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

Abstract

SummaryWeibel 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 test 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% CI), whereas the hopping muscles consume a maximum of 158 ± 8 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 3.5×108 ± 1.2×108 μm3 g-1 in flight muscle and 5.5×107 ± 1.8×107 in the hopping muscles, a 6.4-fold difference in tracheole inner cuticle surface area, which is 3.2×109 ± 1.1×109 μm2 g-1 in flight muscle and 5.0×108 ± 1.7×108 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 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 3.2×1010 ± 3.9×109 μm3 g-1 in flight muscle and only 1.6×109 ± 1.4×108 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 on the molecular level.