Retinal Morphology and Visual Specializations in Three Species of Chimaeras, the Deep-Sea R. pacifica and C. lignaria, and the Vertical Migrator C. milii (Holocephali)

Abstract

The majority of holocephalans live in the mesopelagic zone of the deep ocean, where there is little or no sunlight, but some species migrate to brightly lit shallow waters to reproduce. This study compares the retinal morphology of two species of deep-sea chimaeras, the Pacific spookfish (Rhinochimaera pacifica) and the Carpenter’s chimaera (Chimaera lignaria), with the elephant shark (Callorhinchus milii), a vertical migrator that lives in the mesopelagic zone but migrates to shallow water to reproduce. The two deep-sea chimaera species possess pure rod retinae with long photoreceptor outer segments that might serve to increase visual sensitivity. In contrast, the retina of the elephant shark possesses rods, with an outer-segment length significantly shorter (a mean of 34 µm) than in the deep-sea species, and cones, and therefore the potential for color vision. The retinal ganglion cell distribution closely follows that of the photoreceptor populations in all three species, but there is a lower peak density of these cells in both deep-sea species (215–275 cells/mm2 vs. 769 cells/mm2 in the elephant shark), which represents a significant increase in the convergence of visual information (summation ratio) from photoreceptors to ganglion cells. It is evident that the eyes of deep-sea chimaeras have increased sensitivity to detect objects under low levels of light, but at the expense of both resolution and the capacity for color vision. In contrast, the elephant shark has a lower sensitivity, but the potential for color discrimination and a higher visual acuity.