Multiple cone visual pigments and the potential for trichromatic colour vision in two species of elasmobranch

Abstract

SUMMARY Elasmobranchs (sharks, skates and rays) are the modern descendents of the first jawed vertebrates and, as apex predators, often occupy the highest trophic levels of aquatic (predominantly marine) ecosystems. However, despite their crucial role in the structure of marine communities, their importance both to commercial and to recreational fisheries, and the inherent interest in their role in vertebrate evolution, very little is known about their visual capabilities, especially with regard to whether or not they have the potential for colour vision. Using microspectrophotometry, we show that the retinae of the giant shovelnose ray (Rhinobatos typus) and the eastern shovelnose ray (Aptychotrema rostrata) contain three spectrally distinct cone visual pigments with wavelengths of maximum absorbance(λmax) at 477, 502 and 561 nm and at 459, 492 and 553 nm,respectively. The retinae of R. typus and A. rostrata also contain a single type of rod visual pigment with λmax at 504 and 498 nm, respectively. R. typus, living in the same estuarine waters as A. rostrata, were found to have identical visual pigments to R. typus inhabiting coral reef flats, despite a considerable difference in habitat spectral radiance. This is the first time that multiple cone visual pigments have been measured directly in an elasmobranch. The finding raises the possibility that some species are able to discriminate colour – a visual ability traditionally thought to be lacking in this vertebrate class – and it is evident that the visual ecology of elasmobranchs is far more complex than once thought.

Behavioural evidence for colour vision in an elasmobranch

“…Moreover, colour-opponent responses were recorded from horizontal cells in the retina of the red stingray, Dasyatis akajei (Toyoda et al, 1978), and recent MSP studies have reported the presence of up to three spectrally distinct cone types in three ray species, including G. typus (Hart et al, 2004;Theiss et al, 2007). The results obtained from the present study suggest that G. typus, and most likely other rays with multiple cone types, are capable of discriminating a coloured reward stimulus from a range of different coloured distracter stimuli of varying brightness.…”

“…This is the first conclusive behavioural evidence that any elasmobranch species possesses colour vision. Experiments are underway to investigate the dimensionality of colour vision of G. typus and establish whether this species has a trichromatic visual system based on the three cone types identified using MSP (Hart et al, 2004).…”

“…The evidence for more than one spectral cone type in the ray retina, however, is more convincing, with studies indicating the presence of more than one photopic cone-based mechanism (Govardovskii and Lychakov, 1977;Toyoda et al, 1978). Recently, data obtained using MSP have indicated the presence of up to three spectrally distinct cone pigments in the retina of the giant shovelnose ray, Glaucostegus typus [wavelength of maximum absorbance ( max )477, 502 and 561nm], the eastern shovelnose ray, Aptychotrema rostrata ( max 459, 492 and 553nm) (Hart et al, 2004), and the bluespotted maskray, Neotrygon (Dasyatis) kuhlii ( max 476, 498 and 552nm) (Theiss et al, 2007). These findings raise the possibility that rays have a potentially trichromatic colour vision system.…”

“…Stimuli were chosen based on the known spectral properties of the cone visual pigments of G. typus (Hart et al, 2004). For each cone type, the relative quantum catches (Q) for all coloured reward stimuli, distracter stimuli and the grey background of the Perspex board used in the experiments were calculated as the product of the spectral reflectance (S) of the coloured stimulus (Fig.2A,B), the spectral sensitivity (R) of the cone type corrected for axial path length and the transmittance of the ocular media (Fig.2C), and the irradiance (I) in the experimental arena (Fig.2D) as per Eqn 1 (Vorobyev and Osorio, 1998;Kelber et al, 2003):…”

World in Motion: Perception and Discrimination of Movement in Juvenile Grey Bamboo Sharks (Chiloscyllium griseum)

“…To some extent, this is due to evolutionary differences in the vertebrate eye itself such as spatial or temporal sampling or resolving power (e.g., mammals : Coimbra, Hart, Collin, & Manger, 2013;Hughes, 1977;Mengual, García, Segovia, & Pertusa, 2015;birds: Coimbra, Nolan, Collin, & Hart, 2012;Fite & Rosenfield-Wessels, 1975;Hodos & Leibowitz, 1977;elasmobranchs: Hueter, 1990;Lisney & Collin, 2007Ryan, Hart, Collin, & Hemmi, 2016;Ryan, Hemmi, Collin, & Hart, 2017;Theiss, Collin, & Hart, 2010), cone monochromacy or multichromacy (for review see Osorio & Vorobyev, 2008; see also Bedore et al, 2013;Hart, Lisney, Marshall, & Collin, 2004;Hart, Theiss, Harahush, & Collin, 2011;Van-Eyk, Siebeck, Champ, Marshall, & Hart, 2011), photoreceptor topography (Collin, 1999(Collin, , 2008, the composition of the dioptric system (Collin & Collin, 2001;Hueter et al, 2001;Sivak, 1990) or other adaptive ocular specializations. Moreover, there are differences in the neural processing of visual information in the brain.…”