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First published online May 30, 2008
Journal of Experimental Biology 211, 1978-1991 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.014092
Two-voice complexity from a single side of the syrinx in northern mockingbird Mimus polyglottos vocalizations
1 Department of Biology, Jordan Hall, Indiana University, Bloomington, IN 47405,
USA
2 School of Medicine, Jordan Hall, Indiana University, Bloomington, IN 47405,
USA
3 National Center for Voice and Speech, 1101 13th Street, Denver, CO 80204,
USA
4 Program in Neural Science, Jordan Hall, Indiana University, Bloomington, IN
47405, USA
* Author for correspondence (e-mail: szolling{at}indiana.edu)
Accepted 9 April 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: birdsong, mockingbird, nonlinear phenomena, song learning, vocal production
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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).
Certain features of vocal performance and acoustic complexity associated with
the vocal motor skills of male songbirds may be used by females during mate
selection (e.g. Ballentine et al.,
2004; Forstmeier et al.,
2002; Vallet et al.,
1998). The ability for vocal learning and the production of
increasingly complex vocal signals may have facilitated the radiation of the
songbirds (oscine Passeriformes) into the largest and most diverse order of
birds (Fitzpatrick, 1988;
Vermeij, 1988), but its role
in speciation is controversial (Baptista
and Trail, 1992; Raikow,
1986). Understanding the vocal mechanisms responsible for the spectral and temporal complexity of bird song can provide a valuable insight into the performance constraints and evolution of song diversity. A major source of acoustic complexity in songbirds comes from the versatility of motor control of their duplex vocal organ, but in some species the intrinsic biomechanical properties of the vibratory sound generating structures in the vocal organ may also contribute significantly to song complexity. In this paper, we attempt to assess the contribution each of these sources makes to the vocal diversity of song by the northern mockingbird.
Sources of acoustic complexity
The bipartite syrinx
The songbird's vocal organ, the syrinx, is composed of modified cartilages
at the cranial end of each primary bronchus and the caudal end of the trachea.
Each bronchus contains a pair of fleshy pads, the medial and lateral labia
(King, 1989), which vibrate
when adducted into the respiratory airflow
(Goller and Larsen, 2002) and
provide the bird with two independently controlled sound sources, one in each
bronchus (Suthers, 1990). The
acoustic properties of song generated by each pair of labia are controlled by
the activity of ipsilateral syringeal muscles innervated by the
tracheosyringeal branch of the hypoglossal nerve
(Goller and Suthers, 1996a;
Goller and Suthers,
1996b).
Spectrographic analyses of birdsong
(Borror and Reese, 1956;
Greenewalt, 1968;
Stein, 1968;
Thorpe, 1961) revealed the
presence in many species of two, simultaneous non-harmonically related
frequencies. Greenewalt (Greenewalt,
1968) referred to these as `two-voice' phenomena and hypothesized
the voices originated on opposite sides of the syrinx, a view supported by
subsequent experiments showing varying degrees of song lateralization
following unilateral section of the tracheosyringeal branch of the hypoglossal
nerve (Floody and Arnold,
1997; Lemon, 1973;
Nottebohm, 1971;
Nottebohm and Nottebohm, 1976;
Suthers, 1990;
Suthers et al., 2004;
Williams et al., 1992).
A more detailed understanding of the acoustic contribution each sound
source makes to oscine song has come from techniques for recording airflow
through each side of the syrinx, together with syringeal and respiratory motor
activity during spontaneous song with both sides of the syrinx intact
(Suthers, 1990). These data
show that songbirds exploit their dual sound source to increase vocal
virtuosity in multiple ways, including the production of two-voice elements,
switching phonation between sides to produce abrupt frequency steps between
notes and taking advantage of lateralized functional specializations in the
acoustic properties of each sound source (reviewed in
Suthers, 1999;
Suthers and Goller, 1997;
Suthers and Zollinger,
2004).
Syringeal nonlinear dynamics
In addition to vocal production by coordinated neuromuscular control of the
syrinx and respiratory system, there is evidence that intrinsic, passive,
biomechanical properties of syrinx, particularly the dynamic vibratory
properties of the paired oscillators (the medial and lateral labia) comprising
each sound source, can also result in the production of complex sounds
(Fee, 2002;
Fee et al., 1998;
Mindlin and Laje, 2005).
