Electrostatic facilitation of odorant capture in insects

The sense of smell (olfaction) enables organisms from prokaryotes through invertebrates to humans to detect volatile organic compounds (VOCs). For olfaction to happen, VOCs must first come into direct contact with external structures of the olfactory system. Insects have the particularity of possessing externally facing olfactory systems, an arrangement substantially different from the internalised olfactory epithelia of most vertebrates. Whilst the olfactory process is remarkably well-understood at the molecular and neural level, large questions remain as to how airborne VOCs reach dendritic terminals, where actual detection takes place. Current evidence and theories suggest transport through passive diffusion and/or by active antennal motion. Albeit empirically supported, this process may not act alone and cannot entirely explain the notable efficiency and rapid sampling rate observed in many insect species. We have gathered evidence that the olfactory systems of insects exploit electrostatic enhancement to increase, through local electrostatic Coulomb force, VOC transfer from bulk air to the sensory substrate. We found that the presence of antennal charge is necessary to evoke an electrophysiological (EAG) response, and changing the charged state of isolated antennae of Aphis fabae, Aphidius ervi, Drosophila melanogaster and Bombus terrestris increases EAG responses and sensitivity to test VOCs. Furthermore, antennal surface charge density positively correlates with EAG response amplitude. These experimental findings were supported by comparative modelling of electrostatic and fluid dynamic mechanisms in VOC capture.