Smelling with the mouthparts in spotted lanternfly

Abstract

Deciphering how spotted lanternfly (SLF), an invasive polyphagous planthopper in North America, engages with its environment is a pressing issue with fundamental biological significance and economic importance. This interaction primarily depends on olfaction. However, the cellular basis of olfaction in SLF remains elusive. Here we investigate the neuronal and functional organization of the subapical labial sensory organ using scanning electron microscopy and electrophysiological recordings. This organ is believed to supply planthoppers with crucial sensory information that influences their subsequent feeding behavior. We find in SLF that this organ comprises two identical placoid sensilla, each housing two distinct neurons. The A neuron displays a remarkable sensitivity to changes in airflow speed. Importantly, the same neuron also exhibits robust excitatory responses exclusively to three aldehydes out of a diverse pool of 86 tested odorants and inhibitory responses to 62 other odorants. By contrast, the B neuron solely serves as an olfactory detector, showing strong excitatory responses to 17 odorants and inhibitory responses to only three. The results provide a potential cellular basis for the behavioral responses of SLF to its ecologically relevant stimuli. Our study also identifies new odorants that may be useful for managing this serious pest.