Recent experiments have demonstrated that the labia, much like the vocal folds
in the mammalian larynx (Berry et al.,
1996; Herzel et al.,
1994), comprise a nonlinear physical system
(Fee, 2002;
Fee et al., 1998). As in any
such system, the oscillating masses predictably exhibit certain traits or
behaviors including abrupt bifurcations between different vibratory modes.
Four acoustic phenomena are associated with nonlinear systems
(Wilden et al., 1998). These
`nonlinear phenomena' (NLP) include frequency jumps, subharmonics, biphonation
and deterministic chaos. In addition to the NLP recorded from excised syrinxes
of zebra finches (Fee et al.,
1998), NLP have been identified in the natural vocalizations of a
diverse set of species, including non-songbirds such as doves
(Beckers and ten Cate, 2006)
and parrots (Fletcher, 2000),
frogs (Suthers et al., 2006),
terrestrial and marine mammals (Herzel et
al., 1995; Riede et al.,
2007; Riede et al.,
2000; Riede et al.,
2004; Riede et al.,
1997; Titze et al.,
1993; Tokuda et al.,
2002; Tyson et al.,
2007; Wilden et al.,
1998).
Identifying the source of acoustic complexity in a two-voice vocal system
Because their vocal organ contains two independent sound sources,
spectrographic analyses alone in songbirds cannot always reliably distinguish
between two voices and some kinds of NLP. Frequency jumps produced by rapidly
switching phonation from one side of the syrinx to the other (see
Allan and Suthers, 1994) may be
indistinguishable from frequency jumps resulting from bifurcations due to the
nonlinear dynamics of a single pair of oscillators.
In mammals, biphonation is traditionally defined as the simultaneous
appearance of two independent frequencies
(Berry et al., 1996;
Wilden et al., 1998). The same
definition was applied by Greenewalt
(Greenewalt, 1968) to describe
standard two-voice phenomena in songbirds, but it is now clear that though
both examples contain simultaneous harmonically unrelated frequencies, their
physical basis is quite different. In two-voice phenomena each voice is
generated by a separate set of paired oscillators whereas in biphonation
harmonically unrelated frequencies are generated by the nonlinear properties
of a single set of oscillators (Suthers et
al., 2005).
Additional problems in discerning NLP from two-voice phenomena based solely
on emitted vocalizations were described by Laje, Mindlin and colleagues
(Laje and Mindlin, 2005;
Laje et al., 2008), whose
models of source–source and source–tract interactions in the
oscine syrinx demonstrate that interactions of the two sides of the syrinx can
produce acoustic effects resembling those commonly associated with nonlinear
theory, such as subharmonics and biphonation. Their models support earlier
evidence of source–source coupling in the oscine syrinx
(Nowicki and Capranica, 1986)
and demonstrate that certain complex sounds typically associated with
nonlinear dynamics, such as frequency jumps, subharmonics or biphonation in
birdsong, might also result from acoustic interactions within the syrinx and
trachea of sounds produced on the two sides.
Here we investigate the occurrence of the nonlinear characteristics in spontaneous song of the northern mockingbird, a vocal mimic. By monitoring subsyringeal pressure and airflow through each side of the syrinx we can determine if these nonlinear features are lateralized to one side of the syrinx or produced bilaterally and distinguish them from superficially similar two-voice vocalizations, in order to more accurately estimate their contribution to song complexity.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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90 and 120 syllable types at the
time of the experiment. Tutor sounds were chosen or designed for an experiment
on song production [tutoring details are given elsewhere
(Zollinger and Suthers,
2004)]. While the tutor experience of these mockingbirds was not
specifically designed to investigate nonlinear phenomena, the sounds were
intended to expose juvenile mockingbirds to a wide variety of complex sounds,
including some possible NLP. All birds had been exposed to tutor sounds
containing two simultaneous unrelated frequencies, either in recordings of
heterospecific song or in computer-synthesized tutor sounds. Sounds containing
two independent frequencies were of two general types. The first type
consisted of two distinct tones (between 1 and 7 kHz) with independent rates
of frequency modulation (FM), e.g. Fig.
1A. The second type consisted of a single high fundamental
frequency f0 accompanied by a lower (<750 Hz)
modulating frequency (m0), resulting in a periodic
amplitude modulation (AM) of the waveform with sidebands (e.g.
Fig. 1B). Some tutor sounds
contained frequency jumps, consisting of abrupt step-like changes of 0.5 and 3
kHz in f0, in the frequency range between 1 and 7 kHz.
