The Structure of the Retina of the Eurasian Eagle-Owl and its Relation to Lifestyle

Abstract

The retinal layers of birds are the same as those of other vertebrates; however, some variations exist in morphology, areas of visual acuity, and retinal vascularisation. Moreover, as a result of the relationship between environment, visual perception and behaviour, some variations are observed between diurnal and nocturnal birds. In this study, we have investigated the retina of the Eurasian Eagle-owl ( Bubo bubo hispanicus) by optical microscopy. The results indicate that the retina has features of both nocturnal and diurnal birds. The pigment epithelium cells have long prolongations filled with melanin granules. The rod is the dominant photoreceptor, but simple cones are abundant. Yellow and colourless oil droplets and paraboloid are present in the inner segment of cones. In the inner nuclear layer, the cell bodies of horizontal cells can easily be recognised by a large and pale cytoplasm. Bipolar cell perikarya are identified by their dark nuclei and the round and narrow cytoplasm. Amacrine cells, located in the inner border of the inner nuclear layer, have a round perikarya and lightly stained nuclei. Müller cells bodies, also located in this region, have an irregular shape. Finally, ganglion cells which are characterised by the prominent nuclei and nucleoli vary in size and abundance depending on different regions in the retina. The morphological characteristics of this retina indicate that B. b. hispanicus have a high light sensitivity, the capacity to discriminate colour, a complex visual processing in the inner retina in order to mediate contrast and motion and, possibly, an elevated acuity in areas of high photoreceptor and ganglion cell density.

Evolution, Development and Function of Vertebrate Cone Oil Droplets

“…For example, budgerigars have pigmented cone oil droplets, are active only in daylight, and lose color vision capabilities at light levels that are ten times greater than the threshold of human color vision (Lind and Kelber, 2009 ). In contrast, nocturnal owls and penguins are active in light-limited conditions and have depigmented cone oil droplets, suggesting that they trade off enhanced color discrimination to maximize the sensitivity of their receptors (Bowmaker and Martin, 1978 , 1985 ; Gondo and Ando, 1995 ; Alix et al, 2017 ). In particular, astaxanthin-pigmented red cone oil droplets are conspicuously absent from the retinas of these dim-light active birds.…”

“…Multiple modeling studies have suggested that oil droplets collect light and focus it into the outer segment, enhancing light capture and thereby increasing cone sensitivity (Baylor and Fettiplace, 1975 ; Govardovskii et al, 1981 ; Ives et al, 1983 ; Young and Martin, 1984 ; Stavenga and Wilts, 2014 ). Colorless oil droplets are frequently found in the cones of nocturnal species, as well as in the cones of species intermittently active in dim light (e.g., deep-diving penguins; Bowmaker and Martin, 1978 , 1984 ; Gondo and Ando, 1995 ; Alix et al, 2017 ). Even strongly diurnal species with heavily pigmented oil droplets possess SWS1 cones with colorless oil droplets (Goldsmith et al, 1984 ; Toomey et al, 2015 ), and in some species, depigmentation of all oil droplet types occurs in the central retina, in areas mediating high-acuity vision (Walls and Judd, 1933 ; Hart, 2001a ).…”

“…Nocturnal or dim-light active bird species have very pale or colorless cone oil droplets. The nocturnal tawny owl ( Strix aluco ), snowy owl ( Bubo scandiacus ), Ural owl ( Strix uralensis ) and tawny frogmouth ( Podargus strigoides ) are all noted to have depigmented oil droplets with the red cone droplet being conspicuously absent (Bowmaker and Martin, 1978 ; Gondo and Ando, 1995 ; Hart et al, 2006 ; Alix et al, 2017 ). Similarly, the cone oil droplets of King ( Aptenodytes patagonicus ) and Humboldt ( Spheniscus humboldti ) penguins are relatively depigmented, and these species also lack red cone oil droplets (Bowmaker and Martin, 1985 ; Gondo and Ando, 1995 ).…”

Vision adaptation in the laughing dove (Streptopelia senegalensis, Linnaeus, 1766) inferred from structural, ultrastructural, and genetic characterization

“…Walls (1942) proposed that the light‐collecting function of the oil droplets may be of marginal effectiveness in the ambient‐light conditions as some dim‐light clades completely lost their oil droplets. Colorless oil droplets are also found in intermittently active animals in dim light (Alix et al, 2017). Thus, various spectral filtering abilities of the LD is speculated from different types and pigmentations of the oil droplets.…”

Visual adaptation and retinal characterization of the Garganey (Anas querquedula): Histological and scanning electron microscope observations

“…There are some previously published data describing the gross morphological appearance especially the retina of different avian species (Alix, Segovia, & García, 2017; Bawa & YashRoy, 1972; Braekevelt & Thorlakson, 1993; El‐Beltagy, 2015; Hossler & Olson, 1984; Segovia, García, Gómez‐Torres, & Mengual, 2016). However, the cornea, iris, and choroid received little attention from researchers (Meyer, 1977).…”