The dorsal eye of the dragonfly Sympetrum: specializations for prey detection against the blue sky

Abstract

Dragonflies of the genus Sympetrum have compound eyes conspicuously divided into dorsal and ventral regions. Using anatomical, optical, electrophysiological, in-vivo photochemical and microspectrophotometrical methods, we have investigated the design and physiology of the dorsal part which is characterized by a pale yellow-orange screening pigment and extremely large facets. The upper part of the yellow dorsal region is a pronounced fovea with interommatidial angles approaching 0.3°, contrasting to the much larger values of 1.5°–2° in the rest of the eye. The dorsal eye part is exclusively sensitive to short wavelengths (below 520 nm). It contains predominantly blue-receptors with a sensitivity maximum at 420 nm, and a smaller amount of UV-receptors. The metarhodopsin of the blue-receptors absorbs maximally at 535 nm. The yellow screening pigment transmits longwavelength light (cut-on 580 nm), which increases the conversion rate from metarhodopsin to rhodopsin (see Fig. 11a). We demonstrate that because of the yellow pigment screen nearly all of the photopigment is in the rhodopsin state under natural conditions, thus maximizing sensitivity. Theoretical considerations show that the extremely long rhabdoms (1.1 mm) in the dorsal fovea are motivated for absorption reasons alone. A surprising consequence of the long rhabdoms is that the sensitivity gain, caused by pumping photopigment into the rhodopsin state, is small. To explain this puzzling fact we present arguments for a mechanism producing a gradient of rhodopsin concentration along the rhabdom, which would minimize saturation of transduction units, and hence improve the signal-to-noise ratio at high intensities. The latter is of special importance for the short integration time and high contrast sensitivity these animals need for spotting small prey at long distances.