None of the tutor sound recordings contained subharmonics or chaos; however,
mockingbirds were occasionally exposed to the song of northern cardinals
Cardinalis cardinalis, eastern towhees Pipilo
erythrophthalmus, zebra finches Taeniopygia guttata and ring
doves Streptopelia risoria that were housed in adjacent rooms in the
laboratory, therefore we cannot rule out the possibility that mockingbirds
heard NLP that may have been present in the songs of these other species.
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Surgery and data acquisition
Birds were anesthetized by injection of chloropent (4.1
µlg–1 body mass; recipe from Fort Dodge Animal Health,
Overland Park, KS, USA) into the pectoral muscle. A silastic cannula (Dow
Corning Corp, Midland, MI, USA; i.d. 1.02mm, o.d. 2.16mm) was inserted into a
cranial thoracic air sac for measurement of subsyringeal pressure. The cannula
was attached to a miniature piezoresistive pressure transducer (Fujikura
FPM-02PG, Marietta, GA, USA) mounted on a small backpack attached to an
elastic belt fitted around the bird's thorax.
A mid-ventral incision was made between the clavicles in order to expose
the syrinx through an opening in the interclavicular membrane. The rate of
airflow was recorded by a heated microbead thermistor (Thermometrics, Edison,
NJ, USA, BB05JA202) inserted into each bronchus a few semi-rings caudal to the
syrinx. The interclavicular membrane was sealed around the thermistor leads,
which were routed under the skin to the backpack. Surgical methods are
described in more detail elsewhere
(Suthers et al., 1994;
Zollinger and Suthers, 2004).
Pressure and airflow signals were transmitted from the backpack on leads that
exited through the top of the cage to signal conditioning instruments (Hector
Engineering, Elletsville, IN, USA) and a multi-channel digital data recorder
(Metrum DataTape RSR512, Littleton, CO, USA). Four signals (vocalization, rate
of airflow through the right and left bronchi, and air sac pressure) were
recorded digitally (40 000 samples s–1
channel–1) onto separate tracks on S-VHS 1/2'' magnetic
tape cassettes (Maxell ST-31BQ SVHS, Fair Lawn, NJ, USA) using the Metrum
recorder. Signals were transferred from tape to microcomputer using a Data
Translation board (DT-2821G) and an antialiasing filter (TTE, J87, St Pete
Beach, FL, USA; 8kHz high cut-off, stopband attenuation 60 dB per 1/3 octave).
An experiment lasted 7–10 days, during which the bird could move freely
about its cage. Vocalizations during experiments were recorded with a
directional condenser microphone (Audio-technica AT835b, Stow, OH, USA)
positioned approximately 50 cm in front of the cage.
Two methods were used to determine what each side of the syrinx contributed
to the song. The first method measured airflow through the syrinx; any air
flowing through one side of the syrinx while the other side was closed
indicated that the sound was produced entirely with the open side. In some
recordings, the thermistors responded to air oscillations up to 2 or 3kHz
produced by the acoustic signal from the ipsilateral side of the syrinx. In
these cases it was possible to determine the sound generated by each side when
both sides were phonating (Suthers,
1990). The low frequency components of bronchial signals related
to respiratory or phonatory motor patterns were removed post-recording with a
digital 100 Hz Hanning high-pass filter.
Signals were analyzed using Igor Pro v. 5 (WaveMetrics Inc., Lake Oswego, OR, USA) and Adobe Audition v. 1.5 (Adobe Systems Inc., San Jose, CA, USA). Statistical analysis was conducted using Igor Pro v. 5 and SigmaStat v. 2.03 (SPSS Inc., Chicago, IL, USA). Preoperative song (100–300 min per bird) was recorded from adult birds (>300 days post-hatching) for comparison with pre- and post-surgery repertoires (Avisoft-Recorder v. 1.7, Avisoft Bioacoustics, Berlin, Germany).
For each syllable that spectrographically resembled one of the four NLP, we examined the airflow and pressure recordings, and noted the acoustic contribution of each side of the syrinx. A syllable was defined as a sound in which the air sac pressure was negative prior to the sound, positive during the sound production, and negative after completion of the sound (a single expiratory pulse). Vocalizations were first examined for the occurrence of NLP through visual inspection of narrowband spectrograms (1024 points at 40 000 samples s–1, frame duration 25.6 ms, window duration 75%, Hanning window type) and associated power spectra. Each syllable was scored for the presence of the four NLP described above. If a syllable contained more than one type of NLP it was counted in each category.
