Insect pectinate antennae maximize odor capture efficiency at intermediate flight speeds

Abstract

Flying insects are known to orient themselves over large distances using minute amounts of odors. Some bear pectinate antennae of remarkable architecture thought to improve olfactory performance. The semiporous, multiscale nature of these antennae influences how odor molecules reach their surface. We focus here on the repeating structural building blocks of these antennae in Saturniid moths. This microstructure consists of one ramus or branch and its many hair-like sensilla, responsible for chemical detection. We experimentally determined leakiness, defined as the proportion of air going through the microstructure rather than flowing around it, by particle image velocimetry visualization of the flow around three-dimensional printed scaled-up mock-ups. The combination of these results with a model of mass transfer showed that most pheromone molecules are deflected around the microstructure at low flow velocities, keeping them out of reach. Capture is thus determined by leakiness. By contrast, at high velocities, molecular diffusion is too slow to be effective, and the molecules pass through the structure without being captured. The sensory structure displays maximal odor capture efficiency at intermediate flow speeds, as encountered by the animal during flight. These findings also provide a rationale for the previously described “olfactory lens,” an increase in pheromone reception at the proximal end of the sensors. We posit that it is based on passive mass transfer rather than on physicochemical surface processes.