A Comparative Study of the Distribution and Density of Retinal Ganglion Cells and Visual Acuity in Bothrops Snakes with Differences in the Habitat Use

Abstract

Purpose: The density and distribution of neurons in retinas of vertebrates are associated with specific behaviors and species ecology. The visual system of snakes has adaptations to the species’ habitats, circadian rhythm, and foraging strategies. A previous study revealed a ventral area centralis in a terrestrial snake and a visual streak in a close related arboreal species. In this study, we compared the distribution of ganglion cell layer (GCL) cells in retinas of Viperidae snakes from the genus Bothrops, with differences in the habitat use, namely the arboreal B. insularis, and the semi-arboreal species B. jararaca and B. sazimai. Methods: Three individuals of each species were euthanized with Thionembutal (100 mg/kg). The eyes were enucleated and retinas were dissected and fixed in 4% paraformaldehyde. Retinas were wholemounted and Nissl stained. The density of GCL cells was estimated using a stereological approach with the Stereo Investigator software (MicroBrightField), and isodensity maps were obtained using OriginPro 8.5.1. Visual acuity values were estimated based on the peak density of GCL cells and the eyes focal length. Results: We observed a poorly defined horizontal streak in retinas of the arboreal B. insularis, with higher density in the central retina, while in the semi-arboreal B. jararaca and B. sazimai there were no defined retinal specializations, and the peak cell densities were located in the temporal region. The mean cell density was 4,405 ± 735 cells/mm2 in B. insularis, 4,606 ± 335 cells/mm2 in B. sazimai, and 4,881 ± 746cells/mm2 in B. jararaca. The estimated spatial resolutions were similar among the species and varied from 2.0 to 2.2 cycles per degree. Conclusions: These findings reinforce the hypothesis that retinal specializations are associated with habitat use in snakes. A visual streak may assist in locomotion and hunting among branches, as indicated by the distribution of cells in B. insularis. On the other hand, peak GCL cell density in the temporal retina may facilitate striking behavior in the species that forage on the ground