Comparative visual function in elasmobranchs: Spatial arrangement and ecological correlates of photoreceptor and ganglion cell distributions LENORE LITHERLAND AND SHAUN P. COLLIN Sensory Neurobiology Group, School of Biomedical Science, The University of Queensland, Brisbane, Australia (RECEIVED May 06, 2008; ACCEPTED May 18, 2008) Abstract The topographic analysis of retinal ganglion and photoreceptor cell distributions yields valuable information for assessing the visual capabilities and behavioral ecology of vertebrates. This study examines whole-mounted retinas of four elasmobranch species, the ornate wobbegong, Orectolobus ornatus; the whitetip reef shark, Triaenodon obesus; the epaulette shark, Hemiscyllium ocellatum; and the east Australia shovelnose ray, Aptychotrema rostrata, for regional specializations mediating zones of improved visual ability. These species represent a range of lifestyles: benthic, mid-water, diurnal, and nocturnal. Both photoreceptors (visualized using differential interference contrast optics) and ganglion cells (stained with cresyl violet) in the retina are extensively sampled, and their spatial distribution is found to be nonuniform, exhibiting areae or ‘‘visual streaks.’’ In general, the topographic distributions of both cell populations are in register and match well with respect to the location of regions of high density. However, the location of peaks in rod and cone densities can vary within a retina, indicating that preferential sampling of different regions of the visual field may occur in photopic and scotopic vision. Anatomical measures of the optical limits of resolving power, indicated by intercone spacing, range from 3.8 to 13.1 cycles/deg. Spatial limits of resolving power, calculated from ganglion cell spacing, range from 2.6 to 4.3 cycles/deg. Summation ratios, assessed by direct comparison of cell densities of photoreceptors (input cells) and ganglion cells (output cells), at more than 150 different loci across the retina, show topographic differences in signal convergence (ranging from 25:1 to over 70:1). Species-specific retinal specializations strongly correlate to the habitat and feeding behavior of each species. Keywords: Visual ecology, Retinal topography, Photoreceptors, Ganglion cells, Elasmobranchs Introduction The elasmobranchs (Chondrichthyes: Elasmobranchii) inhabit all major aquatic realms, from freshwater river systems to the abyssal plains of the deep sea. This vertebrate group has survived as top trophic-level predators of aquatic food webs for more than 300 million years and shows considerable interspecific diversity in morphology, ecology, and behavior (Compagno, 1990; Cortes, 1999). To complement their diverse lifestyles, the sensory systems of elasmobranchs boast a variability of specializations, effectively adapting each species to its ecological niche. The inherent variability in both the spectrum and the intensity of light available for vision, within the aquatic environment, means that visual demands vary substantially between species. Visual systems of aquatic vertebrates show adaptations that optimize vision according to the light environment inhabited and the visual tasks performed (Lythgoe, 1979; Guthrie & Muntz, 1993). Many elasmobranchs have well-developed visual systems, and for some species, vision may play a substantial role in predator–prey interactions, habitat selection, and reproductive behavior (for re- view, see Hart et al., 2006). The visual system of elasmobranchs conforms to the universal vertebrate plan (Fernald, 1988; Sivak, 1991; Bozzano & Collin, 2000; Weissburg & Browman, 2005; Hart et al., 2006). Of partic- ular interest for this study are the photoreceptor and ganglion cells of the retina. The photoreceptor cells constitute the photosensitive elements of the eye, and in the majority of elasmobranchs, both rod and cone cells are present (Gilbert, 1963; Gruber et al., 1963; Hamasaki & Gruber, 1965; Rodieck, 1973; Stell & Witkovsky, 1973b; Gruber et al., 1975; Cohen & Gruber, 1985; Gruber & Cohen, 1985; Hueter, 1991; Hart et al., 2006; Theiss et al., 2006). Rod cells, which are inherently more sensitive to light than cone cells, are designed to detect variations in light intensity in dim- light (scotopic) conditions (Rodieck, 1973). Cone cells function most efficiently in bright-light (photopic) conditions, and some species of elasmobranch (notably rays) have multiple cone types, with spectrally distinct visual pigments (Hart et al., 2004; Theiss et al., 2006). Retinal ganglion cells represent the output stage of the retina. Ganglion cell axons form the optic nerve and convey visual information from the retina to the brain. Similar to other vertebrate groups, elasmobranch ganglion cells can be classified Address correspondence and reprint requests to: Lenore Litherland, Sensory Neurobiology Group, School of Biomedical Science, The Uni- versity of Queensland, Brisbane 4072, Australia. E-mail: l.litherland@ uq.edu.au Visual Neuroscience (2008), 25, 549–561. Printed in the USA. Copyright Ó 2008 Cambridge University Press 0952-5238/08 $25.00 doi:10.1017/S0952523808080693 549 https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0952523808080693 Downloaded from https://www.cambridge.org/core. Department of Agriculture & Fisheries, on 23 Jan 2019 at 04:32:14, subject to the Cambridge Core terms of use, available at