Tracheal hyperallometry and spatial constraints in a large beetle

Abstract

Insects exchange respiratory gases with their environment through their gas-filled tracheal system, a branched tracheal tree extending from segmental openings and terminating at fine tissue penetrating tracheoles. It was shown that the tracheal volume increases hyperallometrically with insect body size ($M_b$), both interspecifically and across developmental stages. In this study, we used the sixfold $M_b$ variation in adult Batocera rufomaculata (Cerambicidae; Coleoptera) examining the allometry of adult tracheal volume ($V_{\mathrm{tr}}$). We further explored the effect of sex and sexual maturity on tracheal gas conductance, testing the hypotheses that (i) larger body size and (ii) egg volume in gravid females would result in lower safety margins for tracheal oxygen transport due to structural restriction. We report a hyperallometric tracheal growth in both sexes of adult B. rufomaculata (mean mass exponent of 1.42 ± 0.09), similar in magnitude to previously reported values. Tracheal gas conductance was independent of $M_b$ and reproductive state, but was significantly higher in females compared with males. We suggest that females may have pre-adapted a higher tracheal conductance required for the higher flight power output while gravid. Lack of compliant air sacs and rigid trachea may explain how gravid females retain their $V_{\mathrm{tr}}$. However, we show that $V_{\mathrm{tr}}$ outgrows thoracic dimensions with increased B. rufomaculata size. Hyperallometric growth of the giant cerambycid thoracic trachea could explain the previously reported hypometric scaling of flight muscles in B. rufomaculata, and the compromised long-distance flight performance of larger compared with smaller conspecifics.