Identifying nonlinear phenomena
Spectrographic evaluation
We examined 1000 syllables each from four subjects for acoustic evidence of
NLP (frequency jumps, subharmonics, biphonation or deterministic chaos). This
initial sorting of sounds by visual spectrographic examination is not
sufficient to determine the mechanism of production, but was done to identify
potential NLP for further investigation.
Frequency jumps are sudden changes in fundamental frequency (f0) to a higher or lower f0 (Fig. 2A). A frequency jump was defined as a visible, instantaneous (<5 ms silent interval between adjacent frequencies, as measured from the time waveform) step-change in f0.
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Deterministic chaos (low-dimensional noise) is technically distinguishable
from stochastic noise (high-dimensional chaos) by the number of dimensions
needed to describe it (Tokuda et al.,
2002). However, the distinction can also be made based on telltale
characteristics visible in narrowband spectrograms
(Wilden et al., 1998),
including preceding subharmonics (e.g. Fig.
2B) and the presence of harmonic `windows' in otherwise noisy
segments. We classified sounds as `deterministic chaos' if we observed a
broadband, noisy segment in the spectrogram
(Fig. 2C), plus at least two
additional indications, such as a sudden onset of the noise, preceding
subharmonics or harmonic windows within the noise.
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Mechanism of vocal production
For each putative instance of NLP observed spectrographically, we then
examined concurrent airflow through the right and left sides of the syrinx,
along with subsyringeal air sac pressure. This analysis allowed us to
determine if the occurrence of such sounds could be explained by independent
phonation on the two sides of the syrinx, or if they were produced by a single
source.
In order to test whether the relationships between the occurrence of frequency jumps or subharmonics and changes in either air sac pressure or bronchial airflow were significant, we investigated changes in rates of air flow immediately prior to the bifurcation and at an earlier point in the same syllables. Temporal resolution of the time series was 25 µs. The signal was examined over two 5 ms time intervals (20–25 and 5–0 ms) prior to the bifurcation and 0–5 ms after the bifurcation. Air sac pressure and rate of airflow through the syrinx were normalized to a percentage of maximum flow rate or pressure. The normalized pressure or rate was then regressed against distance (time) to the point of bifurcation. Slopes of these regression lines were tested for differences in variance between groups using SigmaStat 3.11 (Systat Software Inc., San Jose, CA, USA). Because most examples of chaos occurred either for the entire duration of the syllable, or immediately following a period of subharmonics, similar analyses of flow and pressure prior to the onset of chaos were not conducted. Similarly, biphonation usually had a gradual onset or lasted the entire duration of the syllable, precluding a meaningful analysis of flow and pressure fluctuation associated with the bifurcation in these cases.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Frequency jumps
Occurrences of frequency jumps
Unilaterally produced frequency jumps
(Fig. 3) occurred in 1.2% of
syllables overall (mockingbird m108, 0.8%; m123, 1.2%; m130, 1.5%; m152, 1.3%)
bilateral frequency jumps were observed in 4.9% of all syllables (m108, 3.3%;
m123, 3.0%; m130, 6.8%; m152, 6.5%). In unilaterally produced frequency jumps,
the fundamental frequency shifts abruptly up or down with a silent interval
<5 ms between adjacent frequencies. During the jumps there is airflow
through only one side of the syrinx, the other side being closed. The change
in frequency due to the jumps ranged from 45 to 450 Hz. Jumps from both a
higher to lower frequency and lower to higher frequency were observed (47.9%
down-jumps, 52.1% up-jumps). Mimicked copies of tutored frequency jumps
between tone-pairs could spectrographically resemble frequency jumps resulting
from nonlinear dynamics; however, these large steps in frequency
(500–4500 Hz) were always produced bilaterally, by alternating
phonation between the two sides of the syrinx, rather than unilaterally
(Zollinger and Suthers,
2004).
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0).
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Physiology and production of subharmonics
The occurrence of subharmonics in mockingbird song did not correlate with
predictable changes in rates of bronchial airflow or pressure
(Fig. 4B). Rates of airflow
were not significantly different, either in their mean or variance, just prior
to the onset of subharmonics, from these values 5 ms after onset or 25 ms
prior to onset, (25 ms prior, mean 0.33±0.929 s.d., variance 0.86; 5 ms
prior, mean 0.79±1.287 s.d., variance 1.66; 5 ms post, mean
0.41±0.736 s.d., variance 0.54). Differences between groups were not
significant (one-way ANOVA, d.f.=2, SS=2.74, MS=1.37, F=1.34,
P=0.268). Airflow could either increase or decrease and the magnitude
of these changes varied. Whereas many of the instances of subharmonics
coincided with an increasing rate of airflow (43.5% of cases), subharmonics
also occurred during periods of decreasing or constant flow rates (30.4% and
26.1% of cases, respectively).
