Retinal Ganglion Cell Distribution and Spatial Resolving Power in Elasmobranchs

Abstract

The total number, distribution and peak density of presumed retinal ganglion cells was assessed in 10 species of elasmobranch (nine species of shark and one species of batoid) using counts of Nissl-stained cells in retinal wholemounts. The species sampled include a number of active, predatory benthopelagic and pelagic sharks that are found in a variety of coastal and oceanic habitats and represent elasmobranch groups for which information of this nature is currently lacking. The topographic distribution of cells was heterogeneous in all species. Two benthic species, the shark Chiloscyllium punctatum and the batoid Taeniura lymma, have a dorsal or dorso-central horizontal streak of increased cell density, whereas the majority of the benthopelagic and pelagic sharks examined exhibit a more concentric pattern of increasing cell density, culminating in a central area centralis of higher cell density located close to the optic nerve head. The exception is the shark Alopias superciliosus, which possesses a ventral horizontal streak. Variation in retinal ganglion cell topography appears to be related to the visual demands of different habitats and lifestyles, as well as the positioning of the eyes in the head. The upper limits of spatial resolving power were calculated for all 10 species, using peak ganglion cell densities and estimates of focal length taken from cryo-sectioned eyes in combination with information from the literature. Spatial resolving power ranged from 2.02 to 10.56 cycles deg^–1, which is in accordance with previous studies. Species with a lower spatial resolving power tend to be benthic and/or coastal species that feed on benthic invertebrates and fishes. Active, benthopelagic and pelagic species from more oceanic habitats which feed on larger, more active prey, possess a higher resolving power. Additionally, ganglion cells in a juvenile of C. punctatum, were retrogradely-labeled from the optic nerve with biotinylated dextran amine (BDA). A comparison of the BDA- labeled material and tissue stained for Nissl substance indicates that 76% of the cells in the retinal ganglion cell and inner plexiform layers of the central retina in this species are non-ganglion cells.

Reef-use and residency patterns of a baited population of silky sharks, Carcharhinus falciformis, in the Red Sea

“…A fuller moon results in greater nocturnal ambient light, and with potentially very high retinal sensitivity (Bres 1993;Lisney and Collin 2008), some silky sharks may opportunistically extend normal daytime behaviours into the night as the extra ambient light permits. This extension of diurnal behaviour is consistent with the diving behaviour of a juvenile white shark off California, which performed only a small proportion of its dives at night, but the majority of these occurred near the full moon (Dewar et al 2004).…”

Polarization sensitivity and retinal topography of the striped pyjama squid (Sepioloidea lineolata– Quoy/Gaimard 1832)

“…This strongly implies and supports the suggestion that this bottom-dwelling species, which sits buried in the substrate, leaving just the eyes exposed, possibly requires higher visual acuity in its dorsal visual field, again most likely related to detecting potential predators and prey. Cell density peaked at up to 67,500 cells per mm 2 , higher than many of the reef and deep-sea fish species previously studied (Collin and Pettigrew, 1988;Collin et al, 1997), many elasmobranchs (Lisney and Collin, 2008) and even some marine vertebrates such as the harp seal (Mass and Supin, 2003). This strategy results in the animal being more reliant on eye movements to detect and track movement in their visual field while remaining hidden, thus performing OKRs and not OMRs.…”

Visual resolution and contrast sensitivity in two benthic sharks

“…This conclusion is based on their lack of colour vision (Hart et al, 2011;Schluessel et al, 2014) and low spatial resolving power (Hueter, 1990;Lisney and Collin, 2008;Litherland and Collin, 2008). Although they percieve their world through a number of other sensory modalities such as electroreception, olfaction, audition, the mechanosensory lateral line and possibly even magnetoreception (Hueter et al, 2004;Meyer et al, 2005;Gardiner et al, 2012), vision is still important for communication (Ritter and Godknecht, 2000;Martin, 2007), navigation (Parker, 1910;Fuss et al, 2014), as well as the detection and identification of prey and predators (Hobson, 1963;Gilbert, 1970;Strong, 1996;Hammerschlag et al, 2012;Seamone et al, 2014).…”

“…Both contrast sensitivity and spatial resolving power influence an animal's ability to discriminate objects against a background and affect the distance at which detection can occur (Land, 1999;Eckert and Zeil, 2001). Anatomical estimates of spatial resolving power have been obtained for a number of shark species and range from two to 11 cycles per degree (cpd) (Hueter, 1990;Lisney and Collin, 2008;Litherland and Collin, 2008). However, no estimates of contrast sensitivity or behavioural estimates of spatial resolution currently exist, suggesting that categorising sharks as having 'poor' vision may be presumptuous.…”