Fuel and Oxygen Delivery
Metabolic rates during flight exceed resting values by a factor of 50 to 200, and the thoracic muscles of flying insects exhibit the highest mass-specific rates of oxygen consumption known for any locomotor muscle. Mitochondrial densities within flight muscle fibers are correspondingly high, ranging in some insects to values as high as 45% of the total muscle volume. Energy during flight is derived almost entirely from the oxidation of chemical fuels; anaerobic pathways are absent from flight muscles. Metabolic fuels diffuse from the hemolymph surrounding muscle fibers to the point of oxidation within mitochondria, whereas bulk movement of hemolymph within the body cavity transports fuels from the abdominal fat body to the thoracic musculature. The type and composition of the fuel used in flight (i.e., lipids, carbohydrates, or amino acids) vary with phylogenetic association and may even change with time during a single flight duration in some species. Oxygen influx and carbon dioxide efflux during flight occur primarily via diffusion within tracheal pathways, but may be augmented by convective motion. For example, contraction of flight muscles and the associated deformations of the thorax can compress and expand internal air sacs and even first- and second-order tracheal branches. Although most higher order branches within the tracheolar network are unlikely to experience convective pumping, muscular contraction may augment diffusion by deforming tracheoles that invaginate muscle fibers.
One important issue relating to flight energetics concerns the limits of insect body size. In dragonflies, studies of tracheal geometry suggest an upper limit to thoracic radius of about 0.5 cm if diffusion alone supplies oxygen during flight. The thoraces of many extant insects are well above this limit, however, and the relative contribution of convection to oxygen supply has yet to be determined for any insect. The existence of some flight-related constraint on maximum body size is supported by the observation that many large insects (e.g., the giant stick insects of Southeast Asia) are secondarily flightless. In a modern species of dragonfly, flight metabolic rates vary in direct proportion to ambient oxygen concentration, a result that is consistent with diffusion-limited oxygen transport. The existence of widespread gigantism in late Paleozoic insects (and among other arthropods) during periods of elevated atmospheric oxygen concentration provides further evidence for diffusive limits to flight metabolism, and thus body size, of flying insects.
Although selection has presumably acted to minimize mechanical power expenditure, most of the energy consumed during flight is lost as heat in the flight musculature. Estimates for the mechanical efficiency of insect flight muscle range from only 4 to 30%, depending on taxon and assumptions as to the amount of elastic energy storage within the thorax. Thus, a comparatively small fraction of the fuel an insect consumes is available as mechanical power to drive the wings. This mechanical energy must support three requirements: parasite, inertial, and aerodynamic power. Inertial power is the power required to accelerate the wings back and forth during the stroke. Unless inertial power is substantially greater than aerodynamic power, even moderate elastic storage within the thorax renders inertial costs small. Parasite power is the work required to overcome the drag on the animal's body as it moves through the air. Thus, parasite power is negligible at low advance ratios, but increases with the cube of flight speed. The aerodynamic power is the rate of the work the wings perform on the air, which may be further subdivided into induced power, the cost of generating lift, and profile power, the cost of overcoming drag on the wings. Because the lift-to-drag ratio for most wing kinematic patterns capable of generating sufficient lift is quite low, profile power requirements may substantially exceed the induced power, especially in smaller insects. Also, recent measurements of drag on dynamically scaled model insect wings indicate that values of profile power may be two to three times higher than previously thought. Underestimates of aerodynamic power resulting from unrealistically low values for wing drag may explain the low estimates of mechanical efficiency for asynchronous flight muscle.
The variation in power requirements with forward airspeed is of ecological and evolutionary interest because of its implications for optimal foraging and dispersal strategies. Both direct measurements and aerodynamic modeling of bumble bees in forward flight suggest that mechanical power requirements are approximately constant over an airspeed range of 0 to 4.5 m/s. In contrast, calculations for various lepidopteran and odonatan species show substantial increases in mechanical power expenditure, with forward airspeed due to the rise in parasite power. In situations in which parasite power is large relative to aerodynamic power, the choice of airspeed during flight has significant energetic implications. One study with dragonflies suggests, in fact, that maximum flight speeds are determined predominantly by the dramatic increase in body drag and associated power requirements at extreme airspeeds.
As with many features of flight muscle physiology, power production is strongly temperature-dependent, an effect that has several implications for overall flight performance. Measurements on isolated muscles show that mechanical power output typically increases with temperature and is maximal near muscle temperatures characteristic of the free-flying insect. However, the temperature dependence of power output differs greatly among taxa, and although some insects can instantly take off from the surface of glaciers, others must warm their thoraces to 40°C before their muscle generates sufficient power to sustain flight. In insects for which the flight muscles require elevated temperatures to attain adequate performance, the heat generated during flight that results from low muscle contractile efficiency is available as a source with which to regulate thoracic temperature. In small insects, most metabolic heat generated during flight is lost via convective cooling, and body temperature is close if not equal to ambient air temperature. In larger insects, however, metabolic heat gain is high relative to convective loss and body temperatures are correspondingly elevated. Many large insects regulate internal heat distribution via control of hemolymph circulation between the thorax and the abdomen, using the latter to radiate excess heat. The dramatic amounts of heat produced by muscular contraction are illustrated by the capacity of bumble bees and of some moths to maintain thoracic temperatures exceeding 30°C when ambient air temperature is only 2 to 3°C. Evolution of such thermoregulatory capacity in many insects is consistent with strong historical selection on muscle performance to meet the exacting energetic demands of flight. Further evidence supporting the link between thermoregulation and flight is the phenomenon known as preflight warm-up. In larger insect taxa, pronounced contraction of the thoracic muscles and low-amplitude wing vibrations precede flight. These actions elevate thoracic temperature to values at which the muscles yield sufficient mechanical power for takeoff. Ontogenetic variation in the temperature dependence of muscle power output can also be substantial. In some dragonflies, for example, thermal sensitivity of force production by flight muscle is correlated with changes in the expression of myosin isoforms through development. This finding suggests that physiological features of flight performance are matched to particular environmental conditions and selective demands.
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