopelia decaocto;
Slabbekoorn and ten Cate,
1998
; ten Cate et al.,
2002
). Insight into its mechanistic basis might also provide a
better understanding of why frequency modulation is limited in the first
place. To achieve this, we set out to supplement the measurements of Gaunt et
al. (1982
) by recording
spontaneous coo vocalizations, together with concurrent air pressures in the
interclavicular air sac (ICAS) and cranial thoracic air sac (CTAS) and air
flow rate in the trachea. The results lead us to conclude that the mechanism
for amplitude modulation is different from the current model. We also propose
a novel mechanism for frequency modulation.
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Materials and methods |
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Surgical procedures and recording of data
The procedure to record air sac pressure and tracheal flow rate is
described in detail in Suthers et al.
(1994). Therefore, we will
only give a summary here.
After birds were anaesthetized with isoflurane (Abbott Laboratories, North Chicago, IL, USA), a midline incision was made in the skin between the clavicles to expose the trachea as it entered the ICAS membrane. Tracheal airflow was measured with a microbead thermistor probe (BB05JA202N; Thermometrics, Edison, NJ, USA) inserted into the tracheal lumen, just rostrally to the interclavicular membrane. Thermistor wires were routed subcutaneously to connectors on a backpack that the birds wore. The flow rate in the trachea was measured by a feedback circuit in which the current needed to maintain the heated thermistor at a constant temperature was non-linearly proportional to the rate of air flow (Hector Engineering, Elletsville, IN, USA). The response of a clean thermistor to a step function in air flow is approximately 90% full scale in 6 ms. During in vivo measurements, however, its time constant may increase gradually over time due to mucus deposition on the thermistor tip. Both ICAS and CTAS pressures were measured by the same type of piezoresistive silicone diaphragm pressure transducer (FPM-02PG; Fujikura, Marietta, GA, USA), attached to an air sac cannula consisting of a flexible silastic tube (i.d.=1.02 mm; wall thickness=0.57 mm; Dow Corning, Midland, MI, USA). A cannula 18.5 cm long was inserted into the ICAS through a small hole in the interclavicular membrane. From there, it was routed subcutaneously to the backpack carrying the pressure transducer. The CTAS was cannulated by a similar tube 14 cm long inserted into the air sac through the abdominal wall just posterior to the last rib and a few mm lateral to the ventral midline. The cannulae extended 13 mm into the air sacs, and tissue adhesive was used to ensure an air-tight seal.
Recording of data started as soon as the animal started to coo, 14 days after surgery, and continued for 13 weeks. Vocalizations were recorded on a condenser microphone (Audio Technica AT835b or Sennheiser MKH 40) placed 0.51 m in front of the cage. All signals (emitted vocalization on microphone, ICAS pressure or tracheal flow rate, and CTAS pressure) were recorded digitally (20 kilosamples s1) on a rotary storage recorder (model RSR 512; Metrum Information Storage, Littleton, CO, USA) or on a DAT data recorder (model RD135T; TEAC). Coo vocalizations were recorded with either concurrent tracheal flow rate and CTAS pressure signals or with ICAS and CTAS pressure signals. We transferred the recorded signals from tape to a microcomputer by resampling (20 kilosamples s1) using a Data Translation DT-2821G board and a TTE J87 anti-aliasing filter (high cutoff at 8 kHz; stopband attenuation 60 dB per one-third octave).
Because ICAS cannulae were routed subcutaneously, movement of body parts during cooing (e.g. inflating crop) could have applied some external, time-varying pressure to the cannula wall, thereby adding artifactual pressure components to our ICAS recordings. To determine if forces on the cannula wall make a significant contribution to the recorded pressure signal, we recorded vocalization pressure patterns in an additional bird as described for ICAS recordings above, except that the air sac end of the ICAS cannula was sealed by a 3-mm plug of silicon-based dental impression medium (President, Colténe Inc., nr. 4667). Any pressure fluctuations recorded under this condition must be caused by tissue pressure on the wall of the cannula. The results show that such artifactual pressure components are negligible: peak-to-peak pressure amplitudes in recordings with the ICAS cannula plugged are only 0.4% of those in our normal ICAS recordings during vocalization.
The pressure transducers were calibrated and showed a linear response for
the ranges that we encountered in our recordings. Ring doves keep their beak
and nares tightly closed during cooing
(Gaunt et al., 1982), and flow
reversal in the trachea before and after phonation often does not coincide
with an opened beak (G. J. L. Beckers, personal observation). This complicates
the identification of atmospheric pressure levels in our recordings. Since we
were mainly interested in how phonatory characteristics are associated with
changes in air sac pressure, we therefore made no further attempts to
determine absolute pressure levels but used relative pressures instead. For
the analyses of tracheal flow rate, we were also restricted to the use of
relative values, since the relationship between flow rate and thermistor
output is nonlinear and changes over time due to gradual mucus deposition on
the thermistor tip.
