Respiratory patterns and oxygen consumption in singing zebra finches
Department of Biology, University of Utah, Salt Lake City, UT 84112, USA
* Author for correspondence (e-mail: goller{at}biology.utah.edu)
Accepted 5 December 2002
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Summary |
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Key words: song, bird, respiration, metabolic cost, zebra finch, oxygen consumption, Taeniopygia guttata
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Introduction |
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This direct cost can be estimated by assessing changes in metabolic rate
associated with vocal behaviour. To date, the metabolic cost of song
production in passerine birds has been investigated in four species. The
estimated increase in oxygen consumption during song, relative to resting
metabolic rate (RMR), was 1.77-3.44-fold in zebra finches, canaries
(Serinus canaria) and European starlings (Sturnus vulgaris)
(Oberweger and Goller, 2001)
but reached 9-fold in Carolina wrens (Thryothorus ludovicianus;
Eberhardt, 1994
). However, the
wide range found in different species is more likely to reflect methodological
difficulties in studying song in a respirometry chamber than actual
differences in the metabolic cost of song production
(Eberhardt, 1996
;
Gaunt et al., 1996
;
Oberweger and Goller,
2001
).
Aside from the metabolic cost of singing, gas exchange is also of interest
because respiratory patterns during song are very different from the rhythmic
pattern of quiet breathing (e.g. Suthers
and Goller, 1998). Typically, song is generated during expiration,
and the airflow is driven by increased expiratory pressure. The duration of
individual expiratory pulses may vary greatly within a song. Inspirations
taken in between expiratory pulses are typically of short duration, and
inspiratory pressure exceeds that during quiet respiration to enable short but
deep inhalations. Thus, both the rhythm and intensity of respiratory movements
are drastically altered for song production. Many aspects of gas exchange
during the respiratory pattern of song are unexplored. Gas exchange may,
however, play an important role in song organization. For example, respiratory
needs may dictate the duration of syllables, syllable sequence and the
temporal pattern of sound and silent intervals (e.g.
Hartley and Suthers, 1989
;
Suthers and Goller, 1998
).
Such a role would, therefore, put physiological constraints on how sexual
selection can influence the evolution of the temporal pattern of song (e.g.
Podos, 1996
).
Zebra finch song is characterized acoustically by a variable number of
short-duration introductory notes and a stereotyped sequence of distinct
syllables (motif; Zann, 1996).
Males often repeat motifs to form a song bout. The acoustic sequence
corresponds to a distinct respiratory pattern
(Fig. 1). Most syllables are
generated during an expiratory pressure pulse, but a few high-frequency
syllables may also be generated during inspiration
(Goller and Daley, 2001
;
Franz and Goller, 2002
). The
pattern of respiratory pressure is characteristic for each syllable of the
motif. The song motif consists of an alternating sequence of stereotyped
expiratory and equally stereotyped inspiratory pressure pulses (minibreaths;
Wild et al., 1998
).
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To further investigate the metabolic cost of singing and the effect of song
motor patterns on gas exchange, a method is required that allows a higher
temporal resolution of oxygen consumption and avoids other problems of
assessing metabolism in respirometer chambers
(Oberweger and Goller, 2001).
To circumvent the problems with a respirometer chamber, we used a breathing
mask system. The results confirm earlier estimates of the direct metabolic
cost of singing but also explore how the respiratory patterns of song affect
gas exchange.
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Materials and methods |
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Air sac pressure recording
After a male was removed from the aviary and placed in an individual cage,
an elastic belt with a Velcro tab on the back was placed around the thorax. A
leash was attached to the Velcro and led through the top of the cage. It was
connected to a tether arm, which was counterbalanced to support the additional
mass from the backpack (2.5-3 g after transducers were attached; see below),
allowing free lateral and vertical movement in the cage. Birds were also able
to rotate freely but were limited to 2-3 full rotations in the same direction
while data were recorded. Typically, singing resumed 1-3 days after males were
placed on the tether system.
