Retinal specialisations in the dogfish <i>Centroscymnus coelolepis</i> from the Mediterranean deep-sea

Abstract

SUMMARY: The present work attempted to study the importance of vision in Centroscymnus coelolepis, the most abundant shark in the Mediterranean beyond a depth of 1000 m, by using anatomical and histological data. C. coelolepis exhibited large lateral eyes with a large pupil, spherical lens and a tapetum lucidum that gave the eye a strong greenish-golden "eye shine". In the outer retinal layer, a uniform population of rod-like photoreceptors was observed while in the vitreal retina a thick inner plexiform layer comprised up to 30% of the whole retinal thickness. The cell distribution of the ganglion cell layer formed a thin elongated visual streak in the central plane of the eye that provided a horizontal panoramic field of view. A specialised area of higher visual acuity was located caudally at 32-44º from the geometric centre of the retina and 5-10º above the horizontal plane of the eye. This position indicated that the visual axis pointed in a slightly outward-forward direction with respect to the fish body axis. A non-uniform distribution of large ganglion cells was also found in the horizontal plane of the retina that practically coincided with the distribution of the total cell population in the ganglion cell layer. This is the first time that this type of retinal specialisation has been observed in the elasmobranchs. These characteristics indicate that the retina of C. coelolepis is designed not only to increase sensitivity in the horizontal field of view, as was also observed in other sharks, but also to improve motion detection in the same plane. The visual capacities evolved by C. coelolepis make this species adapted for discriminating the horizontal gradation of light that exists in the mesopelagic environment. Similarly, the large ganglion cell distribution observed in its retina seems to be related to its predatory behaviour, since it allows this shark to perceive the movement of bioluminescent prey against a totally dark background.Key words: deep-sea shark, retinal morphology, retinal topography, large ganglion cells, visual axes, diet. RESUMEN: ESPECIALIZACIONES EN LA RETINA DEL TIBURÓN CENTROSCYMNUS COELOLEPIS DEL MEDITERRÁNEO PROFUNDO. -El presente trabajo estudia la importancia de la visión en Centroscymnus coelolepis, el tiburón más abundante en el Mediterráneo por debajo de los 1000 m de profundidad, usando datos anatómicos e histológicos. C. coelolepis posee grandes ojos laterales, una pupila muy ancha, un cristalino esférico y un tapetum lucidum que confiere al ojo un fuerte brillo verde-dorado. En la capa externa de la retina, se observa una población uniforme de fotorreceptores parecidos a los bastones, mientras en la capa interna el estrato plexiforme interno es grueso, ocupando hasta el 30% del entero grosor de la retina. La distribución de las células en la capa ganglionar forma una sutil franja horizontal alargada en correspondencia del plano central del ojo que permite al animal una visión panorámica horizontal. Caudalmente se localizó una área especializada de mejor agudeza visual a...

Relative Eye Size in Elasmobranchs

“…This is supported by the fact that the eyes of the few mesopelagic and bathypelagic elasmobranch species that have been studied contain large numbers of rod photoreceptors, tapetums and relatively low densities of retinal ganglion cells, which are topographically arranged into horizontal streaks of increased cell density, an adaptation for sampling the 'horizon' (i.e., the substrate-water interface, or the horizontal gradient of light in the water column) with an increased spatial resolving power [Bozzano and Collin, 2000;Bozzano et al, 2001;Bozzano, 2004]. However, some mesopelagic and bathypelagic sharks do feed on bioluminescent prey [Bozzano and Collin, 2000;Bozzano et al, 2001;Bozzano, 2004], and sharks from the families Dalatiidae and Etmopteridae known to be bioluminescent themselves [Seigel, 1978;Bone and Marshall, 1982]. Therefore the detection of bioluminescence may be of some importance to these animals and is perhaps mediated by specific areae of increased retinal ganglion cell density, which are found within the horizontal streaks [Bozzano and Collin, 2000;Bozzano, 2004].…”

“…However, some mesopelagic and bathypelagic sharks do feed on bioluminescent prey [Bozzano and Collin, 2000;Bozzano et al, 2001;Bozzano, 2004], and sharks from the families Dalatiidae and Etmopteridae known to be bioluminescent themselves [Seigel, 1978;Bone and Marshall, 1982]. Therefore the detection of bioluminescence may be of some importance to these animals and is perhaps mediated by specific areae of increased retinal ganglion cell density, which are found within the horizontal streaks [Bozzano and Collin, 2000;Bozzano, 2004]. It should be noted, however, that the peak retinal ganglion cell densities of these areae (and therefore the anatomical visual acuity) reported for elasmobranchs that live in the lower mesopelagic and bathypelagic zones are much lower than those reported for foveate teleost fishes that occupy the same habitats [Warrant and Locket, 2004].…”

“…Although the process of preservation (fixation in 10% formalin and storage in ethanol; J. Johnston, personal communication) is likely to result in some shrinkage, the tough cartilaginous sclera of elasmobranch eyeballs is resistant to substantial changes in shape [Hueter, 1980] and the shrinkage of elasmobranch eyeballs that have been measured fresh and have then been fixed in 10% formalin for over five years is less than 2% [T.J. Lisney, unpublished data]; B = from Bozzano [2004]; C = direct measurement from fresh specimens; D = from Howland et al [2004]. Body mass values marked with an asterisk (*) were calculated using length-mass relationships from http://www.fishbase.org.…”

Retinal Ganglion Cell Distribution and Spatial Resolving Power in Elasmobranchs

“…Retinal topography has been described in less than 20 of the approximately 1,100 species of living chondrichthyan [Peterson and Rowe, 1980;Collin, 1988Collin, , 1999Hueter, 1991;Bozzano and Collin, 2000;Bozzano, 2004;Theiss et al, 2007]. An elongated, horizontal streak of increased cell density that stretches across the retinal meridian, containing either a single 'area centralis' (a specific concentric area of increased cell density) or multiple 'areae', is the prominent feature in the majority of species investigated thus far.…”

“…Therefore the retinal ganglion cell mosaic acts as an information 'bottleneck' and places a theoretical upper limit on the spatial resolving power of the eye [Thibos et al, 1987;Pettigrew et al, 1988;Collin and Pettigrew, 1989]. Numerous studies have used ganglion cell spacing in the areas of highest cell density, in combination with a measure of the focal length of the eye, to determine spatial resolving power in a range of fish species [e.g., Collin and Pettigrew, 1989;Collin and Northcutt, 1993;Collin and Ali, 1994;Collin and Partridge, 1996;Wagner et al, 1998;Fritsches et al, 2003;Bailes et al, 2006], including a small number of elasmobranchs [Bozzano and Collin, 2000;Bozzano, 2004;Theiss et al, 2007].…”