Data analysis
Recordings were analyzed with the software program Praat (available from
Paul Boersma and David Weenink,
http://www.praat.org)
version 4.0.5 for Linux. Air sac pressure and tracheal flow rate signals were
low-pass filtered digitally at 100 Hz, using a built-in function of the Praat
program (frequency domain filter, Hann-like shaped band, 100 Hz smoothing).
Although all vocalizations were recorded with a microphone, we used
oscillations associated with near field sound in the tracheal flow and
oscillations in air sac pressure for analyses. These oscillations were
retrieved by band-pass filtering the raw flow and pressure signals at
350800 Hz (50 Hz smoothing). The reason for preferring such signals is
that they do not suffer from the sometimes severe acoustic artifacts that are
introduced in microphone signals if the recording room is not specifically
designed for low-frequency sounds like dove coos (G. J. L. Beckers, personal
observation; see Discussion). We looked for correlates of gating and frequency
modulation in tracheal flow rate and ICAS and CTAS pressure patterns by
printing and visually comparing them together with spectrograms of concurrent
coo vocalizations. This was done for all recordings. We did not differentiate
between nest-, bow- and perch coos since in ring doves there are no apparent
differences in overall acoustic structure. For quantification of relationships
between flow and pressure patterns and the modulation of coo frequency, we
focused on a selection of 10 coos for each combination of recorded variables.
If possible, we selected vocalizations from different recording sessions, and
within sessions we selected recordings with a relatively high signal-to-noise
ratio. For one recording combination (tracheal flow with CTAS pressure in
RD2), however, we only obtained eight coos recorded in a single session. For
each coo, we determined the fundamental frequency (f0) in
consecutive 3-ms time frames, using Praat's autocorrelation function
(Boersma, 1993) and the mean
values of available tracheal flow rate, and ICAS and CTAS signals in these
frames. On average, this resulted in a series of 366 measurement sets per coo.
All data were read into a matrix file, which was imported into SPSS for
Windows, version 10.1, for statistical analyses. Associations between the
modulation of coo frequency and the three recorded physiological variables
were examined quantitatively by computing product-moment correlation
coefficients between concurrent 60-ms time segments (which thus consisted of
20 consecutive 3-ms frames). This was only done for time segments in which the
f0 timefrequency contour was continuous, so we excluded
segments with silent intervals and segments that contained frequency jumps
(see Results). Very rarely, f0 was almost constant within a time
segment. Since correlation coefficients are not informative in such cases, we
excluded segments in which the S.D. of frequency was less than 1 Hz.
Significance tests of the obtained correlation coefficients are not
appropriate because samples are not statistically independent in time series.
Also the strength of correlation should not be given much explanatory power,
because there is no reason to assume that associations, if any, would be
linear. In the case of flow rate, the measurements are known to be nonlinear
in themselves, so a comparison of flow-frequency coefficient magnitudes with
those of pressure variables makes a priori no sense. Instead, we just
used the sign of correlation coefficients (positive or negative) as an
indication of whether or not frequency and a particular physiological variable
varied in the same direction within a 60-ms time segment. For each individual,
we categorized the correlation coefficients of all time segments into two
categories: positive and negative coefficients. If continuous frequency
modulation is consistently associated with one or more of the recorded
physiological variables, then we would expect almost all of their coefficients
to fall into only one of these two categories.
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Results |
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Amplitude modulation and gating
Phonation is always accompanied by air flow through the trachea, while
silent intervals within coos are always accompanied with a stop, or at least
strong reduction, of air flow (Fig.
1A,B). This is also true for the amplitude-modulated part of
e2. The `amplitude modulation' is a series of short sound elements
separated by silent intervals (Fig.
3) and could therefore be considered as a `trill' consisting of
separate `notes'. The heated thermistors record air flow rate but not the
direction of air flow. Gaunt et al.
(1982) have shown, however,
that tracheal pressures are always much lower than air sac pressures during
ring dove vocalizations, so all air flow during phonation
(Fig. 1B) must be in an
expiratory direction through the syrinx.
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Pressure patterns in the CTAS (Figs
1C,
2C) and ICAS
(Fig. 2B) are high during
phonation (e1 and e2) and reduced during the silent interval
p. A similar pressure pattern was reported for the PTAS by Gaunt et
al. (1982). This overall
pattern of high pressure during phonation and low pressure during silent
intervals, however, does not hold for the amplitude-modulated part of
e2. During the first part of e2, there is a continuous,
gradual rise in both ICAS and CTAS pressure, with no reduction during the
silent intervals between sound pulses (Fig.
