Abstract
The structure of tubular transport networks is thought to underlie much of biological regularity, from individuals to ecosystems. A core assumption of transport network models is either area-preserving or area-increasing branching, such that the summed cross-sectional area of all child branches is equal to or greater than the cross-sectional area of their respective parent branch. For insects, the most diverse group of animals, the assumption of area-preserving branching of tracheae is, however, based on measurements of a single individual and an assumption of gas exchange by diffusion. Here we show that ants exhibit neither area-preserving nor area-increasing branching in their abdominal tracheal systems. We find for 20 species of ants that the sum of child tracheal cross-sectional areas is typically less than that of the parent branch (area-decreasing). The radius, rather than the area, of the parent branch is conserved across the sum of child branches. Interpretation of the tracheal system as one optimized for the release of carbon dioxide, while readily catering to oxygen demand, explains the branching pattern. Our results, together with widespread demonstration that gas exchange in insects includes, and is often dominated by, convection, indicate that for generality, network transport models must include consideration of systems with different architectures.
Author summary
A fundamental assumption of models of the transport of substances through networks of tubes, such as circulatory systems in animals and vascular systems in plants, is that the total cross-sectional area of the tubes remains constant irrespective of the branching level, or that it increases slightly in the direction from the largest to the smallest tubes. One large tube should have the same or a slightly smaller area than the sum of the next two tubes after a branching. The assumption of such a pattern underpins one of biology's most influential ideas-the metabolic theory of ecology. Surprisingly, the assumption has never been systematically examined for insects-the planet's most diverse group of animals which deliver oxygen to and remove carbon monoxide from their bodies using a network of tubes known as tracheae. Until recently, it has been technologically very challenging to do so. Here, we use x-ray synchrotron tomography to overcome this challenge. We show that tracheal branching in 20 species of ants does not follow this pattern. Rather, cross-sectional area reduces in an inwards direction. We then use modelling to show that such a pattern facilitates outward CO2 release, a process more challenging for insects than moving oxygen inwards. Our work suggests that much still needs to be done to understand the fundamental assumptions underlying network transport models and how they apply more generally across life-especially in the context of why metabolic rate scales with body size.