Morphological Plasticity of the Retina of Viperidae Snakes Is Associated With Ontogenetic Changes in Ecology and Behavior.

Juliana H Tashiro,Dora F Ventura,Einat Hauzman

doi:10.3389/fnana.2021.770804

Abstract

Snakes of the Viperidae family have retinas adapted to low light conditions, with high packaging of rod-photoreceptors containing the rhodopsin photopigment (RH1), and three types of cone-photoreceptors, large single and double cones with long-wavelength sensitive opsins (LWS), and small single cones with short-wavelength sensitive opsins (SWS1). In this study, we compared the density and distribution of photoreceptors and ganglion cell layer (GCL) cells in whole-mounted retinas of two viperid snakes, the lancehead Bothrops jararaca and the rattlesnake Crotalus durissus, and we estimated the upper limits of spatial resolving power based on anatomical data. The ground-dwelling C. durissus inhabits savannah-like habitats and actively searches for places to hide before using the sit-and-wait hunting strategy to ambush rodents. B. jararaca inhabits forested areas and has ontogenetic changes in ecology and behavior. Adults are terrestrial and use similar hunting strategies to those used by rattlesnakes to prey on rodents. Juveniles are semi-arboreal and use the sit-and-wait strategy and caudal luring to attract ectothermic prey. Our analyses showed that neuronal densities were similar for the two species, but their patterns of distribution were different between and within species. In adults and juveniles of C. durissus, cones were distributed in poorly defined visual streaks and rods were concentrated in the dorsal retina, indicating higher sensitivity in the lower visual field. In adults of B. jararaca, both cones and rods were distributed in poorly defined visual streaks, while in juveniles, rods were concentrated in the dorsal retina and cones in the ventral retina, enhancing sensitivity in the lower visual field and visual acuity in the upper field. The GCL cells had peak densities in the temporal retina of C. durissus and adults of B. jararaca, indicating higher acuity in the frontal field. In juveniles of B. jararaca, the peak density of GCL cells in the ventral retina indicates better acuity in the upper field. The estimated visual acuity varied from 2.3 to 2.8 cycles per degree. Our results showed interspecific differences and suggest ontogenetic plasticity of the retinal architecture associated with changes in the niche occupied by viperid snakes, and highlight the importance of the retinal topography for visual ecology and behavior of snakes.

Highlights

The highly diverse group of Snakes, with more than 3,800 species (Uetz et al, 2020) has a fascinating diversity of retinal morphology, especially regarding the photoreceptor types (Walls, 1942; Underwood, 1967a, 1970; Caprette, 2005; Hauzman et al, 2017; Hauzman, 2020)
In juveniles of B. jararaca the ganglion cell layer (GCL) cells were concentrated in the ventral retina with a decreasing ventral-dorsal gradient and peak density located in the ventral area (Figure 10 and Supplementary Figure 6)
Interspecific differences in the density and distribution of retinal neurons were identified in the viperid snakes B. jararaca and C. durissus

Summary

Introduction

The highly diverse group of Snakes, with more than 3,800 species (Uetz et al, 2020) has a fascinating diversity of retinal morphology, especially regarding the photoreceptor types (Walls, 1942; Underwood, 1967a, 1970; Caprette, 2005; Hauzman et al, 2017; Hauzman, 2020). This group represents a valuable model to test hypotheses of correlation between the types of retinal specialization and species ecology and behavior. Two main types of retinal specializations, visual streak and area centralis, were described in many vertebrates and are usually associated with the habitat occupied by the species (Hughes, 1977; Moore et al, 2017). Areae centrales are concentric regions of higher cell density usually found in species that occupy closed environments such as forests, where the horizon is obstructed by vegetation (Hughes, 1977; Collin, 2008; Moore et al, 2017)

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