3B). In the last part of the trill, pressures start to oscillate
with increasing amplitude. Sometimes, a slight oscillation of pressure can
also be seen in the first part of the trill, but always in a gradually rising
pressure pattern. Pressure oscillations continue for one cycle into the part
of e2 that is not trilled. The start and end of sound pulses always
coincide with the start and end of airflow
(Fig. 3A), but the relationship
between sound pulses and pressure cycles is less simple. The pressure
reduction phase of a cycle starts at or shortly after the start of a short
sound element, but overall the correspondence between the cycle phases of
phonation and pressure is variable (Fig.
3B). The lowest parts of the pressure cycles do not coincide with
the silent intervals of the trill.
Frequency modulation
Frequency modulation patterns are considerably more complex than previously
recognized. For the five doves tested, f0 is modulated over a
bandwidth averaging 354 Hz. The mean centre frequency of this band is at 563
Hz, so f0 is modulated for about one octave in ring dove coos
All coos include two types of frequency modulation: continuous frequency modulation and abrupt frequency jumps. Continuous frequency modulation is characterized by a gradual change of f0 over time. At frequency jumps, the gradual f0 timefrequency contour is momentarily disrupted, as f0 almost instantaneously (within 10 ms) jumps to a different frequency range. Frequency differences before and after jumps range from about 50 Hz to 150 Hz, either up or down (see example in Fig. 4). Phonation, however, is not interrupted at frequency jumps, although changes in amplitude can often be observed. The arrows and broken lines in Figs 1A, 2A indicate examples of frequency jumps in complete coo vocalizations. The occurrence and timing of jumps, however, can vary considerably between coos.
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Frequency jumps are often accompanied by a sudden, small increase or decrease in tracheal flow rate, but the directions of change in frequency and rate of change in flow are not always the same. We did not observe any systematic changes in air sac pressures that can be linked to frequency jumps.
Continuous frequency modulation correlates to patterns of ICAS pressure change (for example compare Fig. 2A and Fig. 2B). Visual examination of all the recordings revealed that sound segments not interrupted by silent intervals or frequency jumps can always be scaled to match concurrent ICAS patterns. In low-noise recordings, even the fine structure of ICAS pressure and f0 modulation is correlated (Fig. 5).
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To verify whether or not there is a consistent pressure association between ICAS pressure and f0 modulation, we created scatterplots of ICAS pressure and coo frequency for each individual coo (three doves, 30 coos; e.g. Fig. 6AC). All these scatterplots showed a positive, predominantly linear relationship between ICAS pressure and coo frequency within segments between frequency jumps. At frequency jumps, the slope of this relationship usually changes somewhat. The close correspondence between ICAS pressure and frequency modulation only breaks at the onset and offset of phonation in the short sound pulses of the amplitude modulation. However, these transients are maximally 10 ms in duration and constitute less than 5% of the coo sound. Moreover, scatterplots show that when this occurs, the overall relationship in amplitude-modulated parts remains linear and positive (see, for example, Fig. 6A, in which the yellow and light-green parts are from the amplitude modulation).
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Tracheal flow rate and CTAS pressure are also often, but not always, positively correlated with continuous frequency-modulation patterns. Sometimes these parameters change in a direction opposite to that of frequency over major portions of e1 or e2 (compare, for example, the frequency pattern with CTAS signals in Figs 1 and 2). Scatterplots of the focal coo selections show segments where tracheal flow rate or CTAS pressure correlate negatively with frequency modulation (three doves, 28 coos, and five doves, 58 coos, respectively; e.g. Fig. 6DF and Fig. 6GI). Frequently, a switch from positive to negative relationships, or vice versa, occurs even within continuous segments of phonation.
A quantitative analysis of the coo selections reinforces these qualitative observations (Fig. 7). In 99.8% of all 60-ms segments of continuous phonation, correlation coefficients of ICAS pressures with f0 are positive (N=332, three doves). For tracheal air flow and CTAS pressure, this is only 70.1% and 67.1%, respectively (N=221, three doves, and N=553, five doves, respectively), and hence the association between f0 and these variables is not consistent.
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It is evident from our concurrent recordings of pressure in the CTAS and ICAS (Fig. 2) that, despite their obvious similarity, the pressures in these air sacs sometimes vary independently from each other in their direction of change during some portions of the coo. This unexpected finding has not been reported during vocalization in other birds. In this paper, we focus on the relationship between air sac pressure patterns and acoustic modulation. The possible significance of differences in air sac pressure patterns between air sacs will be addressed elsewhere.
