Eye growth in sharks: Ecological implications for changes in retinal topography and visual resolution

Abstract

The visual abilities of sharks show substantial interspecific variability. In addition, sharks may change their habitat and feeding strategy throughout life. As the eyes of sharks continue to grow throughout the animal's lifetime, ontogenetic variability in visual ability may also occur. The topographic analysis of the photoreceptor and ganglion cell distributions can identify visual specializations and assess changes in visual abilities that may occur concurrently with eye growth. This study examines an ontogenetic series of whole-mounted retinas in two elasmobranch species, the sandbar shark, Carcharhinus plumbeus, and the shortspine spurdog, Squalus mitsukurii, to identify regional specializations mediating zones for improved spatial resolution. The study examines retinal morphology and presents data on summation ratios between photoreceptor and ganglion cell layers, anatomically determined peak spatial resolving power, and the angular extent of the visual field. Peak densities of photoreceptors and ganglion cells occur in similar retinal locations. The topographic distribution of neurons in the ganglion cell layer does not differ substantially with eye growth. However, predicted peak spatial resolution increases with eye growth from 4.3 to 8.9 cycles/deg in C. plumbeus and from 5.7 to 7.2 cycles/deg in S. mitsukurii. The topographic distribution of different-sized ganglion cells is also mapped in C. plumbeus, and a population of large ganglion cells (soma area 120-350 microm2) form a narrow horizontal streak across the retinal meridian, while the spatial distribution of ordinary-sized ganglion cells (soma area 30-120 microm2) forms an area in the central retina. Species-specific retinal specializations highlight differences in visually mediated behaviors and foraging strategies between C. plumbeus and S. mitsukurii.