Surgery was performed once singing resumed. Birds were deprived of food and water for 1 h before surgery. Using isoflourane anaesthetic, a small hole was made in the abdominal wall into the left posterior thoracic air sac, and the tip of a flexible cannula (Silastic tubing; 1.65 mm o.d., 6 cm length) was inserted into this hole. The cannula was sutured to the rib cage. The cannula insertion site was sealed with tissue adhesive (Nexaband) to prevent leakage of air. The free end of the tube was connected to a piezoresistive pressure transducer (FPM-02PG; Fujikura, Tokyo, Japan), which was mounted on the Velcro tab.
Oxygen measurements
Oxygen consumption was measured using a custom-made mask system. Each bird
was fitted with a head net (Fig.
2) made from elastic thread (approximately 1 mm diameter) several
days before surgery. The head net was fitted to the specific dimensions of
each individual bird, such that an elastic ring was situated at the base of
the beak and the other segments provided a tight enough fit to prevent
movement. A 1 cm-long piece of polyethylene tubing (1.57 mm o.d., 1.14 mm
i.d.) was sewn to the top of the head net to serve as an air outlet, and a 2
cm-long piece at the bottom of the net served as an air inlet.
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The elastic beak ring served as an anchor for a rigid plastic ring (1.2 cm
diameter), around which the mask, made of balloon material, was stretched.
Mask volume was approximately 1 ml. The plastic ring was attached to the
elastic beak ring of the head net using dental impression medium (Reprosil,
hydrophilic vinyl polysiloxane impression material, Type I, very high
viscosity), forming a seal around the beak against the face. The ring was
large enough that the bird could open and close its beak freely and beak
movements during singing were not impeded. The mask outlet tube was connected
to Silastic tubing (0.76 mm i.d., 1.65 mm o.d.), which was guided over the top
of the head to the backpack and from there up the length of the leash. A
second set of identical tubing was run from the backpack to the `reference'
channel of the oxygen analyzer (see below). For both channels, tubing from the
bird was run through a small chamber filled with desiccant (Drierite) and
CO2 absorbent (Ascarite). From there, tygon tubing (10 cm) led to
the oxygen analyzer through a partially inflated condom to buffer small
fluctuations in pumping pressure (Ellington
et al., 1990). All tubing was kept as short as possible to
optimize the temporal resolution of the system.
A flow control unit (R-2; Applied Electrochemistry, Pittsburgh, PA, USA) was used to pull air through the analyzer. The percentage difference in oxygen content between the air of the two channels was measured with an Applied Electrochemistry S-3A/2 oxygen analyzer (N 37M sensor). All oxygen measurements were taken at room temperature (21-23°C). The sensor was calibrated with room air (20.95% oxygen) before each recording session. The flow rate was kept at 860 ml min-1. Once the sensor reading had stabilized at zero, the analyzer was connected to the mask on a bird. Recording started after an adjustment period of 15-20 min and lasted for up to 2 h. All birds were observed throughout the recording period, and information about their locomotor activity was noted for each song bout.
Testing the mask system
Our system for measuring oxygen consumption was tested for several possible
sources of error: (1) leakage of air at the mask attachment site, (2) pressure
conditions inside the mask during breathing and (3) the possibility of partial
re-breathing of exhaled air. To test for the occurrence of the first two
potential sources of error, we attached a piezoresistive pressure transducer
via a T-connector to the inlet tube. The pressure conditions inside
the mask were slightly subatmospheric during both respiratory phases. This
indicates that there were no leaks in the mask system. At the same time, it
confirms that breathing activity does not affect the pressure inside the mask
to the extent that flow reversals occurred during either respiratory
phase.
We used tracheal flow measurements (see below) to determine the volume of air that was exchanged during quiet breathing and song syllables. Extrapolating from the highest flow rate during song, we estimate the exchanged volume to be maximally 180 ml min-1 (data from three birds). Because the flow rate through the mask system was 860 ml min-1 and the volume of the mask was 1 ml, the air in the mask was sufficiently replenished to prevent re-breathing of exhaled air by the bird.