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Discussion |
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The strong, positive association between f0 modulation and ICAS
pressure is likely to be a causal one. It has been shown in a related
(Johnson et al., 2001)
columbid species, Columba livia, that the source of coo vocalizations
is the vibrating LTMs, located in the lateral walls of the tracheal part of
the syrinx (Goller and Larsen,
1997b
; Larsen and Goller,
1999
). Phonation frequency is ultimately determined by the
resonant frequency of these membranes, which depends on their geometry and
density and the tension applied to them
(Fletcher, 1992
). The syrinx
is located within the ICAS, and the external surface of the LTMs are in direct
contact with ICAS space (King,
1989
). It is therefore plausible that variation in ICAS pressure
directly modulates LTM tension, and thus the frequency of phonation.
Nevertheless, the possibility remains that it is not ICAS pressure that
modulates f0 but a third factor that causes concurrent changes in
both f0 and ICAS pressure. However, in the light of our finding
that tracheal flow rate is not consistently associated with f0
modulation, it is difficult to envision a credible alternative
explanation.
Several factors might play a role in regulating pressure in the ICAS. Perhaps the most obvious is the activity of various respiratory muscles responsible for expanding or compressing the air sacs. ICAS pressure might also be affected by changes in syringeal resistance, perhaps caused by an abductive action of the tracheolateralis muscles, the caudal ends of which insert directly on the external surface of the LTMs. There is a potential for complex interactions between control parameters that may help maintain a causal relationship between ICAS pressure and f0 over a wide range of physiological conditions. A full understanding of these mechanisms will require detailed knowledge of the roles of different muscle groups.
The occurrence of sudden frequency jumps in bird vocalizations has been
reported for Eurasian collared doves, Streptopelia decaocto
(Gürtler, 1973;
ten Cate, 1992
;
Ballintijn and ten Cate, 1998
),
which are closely related to ring doves
(Johnson et al., 2001
). In
this species, frequency jumps have been shown to have communicative meaning
(Slabbekoorn and ten Cate,
1998
; ten Cate et al.,
2002
). Frequency jumps have also been reported to occur in
vocalizations of zebra finches, Taeniopygia guttata, where they are
attributed to mode locking in the syringeal dynamics
(Fee et al., 1998
). Mode
locking happens when a nonlinear interaction constrains two oscillating
components of a system to maintain a small integer ratio of frequencies.
Mode-locking transitions may occur because the characteristic frequency of one
component is changed relative to the other, and the oscillation frequency
suddenly jumps to achieve a new stable integer ratio. We believe that
mode-locking transitions are also a likely explanation for frequency jumps in
ring doves, because other types of dynamical behaviour that the nonlinear
interaction of two oscillatory components can lead to, i.e. sudden transitions
to subharmonic and chaotic phonation
(Wilden et al., 1998
), are
apparent in the normal vocalizations of related dove species (such as
Streptopelia tranquebarica and Streptopelia orientalis) and,
occasionally, in aberrant ring dove coos (G. J. L. Beckers, personal
observations).
The existing model for the trill-type amplitude modulation in ring dove
coos, namely an oscillatory driving air sac pressure caused by the pulsatile
action of expiratory muscles (Gaunt et
al., 1982), is not compatible with our results. We did find
oscillations in air sac pressures but only during the last part of the trill.
A close re-examination of the figures published by Gaunt et al.
(1982
) shows that this is also
the case for PTAS pressure. Amplitude modulation is already present well
before air sac pressures start to oscillate, when air sac pressures gradually
increase, but tracheal air flow and phonation nevertheless stop in cyclic
intervals (Fig. 3).
The absence of pressure oscillations in the first part of the trill is not due to a limit in the high-frequency response of the pressure transducer. The expected oscillation frequency here of about 25 Hz is well below the 100 Hz low-pass filter that we used to remove acoustic pressure oscillations of 350800 Hz. In songbirds, this transducer system records sound pressure fluctuations up to at least several kHz. Besides the lack of strong air sac pressure oscillation in the first part of the trill, there is other evidence that oscillating air sac pressure is not the cause of the trill. If the cyclic reduction in air sac pressure were the cause of a reduction or cessation of phonation, then the lowest parts of the pressure cycle should coincide with the silent intervals between sound pulses. However, this is not the case (Fig. 3B). The lowest parts of the pressure cycles are located during the sound pulses, and silent intervals often occur when pressure is relatively high. Furthermore, if air sac pressure oscillation caused amplitude modulation, we would expect amplitude modulation to end during or shortly after the last pressure cycle. Yet our recordings show that the amplitude modulation always ends before the start of the last pressure cycle (Fig. 3B).