Biphonation and two-voice phenomena
Occurrences of biphonation and two-voice phenomena
The simultaneous presence of two or more independent frequencies was very
common in the acoustic signals of these mockingbirds (68.0% of all syllables;
individually: m108, 69.6%; m123, 62.1%; m130, 94.4%; m152, 45.8%). Sounds
containing two independent frequencies were often produced during bilateral
vocalization indicated by simultaneous airflow through both sides of the
syrinx (63.7% of total syllables, 93.7% of sounds with 
2 independent
frequencies), and therefore meet the traditional definition of two-voice
phenomena. When a single f0 with sidebands was observed
concurrent with bilateral airflow, we did not count these as NLP since the
contribution of the two voices to the sound was not clear
(Table 2, SB-2VC column).
Mockingbirds also produced biphonic sounds, i.e. two harmonically unrelated
sounds using one side of the syrinx, the other side being closed (4.3% of
total syllables, 6.3% of sounds with 2 independent frequencies). We found
unilateral biphonation of both types illustrated in the synthesized examples
(Fig. 1A,B). Examples of `type
A' biphonation (Fig. 6) were
less common than `type B' biphonation (Fig.
7, arrow a), but both were observed in mockingbird
vocalizations.
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Since oscines have two theoretically independent sound sources (a pair of vibratory tissues within each side of the syrinx) we looked for examples of two simultaneous biphonic sounds, or `dual biphonation' such as illustrated in Fig. 1C,D. Mockingbirds did produce dual biphonation, or two-voice syllables in which each `voice' was biphonic (Fig. 7, arrow b and Fig. 8). Type B `dual biphonation' (e.g. each side producing a different biphonic sound, each consisting of a fundamental frequency and an independent modulating frequency) represented between 0.8 and 15.1% of syllables examined per bird (7.1±6.35%, mean ± s.d.). Interestingly, in every case of bilateral biphonation, the modulating frequency (m0) of the two voices was the same for both right- and left-produced carrier frequencies (i.e. voices), even when m0 was itself frequency modulated. We did not find any examples of simultaneous bilateral production of type A biphonation.
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Physiology and production of biphonation and two-voice phenomena
Examples of type A biphonation produced with airflow through only a single
side of the syrinx are shown in Fig.
6, arrows a and b. A power spectrum of the sound at arrow b shows
the first fundamental frequency (f0) at 946 Hz and a
second fundamental frequency (g0) at 1505 Hz. Second
harmonics of f0 and g0 are visible at
1892 Hz and 3010 Hz, respectively. Other peaks correspond to linear
combination products of f0 and g0, as
labelled. At arrow a, the lower frequency (f0) is 990 Hz,
and the higher frequency is 1505 Hz.
An example of type B unilateral biphonation is shown in Fig. 7 (first syllable). Across our sample, the modulating frequencies (m0) in type B biphonation ranged from 57 to 540Hz. For type B unilateral biphonation, the spacing of the sidebands in the frequency domain corresponds to the rate of AM in the sound waveform. Examination of the waveform during the first syllable (top trace, Fig. 7B) shows the period of the AM pattern is approximately 11.5 ms, and sidebands 115 Hz above and below f0 in a power spectrum (Fig. 7C).
Examples of two-voice biphonation are shown in Fig. 7 (second syllable) and Fig. 8. At the start of the second syllable in Fig. 7 the bird opens both sides of the syrinx to produce a two-voice syllable in which each side generates independent fundamental frequencies, and both fundamentals (f0 and g0) are flanked by sidebands. In this second syllable, the sidebands are equal distance from both f0 and g0, and the modulating frequency (m0) is the same for both. Comparing 35 ms segments from the center of each syllable in the pair (Fig. 7B), a 115 Hz modulation pattern is apparent in both. However, compared with the waveform of the unilaterally produced syllable (Fig. 7B, top trace), addition of a second fundamental (g0), and airflow through the second side of the syrinx, results in an additional AM pattern on the sound waveform of 550 Hz (Fig. 7B, bottom trace). This 550 Hz modulation during the two-voice syllable is likely the result of beating (sinusoidal oscillations in amplitude resulting from the linear interaction of two similar frequencies). The observed frequency of 550 Hz amplitude modulation is equal to the difference in frequency of g0–f0 (2695–2145 Hz in Fig. 7).