Data recording
Song was recorded with a microphone (AT8356; Audiotechnica, Stow, OH, USA)
placed in front of the cage. The microphone output was amplified (100x;
Brownlee 410, San Jose, CA, USA). The analogue output voltage from the oxygen
analyzer (percentage difference between the two air channels) was recorded
simultaneously with song and the voltage output of the pressure transducer
using a multi-channel digital recorder (135T; TEAC, Tokyo, Japan). All signals
were recorded with a 24 kHz digitization rate.
Oxygen analysis
Air sac pressure and oxygen signals were digitized (sample rate = 5 kHz)
for analysis using SIGNAL 3.1 (Engineering Design, Belmont, MA, USA) software
and a DT-2821 AD board (Data Translation, Marlboro, MA, USA). Recorded oxygen
values were corrected for standard conditions. The following equation for a
mask system (Withers, 1977)
was used to calculate the volumes of consumed oxygen (ml min-1):
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Oxygen consumption during song was related to pre-song activity. However, baseline oxygen consumption was difficult to determine in some cases. Movement, as well as respiratory changes due to excitement caused by presentation of the female, led to increases in oxygen consumption similar in magnitude to those found for song (Fig. 3). In these cases, the segment of the oxygen trace that corresponded to the song bout could not be identified unambiguously. Oxygen baseline determinations were therefore made only for those recordings that had a stable period within 5-10 s before song. For an individual song bout, the volume of consumed oxygen (song O2-volume) was determined by integrating the corresponding segment of the oxygen consumption trace above pre-song baseline. This O2-volume was then divided by body mass to calculate the mass-specific O2-volume.
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There was a delay between the occurrence of respiratory events and the time that they were registered by the oxygen analyzer. This delay was determined for each bird and each recording session using defecation events. Defecation causes distinct pressurization in the air sacs but the airways are simultaneously closed, preventing exhalation (Fig. 3; airflow data not displayed). This interruption of normal breathing (500-900 ms) causes a sharp decrease in O2 consumption. The time from the peak in air sac pressure to the lowest point in the oxygen trace was used to determine the time delay between the pressure and oxygen recordings.
The total duration of the song bout was measured using the air sac pressure recordings because the mask system made acoustic measurements variable in quality. Song duration was calculated by subtracting the inter-song intervals from the total bout length. The relationship between oxygen consumption and the respiratory pattern was investigated by determining the respiratory volume and duration of each expiration and inspiration. Segments of quiet respiration for each recording were used to determine the ambient pressure level, which marks the switching points between respiratory phases. Points where the pressure trace crossed the zero line were used to determine the duration of each phase. Respiratory volume of expirations and inspirations was calculated by integrating each area above and beneath the ambient pressure line, respectively. After a translation along the time axis (rotation function in SIGNAL) of the oxygen trace to correct for the time delay, a corresponding average oxygen consumption level was determined for each segment in the pressure trace for comparison.
Tracheal flow measurements
In three male zebra finches, tracheal airflow was measured simultaneously
with air sac pressure. Flow was monitored with a microbead thermistor
(BB05JA202, Thermometrics, Edison, NJ, USA), which was surgically implanted
into the lumen of the base of the trachea (more detailed descriptions of the
procedures are presented in Hartley and
Suthers, 1989; Suthers et al.,
1994
). A feedback circuit (Hector Engineering, Ellettsville, IN,
USA) supplied current to heat the thermistor to a constant temperature
(approximately 60°C). The voltage needed to maintain this temperature was
proportional to the airflow past the thermistor bead. After song was recorded,
birds were euthanized and air was supplied with a known flow rate through the
air sac cannula to calibrate the non-linear voltage output of the thermistor.
With this technique, calibrations were only obtained for expiratory airflow.
Airflow data were linearized with calibration values to calculate approximate
volumes of air for single expiratory pulses during quiet respiration and song.