We can only explain the pressure and flow patterns during the trill by the repetitive opening and closing of some kind of valve regulating airflow. The rapid series of notes thus appears to be produced by a mechanism of pulsatile expiration in which the airway repetitively opens and closes while the continuous activity of expiratory muscles generates a gradually increasing air sac pressure. Each sound is produced by the opening of a pneumatic valve to release a puff of air through the syrinx. The timing of each sound pulse, then, is determined by the gating of airflow, not by modulation of expiratory muscle activity.
It is interesting that ring doves appear to generate rapid trills using the
same mechanism of pulsatile expiration as do various songbirds such as
canaries (Serinus canaria;
Suthers, 1997) and northern
cardinals (Cardinalis cardinalis;
Suthers and Goller, 1997
). In
songbirds, the medial and lateral labia appear to act as a pneumatic valve at
the cranial end of each bronchus. In ring doves, such action might be
performed by completely adducting the LTMs. The valve is apparently located in
the syrinx instead of the glottis since tracheal pressure remains low during
closure (Gaunt et al., 1982
).
Gaunt et al. (1982
) have shown
that the syringeal muscles (sternotrachealis and tracheolatealis) exhibit
pulsatile EMG patterns during the amplitude-modulated part of ring dove coos.
Since these muscles are likely to cause adduction and abduction of the LTM
membranes, this suggests that the LTM membranes could indeed be involved in
such gating action. Pulsatile expiration, presumably controlled by syringeal
muscles, is also used by budgerigars (Melopsittacus undulatus) to
produce a rapid sequence of notes
(Suthers, 2001
).
The oscillation of air sac pressures during the last part of the trill
could be caused by rhythmic contractions of expiratory muscles, perhaps to
achieve frequency modulation and add more complexity to the coo. However, an
alternative explanation is that pressure oscillations are a consequence of the
gating action of a pneumatic valve. The `burst' of air flow at the onset of a
sound pulse, immediately after a silent interval with reduced or zero flow,
may momentarily cause a reduction in subsyringeal air pressure, which, after a
time lag, is compensated for by the action of abdominal muscles. Three
observations fit this idea: (1) pressure begins to drop at, or shortly after,
the start of a sound pulse; (2) pressure oscillations become evident only at
relatively high flow rates and pulse durations, and their amplitude increases
as both the air flow rate and duration of a sound pulse increase
(Fig. 1); and (3) Gaunt et al.
(1982) report, with respect to
the pressure oscillation, that "abdominal muscular activity is highest
during dips in the pressure curve. Each EMG pulse begins shortly after
pressure begins to drop from a maximum and continues until pressure again
reaches the level at which activity began". Such an EMG pattern suggests
a compensatory action of expiratory muscles against the sudden pressure
drop.
Gaunt et al. (1982)
recognized two types of amplitude modulation in ring doves: the trill-type
amplitude modulation that we addressed above and a more subtle, beat-like
amplitude modulation, which we do not address in this study. In
microphone-recorded vocalizations, we too have observed a phenomenon of
partial or complete beat cycles occurring, intermittently, in all parts of the
coo. Coo sounds in tracheal flow or air sac pressure recordings, however,
never show this phenomenon. Hypothetically, it is possible that such
modulation originates from interaction of the sound source signal with a
resonance filter elsewhere in the animal. Resonance filtering of source
signals has recently been found in ring doves (G. J. L. Beckers, R. A. Suthers
and C. ten Cate, unpublished data). However, interference through reflected
sound waves and the formation of standing waves in enclosed rooms can also
generate beat-like amplitude modulation
(Kinsler et al., 2000
). To
test whether room acoustics could indeed introduce such strong beat
modulations as observed by us and reported by Gaunt et al.
(1982
), we created synthetic
ring dove coos with normal frequency modulation but constant amplitude using
the analytic signal technique as described by Mbu Nyamsi et al.
(1994
). Analysis of such
signals generated by a speaker revealed that, indeed, strong beat-like
amplitude modulations had been introduced, even when recorded in `acoustic
chambers' padded with acoustic foam. Recordings outside in the open field did
not show such beat phenomena. Because we cannot distinguish between beat-like
amplitude modulation produced by the dove, if any, and that caused by the
acoustics of the room, we do not further investigate this phenomenon.
Our finding that pressure in the CTAS and ICAS can vary independently is
new and, potentially, has implications for sound production. Brackenbury
(1971) reported that during
quiet respiration there is only a small gradient between the cranial and
caudally located air sacs of geese (Anser anser). The direction of
this gradient is reversed with the respiratory cycle. Gaunt et al.
