Vision in the southern hemisphere lampreyMordacia mordax: Spatial distribution, spectral absorption characteristics, and optical sensitivity of a single class of retinal photoreceptor

Abstract

The dorso-laterally located eyes of the southern hemisphere lamprey Mordacia mordax (Agnatha) contain a single morphological type of retinal photoreceptor, which possesses ultrastructural characteristics of both rods and cones. This photoreceptor has a large refractile ellipsosome in the inner segment and a long cylindrical outer segment surrounded by a retinal pigment epithelium that contains two types of tapetal reflectors. The photoreceptors form a hexagonal array and attain their peak density (33,200 receptors0mm 2 ) in the ventro-temporal retina. Using the size and spacing of the photoreceptors and direct measures of aperture size and eye dimensions, the peak spatial resolving power and optical sensitivity are estimated to be 1.7 cycles deg Ϫ1 (minimum separable angle of 34 ' 7 '' ) and 0.64 mm 2 steradian (white light) and 1.38 mm 2 steradian (preferred wavelength or l max ), respectively. Microspectrophotometry reveals that the visual pigment located within the outer segment is a rhodopsin with a wavelength of maximum absorbance (l max ) at 514 nm. The ellipsosome has very low absorptance (Ͻ0.05) across the measured spectrum (350-750 nm) and probably does not act as a spectral filter. In contrast to all other lampreys studied, the optimized receptor packing, the large width of the ellipsosome-bearing inner segment, together with the presence of a retinal tapetum in the photophobic Mordacia, all represent adaptations for low light vision and optimizing photon capture.

Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup

“…A smooth transition of features from stage to stage is apparent, compatible with the sequential acquisition of these features in ancestral forms. The stages we have illustrated are: the ascidian larva ocellus 58,77 , the hagfish eye 36,[39][40][41][42][43] , the lamprey pineal organ 48,78,79 , the lamprey retina 36,[80][81][82][83][84][85] and the jawedvertebrate retina.…”

Retinal Amino Acid Neurochemistry of the Southern Hemisphere Lamprey, Geotria australis

“…However, upstream migrants (older fish returning from the sea into freshwater to breed) have retinas dominated by large photoreceptor cells [30], [31], [37]. The yellow myeloid pigment present in one of the photoreceptor types (C2) of the downstream migrants is also replaced in the upstream migrating G. australis with a large unpigmented ellipsosome, resulting in a shift in the peak spectral sensitivity (λ max ) from 492 nm to 552 nm [30], [32], [38]. These changes possibly reflect selective pressures produced by the changing light environment as adult lampreys in the ocean avoid avian predators at the surface when they move back up to their natal streams by adopting a scotopic lifestyle [3], [30].…”

Retinal temporal resolution and contrast sensitivity in the parasitic lampreyMordacia mordaxand its non-parasitic derivativeM.praecox

“…FFF) is greater in the fully metamorphosed M. mordax, as these individuals are parasitic and require vision to detect prey, whereas the mature non-parasitic derivative M. praecox requires no such ability as this species does not feed after completing the larval phase. As there is morphological evidence to suggest that the retina of M. mordax contains only one photoreceptor type (Collin and Potter, 2000;Collin et al, 2004), we hypothesise that all retinal photoreceptors will exhibit the same temporal response characteristics. Our results provide only the second recorded cFFF values and the first quantification of CS for agnathan fishes.…”

“…by the low anatomical spatial resolving power of 1.7 cycles deg −1 in the downstream migrant of M. mordax (Collin et al, 2004). The possession of a retinal tapetum (Collin and Potter, 2000) also increases sensitivity by effectively doubling the length of the outer segment, which suggests that there is more visual pigment available for light absorption (Land and Nilsson, 2012;Rovamo and Raninen, 1988).…”

“…The retina of M. mordax possesses adaptations that increase optical sensitivity including: (1) a reflective tapetum within the retinal pigment epithelium (Collin and Potter, 2000), (2) a large single rod-like photoreceptor with a long outer segment (Collin and Potter, 2000;Collin et al, 2004), and (3) a large ellipsosome within the inner segment of the photoreceptor that would focus (refract) light onto the outer segment (Collin and Potter, 2000). In spite of the uniqueness of the visual system of this lamprey species, and despite the detailed knowledge of retinal morphology in M. mordax, there have been no studies on the physiology of their visual system.…”