Absolute values are only an approximation, because during calibration the
possibility of slight positioning differences of the bead compared with the
position during song cannot be excluded.
All experimental procedures were approved by the Institutional Animal Care and Use Committee of the University of Utah.
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Results |
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Oxygen consumption during song
Song was accompanied by characteristic profiles in oxygen consumption. At
the beginning of song, oxygen consumption initially decreased relative to
pre-song levels. During song, there was a consistent increase followed by a
post-song decrease in O2 consumption. When longer bouts were sung,
the oxygen trace showed motif-by-motif oscillations
(Fig. 5). However, oxygen
consumption decreased from the first motif to later motifs of the bout. During
long bouts, the decline in the oxygen peak associated with each motif levelled
off towards the end of the bout. Sometimes the distinct peak during song was
masked by other activities, such as movements shortly before or during song.
Because it was impossible to determine how much such activity contributed to
the oxygen consumption during song, these song bouts were not used for
analysis.
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Metabolic cost of singing
We measured the cost of song using different analysis techniques for
comparative purposes. Measurements of the volume of oxygen consumed in excess
of the pre-song baseline level (song O2-volume) yielded a mean cost
of singing of 85.7 µl O2 g-1 min-1
(Table 1). Song
O2-volumes increased with increasing song duration
(Fig. 6A). The slope of this
relationship indicates a decreasing cost of singing with increasing song
duration. However, this trend can be attributed to the observation that oxygen
consumption was highest for the first motif and then slowly decreased to a
constant level for subsequent motifs (Fig.
5). The initial high level for the first motif is related to the
decrease in oxygen consumption before the song (see below).
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Interindividual differences in song O2-volume per motif can be largely explained by motif duration. The average song O2-volume per song motif increased with motif duration (Fig. 6B) for the six individuals. Song duration measurements do not include the variable number of introductory notes.
Metabolic cost was also measured as mean oxygen consumption during song
(Table 1). Song
O2 depended
strongly on pre-song
O2
(Fig. 6C), which varied
substantially between different song bouts within and among individuals
(Table 1; Fig. 6C). If the difference
between song
O2
and pre-song
O2
is calculated to estimate the metabolic cost of song, values are consistently
lower than those resulting from the data on song O2-volume. This
difference can be largely explained by the longer duration of the oxygen peak,
which is used to calculate mean
O2, compared
with song duration, which enters the calculation of song O2-volume
rate (Table 1).
Respiratory patterns of song
Song was elicited by presenting a female to the male in a separate cage.
Presentation of the female typically resulted in an increase of respiration
and oxygen consumption 5-20 s before the song bout occurred (Figs
3,
4). This increase in
O2 could be
greater than 2-fold and was accompanied by faster respiratory rate and deeper
breaths. The increase prior to song was shorter and of smaller amplitude when
the cage with the female was sitting in front of the male's cage for a longer
period of time.
A song bout was consistently accompanied by a short, but marked, decrease
in O2 shortly
before the peak. In four of the birds, the decrease before song coincided with
the introductory notes of the first motif. However, no significant correlation
was found between the number and duration of introductory note series and the
decrease in
O2.
In the other two birds (R31 and B1), the decrease in
O2 began before
the introductory notes. For these birds, a change in quiet respiration before
song corresponded to the decrease in
O2. The
amplitude of respiratory pressure decreased and respiratory rate declined,
resulting in lower values of calculated respiratory activity
(Fig. 4). Although these values
do not take possible changes in syringeal resistance into consideration,
tracheal airflow data in other individuals show that no marked changes in
syringeal resistance are noticeable a few seconds before song is
initiated.
This decrease in
O2 shortly
before song probably contributes to the metabolic peak that is associated with
the first motif.
O2 decreases
slightly with each motif until a constant level is reached after 4-5 motifs
(e.g. Fig. 5). Individual
motifs can be clearly distinguished in most birds by small fluctuations in
O2 throughout
the bout. This indicates that the release of expired air during the song motif
varies or that O2-content of expired gas is not constant.
