Poor Leg Plumbing Design Saves Earth From Giant Bugs

Abstract

Understanding the causes and consequences of the evolution of large or small body size remains one of the important challenges of evolutionary biology. Insects have an unusual respiratory system, transporting oxygen in the gas phase via air-filled tracheae. The possession of this unique system has been hypothesized to limit insect size, but if so, the mechanisms remain unclear. We investigated this question by assessing how spatial investment in tracheal system structure varies with insect body size. Based on comparisons with vertebrates, we expect either geometric isometry in tracheal system scaling (as found in lungs) or hypometric scaling (as found in vertebrate capillaries), with the latter matching the hypometric scaling of metabolic rate found for most animals. We tested these expectations by measuring the 3D morphology of tracheal systems of ten species each of cockroaches and scarab beetles. In both groups, body mass varied by more than an order of magnitude across species, which included some of the largest extant species of insect. Cockroaches were imaged at Argonne National Laboratory using synchrotron x-ray microcomputed tomography (SR-µCT), and scarab beetles were imaged at Virginia Tech using tabletop µCT. We measured the fraction of body volume occupied by the tracheal system for the major body compartments. In general, the tracheal system scaled isometrically in the head, thorax, and abdomen. However, within the femurs of the legs, tracheal volume scaled strongly hypermetrically, resulting from an increase in number (in roaches) and size (in scarabs) of tracheae and/or air sacs. Extrapolations suggest that the femurs would be completely full of tracheae at 100-200 g body size, consistent with the hypothesis that the need for hypermetric scaling of leg tracheal supply provides at least a partial maximal limit on insect size.