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During elevated locomotor activity such as flight, Drosophila satisfies its increased respiratory demands by increasing the total spiracle opening area of the tracheal gas exchange system. It has been assumed that in a diffusion-based system, each spiracle contributes to oxygen flux into and carbon dioxide flux out of the tracheal system according to the size of its opening. We evaluated this hypothesis by determining how a reduction in size and interference with the spatial distribution of gas exchange areas impair flight muscle function and aerodynamic force production in the small fruit fly Drosophila melanogaster. This was done by selectively blocking thoracic spiracles of tethered flies flying inside a flight simulator. Flow-through respirometry and simultaneous measurements of flight force production and wing kinematics revealed a negligible functional safety margin for respiration. Maximum locomotor performance was only achieved by unmanipulated flies, supporting the general assumption that at the animal's maximum locomotor capacity, maximum spiracle opening area matches respiratory need. The maximum total buffer capacity for carbon dioxide in Drosophila amounts to approximately 33.5 μl g-1 body mass, estimated from the temporal integral of carbon dioxide release rate during the resting period after flight. By comparing flight variables in unmanipulated and ‘spiracle-blocked’ flies at comparable flight forces, we found that (i) stroke amplitude, stroke frequency and the chemo-mechanical conversion efficiency of the indirect flight musculature were broadly independent of the arrangement of spiracle conductance, while (ii) muscle mechanical power significantly increased, and (iii) mean lift coefficient and aerodynamic efficiency significantly decreased up to approximately 50% with an increasing number of blocked spiracles. The data suggest that Drosophila apparently maximizes the total efficiency of its locomotor system for flight by allowing oxygen delivery to the flight musculature through multiple spiracles of the thorax. [ABSTRACT FROM AUTHOR]

The high power output of flight muscles places special demands on the respiratory gas exchange system in insects. In small insects, respiration relies on diffusion, and for elevated locomotor performance such as flight, instantaneous gas exchange rates typically co-vary with the animal's metabolic activity. By contrast, under certain conditions, instantaneous release rate of carbon dioxide from the fruit fly Drosophila flying in a virtual-reality flight arena may oscillate distinctly at low frequency (0.37±0.055 Hz), even though flight muscle mechanical power output requires constant metabolic activity. Crass-correlation analysis suggests that this uncoupling between respiratory and metabolic rate is not driven by conventional types of convective flow reinforcement such as abdominal pumping, but might result from two unusual mechanisms for tracheal breathing. Simplified analytical modeling of diffusive tracheal gas exchange suggests that cyclic release patterns in the insect occur as a consequence of the stochastically synchronized control of spiracle opening area by the four large thoracic spiracles. Alternatively, in-flight motion analysis of the abdomen and proboscis using infra-red video imaging suggests utilization of the proboscis extension reflex (PER) for tracheal convection. Although the respiratory benefit of synchronized spiracle opening activity in the fruit fly is unclear, proboscis-induced tracheal convection might potentially help to balance the local oxygen supply between different body compartments of the flying animal. [ABSTRACT FROM AUTHOR]

Flightin is a multiply phosphorylated, myosin-binding protein found specifically in indirect flight muscles (IFM) of Drosophila. A null mutation in the flightin gene (fln0) compromises thick filament assembly and muscle integrity resulting in muscle degeneration and lost of flight ability. Using P-element-mediated transformation with the full-length flightin gene driven by the Actin88F promoter, we have achieved rescue of all fln0-related ultrastructural and functional defects of the IFM. Transgenic P[fln+]fln0 'rescued' flies have fewer thick filaments per myofbril than wild-type flies (782±13 vs 945±9) but have otherwise normal IFM. Transgenic P[fln+]fln+ 'tetraploid' flies have a normal number of thick filaments. The flightin protein levels in both transgenic strains are similar to wild type. By contrast, flightin levels are reduced in a myosin heavy chain tetraploid strain that produces excess myosin and excess thick filaments. These results suggest that regulation of flightin protein level is independent of gene copy number and that the number of thick filaments assembled per myofibril is influenced independently by myosin and flightin expression. We measured mechanical properties of IFM skinned fibers by sinusoidal analysis and found no significant differences in active viscoelastic properties of flightin-rescued and tetraploid transgenic flies vs wild type. The ability of the fln+ transgene to overcome deficits in dynamic stiffness and power output in fln0 suggest that the flightin protein contributes directly to fiber stiffness and stretch activation. However, flight parameters at maximum locomotor capacity, measured in a virtual reality flight simulator, are slightly compromised for both transgenic strains. P[fln+]fln0 and P[fln+]fln+ flies generated enough flight force to sustain hovering flight but showed reduced capability to produce forces in excess of hovering flight force. Both strains showed reductions in stroke frequency but only P[fln+]fln+ showed reductions in stroke amplitude. Muscle and aerodynamic efficiency are similar among the two transgenic strains and wild type. These results illustrate the importance of flightin in flight muscle development and function. [ABSTRACT FROM AUTHOR]