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Respiratory patterns and oxygen consumption in singing zebra finches

Michele Franz and Franz Goller^*

Department of Biology, University of Utah, Salt Lake City, UT 84112, USA

View larger version (36K): [in a new window]   Fig. 1. Zebra finch song consists of a stereotyped sequence of distinct syllables (motif). Song is illustrated as oscillogram (A) and spectrogram (top panel). The air sac pressure (P) pattern for song is equally stereotyped; the horizontal line indicates ambient pressure. Numbers mark the different expiratory pressure pulses of the motif, which is preceded by two introductory notes (i).

View larger version (105K): [in a new window]   Fig. 2. Schematic illustration of the mask system used to measure oxygen consumption. The key components are labelled. Inlet and outlet tubes were routed from the mask to a backpack and then to the oxygen analyzer.

View larger version (18K): [in a new window]   Fig. 3. The mask system provided enough temporal resolution to see small oscillations in oxygen consumption rate (O2) that corresponded to individual breath cycles, measured as air sac pressure (P). The horizontal line represents ambient pressure; air sac pressure above and below the line correspond to expiration and inspiration, respectively. Respiratory changes caused by defecation, presentation of the female and song have rapid responses in the oxygen consumption of the bird. Defecation (marked by first arrow) has a distinct pressurization in the air sacs with simultaneous closure of the airways (airflow data are not displayed). It is accompanied by a pronounced decrease in oxygen consumption. Note that the defecation event is followed by two calls (substantially higher pressure peaks). Elevated respiratory rate caused by female presentation (second arrow) is accompanied by increased oxygen consumption, as is subsequent song (third arrow marks the first of two song bouts).

View larger version (34K): [in a new window]   Fig. 4. Respiratory changes cause fluctuations in oxygen consumption. (A) The pattern of oxygen consumption (O2) and respiration (air sac pressure, P) can vary substantially and rapidly. The horizontal line in the pressure trace represents ambient pressure. (B,C) The volume and duration of each expiratory and inspiratory pressure pulse were calculated along with the mean oxygen consumption rate (O2) for that segment. Data points for expiration and inspiration are values calculated by dividing the volume of each pulse by its corresponding duration, giving an estimate of respiratory rate and effort. Whereas in B the axes for expiratory and inspiratory effort are scaled to illustrate small fluctuations unrelated to song, C shows these data at full scale. These traces illustrate that oxygen consumption reflects even small fluctuations in respiratory activity. As respiratory activity increases (marked by first arrow in A), demonstrated by shorter air sac pressure pulses of higher amplitude, O2 also increases. Shortly before song (second arrow in A) there is a small decrease in oxygen consumption that corresponds to a decrease in respiratory rate (long duration and small amplitude pressure pulses). Respiration increases during song followed by a distinct peak in O2. After song there is a significant decrease in respiration (pulses of short amplitude and duration) and a large decrease in oxygen consumption. Note that vocalizations are characterized by markedly increased amplitude of air sac pressure, as illustrated by the song bout, but also by several calls around the 10 s and 50 s mark (A). Because the syringeal resistance changes for vocalization and airflow patterns change, this altered pressure is not accompanied by a correspondingly large change in oxygen consumption.

View larger version (22K): [in a new window]   Fig. 5. Oxygen consumption fluctuates during a song bout. Longer song bouts showed oxygen consumption rate (O2) oscillations (top) that corresponded to motif repetitions in the pressure pattern (P). The first of the five motifs has the highest peak in O2. The level of the O2 peak lowers for each subsequent motif until stabilizing at the end. Broken vertical lines represent the beginning of subsequent motifs.

View larger version (13K): [in a new window]   Fig. 6. (A) The volume of oxygen consumed during song (V) increases with duration (D) of song bouts (regression equation: V=0.437+0.00124D; r=0.797, F=64.409, P<0.0001). Different symbols represent data points from different individuals (N as in Table 1). (B) Individuals with a longer motif duration (d) consumed a larger volume of oxygen (v) per motif (regression equation: v=-0.210+0.0017d; r=0.9024, F=17.54, P=0.014). (C) Song oxygen consumption rate (s) is closely related to pre-song oxygen consumption rate levels (p) (regression equation: s=0.075+0.904p; r=0.967, F=529.02, P<0.0001). The broken line indicates equal values on the x- and y-axes.

View larger version (24K): [in a new window]   Fig. 7. Significant apnea can occur after song. (A) After a deep inspiration following the song bout, respiratory movements cease for several seconds, as indicated by air sac pressure (P) measurements. Oxygen consumption rate (O2) also declines and remains at zero for 200 ms during apnea. O2 increases again as normal respiratory movements are resumed. (B) Tracheal airflow (F), recorded simultaneously with air sac pressure in another individual, confirms that apnea is correctly inferred from air sac pressure patterns. Airflow is near zero for more than 1 s following the song bout.

View larger version (15K): [in a new window]   Fig. 8. The duration of irregular respiration (from decreased amplitude and rate of respiration to complete apnea; D) corresponds to the volume by which oxygen consumption declines (V) after song (regression equation: V=-0.016+3.092x10-5D; r=0.832, F=76.616, P<0.0001). Different symbols represent different birds.

View larger version (11K): [in a new window]   Fig. 9. The factorial increase of song metabolic rate to pre-song metabolic rate decreases with increasing pre-song oxygen consumption rate (O2). Different symbols identify data points from different individuals.