Retinal Ganglion Cell Topography in Elasmobranchs

Abstract

Retinal wholemounts are used to examine the topographic distribution of retinal cells within the ganglion cell layer in a range of elasmobranchs from different depths. The retina is examined for regional specializations for acute vision in six species of selachians, Galeocerdo cuvieri, Hemiscyllium ocellatum, Scyliorhinus canicula, Galeus melastomus, Etmopterus spinax, Isistius brasiliensis, one species of batoid, Raja bigelowi and one species of chimaera, Hydrolagus mirabilis. These species represent a range of lifestyles including pelagic, mesopelagic and benthic habitats, living from shallow water to the sea bottom at a depth of more than 3000 m. The topography of cells within the ganglion cell layer is non-uniform and changes markedly across the retina. Most species possess an increased density of cells across the horizontal (dorsal) meridian or visual streak, with a density range of 500 to 2,500 cells per mm² with one or more regional increases in density lying within this specialized horizontal area. It is proposed that the higher spatial resolving power provided by the horizontal streak in these species mediates panoramic vision in the lower frontal visual field. Only I. brasiliensis possesses a concentric arrangement of retinal iso-density contours in temporal retina or an area centralis, thereby increasing spatial resolving power in a more specialized part of the visual field, an adaptation for its unusual feeding behavior. In Nissl-stained material, amacrine and ganglion cell populations could be distinguished on the criteria of soma size, soma shape and nuclear staining. Quantitative analyses show that the proportion of amacrine cells lying within the ganglion cell layer is non-uniform and ranges between 0.4 and 12.3% in specialized retinal areas and between 8.2 and 48.1% in the peripheral non-specialized regions. Analyses of soma area of the total population of cells in the ganglion cell layer also show that the pelagic species possess significantly smaller soma (9–186 μm²) than benthic and/or deep-sea species (16–338 μm²), and that a number of different morphological classes of cells are present including a small population of giant ganglion cells.

Retinal specialisations in the dogfish <i>Centroscymnus coelolepis</i> from the Mediterranean deep-sea

“…Carrassón et al (1992) postulated that this increase in depth distribution in the Mediterranean could be to avoid competing against other species with similar trophic habits, such as Galeus melastomus and Etmopterus spinax. Comparing the topography of retinal cells in the ganglion cell layer of C. coelolepis with the topography of G. melastomus and E. spinax described by Bozzano and Collin (2000), similar retinal distribution patterns can be observed, especially between C. coelolepis and E. spinax. Similarly to the latter species, the retinal isodensity contour map of C. coelolepis reveals a thin horizontal visual streak in the central plane of the retina that provides a panoramic field of vision that extends horizontally.…”

“…The theoretical visual acuity of C. coelolepis of 7.2-7.4 cycles per degree is higher than the acuity observed in G. melastomus (3.8) and in E. spinax (2.8), the third most abundant dogfish in the deep Mediterranean, which is found down to 2000 m. Taking into account that the visual acuity in pelagic sharks (i.e. Galeocerdo cuvieri and Negaprion brevirostris) is 6.4 and 6.7 cycles per degree (Hueter, 1991;Bozzano and Collin, 2000), C. coelolepis therefore possesses a good theoretical visual acuity.…”

“…In a species like C. coelolepis, whose depth distribution range in the Mediterranean lies almost exclusively below the limit of daylight penetration where no visual horizon exists, it is surprising to find the need for visual horizon discrimination, which is characteristic of species that live in the epi-or mesopelagic environment (Collin and Pettigrew, 1988;Collin and Partridge, 1997;Bozzano and Collin, 2000). Thus, it is possible to hypothesise that the deeper distribution of this species in the Mediterranean is indeed a secondary adaptation in order to avoid competition with other species.…”

“…In 1991, Crescitelli (1991) found that visual pigment in the brown cat shark Apristurus brunneus, trawled from a depth of 550 m, absorbed maximally at 483 nm. Bozzano and Collin (2000) also investigated visual specialisation in terms of retinal topography and visual acuity in a range of species occupying different habitats and depths, from the surface to a depth of 3000 m.…”

Evaluating the landscape of fear between apex predatory sharks and mobile sea turtles across a large dynamic seascape

“…In addition to possessing specialized teeth morphology permitting them to prey on sea turtles (Witzell 1987), tiger shark eyesight may be adapted for surface capture of prey such as sea turtles. Specifically, their visual streak (the area of highest acuity in the retina) is located on the ventral surface of the retina, giving the tiger shark highest visual acuity and spatial resolution in the upper visual field (Bonazzo andCollin 2000, Hart et al 2006), which probably enhances their ability to distinguish turtles at the surface when sharks are hunting from below. In the Northwest Atlantic Ocean, loggerhead sea turtles (Caretta caretta) are a common prey item of tiger sharks (Castro 2011).…”