(1973
) recorded pressure in
the posterior thoracic, anterior thoracic and interclavicular air sacs of
starlings (Sturnus vulgaris) and noted a similar pressure gradient
only during distress calls, which they deemed to be of no significance to
vocalization. The differences in pressure patterns that we report here in
vocalizing doves, however, have not been described in other birds and suggest
the possibility of independent control of pressure in different air sacs, not
simply a caudocranial gradient between them. The means by which such pressure
differences are produced is unknown. Possible mechanisms include changes in
the rate of air flow into or out of individual air sacs or the possibility
that certain respiratory muscles act selectively on different air sacs. If the
pressure in the ICAS can be varied independently from the pressure inside the
syrinx, it could alter the pressure gradient across the LTMs and affect sound
production by changing their position or tension.
Our spectrograms of ring dove coos (Figs
1,
2) show that frequency
modulation is much more complex than previously reported
(Nottebohm and Nottebohm,
1971; Gaunt et al.,
1982
). Undoubtedly, a major reason for this difference in
interpretation is the current availability of superior, digital techniques for
spectrographic representation. An additional reason may be that frequency
ranges in birdsong are often viewed spectrographically on an absolute and
linear frequency scale, usually spanning a considerable part of our hearing
range. Frequency modulation between 0.4 kHz and 0.8 kHz does not appear
impressive on such a scale. Perceptually, however, both to humans (e.g.
Moore, 1997
) and birds (e.g.
Dooling, 1982
), it is more
appropriate to consider f0 variation in terms of proportions. Our
measurements show that from such a point of view the difference between the
minimum and maximum f0 in individual ring doves is about a factor
of two (one octave), which is not negligible. Acoustic analyses of turtle-dove
perch-coos by Slabbekoorn et al.
(1999
) show that this is also
typical for the other 15 species in the Streptopelia genus. Moreover,
even limited frequency modulation has important communicative function in the
Eurasian collared dove, the sister species of the ring dove
(Slabbekoorn and ten Cate,
1998
; ten Cate et al.,
2002
).
Recently, it has been shown that much of the complexity of the song of
canaries (Gardner et al.,
2001) and chingolo sparrows (Zonotrichia capensis;
Laje et al., 2002
) can be
modelled by smooth and simple variations of only a few parameters. Despite
their complexity, frequency modulation patterns in ring dove coos may also
arise from only two relatively simple, centrally coordinated motor variables.
First, simple and smooth air sac pressure gestures determine the overall
phonation and continuous frequency modulation patterns. Second, amplitude
modulation is caused by the cyclic gating action of a valve. Much of the
remaining complexity, such as oscillatory frequency modulation and frequency
jumps, can be explained on the basis of feedback and intrinsic nonlinear
properties of the syrinx.
What is the significance of our findings with respect to other bird
species? We provide, to our knowledge for the first time, a mechanistic
explanation for frequency modulation of phonation in a non-songbird. ICAS
pressure may also modulate frequency in the vocalizations of other
non-songbirds, given the fact that LTMs occur in many non-songbirds
(King, 1989) and assuming that
the finding of LTMs as the sound generator in a pigeon and a parrot species
(Goller and Larsen, 1997b
) can
be extended to other non-songbirds. Frequency modulation in songbirds
(Miskimen, 1951
;
Goller and Suthers, 1996
;
Larsen and Goller, 2002
), and
possibly parrots (Larsen and Goller,
2002
), is achieved through the action of specialized syringeal
musculature. A mechanism of frequency modulation by ICAS pressure variation
could explain why many non-songbird species often exhibit rather limited
frequency modulation, on an absolute scale, as compared with songbirds.
Muscles that modulate ICAS pressure can only indirectly vary tension of the
sound-generating structures and are not specialized in this task, as
modulation of ICAS pressure is also essential for, and possibly constrained
by, other physiological functions such as respiration. Moreover, the level of
fluid power during bird vocalization depends on the level of air sac pressure
(Brackenbury, 1977
) and is
positively correlated with sound intensity for the species investigated
(Suthers and Goller, 1997
;
Gaunt et al., 1976
). The
overall modulation of frequency and sound intensity are thus likely to be
coupled in ring doves, and possibly other non-songbirds. A future study should
investigate the possibility that maximizing vocal intensity, an important
property of long-distance signals, may constrain frequency modulation.
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Acknowledgments |
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References |
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Ballintijn, M. R. and ten Cate, C. (1998).
Sound production in the collared dove: a test of the `whistle' hypothesis.
J. Exp. Biol. 201,1637
-1649.
Baptista, L., Trail, P. W. and Horblit, H. M. (1997). Family columbidae (pigeons and doves). In Sandgrouse to Cuckoos, Handbook of the Birds of the World, vol. 4 (ed. J. del Hoyo, A. Elliot and J. Sargatal), pp. 60-243. Barcelona: Lynx Edicions.
