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.

Vision in avian emberizid foragers: maximizing both binocular vision and fronto-lateral visual acuity

“…After extraction of the retina, it was whole-mounted and stained with Cresyl Violet for visualization of ganglion cells and counting, following the whole-mount technique described in detail in Ullmann et al (2012). A thorough description of our methods to process the retinal tissue and count retinal ganglion cells (using standard cytological criteria) has been recently published in Baumhardt et al (2014). We chose to stain ganglion cells because they have been proposed to be the information bottlenecks from the retina to the visual centers of the brain (Collin, 1999) and therefore have an important role in visual acuity (McIlwain, 1996).…”

“…We differentiated retinal ganglion cells from all other cell types throughout the entire retina, however nearly every cell within the high ganglion cell density regions was counted because the non-ganglion cell population declines below 1% of the total cell count (Ehrlich, 1981). We discuss this approach to differentiating ganglion cells in detail in Fernández-Juricic et al (2011b) and Baumhardt et al (2014).…”

“…In Passeriformes, the bill usually projects towards the binocular field (e.g. Tyrrell et al, 2013;Baumhardt et al, 2014). The implication is that larger bills can block areas of binocular overlap leaving them covered only by monocular vision (i.e.…”

Does retinal configuration make the head and eyes of foveate birds move?

“…However, spatial resolving power may not be the only factor accounting for the patterns observed, as the densities of photoreceptors involved in both chromatic and achromatic vision in birds also increase from the retinal periphery to the fovea20. Therefore, it is also possible that chromatic and achromatic visual contrast and contrast sensitivity are also associated with the changes in spatial resolving power across different parts of the retina.…”

Dynamic Status Signal Reflects Outcome of Social Interactions, but Not Energetic Stress

“…We used the program pavo in R (Maia et al, 2013) to calculate S and L within dominants before and after trials, and within subordinates before and after trials. We calculated S and L across the avian visual spectrum (320-700 nm) using an American goldfinch visual model (Baumhardt et al, 2014), assuming a standard daylight illuminant ("D65" in pavo) and an idealized homogeneous background based on formulae presented in Vorobyev et al (1998) and Siddiqi et al (2004) as executed in pavo (Maia et al, 2013).…”