In another example of two-voice biphonation (Fig. 8), the two carrier frequencies (f0 and g0; representing the left and right voice, respectively) are frequency modulated (FM) in opposite directions. During the first 50 ms of the syllable in Fig. 8A, both the right and left sides of the syrinx are open and the bird sings two converging FM sounds, each with sidebands. Unlike the second syllable in Fig. 7, the two-voice biphonation during the first part of the syllable in Fig. 8 does not result in the appearance of a pronounced beating pattern in the waveform. However, in all cases of two-voice biphonation, m0 was always the same on the two sides of the syrinx, even if the FM pattern of f0 and g0 were opposite (upsweeping or downsweeping, respectively). The source of m0 in mockingbirds is not known.
Deterministic chaos
Occurrences of deterministic chaos
Syllables containing apparent deterministic chaos were present in 8.3% of
syllables (individually, m108, 6.3%; m123, 5.0%; m130, 6.7%, m152; 15.3%).
Chaotic sounds occurred in vocalizations accompanied by unilateral airflow
(Fig. 5) as well as those
produced during bilateral airflow (Fig.
9). Most examples of chaos in the repertoires of these birds were
produced with bilateral syringeal airflow (m108, 2.9%; m123, 4.5%; m130, 5.9%;
m152, 13.2% of syllables sampled), however, examples of unilaterally-produced
aperiodic sounds were also present (1.7% of all syllables sampled for all
birds. Individually: m108, 3.4%; m123, 0.5%; m130, 0.8%; m152, 2.1% of
syllables sampled). In each case, the apparent chaos took the form of
broadband noise with a sudden onset. Chaotic segments were sometimes preceded
by or followed by subharmonics (Fig.
5), and harmonic windows within the `noisy' segment (e.g.
Fig. 9A, arrow b) were commonly
observed.
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). During a singing bout mockingbirds may
include several repetitions of loud and soft hews and chat calls in addition
to the mimicked syllables learned from tutors. Loud hew calls are broadband
sounds with an abrupt onset and offset, and a duration of 214–600 ms
(mean=359.7±110.03 ms, N=61). Loud hew calls were always
produced bilaterally, but quiet hew calls were typically produced
unilaterally. Soft hews are not only quieter than loud hews, but are more
restricted in bandwidth. Chat calls are short (ranging between 34–88 ms,
mean=56.3±17.37 ms, N=30) broadband explosive sounds, produced
bilaterally.
All four of the birds in this study included `loud hew' calls in their song repertoires. We examined the rate of airflow and sound recorded in each bronchus for 67 loud hew calls from the four birds in this study (to increase sample size, we used an additional 50 loud hews that were not in the 4000 syllables used for NLP count). Although always produced with airflow through both sides of the syrinx, the chaotic nature of the hew calls often appeared to be the result of chaotic oscillations from only a single side of the syrinx. Fig. 9 shows the contribution to sound from the right and left sides during hew calls produced by mockingbird m130, as recorded in the right and left bronchus by the thermistors. The frequency response of the thermistors rolls off at about 3 or 4 kHz, so it is not possible to completely rule out a chaotic contribution at higher frequencies on the left side. However, the presence of rapid fluctuations in the air flow rate through the right side (FR in Fig. 9A,B) and their absence in the flow rate on the left side (FL in Fig. 9A,B) suggests that the two sides are behaving differently when producing these chaotic sounds. In most hew calls (51 of 67) the right side alone appeared responsible for most of the aperiodicity, while the left side's contribution was more tonal. In these 51 cases, the rate of airflow in the right side shows an aperiodic, rapid modulation, which is not present in the flow on the left. In 5 of 67 calls, the left side appeared responsible for most of aperiodicity, and a strong aperiodic fluctuation in left flow rate throughout the duration of the call, while the flow rates on the right side were more constant. In 11 of 67 calls, the two sides appeared to contribute equally, or the relative contribution of the right and left sides could not be determined from the bronchial flow signals.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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), and NLP
have been identified in the natural vocalizations of intact birds with only a
single sound source (e.g. a tracheal syrinx), such as parrots and doves
(Beckers et al., 2003;
Fletcher, 2000;
Lavenex, 1999). But in
songbirds, the presence of the `two voices' makes it difficult to identify
some kinds of NLP on the basis of vocalizations alone. By recording the
respiratory dynamics of vocalization on each side of the syrinx of intact,
singing mockingbirds, we found unilaterally produced NLP in about 8% of all
syllables. This represents only about one-sixth of the sounds containing
apparent biphonation, chaos, frequency jumps or subharmonics based on
spectrographic analysis alone (48.7%). The relatively small ratio of NLP to
harmonic sounds in our sample suggests that while the exploitation of the
passive biomechanical properties of the syrinx is a possible strategy for
production of complex sounds, mockingbirds rely primarily on their `two
voices' for the rich diversity of complex sounds in their repertoires.