To address this issue, we estimated volumes of exchanged air during quiet respiration and song. Typically, the volume of air exchanged during introductory notes and short syllables of the motif was lower than or equal to that during quiet respiration. The volume of long syllables of the motif was substantially higher than during quiet respiration in two of the birds and not much higher in one individual (Table 2). This indicates that there is individual variability in air exchange during the song motif and that the volume of air exchanged during different syllables of the motif may be quite variable.
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At the end of the song bout, a marked decrease in
O2 occurred
consistently. This decrease below the pre-song baseline level lasted from 0.5
s to several seconds and varied from a few µl of O2 to several
ml. In some instances, oxygen consumption was reduced to zero
(Fig. 7A). The decrease in
O2 coincided
with a decrease in respiratory activity (Figs
4,
5,
7), which ranged from a reduced
rate and amplitude to complete apnea (Fig.
7A,B). The reduction in respiratory activity after song bouts
predicted the reduction in
O2
(Fig. 8) but varied among
individuals. Within individuals, the duration of apnea was generally
positively correlated to song duration. In the three individuals, regression
coefficients were significant (r=0.71-0.97, P=0.021-0.026),
and in two individuals there was a positive but non-significant trend.
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Of the three males in which tracheal flow was recorded, one (R44) showed no marked changes in respiration after song, whereas two (R42 and R35) showed a pronounced decline. Airflow during the song motif was not much higher than that during quiet respiration for R44 and was substantially higher in the other two individuals (Table 2), suggesting that the volume of air exchanged during the song motif is related to the amount of reduction in respiration.
This pronounced reduction in post-song respiratory activity was followed by
a subsequent increase in respiration and
O2 in comparison
with pre-song levels. It was difficult to measure the exact volume of the
increase because it declined gradually to new levels and was often masked by
post-song locomotor activity. It appears, however, that the increase
correlated with the duration and amplitude of the post-song reduction in
respiration and
O2.
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Discussion |
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Metabolic cost of singing
The metabolic cost of avian vocalization has been studied in some detail
(e.g. Horn et al., 1995;
McCarty, 1996
;
Jurisevic et al., 1999
;
Bachmann and Chappell, 1998
;
Chappell et al., 1995
). Song
production in songbirds has received less experimental attention
(Eberhardt, 1994
;
Oberweger and Goller, 2001
)
but has been subject to extensive discussion
(Gaunt et al., 1996
;
Eberhardt, 1996
). While
metabolic rate during song was found to be high in Carolina wrens (maximum
increase was up to 9-fold over resting metabolic rate;
Eberhardt, 1994
), oxygen
consumption of three other species increased much less during song
(1.77-3.41-fold over RMR; Oberweger and
Goller, 2001
). Oberweger and Goller suggest that this discrepancy
might be attributable to differences in how the energetic cost of song was
assessed. The present study confirms that reporting the metabolic cost of song
as an increase over basal metabolic rate (BMR) or RMR can be misleading. In
male zebra finches, mean song
O2 varies
substantially within and among individuals, but this variation can be largely
explained by variations in pre-song
O2
(Fig. 6C). Overall, the range
of pre-song
O2
values (approximately 0.03-0.26 ml g-1 min-1) is at
least 4-fold greater than the mean difference between song
O2 and pre-song
O2
(approximately 0.05 ml g-1 min-1), which results in
erroneous estimates of the cost of singing by calculating a factorial increase
(song
O2/RMR).
Average
O2
measurements during song are, therefore, not a reliable estimate of the cost
of song production in zebra finches (the present study). A similar conclusion
was reached for other species (Oberweger
and Goller, 2001
) and might explain the unusually high estimates
of song metabolic rate in wild-caught Carolina wrens
(Eberhardt, 1994
).
