The eyes of five ray species (Taeniura lymma, Neotrygon kuhlii, Pastinachus atrus, Himantura uarnak and Urogymnus asperrimus) from the same taxonomic family (Dasyatidae) and the same geographic region (Ningaloo Reef, Western Australia) were studied to identify differences in retinal specializations that may reflect niche specialization. The topographic distributions of photoreceptors (rods and all cones) and ganglion cells were assessed and used to identify localized peaks in cell densities that indicate specializations for acute vision. These data were also used to calculate summation ratios of photoreceptors to ganglion cells in each species and estimate the anatomical spatial resolving power of the eye. Subtle differences in the distribution of retinal neurons appear to be related to the ecology of these closely related species of stingrays. The main specialization in the retinal cell density distribution is the dorsal streak that allows these animals to scan the substrate for potential prey. The blue-spotted fantail ray, T. lymma, showed the highest peak density of rods (86,700 rods mm-2) suggesting a specialization for scotopic vision. The highest peak density of cones (9,970 cones mm-2) was found in H. uarnak, and the highest peak density of ganglion cells (4,500 cells mm-2) was found in P. atrus. The proportion of rods to cones in the dorsal streak was higher in the two smaller species (12.5-14:1 in T. lymma and N. kuhlii) than the larger stingrays (6-8:1 in P. atrus, H. uarnak and U. asperrimus). Visual specializations in different sympatric species are subtle but may reflect specializations to specific ecological niches.

Keywords:
Visual specialization, Retina, Dasyatidae, Ganglion cells, Photoreceptors, Spatial resolving power, Sympatric species, Speciation
1.
Ahnelt PK, Schubert C, Kubber-Heiss A, Schiviz A, Anger E (2006): Independent variation of retinal S and M cone photoreceptor topographies: a survey of four families of mammals. Vis Neurosci 23:429-435.
2.
Andrade da Costa BLS, Hokoç JN (2000): Photoreceptor topography of the retina in the New World monkey Cebus apella. Vision Res 40:2395-2409.
3.
Aschliman NC, Nishida M, Miya M, Inoue JG, Rosana KM, Naylor GJ (2012): Body plan convergence in the evolution of skates and rays (Chondrichthyes: Batoidea). Mol Phylogenet Evol 63:28-42.
4.
Blonder BI, Alevizon WS (1988): Prey discrimination and electroreception in the stingray Dasyatis sabina. Copeia 1988:33-36.
5.
Bozzano A (2004): Retinal specialisations in the dogfish Centroscymnus coelolepis from the Mediterranean deep-sea. Sci Mar 68:185-195.
6.
Bozzano A, Collin SP (2000): Retinal ganglion cell topography in elasmobranchs. Brain Behav Evol 55:191-208.
7.
Braekevelt C (1994): Retinal photoreceptor fine structure in the short-tailed stingray. Dasyatis brevicaudata. Histol Histopathol 9:507-514.
8.
Coimbra JP, Trévia N, Marceliano MLV, da Silveira Andrade-Da-Costa BL, Picanço-Diniz CW, Yamada ES (2009): Number and distribution of neurons in the retinal ganglion cell layer in relation to foraging behaviors of tyrant flycatchers. J Comp Neurol 514:66-73.
9.
Collin SP (1988): The retina of the shovel-nosed ray, Rhinobatos batillum (Rhinobatidae): morphology and quantitative analysis of the ganglion, amacrine and bipolar cell populations. Exp Biol 47:195.
10.
Collin SP, Pettigrew JD (1988a): Retinal ganglion-cell topography in teleosts - a comparison between Nissl-stained material and retrograde labeling from the optic-nerve. J Comp Neurol 276:412-422.
11.
Collin SP, Pettigrew JD (1988b): Retinal topography in reef teleosts. I. Some species with well-developed areae but poorly-developed streaks. Brain Behav Evol 31:269-282.
12.
Collin SP, Pettigrew JD (1989): Quantitative comparison of the limits on visual spatial resolution set by the ganglion cell layer in 12 species of reef teleosts. Brain Behav Evol 34:184-192.
13.
Collin SP, Whitehead D (2004): The functional roles of passive electroreception in non-electric fishes. Animal Biol 54:1-25.
14.
Compagno LJV, Dando M, Fowler S (2005): Sharks of the World. Princeton, Princeton University Press.
15.
Connell JH (1978): Diversity in tropical rain forests and coral reefs. Science 199:1302-1310.
16.
