Interspecific Visual Adaptations among Wobbegong Sharks (Orectolobidae)

Abstract

Several visual traits have previously been assessed in elasmobranchs; however, few studies have examined and compared multiple visual attributes within a particular genus. The primary advantage of studying closely related species is that any differences between them are more likely to reflect functional ecological adaptations rather than the effects of phylogenetic separation. In this study, the visual capabilities of 4 wobbegong shark species, which vary in life-history and/or habitat, were examined: the western wobbegong (Orectolobus hutchinsi), the spotted wobbegong (O. maculatus), the ornate wobbegong (O. ornatus) and the dwarf spotted wobbegong (O. parvimaculatus). The retinae of all 4 wobbegong species are duplex; rod and cone photoreceptors can be distinguished easily on the basis of morphology. Some variation in relative eye size exists, with O. parvimaculatus possessing the largest eyes. The topographic distribution of cells within the ganglion cell layer of O. hutchinsi reveals a weakly elongated central visual streak of increased cell density, mediating a higher spatial resolving power of 2.06 cycles deg^–1 in the frontal visual field. Retinal topography of O. maculatus and O. parvimaculatus is similar, with both possessing a dorsal horizontal streak facilitating an increased spatial resolving power of 3.51 cycles deg^–1 and 3.91 cycles deg^–1, respectively, in the lower visual field. O. parvimaculatus also possesses an area of increased cell density in the naso-ventral region of the retina, mediating acute vision in the upper caudal region of the visual field. While all 4 species have visual systems optimised for increased visual sensitivity, O. maculatus and O. parvimaculatus appear to be particularly well suited to activity under low light conditions.

Vision in elasmobranchs and their relatives: 21st century advances

“…Some elasmobranchs are capable of extensive pupillary movements and exhibit a wide and varied range of pupil shapes (Hart et al , 2006; McComb & Kajiura, 2008; Litherland et al , 2009 a ; McComb et al , 2009; Theiss et al , 2010; also see Fig. 1).…”

“…Chondrichthyans have received more attention in recent years in terms of retinal topography, with most studies focusing on the distribution of RGCs (Hueter, 1991; Bozzano & Collin, 2000; Bozzano, 2004; Theiss et al , 2007; Lisney & Collin, 2008; Litherland & Collin, 2008; Litherland et al , 2009 b ; Theiss et al , 2010). Clear trends are now evident where, for the most part, RGC topography in elasmobranchs appears to correlate well with their ecology as per the terrain theory of Hughes (1977).…”

“… Isodensity contour maps illustrating the topography of cells in the retinal ganglion cell layer in six species of cartilaginous fish: (a) Carcharhinus amblyrhynchos , (b) Chiloscyllium punctatum , (c) Neotrygon kuhlii , (d) Galeocedo cuvier , (e) Orectolobus hutchinsi and (f) Hydrolagus mirablilis . Isodensity contour maps adapted from (a and b) Lisney & Collin (2008), (c) Theiss et al (2007), (d and f) Bozzano & Collin (2000), (e) Theiss et al (2010). Increases in cell density are shown in progressively lighter shades of grey.…”

“…Orectolobids employ a sit‐and‐wait predatory strategy to ambush highly mobile prey such as teleosts and cephalopods (Huveneers et al , 2007), yet still retain a visual streak (Fig. 6), suggesting that habitat rather than diet may be the driving factor for retinal topography in these animals (Theiss et al , 2010).…”

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.…”