Two-voice complexity may be easier to control than NLP and the availability of
two sound sources might reduce the need for birds to rely on NLP, which are
potentially less predictable, to increase vocal diversity. Nonetheless, our
analysis of the peripheral vocal and respiratory dynamics associated with NLP
provides insights into how songbirds might exploit the properties of each of
its two sound sources, alone or in combination, to produce or avoid complex
sounds. For example, a songbird might produce biphonation simultaneously with
both `voices' resulting in sounds with up to four unrelated frequencies, such
as those described by Thorpe (Thorpe,
1961).
We found unilateral biphonation of two types in mockingbird song: as two
harmonically unrelated fundamental frequencies, each independently modulated
(Fig. 6), and as one
f0 modulated by a second, lower frequency, appearing as
sidebands parallel to the f0 in a narrowband spectrogram
(Fig. 7). It is important to
note that while sidebands indicate the occurrence of two independent
frequencies, there are several ways in which they may be produced. In
biphonation, sidebands result from one f0 modulated by a
second, lower frequency (Greenewalt,
1968; Lavenex,
1999). Experiments with an excised larynx and computer modelling
have shown that the mammalian vocal folds, vibrating asymmetrically, can
produce AM with accompanying sidebands that are the result of linear
combinations of the two fundamentals (e.g.
2g0–f0,
2f0–g0)
(Giovanni et al., 1999;
Herzel et al., 1995;
Mergell and Herzel, 1997;
Neubauer et al., 2001). In
such cases, the two vocal folds oscillate at slightly different frequencies,
each producing a separate sound pressure wave that is close to the other in
fundamental frequency. If the same phenomenon can occur during oscillation of
the medial and lateral labia in songbirds, biphonic vocalizations might be the
result of either a higher f0 with a lower modulating
frequency (e.g. Fig. 1B), or
the interaction of two higher tones, which are close in fundamental frequency
(Fig. 1A). In either case,
neither unilateral biphonation nor dual (two-voice) biphonation, together with
their syringeal motor correlates, has been previously described in intact
songbirds.
Production and control of nonlinear phenomena
We hypothesize that although production of NLP is a passive biomechanical
process, birds may sometimes exert voluntary control over the conditions under
which it occurs. However, in other cases NLP might be `unintentional,'
resulting from instabilities of the vocal system. The occurrence of NLP in
mammalian vocalizations increases as sound level and frequency increase,
suggesting it may be produced by driving the vocal system to its performance
limit (Riede et al., 2007) and
past threshold points that mark boundaries between stable vibratory modes.
In a zebra finch excised syrinx preparation, it was demonstrated that a
linear increase in subsyringeal pressure results in bifurcations between
different vibratory modes (Fee et al.,
1998). The absence of a consistent relationship between the
occurrence of NLP and a detectable increase in rates of bronchial air flow,
subsyringeal air sac pressure, or f0 in our mockingbirds
may reflect the availability of respiratory, syringeal and upper vocal tract
neuromuscular control in our live birds. Although we did not observe a
consistent pattern in the direction or rate of bronchial airflow or in
subsyringeal pressure associated with the occurrence of NLP, the fact that
frequency jumps were significantly (but not always) correlated with increased
variability in the rate of airflow is consistent with the hypothesis that at
least some NLP reflects a failure in vocal motor control. Nonlinear theory
suggests that even very small changes in control parameters such as subglottal
pressure can result in production of NLP. There are many potential control
parameters that we did not measure, such as syringeal resistance, the tension
of the oscillating labia or the pressure and flow profiles across their
surface.
Source–source and source–tract interactions
We found several cases of airflow through both sides of the syrinx
generating three independent frequencies (f0,
g0 and m0). Nowicki and Capranica
(Nowicki and Capranica, 1986)
reported evidence for a source–vocal tract coupling in the
amplitude-modulated calls of black-capped chickadees (Parus
atricapillus), and speculated on possible source–source (acoustic
or mechanical) coupling. Our observation that in each case of bilateral
biphonation the frequency of the amplitude modulation (m0)
was the same for both the left- and right-produced fundamentals supports their
hypothesis of source–source coupling in the oscine syrinx.
