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First published online September 16, 2005
Journal of Experimental Biology 208, 3645-3654 (2005)
Published by The Company of Biologists 2005
doi: 10.1242/jeb.01788

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Unconventional mechanisms control cyclic respiratory gas release in flying Drosophila

Fritz-Olaf Lehmann^* and Nicole Heymann

Department of Neurobiology, University of Ulm, Albert-Einstein-Allee 11, 89081 Ulm, Germany

View larger version (28K): [in a new window]   Fig. 1. Oscillatory release of CO2 during tethered flight in a single fruit fly Drosophila, flying in a flow-through respirometic chamber of a virtual-reality flight arena and exhibiting only small fluctuations in metabolic rate. (A) Location of spiracle openings on one side of Drosophila: sp1, mesothoracic spiracle; sp2, metathoracic spiracle; sp3–9, abdominal spiracles. (B) Muscle mass-specific mechanical power output of the asynchronous indirect flight muscles (IFM) in vivo was calculated from simultaneous measurements of aerodynamic production, flight force production, wing stroke amplitude and frequency (left scale, top trace). Bottom trace shows muscle mass-specific CO2 release rate (right scale). In the bar below, blue indicates the oscillatory phase of gas release; gray, non-cyclic gas release. (C) Temporal distributions of oscillatory CO2 release patterns (blue) of 12 fruit flies flown under three different experimental conditions (shown in the pictograms): (I) fruit flies vary metabolic rate in response to visual stimulation by external open-loop vertical motion of horizontal stripe patterns while simultaneously themselves stabilizing the azimuth position of a closed-loop vertical stripe using the relative difference in wing stroke amplitude (dark gray, left; see Materials and methods); (II) flight under visual-closed-loop conditions but in the absence of lift stimuli (yellow, middle); and (III) flight in absence of any moving visual objects (gray, right). Data show that oscillatory releases of CO2 occur randomly and are essentially restricted to flight sequences without any visual stimulation of the surrounding panorama (stationary patterns).

View larger version (26K): [in a new window]   Fig. 2. Temporal occurrence and frequency of cyclic gas exchange patterns in flying Drosophila. (A) Cyclic gas release often consists of multiple consecutive CO2 release cycles in a burst (gray). (B) Frequency of occurrence of cyclic bursts containing different numbers of cyclic CO2 `waves'. N=12 flight sequences, as shown in Fig. 1C (12 flies). (C) Frequency of consecutive CO2 cycles in a single fly. (D) Mean frequency of CO2 oscillations measured in 12 flies. Red dotted line, mean value derived from all 12 flies. Values are means ± S.D.

View larger version (44K): [in a new window]   Fig. 3. Potential mechanisms of oscillatory CO2 release patterns in Drosophila. (A–C) Infra-red video images show the flying fly from below, while recording wing kinematics, flight force production and the release of flight muscle-specific CO2. Four UV light-activated fluorescent markers on the animal's abdomen (B) allow video-based in-flight tracking of abdominal pumping movements, and light intensity changes within the measurement area (red box) indicate proboscis movements during flight (C). (D–F) Simultaneously recorded flight data of (D) CO2 release, (E) abdominal length and width changes based on movement of markers in B and (F) occurrence of the proboscis extension reflex (PER), during a 40 s flight sequence. A PER value of zero indicates that the proboscis is fully retracted, whereas a value of 1.0 means full extension. Gray bars indicate examples where CO2 release decreases (inhalation) as the fly extends the proboscis. No moving visual stimuli were displayed in the surrounding panorama. (G–I) Cross-correlation coefficients r are plotted between (G) the derivative of muscle mass-specific mechanical power output of the flight muscles and the derivative of CO2 release, (H) the derivative in abdominal length and CO2 release, and (I) the derivative of proboscis movements and CO2 release. L = cross-correlation temporal phase shift between data sets (phase lag). Each cross-correlation analysis was performed for six flight sequences over time t, using a sliding data window with 0.5t width. Length of the flight sequences was 141±77 s (mean ± S.D., N=3 flies). In this analysis we limited our data set to flies that showed pronounced and long-lasting gas release oscillations. Mean correlation coefficient r is plotted in black; gray areas indicate S.D.

View larger version (30K): [in a new window]   Fig. 4. Analytical modeling of spiracle function. (A) Schematics of the diffusive model, as used in the present study. CO2 flux into and out of the tracheal system depends on the pressure difference (PMCO2–PTCO2 and PTCO2–PACO2) multiplied by the conductance for CO2 through the cytoplasm and the spiracle opening, GC and GS, respectively. IFM, indirect flight muscle; M, metabolic rate of the flight muscle; T, temporal flux of CO2 molecules entering the tracheoles of the tracheal system; S, gas flux through the spiracle. More details are given in the Materials and methods. (B) Example of simulated instantaneous tracheal partial pressure of CO2 as controlled by a single model spiracle. Switching opening behavior of the model spiracle stabilizes PTCO2 near a threshold value Ts (red, left scale). Temporal sum of T is shown in blue (right scale). (C) Example of simulated total release rate of CO2 of four autonomously working model spiracles, as shown in B. Due to temporal beat, the four modeled spiracle openings may synchronize (oscillatory gas release, blue) or may work out of phase (non-oscillatory release, gray). (D) Relative amplitude of Fast-Fourier Transformation (FFT) analysis of simulated data traces. Location of peak (black) indicates the principle frequency component of the FFT spectrum. Model parameters are: Ts=1.0, Gc=1.0, GS,max=0.1, PMCO2=1.05. Gray area in D shows S.D. of mean value (black) obtained from 20 different randomly distributed starting values for PTCO2. t=total length of normalized time domain (0–1).

View larger version (40K): [in a new window]   Fig. 5. Total CO2 gas release rate through 4 autonomously working spiracles, modeled by a simple analytical approach for tracheal gas exchange. In all simulations spiracle threshold value for opening Ts was set to 1.0. (A) The likelihood of cycling gas release due to synchronization of spiracle opening activity depends on the ratio between the modeled muscular partial pressure of the gas PMCO2 and the spiracle threshold value Ts. At model parameters of Gc=1.0 and GS,max=0.1, ratios around 1.05 produce gas release traces similar to the release pattern produced by the flying fly. (B) Relative amplitude of Fast-Fourier Transformation (FFT) analysis of the simulated traces shown in A. The main frequency component and thus cyclic response of the model disappears when PMCO2/Ts ratio is below or above approximately 1.05 (red). Traces represent mean values of ten simulated model runs that have been smoothed using a 3-point running average, respectively. (C) Changes in CO2 release pattern in response to variations of maximum spiracle opening conductance (GS,max) expressed as the ratio between GS,max and CO2 conductance of the cytoplasm (Gc). At a parameter setting of Ts=1.0, Gc=1.0 and PMCO2=1.05, cyclic release patterns disappear at ratio below approximately 0.1 but persist at higher ratios. (D) FFT amplitude spectrum of the model traces shown in C. For more information see explanation in B.

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