Beckers, G. J. L., Goossens, B. M. A. and ten Cate, C. (in press). Perceptual salience of acoustic differences between conspecific and allospecific vocalisations in African collared-doves. Anim. Behav.
Boersma, P. (1993). Accurate short-term analysis of the fundamental frequency and the harmonics-to-noise ratio of a sampled sound. P. I. Phon. Sci. U. Amst. 17, 97-110.
Brackenbury, J. H. (1971). Airflow dynamics in the avian lung as determined by direct and indirect methods. Resp. Physiol. 13,319 -329.[CrossRef][Medline]
Brackenbury, J. H. (1973). Respiratory mechanics in the birds. Comp. Biochem. Physiol. 44,599 -611.
Brackenbury, J. H. (1977). Physiological energetics of cock-crow. Nature 270,433 -435.
Brackenbury, J. H. (1980). Control of sound production in the syrinx of the fowl Gallus gallus. J. Exp. Biol. 85,239 -251.
Cheng, M. F., Peng, J. P. and Johnson, P.
(1998). Hypothalamic neurons preferentially respond to female
nest coo stimulation: demonstration of direct acoustic stimulation of
luteinizing hormone release. J. Neurosci.
18,5477
-5489.
de Kort, S. R. and ten Cate, C. (2001). Response to interspecific vocalizations is affected by degree of phylogenetic relatedness in Streptopelia doves. Anim. Behav. 61,239 -247.[CrossRef][Medline]
Dooling, R. J. (1982). Auditory perception in birds. In Acoustic Communication in Birds, vol.1 (D. E. Kroodsma and E. H. Miller), pp.95 130. New York: Academic Press.
Fee, M. S., Shraiman, B., Pesaran, B. and Mitra, P. P. (1998). The role of nonlinear dynamics of the syrinx in the vocalizations of a songbird. Nature 395,67 71.[CrossRef][Medline]
Fletcher, N. H. (1992). Acoustic Systems in Biology. Oxford: Oxford University Press.
Fletcher, N. H. (2000). A class of chaotic bird calls? J. Acoust. Soc. Am. 108,821 -826.[CrossRef][Medline]
Gardner, T., Cecchi, G., Magnasco, M., Laje, R. and Mindlin, G. B. (2001). Simple motor gestures for birdsongs. Phys. Rev. Lett. 87, art. no. 208101.
Gaunt, A. S. (1983). A hypothesis concerning the relationship of syringeal structure to vocal abilities. Auk 100,853 -862.
Gaunt, A. S., Gaunt, S. L. L. and Casey, R. M. (1982). Syringeal mechanisms reassessed: evidence from Streptopelia. Auk 99,474 -494.
Gaunt, A. S., Gaunt, S. L. L. and Hector, D. H. (1976). Mechanics of the syrinx in Gallus gallus. I A comparison of pressure events in chickens to those in oscines. Condor 78,208 -223.
Gaunt, A. S., Gaunt, S. L. L. and Hector, D. H. (1977). Mechanics of the syrinx in Gallus gallus.II Electromyographic studies of ad libitum vocalizations. J. Morphol. 152,1 -20.[Medline]
Gaunt, A. S., Stein, R. C. and Gaunt, S. L. L. (1973). Pressure and air flow during distress calls of the starling, Sturnus vulgaris (Aves; Passeriformes). J. Exp. Zool. 183,241 -262.
Goller, F. and Larsen, O. N. (1997a). In
situ biomechanics of the syrinx and sound generation in pigeons.J. Exp. Biol. 200,2165
-2176.
Goller, F. and Larsen, O. N. (1997b). A new
mechanism of sound generation in song-birds. Proc. Natl. Acad. Sci.
USA 94,14787
-14791.
Goller, F. and Suthers, R. A. (1996). Role of
syringeal muscles in controlling the phonology of bird song. J.
Neurophysiol. 76,287
-299.
Goodwin, D. (1983). Pigeons and Doves of the World. London: British Museum of Natural History.
Gürtler, W. (1973). Artisolierende Parameter der Rivierrufs der Türkentaube (Streptopelia decaocto). J. Ornithol. 114,305 -316.
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.
Johnson, K. P., de Kort, S., Dinwoodey, K., Mateman, A. C., ten Cate, C., Lessells, C. M. and Clayton, D. H. (2001). A molecular phylogeny of the dove genus Streptopelia.Auk 118,874 -887.
King, A. S. (1989). Functional anatomy of the syrinx. In Form and Function in Birds, vol.4 (A. S. King and J. McLelland), pp.105 -192. London: Academic Press.
