Do American goldfinches see their world like passive prey foragers? A study on visual fields, retinal topography, and sensitivity of photoreceptors

Abstract

Several species of the most diverse avian order, Passeriformes, specialize in foraging on passive prey, although relatively little is known about their visual systems. We tested whether some components of the visual system of the American goldfinch (Spinus tristis), a granivorous bird, followed the profile of species seeking passive food items (small eye size relative to body mass, narrow binocular fields and blind areas, centrally located retinal specialization projecting laterally, ultraviolet-sensitive vision). We measured eye size, visual field configuration, the degree of eye movement, variations in the density of ganglion cells and cone photoreceptors, and the sensitivity of photoreceptor visual pigments and oil droplets. Goldfinches had relatively large binocular (46°) and lateral (134°) visual fields with a high degree of eye movement (66° at the plane of the bill). They had a single centrotemporally located fovea that projects laterally, but can be moved closer to the edge of the binocular field by converging the eyes. Goldfinches could also increase their panoramic vision by diverging their eyes while handling food items in head-up positions. The distribution of photoreceptors indicated that the highest density of single and double cones was surrounding the fovea, making it the center of chromatic and achromatic vision and motion detection. Goldfinches possessed a tetrachromatic ultraviolet visual system with visual pigment peak sensitivities of 399 nm (ultraviolet-sensitive cone), 442 nm (short-wavelength-sensitive cone), 512 nm (medium-wavelength-sensitive cone), and 580 nm (long-wavelength-sensitive cone). Overall, the visual system of American goldfinches showed characteristics of passive as well as active prey foragers, with a single-fovea configuration and a large degree of eye movement that would enhance food searching and handling with their relatively wide binocular fields.