Visual Eyes: A Quantitative Analysis of the Photoreceptor Layer in Deep-Sea Sharks

Abstract

The marine environment presents unique visual challenges for a range of organisms, particularly those dwelling at great depths, where sunlight may either be absent or drop to very low levels. Under these environmental conditions, the visual system must maximise light absorption in order to enhance the detection of prey, predators and potential mates. Using stereological analysis of retinal wholemounts, the distribution and number of photoreceptors (rods) was determined for 5 deep-sea shark species from a range of depths (46-1,500 m). All species possessed areas of increased photoreceptor density (with peaks between 41,000 and 82,000 rods/mm²) within discrete regions of the retina. The total number of rods in the photoreceptor layer also varied between 17 × 10⁶ and 63 × 10⁶. It is evident that increasing sensitivity of the retina is an important adaptation to life in the deep sea. The location of discrete areas of high cell density within the photoreceptor layer of the retina corresponds to discrete areas of the visual field that are sampled at a higher intensity, hence increasing sensitivity. The location of these areas of increased sensitivity differed between the species of this study. The disparity of areas of increased sensitivity seen between species is thought to reflect distinctive predator avoidance and prey capture strategies. This study reveals that the visual demands of deep-sea sharks vary interspecifically and that sampling of each species' visual field is not solely determined by its habitat.

The Retina of Ansorge's Cusimanse <b><i>(Crossarchus ansorgei)</i></b>: Number, Topography and Convergence of Photoreceptors and Ganglion Cells in Relation to Ecology and Behavior

“…The harvesting and use of this specimen was approved by the University of the Witwatersrand Animal Ethics Committee (2008/36/1) and the University of Western Australia Ethics Committee (RA/3/100/927). Because other studies in many vertebrate species have shown that interindividual variation in the total number and topographic distribution of both photoreceptors and retinal ganglion cells is generally low [Lisney et al, 2012;Coimbra et al, 2013;Lisney et al, 2013a, b;Newman et al, 2013;Coimbra et al, 2014a, b;de Busserolles et al, 2014a, b;Coimbra et al, 2015], the eyes from this single specimen of Ansorge's cusimanse can be considered representative for the characterization of the retinal topographic specializations in this species. In addition, given the overall lack of information about the biology of Ansorge's cusimanses, we found it important to study the retinal topographic specializations in this species to predict the importance of vision in the use of habitat and behavior.…”

Retinal topography maps in R: New tools for the analysis and visualization of spatial retinal data

“…In the 19th century, retinal topography maps were mentioned by von Graefe (1865, p. 22, ''Netzhautkarte'') and, to our best knowledge, were formally introduced by Stone (1965). Retinal topography maps have since been widely used, with many recent publications (e.g., Ahnelt, Schubert, Kübber-Heiss, Schiviz, & Anger, 2006;Coimbra, Nolan, Collin, & Hart, 2012;Coimbra, Collin, & Hart, 2013, 2014a, 2014bLandgren, Fritsches, Brill, & Warrant, 2014;Lisney, T. J., Stecyk, K., Kolominsky, J., Graves et al, 2013;Lisney, T. J., Stecyk, K., Kolominsky, J., Schmidt et al, 2013;Moore, Doppler, Young, & Fernandez-Juricic, 2013;Newman, Marshall, & Collin, 2013;Schiviz, Ruf, Kuebber-Heiss, Schubert, & Ahnelt, 2008;Ullmann et al, 2012). Comparative analyses over the last few decades have yielded maps for several hundred vertebrates, many of which (approx.…”

Scene through the eyes of an apex predator: a comparative analysis of the shark visual system

“…Most studies have thus far concentrated on the distribution of retinal ganglion cells based on their large size and accessibility. However, where photoreceptors have been stereologically sampled, similar patterns have been revealed, that is, in the ornate wobbegong, Orectolobus ornatus; the whitetip reef shark, Triaenodon obesus; the epaulette shark, Hemiscyllium ocellatum; the sandbar shark, Carcharhinus plumbeus; and six species of deep‐dwelling sharks …”

“…However, in some species where the head is dorso‐ventrally flattened, that is, in the Sphyrnidae family of hammerhead sharks, the eyes are elongated rostro‐caudally, with a greater equatorial eye diameter than axial eye diameter. Absolute eye size varies from over 62 mm in the pelagic, big‐eyed thresher shark ( Alopias superciliosus) to less than 3 mm in the deep‐sea, longsnout dogfish ( Deania quadrispinosum ) . Oceanic and shallow benthopelagic species, which predate on active, mobile prey, typically possess larger eyes than coastal benthic sharks when body size is taken into account .…”

“…In comparison to other retinal cell types, the photoreceptor and ganglion cell types have been the most widely studied in sharks . The retina of most species of sharks has been found to possess both rods and cones and is therefore considered duplex, although there are some deep‐sea and nocturnal exceptions . Rods operate in low light or scotopic conditions, while cones operate in bright or photopic conditions.…”