The Influence of Photoreceptor Size and Distribution on Optical Sensitivity in the Eyes of Lanternfishes (Myctophidae)

Abstract

The mesopelagic zone of the deep-sea (200-1000 m) is characterised by exponentially diminishing levels of downwelling sunlight and by the predominance of bioluminescence emissions. The ability of mesopelagic organisms to detect and behaviourally react to downwelling sunlight and/or bioluminescence will depend on the visual task and ultimately on the eyes and their capacity for detecting low levels of illumination and intermittent point sources of bioluminescent light. In this study, we investigate the diversity of the visual system of the lanternfish (Myctophidae). We focus specifically on the photoreceptor cells by examining their size, arrangement, topographic distribution and contribution to optical sensitivity in 53 different species from 18 genera. We also examine the influence(s) of both phylogeny and ecology on these photoreceptor variables using phylogenetic comparative analyses in order to understand the constraints placed on the visual systems of this large group of mesopelagic fishes at the first stage of retinal processing. We report great diversity in the visual system of the Myctophidae at the level of the photoreceptors. Photoreceptor distribution reveals clear interspecific differences in visual specialisations (areas of high rod photoreceptor density), indicating potential interspecific differences in interactions with prey, predators and/or mates. A great diversity in photoreceptor design (length and diameter) and density is also present. Overall, the myctophid eye is very sensitive compared to other teleosts and each species seems to be specialised for the detection of a specific signal (downwelling light or bioluminescence), potentially reflecting different visual demands for survival. Phylogenetic comparative analyses highlight several relationships between photoreceptor characteristics and the ecological variables tested (depth distribution and luminous tissue patterns). Depth distribution at night was a significant factor in most of the models tested, indicating that vision at night is of great importance for lanternfishes and may drive the evolution of their photoreceptor design.

Retinal specialization through spatially varying cell densities and opsin coexpression in cichlid fish

“…Following the protocols described in de Busserolles et al (2014aBusserolles et al ( , 2014b, topographic distribution of single cones, double cones, total cones and ganglion cells were assessed using the optical fractionator technique (West, 1991) modified by Coimbra et al (2009Coimbra et al ( , 2012 for use in retinal whole mounts. Briefly, for each whole mount, the outline of the retina was digitized using a ×5 objective (numerical aperture 0.16) mounted on a compound microscope (Zeiss Imager.Z2) equipped with a motorized stage (MAC 6000 System, Microbrightfield, USA), a digital colour camera (Microbrightfield) and a computer running StereoInvestigator software (Microbrightfield).…”

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

“…In addition to the generalist specialization, L. parvicauda does not appear to possess a very sensitive visual system due to its relatively small eyes [de Busserolles et al, 2013] and low summation ratios (around 20: 1 in the peak area and 50: 1 in the periphery) compared to other myctophids (i.e. M. brachygnathum 200: 1 in the peak area and 500: 1 in the non-specialized region) [de Busserolles et al, 2014b;this study]. Even though L. parvicauda possesses adaptations to enhance photon capture over the whole retina (i.e.…”

“…In a relatively dark environment, where inter-specific interactions are mostly achieved through bright, bioluminescent flashes, as found in the mesopelagic zone, sensitivity may have become more important than acuity. As most lanternfishes possess very sensitive eyes [de Busserolles et al, 2014b], prey detection at longer distances is most likely achieved by the detection of a light signal or through the use of other sensory systems (olfaction or audition), with acuity only playing a role at close range.…”

“…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].…”

Disruptive colouration in reef fish: does matching the background reduce predation risk?

“…Retinal whole-mounts were generated by removing the retina from the eye, fixing the tissue and then mounting the entire retina on a slide with the photoreceptors pointing towards the viewer. Photoreceptors were then counted using specialised software on a modified microscope, using design-based stereology methods similar to those previously published elsewhere (Coimbra et al, 2012;de Busserolles et al, 2014a;Ullmann et al, 2012) and described in detail in the Appendix.…”