Eye Shape and Retinal Topography in Owls (Aves: Strigiformes)

Abstract

The eyes of vertebrates show adaptations to the visual environments in which they evolve. For example, eye shape is associated with activity pattern, while retinal topography is related to the symmetry or ‘openness’ of the habitat of a species. Although these relationships are well documented in many vertebrates including birds, the extent to which they hold true for species within the same avian order is not well understood. Owls (Strigiformes) represent an ideal group for the study of interspecific variation in the avian visual system because they are one of very few avian orders to contain species that vary in both activity pattern and habitat preference. Here, we examined interspecific variation in eye shape and retinal topography in nine species of owl. Eye shape (the ratio of corneal diameter to eye axial length) differed among species, with nocturnal species having relatively larger corneal diameters than diurnal species. All the owl species have an area of high retinal ganglion cell (RGC) density in the temporal retina and a visual streak of increased cell density extending across the central retina from temporal to nasal. However, the organization and degree of elongation of the visual streak varied considerably among species and this variation was quantified using H:V ratios. Species that live in open habitats and/or that are more diurnally active have well-defined, elongated visual streaks and high H:V ratios (3.88–2.33). In contrast, most nocturnal and/or forest-dwelling owls have a poorly defined visual streak, a more radially symmetrical arrangement of RGCs and lower H:V ratios (1.77–1.27). The results of a hierarchical cluster analysis indicate that the apparent interspecific variation is associated with activity pattern and habitat as opposed to the phylogenetic relationships among species. In seven species, the presence of a fovea was confirmed and it is suggested that all strigid owls may possess a fovea, whereas the tytonid barn owl (Tyto alba) does not. A size-frequency analysis of cell soma area indicates that a number of different RGC classes are represented in owls, including a population of large RGCs (cell soma area >150 µm²) that resemble the giant RGCs reported in other vertebrates. In conclusion, eye shape and retinal topography in owls vary among species and this variation is associated with different activity patterns and habitat preferences, thereby supporting similar observations in other vertebrates.

Eye shape and the nocturnal bottleneck of mammals

“…Some precedent for the existence of such long-lasting phylogenetic effects is provided by the existence of 'nocturnal' eye shapes in other diurnal amniote groups [10]. Some diurnal owls and diurnal geckos retain relatively large corneas compared with diurnal birds and lizards generally [7,9] (but see [51]). Similarly, both owls and geckos probably diversified as predominantly nocturnal radiations [52,53].…”

Vision on the high seas: spatial resolution and optical sensitivity in two procellariiform seabirds with different foraging strategies

“…However, Hayes and Brooke (1990) have found that the Kerguelen petrel (Aphrodroma brevirostris) lacks a visual streak, but has a concentric distribution of the RGC density lines. Therefore, not only the 'openness' of the habitat, but also other factors like foraging strategy, prey capture technique, activity pattern and phylogenetic relatedness might influence the evolution of the RGC distribution in the retina (Hayes and Brooke, 1990;Lisney et al, 2012aLisney et al, ,b, 2013.…”

“…For example, in an open terrain such as a savannah or the open ocean, all approaching objects are represented in a horizontal band on the retina (for a detailed explanation, see Hughes, 1977). Therefore, birds such as ostrich (Struthio camelus), little penguin (Eudyptula minor), king penguin (Aptenodytes patagonicus), and several species of owls (Strigiformes), waterfowl (Anseriformes: Anatidae) and procellariiform seabirds (Procellariiformes) have an elongated area of higher RGC density stretching across the retina called the visual streak (Hayes and Brooke, 1990;Boire et al, 2001;Coimbra et al, 2012;Lisney et al, 2012aLisney et al, , 2013. This conformation of RGCs allows them to see fine details at the horizon without moving the head or eyes (Hughes, 1977).…”

Do American Goldfinches See Their World Like Passive Prey Foragers? A Study on Visual Fields, Retinal Topography, and Sensitivity of Photoreceptors

“…The retina was then washed in PBS and flattened on a gelatinized slide [Stone, 1981;Ullmann et al, 2012]. The pecten was removed prior to flattening to enable the retina to lie completely flat on the slide [Lisney et al, 2012[Lisney et al, , 2013. Additionally, this method minimized problems with asymmetric shrinkage across the retina [Ullmann et al, 2012] that could become prevalent if certain points of the retina remained partially adhered to the ora serrata or the area around the pecten.…”

“…In general, species that hunt active prey, like falcons, hawks, owls, and flycatchers, have been reported to have higher cell densities in their retinal specializations (and in some cases more than one retinal specialization per retina) than species that feed on passive prey [e.g. Reymond, 1985Reymond, , 1987Coimbra et al, 2006Coimbra et al, , 2009Dolan and Fernández-Juricic, 2010;Fernández-Juricic et al, 2011a;Lisney et al, 2012]. Consequently, we predicted that American goldfinches would have a single fovea with a relatively low density of retinal ganglion cells compared to species which forage on active prey.…”