Physiological optics in the hummingbird hawkmoth: a compound eye without ommatidia

The fast-flying day-active hawkmoth Macroglossum stellatarum (Lepidoptera: Sphingidae) has a remarkable refracting superposition eye that departs radically from the classical principles of Exnerian superposition optics. Unlike its classical counterparts, this superposition eye is highly aspherical and contains extensive gradients of resolution and sensitivity. While such features are well known in apposition eyes, they were thought to be impossible in superposition eyes because of the imaging principle inherent in this design. We provide the first account of a superposition eye where these gradients are not only possible, but also produce superposition eyes of unsurpassed quality. Using goniometry and ophthalmoscopy, we find that superposition images formed in the eye are close to the diffraction limit. Moreover, the photoreceptors of the superposition eyes of M. stellatarum are organised to form local acute zones, one of which is frontal and slightly ventral, and another of which provides improved resolution along the equator of the eye. This angular packing of rhabdoms bears no resemblance to the angular packing of the overlying corneal facets. In fact, this eye has many more rhabdoms than facets, with up to four rhabdoms per facet in the frontal eye, a situation which means that M. stellatarum does not possess ommatidia in the accepted sense. The size of the facets and the area of the superposition aperture are both maximal at the frontal retinal acute zone. By having larger facets, a wider aperture and denser rhabdom packing, the frontal acute zone of M. stellatarum provides the eye with its sharpest and brightest image and samples the image with the densest photoreceptor matrix. It is this eye region that M. stellatarum uses to fixate flower entrances during hovering and feeding. This radical departure from classical Exnerian principles has resulted in a superposition eye which has not only high sensitivity but also outstanding spatial resolution.