Variations in retinal photoreceptor topography and the organization of the rod-free zone reflect behavioral diversity in Australian passerines.

Abstract

The avian retina possesses one of the most diverse complements of photoreceptor types among vertebrates but little is known about their spatial distribution. Here we used retinal wholemounts and stereological methods to present the first complete maps of the topographic distribution of rods and cones in four species of Australian passerines with diverse trophic specializations. All species studied have one central and one temporal rod-free zone. In the insectivorous yellow-rumped thornbill, the central rod-free zone is unusually large, occupying ∼17% (56°) of the retinal area (angular subtense), whereas in nectarivorous and frugivorous species it represents only ∼0.1% (5-7°) to 0.3% (10°) of the retinal area (angular subtense). In contrast, the temporal rod-free zone varies little between species (∼0.02-0.4%; 2-10°). In all species, rods follow a pronounced dorsoventral gradient with highest densities in the ventral retina. The topographic distribution of cones is concentric and reveals a central fovea and a temporal area. In the yellow-rumped thornbill, cone densities form an extended plateau surrounding the fovea, beyond which densities fall rapidly towards the retinal periphery. For the other species, cone densities decline gradually along a foveal to peripheral gradient. Estimates of spatial resolving power calculated using cone peak densities are higher in the central fovea (19-41 cycles/degree) than in the temporal area (9-15 cycles/degree). In conclusion, we suggest that the unusual organization of the rod-free zone and the distinct topographic distribution of rods and cones correlate with specific ecological needs for enhanced visual sensitivity and spatial resolution in these birds.