Song O2-volume is used here to estimate the cost of singing
relative to that of pre-song metabolism. Data obtained with the mask system
can be compared with the same estimates made from oxygen consumption
measurements in a respirometer chamber. Oberweger and Goller
(2001) induced singing in male
zebra finches by presenting a female in front of a small transparent window in
the opaque chamber. Males perched near this window and sang directly into the
air outlet of the respirometer chamber. Estimates for the cost of singing over
pre-song levels obtained with this method (1.2-1.36-fold increase) are close
to those for the mask system (1.23-1.5-fold increase for five birds; 2.35-fold
increase for B8). Although there is a good agreement overall, the
interindividual differences again illustrate the limitations of reporting cost
as a factorial increase. Variation in pre-song metabolic rate can explain a
large degree of variability in the factorial increase for song
(Fig. 9).
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Our measurements also allow comparison between the volumetric measurements
(song O2-volume) and mean song
O2 data. The
volumetric data indicate, on average, a 1.369-fold higher cost of singing if
calculated as a rate (i.e. per unit time;
Table 1). The main reason for
this discrepancy is the fact that the duration of increased oxygen consumption
during the song bout is somewhat greater (200-900 ms) than the duration of the
song bout itself. Because the former is used in the calculation of the mean
O2 and the
latter in the song O2-volume, calculations using the mean
O2 values
underestimate the cost of song production
(Table 1). The small difference
between song bout duration and the duration of increased oxygen consumption
can probably be attributed to the washout characteristics of the mask
system.
In conclusion, we suggest that the absolute cost of song production can be
estimated most reliably as the volume of oxygen consumed over pre-song
metabolic rate (Fig. 6A,B).
Oberweger and Goller (2001)
used such estimates for comparisons among different taxa and found these
comparisons to be more meaningful than if factorial increases are used.
However, changes in ventilation patterns before and after song are tightly
linked with the song motor pattern and therefore need to be considered in
assessing the effective cost of singing behaviour in zebra finches (see
below).
Interindividual differences in metabolic cost
The predominant cost of singing presumably reflects muscle activity
generating the fluid dynamic energy (airflow) for sound production. In
addition, muscle activity controlling sound characteristics (syringeal
muscles) and sound modification (upper vocal tract) must also contribute to
the direct cost of singing. These direct costs are accompanied by indirect
costs resulting from postural changes and non-specific song-related movements
(e.g. courtship dance in zebra finches
(Zann, 1996;
Williams, 2001
).
In zebra finches, song is generated by a series of alternating expiratory
and inspiratory pressure pulses. The respiratory rhythm of song differs from
that of quiet respiration by its irregularity and rapid switching events
between the respiratory phases. The amplitude of expiratory and inspiratory
pressure pulses is drastically increased compared with that of quiet
respiration. This increase is effected by increased activity of respiratory
muscles (Wild et al., 1998)
and by increased syringeal resistance, which results from a combination of
passive forces (Bernoulli) and valving action by syringeal muscles
(Goller and Suthers, 1996b
;
Goller and Larsen, 2002
).
Because the coarse respiratory pattern of song is similar among all individuals used in this study, we expect the major direct cost of song production to be similar for our individuals. However, small differences in the acoustic structure of song, air sac pressure patterns and flow rates during phonation exist among individuals, indicating that some interindividual variability in the metabolic cost to produce song may exist. Song O2-volume per motif increased with increasing motif duration (Fig. 6B), confirming that the restructuring of respiratory movements constitutes the major cost of song. Variability in additional costs may be reflected in the limited variation of song O2-volume measurements from this linear relationship with motif duration. However, it is likely that resolving such minor differences reliably may be beyond the power of the currently available techniques and equipment.
Respiratory events and oxygen consumption
Song in zebra finches changes the normal pattern of quiet respiration and,
consequently, gas exchange in complex ways. These changes are not confined to
the motor activity of singing, but consistent alteration of respiration occurs
before and after the song bout. Several seconds before the initiation of song,
respiratory rate and amplitude increase followed by an increase in oxygen
consumption. The increase is more pronounced if a female is presented in a
separate cage to elicit singing but is also present if the cage with the
female is sitting near the male's cage for an extended period of time. This
respiratory change with increased oxygen consumption suggests that a
motivational change takes place up to 20 s before the actual motor action of
singing is initiated. It would be interesting to know whether this
motivational change (arousal; Zann,
1996) is linked to the motor program for song production (e.g.
