Symmorphosis and the insect respiratory system: allometric variation

Abstract

SUMMARYTaylor and Weibel's theory of symmorphosis predicts that structures of the respiratory system are matched to maximum functional requirements with minimal excess capacity. We tested this hypothesis in the respiratory system of the migratory locust . Therefore, the principles of symmorphosis are upheld at each step of the oxygen cascade in the respiratory system of the migratory locust. Supplementary material available online at

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

“…Maximum oxygen uptake by flight muscle during tethered flight is 967±76molh -1 g -1 (body mass specific, ±95% confidence interval CI), whereas the hopping muscles consume a maximum of 158±8mol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 3.5ϫ10 g Insect respiratory symmorphosis An allometric assessment of the migratory locust Locusta migratoria respiratory system has shown that throughout ontogeny the hopping muscles' aerobic capacity scales in proportion with the total volume, surface area and anatomical diffusing capacity of the tracheoles, and the total volume and inner membrane surface area of the mitochondria (Snelling et al, 2011b). The study therefore provides strong evidence that the insect respiratory system conforms to the economic design principles of symmorphosis.…”

“…The fixation and embedding process was performed over 5 consecutive days as detailed in an earlier study (Snelling et al, 2011b), and was identical for flight and hopping muscle. Briefly, immediately following dissection, the tissue pieces were immersed into a chemical fixative solution of 2.5% glutaraldehyde and 2% formaldehyde in 0.2moll -1 phosphate buffer with pH7.4.…”

“…These values were multiplied by two to provide a volume estimate for the whole pterothorax/both femurs per locust. Full details of these measurements and calculations are provided in an earlier study (Snelling et al, 2011b).…”

“…Sections were placed onto 3mm copper mesh grids, stained with lead citrate, and viewed with a transmission electron microscope (CM 100, Philips, Eindhoven, The Netherlands) where random 8bit, 1280ϫ1024pixel resolution images were captured with a mounted digital camera (MegaView II, Soft Imaging System, Olympus) at appropriate magnifications (Table1). To obtain unbiased sampling of the flight muscle and femur, the number of random images taken from each section was adjusted relative to the amount of muscle present (Snelling et al, 2011b). All images were exported to CorelDRAW where they were analysed using stereological principles (Cruz-Orive and Weibel, 1990;Howard and Reed, 1998;Mayhew, 1991) appropriate for vertical sections (Baddeley et al, 1986).…”

“…It has also been suggested that optimal matching between structural elements in a system becomes increasingly unlikely as the number of elements increases, along with the number of functions performed by each element (Dudley and Gans, 1991). On this basis, the insect respiratory system might offer a more suitable model as oxygen delivery occurs entirely along the tubular branching networks of the tracheal system, which ultimately terminate as small blind-ending tracheoles that function primarily to service the aerobic needs of nearby cells (Snelling et al, 2011b;Wigglesworth, 1983). The structure of the tracheal system is less likely to be constrained by its need to eliminate carbon dioxide, as the high liquid solubility of this gas allows it to diffuse rapidly through the insect's tissues and haemolymph, as well as diffusing laterally across the walls of larger tracheae and air sacs (Schmitz and Perry, 1999;Wigglesworth, 1965).…”