The eyes of lanternfishes (Myctophidae, Teleostei): Novel ocular specializations for vision in dim light

Abstract

Lanternfishes are one of the most abundant groups of mesopelagic fishes in the world's oceans and play a critical role in biomass vertical turnover. Despite their importance, very little is known about their physiology or how they use their sensory systems to survive in the extreme conditions of the deep sea. In this study, we provide a comprehensive description of the general morphology of the myctophid eye, based on analysis of 53 different species, to understand better their visual capabilities. Results confirm that myctophids possess several visual adaptations for dim-light conditions, including enlarged eyes, an aphakic gap, a tapetum lucidum, and a pure rod retina with high densities of long photoreceptors. Two novel retinal specializations were also discovered. The first specialization is a fundal pigmentation in adult eyes, found within an isolated retinal region (typically central retina) composed of modified pigment epithelial cells, which we hypothesize to be the remnant of a more pronounced visual specialization important in larval stages. The second specialization is an aggregation of extracellular microtubular-like structures found within the sclerad region of the inner nuclear layer of the retina. We hypothesize that the marked interspecific differences in the hypertrophy of these microtubular-like structures may be related to inherent differences in visual function. A general interspecific variability in other parts of the eye is also revealed and examined in this study. The contribution of both ecology and phylogeny to the evolution of ocular specializations and vision in dim light are discussed.

Retinal Ganglion Cell Distribution and Spatial Resolving Power in Deep-Sea Lanternfishes (Myctophidae)

“…Even though L. parvicauda possesses adaptations to enhance photon capture over the whole retina (i.e. circumlental aphakic gap and tapetum lucidum) [de Busserolles et al, 2014a], these findings indicate that this species possesses a less specialized visual system than the 2 other species mentioned above. Wagner [2001] investigated brain areas in mesopelagic fishes and showed that different myctophid species rely more or less heavily on different sensory systems.…”

“…6 ). The area temporalis found in D. mollis (this study), associated with the presence of a nasal aphakic gap [de Busserolles et al, 2014a], provides the potential for binocular vision ( fig. 6 ) and may enhance acuity directly in the illuminated region in front of the fish, a powerful predatory strategy.…”

“…Myctophids also show marked intra-and interspecific variation in the depths they occupy [Karnella, 1987], their migration patterns [Watanabe et al, 1999] and the location of their luminous organs [Nafpaktitis and Nafpaktitis, 1969;Paxton, 1972;Nafpaktitis et al, 1977Nafpaktitis et al, , 1978Zahuranec, 2000;Herring, 2007;de Busserolles et al, 2013]. Recently, marked differences in the visual system of this large group of fishes have been revealed [de Busserolles et al, 2013[de Busserolles et al, , 2014a, including large variations in photoreceptor distribution across the retina [de Busserolles et al, 2014b].…”

Spectral Tuning in the Eyes of Deep-Sea Lanternfishes (Myctophidae): A Novel Sexually Dimorphic Intra-Ocular Filter

“…Absorbance spectra (330-800 nm) were made using a computer-controlled single-beam wavelength-scanning microspectrophotometer [Hart et al, 2004[Hart et al, , 2011[Hart et al, , 2012. Due to the very small diameter of the rod photoreceptors of the lanternfish species analysed (<1 μm [de Busserolles et al, 2014b]), longitudinal 'endon' absorbance spectra were measured from patches of rod outer segments. A sample scan was made by aligning the measuring beam (typical dimensions 10 × 10 μm) within a patch of rods in a specific part of the retina and recording the amount of light transmitted at each wavelength across the spectrum.…”

“…We used visual pigment templates [Govardovskii et al, 2000] of appropriate λ max for the modelling. Normalised absorbance templates were converted to axial outer segment absorptance by assuming a visual pigment specific (decadic) absorbance of 0.013 μm -1 (rhodopsin [Turner et al, 2009]) and a rod outer segment length of 39 μm for S. evermanni [de Busserolles et al, 2014b] and 45 μm for M. obtusirostre as per a similar species ( M. brachygnathum [de Busserolles et al, 2014b]). Measurements of ocular media transmittance could not be made from fresh specimens at sea and so were excluded from the modelling.…”