Symmorphosis and the insect respiratory system: a comparison between flight and hopping muscle

Abstract

Weibel and Taylor's theory of symmorphosis predicts that the structural components of the respiratory system are quantitatively adjusted to satisfy, but not exceed, an animal's maximum requirement for oxygen. We tested this in the respiratory system of the adult migratory locust Locusta migratoria by comparing the aerobic capacity of hopping and flight muscle with the morphology of the oxygen cascade. Maximum oxygen uptake by flight muscle during tethered flight is 967±76 μmol h(-1) g(-1) (body mass specific, ±95% confidence interval CI), whereas the hopping muscles consume a maximum of 158±8 μmol h(-1) g(-1) during jumping. The 6.1-fold difference in aerobic capacity between the two muscles is matched by a 6.4-fold difference in tracheole lumen volume, which is 3.5×10(8)±1.2×10(8) μm(3) g(-1) in flight muscle and 5.5×10(7)±1.8×10(7) μm(3) g(-1) in the hopping muscles, a 6.4-fold difference in tracheole inner cuticle surface area, which is 3.2×10(9)±1.1×10(9) μm(2) g(-1) in flight muscle and 5.0×10(8)±1.7×10(8) μm(2) g(-1) in the hopping muscles, and a 6.8-fold difference in tracheole radial diffusing capacity, which is 113±47 μmol kPa(-1) h(-1) g(-1) in flight muscle and 16.7±6.5 μmol kPa(-1) h(-1) g(-1) in the hopping muscles. However, there is little congruence between the 6.1-fold difference in aerobic capacity and the 19.8-fold difference in mitochondrial volume, which is 3.2×10(10)±3.9×10(9) μm(3) g(-1) in flight muscle and only 1.6×10(9)±1.4×10(8) μm(3) g(-1) in the hopping muscles. Therefore, symmorphosis is upheld in the design of the tracheal system, but not in relation to the amount of mitochondria, which might be due to other factors operating at the molecular level.