Margoliash, 1997
;
Wild, 1997
) and how
respiratory changes for both events are coordinated.
Male zebra finches sometimes also sing undirected song, where song is not
directed to a conspecific (Zann,
1996). The above-described motivational changes may not occur
prior to undirected song, which is described as a non-aroused state
(Zann, 1996
). Because our
birds did not sing undirected song during the 2-h periods with the mask, no
direct comparison between the metabolic costs can be made. Heart rate
measurements during song indicate a smaller increase in the pre-song period
for undirected song (M.F. and F.G., unpublished observation), suggesting a
lower motivational state.
Shortly before the song bout, respiratory depth and rate descrease briefly, at least in some individuals, causing a reduced rate of oxygen consumption. Neural mechanisms underlying this change are unknown. In other individuals, the decrease in oxygen consumption also coincided with the train of introductory notes preceding the first song motif. This suggests that the rapid alternating between short expiratory pulses and minibreaths during the series of introductory notes either reduces the time air resides in the lung for gas exchange or the exchanged volume is lower than during quiet respiration, leading to lower oxygen consumption. The differences in the ratio of tracheal airflow before song and during introductory notes for the three males (Table 2) indicate that both possibilities may account for the observed reduction in metabolic rate.
The expiratory pressure pulses of the song motif vary in duration and amplitude, and the volume of exhaled air is also variable. Typically, long syllables occur at the end of the motif. This variability between expiratory pulses of the motif is reflected in the oxygen consumption. Each motif of the bout was distinguishable by a small fluctuation in the oxygen consumption trace, such that the long pressure pulses corresponded to rising oxygen consumption. Although flow rate does not differ systematically between expiratory pulses of short and long duration, a long-duration expiration must result in a greater volume of expired air over a period of time during which a number of short syllables and minibreaths might occur. Consequently, increased oxygen consumption will be registered for this time period, even if flow rates and oxygen extraction at the respiratory surfaces remained the same. The methods of the present study are not sensitive enough to allow determination of oxygen extraction efficiency.
The volume of air exchanged during the motif is likely to influence the subsequent respiratory pattern. The airflow data indicate that the volume of exhaled air during the long pressure pulses of the motif varies among individuals, and those with more marked hyperventilation also show more post-song reduction in respiration. Although the airflow data were collected in other individuals than the ones used for the metabolic measurements, we suggest that the degree of hyperventilation also varies among those individuals, accounting for varying degrees of reduced post-song respiration, ranging from only slightly reduced respiratory depth and rate to complete apnea.
This interpretation is supported by physiological evidence collected in
singing canaries (Hartley and Suthers,
1989). Although infrequent, apnea up to 0.6 s after song was
recorded, while the volumes of expired and inspired air were closely matched
during preceding song. Data extrapolated from the tables using the mean tidal
volumes and the frequency show variable flow rates (up to 3-fold increase over
quiet respiration) for this bird (no. 2) depending on the syllable type. The
variability in flow rate for particular syllables and variability in
repetition rates of each syllable may explain why apnea was found only
infrequently in canaries (Hartley and
Suthers, 1989
).
The amplitude of respiratory movements is probably mediated by
CO2 receptors in the lung (for a review, see
Fedde and Kuhlmann, 1978).
Apnea can be produced in birds by passing air, oxygen or hydrogen over the
lungs. Peterson and Fedde
(1968
) demonstrated in the
chicken (Gallus domesticus) that apnea was caused by lowering the
intrapulmonary CO2 concentration and that CO2 receptors
in the lung have rapid responses to changes in the CO2
concentration. Below a certain CO2 concentration, some receptors
discharge irregularly and may even cease to fire action potentials. Cessation
or experimental interruption of their connections to the brain markedly
decreases respiratory rate (Fedde et al.,
1963
).