Kinsler, L. E., Frey, A. R., Coppens, A. B. and Sanders, J. V. (2000). Fundamentals of Acoustics. Fourth edition. New York: John Wiley & Sons.
Lade, B. I. and Thorpe, W. H. (1964). Dove songs as innately coded patterns of specific behaviour. Nature 202,366 -368.
Laje, R., Gardner, T. J. and Mindlin, G. B. (2002). Neuromuscular control of vocalizations in birdsong: a model. Phys. Rev. E 65, art. no. 051921.
Larsen, O. N. and Goller, F. (1999). Role of syringeal vibrations in birds vocalizations. Proc. R. Soc. Lond. B Biol. Sci. 266,1609 -1615.[CrossRef]
Larsen, O. N. and Goller, F. (2002). Direct
observation of syringeal muscle function in songbirds and a parrot.
J. Exp. Biol. 205,25
-35.
Lehrman, D. S. (1965). Interaction between internal and external environments in the regulation of the reproductive cycle of the ring dove. In Sex and Behaviour (F. A. Beach), pp. 355-380. New York: Wiley.
Lockner, F. R. and Murrish, D. E. (1975). Interclavicular air sac pressures and vocalization in mallard ducks Anas platyrhynchos. Comp. Biochem. Physiol. A 52,183 -187.[Medline]
Mbu Nyamsi, R. G., Aubin, T. and Bremond, J. C. (1994). On the extraction of some time dependent parameters of an acoustic signal by means of the analytic signal concept. its application to animal sound study. Bioacoustics 5, 187-203.
Miller, W. J. and Miller, L. S. (1958). Synopsis of behaviour traits of the ring neck dove. Anim. Behav. 6,3 -8.
Miskimen, M. (1951). Sound production in passerine birds. Auk 68,493 -504.
Moore, B. C. J. (1997). An Introduction to the Psychology of Hearing. Fourth edition. San Diego: Academic Press.
Nottebohm, F. (1976). Phonation in the orange-winged Amazon parrot, Amazona amazonica. J. Comp. Physiol A 108,157 -170.
Nottebohm, F. and Nottebohm, M. E. (1971). Vocalizations and breeding behavior of surgically deafened ring doves, Streptopelia risoria. Anim. Behav. 19,313 -327.[Medline]
Rüppell, W. (1933). Physiologie und Akustik der Vogelstimme. J. Ornithol. 81,433 -542.
Slabbekoorn, H., de Kort, S. and ten Cate, C. (1999). Comparative analysis of perch-coo vocalizations in Streptopelia doves. Auk 116,737 -748.
Slabbekoorn, H. and ten Cate, C. (1998). Perceptual tuning to frequency characteristics of territorial signals in collared doves. Anim. Behav. 55,847 -857.[CrossRef]
Suthers, R. A. (1997). Peripheral control and lateralization of birdsong. J. Neurobiol. 33,632 -652.[CrossRef][Medline]
Suthers, R. A. (2001). Peripheral vocal mechanisms in birds: are songbirds special? Neth. J. Zool. 52,217 -242.
Suthers, R. A. and Goller, F. (1997). Motor correlates of vocal diversity in songbirds. In Current Ornithology, vol. 14 (V. Nolan, Jr, E. Ketterson and S. F. Thompson), pp. 235-288. New York: Plenum Press.
Suthers, R. A., Goller, F. and Hartley, R. S. (1994). Motor dynamics of song production by mimic thrushes. J. Neurobiol. 25,917 -936.[Medline]
Suthers, R. A., Goller, F. and Pytte, C. (1999). The neuromuscular control of birdsong. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 354,927 -939.[CrossRef][Medline]
Suthers, R. A. and Hector, D. H. (1985). The physiology of vocalization by the echolocating oilbird, Steatornis caripensis. J. Comp. Physiol. A 156,243 -266.
ten Cate, C. (1992). Coo types in the collared dove Streptopelia decaocto: one theme, distinctive variations. Bioacoustics 4,161 -183.
ten Cate, C., Slabbekoorn, H. and Ballintijn, M. R. (2002). Birdsong and male male competition: causes and consequences of vocal variability in the collared dove (Streptopelia decaocto). Adv. Study Behav. 31, 31-75.
Wilden, I., Herzel, H., Peters, G. and Tembrock, G. (1998). Subharmonics, biphonation, and deterministic chaos in mammal vocalization. Bioacoustics 9, 171-196.
Youngren, O. M., Peek, F. W. and Phillips, R. E. (1974). Repetitive vocalizations evoked by local electrical stimulation of avian brains. III Evoked activity in the tracheal muscles of the chicken (Gallus gallus). Brain Behav. Evolut. 9,393 -421.