Possible mechanisms of source–filter and source–source
interactions were investigated recently using computational models
(Laje and Mindlin, 2005;
Laje et al., 2008), which
demonstrate that such interactions could indeed produce the complex,
multi-frequency sounds observed in birdsong. Laje and Mindlin's results are
relevant to our observations, because they demonstrate how sounds, such as
subharmonics, previously presumed to be NLP in intact songbirds such as zebra
finches (e.g. Fee et al.,
1998), could alternatively be the result of acoustic interactions
between the two sides. In addition, Nelson
(Nelson, 2004) describes how
rapid FM within a song element in eastern towhees can produce an AM-like
sideband pattern in narrowband spectrograms, and further speculated on an
as-yet-unidentified third independent modulator in the syrinx, but further
evidence for the identity or existence of such a structure is lacking.
These simulations and models demonstrate that crosstalk between a
fundamental frequency and resonance frequencies may affect the vibration of
the source. The likelihood of an interaction of sound source and vocal tract
filter increases if vocal tract impedance is adjusted to match the impedance
of the source (Titze, 2008). A
highly variable vocal tract system with complex motor patterns has been
demonstrated in songbirds (Fletcher et
al., 2006; Riede et al.,
2006), and thus one may expect that songbirds, like humans, have a
variety of vocal `tools' at their disposal to avoid or minimize the occurrence
of involuntary NLP during song.
Deterministic chaos in calls and song
Periods of deterministic chaos can theoretically occur in any system of
coupled oscillators, such as the paired labia within each side of a songbird
syrinx. Whereas chaos may or may not be a common feature of learned song, the
unlearned calls of many songbirds, such as alarm calls, contact calls and
aggressive calls, are often characterized by broadband, noisy, `buzzy' or
`harsh' sounds (Marler,
2004).
Although our data show that mockingbirds may have some control over the
respiratory and syringeal parameters necessary to allow the production of
chaotic sounds, as evidenced by the chaotic nature of three very common call
types, chaotic vibratory modes are also presumably induced involuntarily at
times. Broadband, aperiodic sounds were found within a small number of
otherwise pure-tonal song elements. These erratic occurrences of chaos may be
more akin to those described in the mammalian literature, which are often
attributed to pathologies (Herzel et al.,
1994; Mende et al.,
1990), instabilities in the vocal system
(Mergell et al., 2000),
increasing or maximizing frequency or amplitude levels
(Berry, 2001;
Brown et al., 2003;
Riede et al., 2007), or abrupt
desynchronization of the vibrating labia
(Neubauer et al., 2001).
Instances of chaotic sounds within more tonal vocalizations were likely
involuntary, as they rarely occurred more than once in the same syllable type
from the same bird.
Possible communicative roles of nonlinear phenomena
Several communicative functions of NLP have been hypothesized. For
instance, it has been suggested that increased vocal `roughness' might be an
honest indicator of poor reproductive fitness
(Goller, 1998) or health
status (Herzel et al., 1994;
Riede et al., 1997). A
preference for pure-tonal over harmonic or aperiodic vocalizations has been
shown for some songbirds (Strote and
Nowicki, 1996). An alternative, seemingly contradictory,
hypothesis suggests that animals might exploit the nonlinear properties of
their vocal systems to increase vocal complexity, and that NLP could aid in
individual recognition in some species
(Fee et al., 1998;
Fitch et al., 2002;
Volodina et al., 2006;
Wilden et al., 1998).
Additionally, NLP may function to increase the auditory impact of calls
(Owren, 2003;
Owren and Rendall, 2001), and
so could be useful both for attracting allies or mates, as well as for
signalling status or physical condition. While it is still not clear what, if
any, adaptive advantages or selective pressures are associated with NLP in
animal vocalizations, the literature is becoming increasingly rich with
examples of these phenomena in an ever-widening range of taxa. The extent to
which birds use nonlinear phenomena as salient features in vocal communication
varies significantly between species. Species differences in the inclusion of
NLP in their vocal signals may reflect the need, in part, to achieve an
appropriate balance between syllable stereotypy and syllable diversity.
LIST OF ABBREVIATIONS
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2=0.8; 5–0 ms prior, 