The bout of reduced respiration is followed by increased respiratory activity and higher oxygen consumption. Although it is difficult to quantify the duration of the increase, we suggest that it is a consequence of the post-song reduction and not of the song bout itself. Neither reduced respiration nor the following increase was entered into our estimate of the metabolic cost of singing.
In conclusion, singing behaviour in zebra finches includes direct and
indirect costs. Whereas we report the cost of generating the song bout with
some confidence (see above; direct cost), it is more difficult to assess
indirect costs related to motivation and the courtship dance
(Williams, 2001) and various
changes in respiratory patterns before and after song. Because the
experimental situation is likely to have affected the intensity of the
courtship behaviour, we did not measure indirect costs associated with singing
behaviour here. Zebra finches in our setup directed their song to the female
in the adjacent cage but did not perform courtship dances of normal intensity.
The tethering procedure and the mask may have physically impeded males or
altered their motivational state, preventing normal courtship dancing.
Minibreaths and gas exchange
Minibreaths are short, typically silent inspirations in between expiratory
pulses of song. Minibreaths replenish the air expelled during the phonatory
expiration (Hartley and Suthers,
1989; Goller and Daley,
2001
) but it is unclear whether very short minibreaths allow gas
exchange to take place in the lung. In Waterslager canaries, minibreaths can
be as short as 15 ms with an inhaled volume that is less than the tracheal
deadspace (as low as 0.09 ml; Hartley and
Suthers, 1989
). The song organization of zebra finches is
different to that of canaries and can therefore only give limited insight into
this question. The duration of song bouts is typically not as long as song
duration in canaries and does not consist of sustained repetitions of
individual syllable types (phrases). While some minibreaths of zebra finch
song are as short as 15-20 ms, airflow data suggest that the volume exhaled
during short syllables is typically greater than the tracheal deadspace (F.G.,
unpublished data). Oxygen consumption occurred throughout the motif, with
fluctuations during different syllables probably reflecting the volume of
exhaled air per unit time (see above). It is possible that rapid alternating
between expiration and inspiration reduces residence time of inhaled air near
the gas exchange surfaces of the lung, which would result in higher oxygen
content of exhaled air. Although this possibility cannot be excluded, it is
unlikely in zebra finches considering that, during quiet respiration, a
specific volume of inhaled air is not exhaled during the same respiratory
cycle (Bretz and Schmidt-Nielsen,
1972
). However, such a mechanism may be more important in canaries
with long phrases of short syllables produced at high minibreath rates
(Hartley and Suthers, 1989
).
Although song in a respirometer chamber did not cause a measurable oxygen debt
in canaries (Oberweger and Goller,
2001
), it is not clear whether such a debt occurs during
particular phrases but is repaid during other phrases of a long-duration song.
Oxygen requirements would therefore constrain syllable sequence (i.e. syntax)
but do not appear to constrain song duration in canaries or song bout duration
in zebra finches.
In summary, respiratory physiology of singing behaviour presents
multi-faceted aspects to our thinking about song evolution
(Searcy and Anderson, 1986;
Searcy and Yasukawa, 1996
). It
can give insight into how the respiratory aspects of song can provide
information about the quality of the singing male and thus affect song
evolution. The direct metabolic cost of generating and modifying song is the
most obvious aspect. However, the similar nature of respiratory patterns among
individuals appears to result in only small variation in the metabolic cost
regardless of the acoustic structure of the song. Gas exchange during song may
affect song syntax and duration. Considerable differences in air exchange
during song exist between different syllables within and among individuals,
suggesting that maintaining gas exchange is an important possible constraint.
Surprisingly, in the zebra finch, it is hyperventilation and not a lack of
oxygen that influences respiratory patterns even seconds after the song. Other
species may face the opposite problem of providing enough oxygen during song,
indicating that the need for maintaining gas exchange may pose a severe
constraint on respiratory motor patterns for song.
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