Curcio CA, Sloan KR, Kalina RE, Hendrickson AE (1990): Human photoreceptor topography. J Comp Neurol 292:497-523.
17.
Franco ECS, Finlay BL, Silveira LCL, Yamada ES, Crowley JC (2000): Conservation of absolute foveal area in New World monkeys. Brain Behav Evol 56:276-286.
18.
Garza-Gisholt E, Hemmi JM, Hart NS, Collin SP (2014): A comparison of spatial analysis methods for the construction of topographic maps of retinal cell density. PLoS One 9:e93485.
19.
Gruber SH, Cohen JL (1978): Visual system of the elasmobranchs: state of the art 1960-1975; in Hodgson ES, Mathewson RF (eds): Sensory Biology of Sharks, Skates and Rays. Arlington, Technical Information Division, Naval Research Laboratory.
20.
Hamasaki D, Gruber S (1965): The photoreceptors of the nurse shark, Ginglymostoma cirratum and the sting ray, Dasyatis sayi. Bull Mar Sci 15:1051-1059.
21.
Hart NS (2002): Vision in the peafowl (Aves: Pavo cristatus). J Exp Biol 205:3295-3935.
22.
Hart NS, Lisney TJ, Collin SP (2006): Visual communication in elasmobranchs; in Ladich F, Collin SP, Moller P, Kapoor BG (eds): Communication in Fishes. Enfield, Science Publishers.
23.
Heupel MR, Bennett MB (1998): Observations on the diet and feeding habits of the epaulette shark, Hemiscyllium ocellatum (Bonnaterre), on Heron Island Reef, Great Barrier Reef, Australia. Mar Freshwater Res 49:753-756.
24.
Hoegh-Guldberg O (1999): Climate change, coral bleaching and the future of the world's coral reefs. Mar Freshwater Res 50:839-866.
25.
Hueter RE (1991): Adaptations for spatial vision in sharks. J Exp Zool 256:130-141.
26.
Hueter RE, Murphy CJ, Howland M, Sivak JG, Paul-Murphy JR, Howland HC (2001): Refractive state and accommodation in the eyes of free-swimming versus restrained juvenile lemon sharks (Negaprion brevirostris). Vision Res 41:1885-1889.
27.
Hughes A (1975): A comparison of retinal ganglion cell topography in the plains and tree kangaroo. J Physiol 244:61P.
28.
Kempster RM, Garza-Gisholt E, Egeberg CA, Hart NS, O'Shea OR, Collin SP (2013): Sexual dimorphism of the electrosensory system: a quantitative analysis of nerve axons in the dorsal anterior lateral line nerve of the blue-spotted fantail stingray (Taeniura lymma). Brain Behav Evol 81:226-235.
29.
Kleypas JA, Mcmanus JW, Menez LAB (1999): Environmental limits to coral reef development: where do we draw the line? Am Zool 39:146-159.
30.
Last PR, Stevens JD (2009): Sharks and Rays of Australia. Collingwood, Csiro Publishing.
31.
Lisney TJ, Collin SP (2007): Relative eye size in elasmobranchs. Brain Behav Evol 69:266-279.
32.
Lisney TJ, Collin SP (2008): Retinal ganglion cell distribution and spatial resolving power in elasmobranchs. Brain Behav Evol 72:59-77.
33.
Litherland L, Collin SP (2008): Comparative visual function in elasmobranchs: spatial arrangement and ecological correlates of photoreceptor and ganglion cell distributions. Vis Neurosci 25:549-561.
34.
Logiudice FT, Laird RJ (1994): Morphology and density distribution of cone photoreceptor in the retina of the Atlantic stingray, Dasyatis sabina. J Morphol 221:277-289.
35.
Lythgoe JN (1979): The Ecology of Vision. Oxford, Clarendon Press.
36.
Marshall AD, Kyne PM, Bennett MB (2008): Comparing the diet of two sympatric urolophid elasmobranchs (Trygonoptera testacea Müller and Henle and Urolophus kapalensis Yearsley and Last): evidence of ontogenetic shifts and possible resource partitioning. J Fish Biol 72:883-898.
37.
Marshall NJ, Jennings K, McFarland WN, Loew ER, Losey GS, Montgomery WL (2003): Visual biology of Hawaiian coral reef fishes. III. Environmental light and an integrated approach to the ecology of reef fish vision. Copeia 2003:467-480.
38.
Marshall NJ, Vorobyev M (2003): The design of color signals and color vision in fishes; in Collin SP, Marshall NJ (eds): Sensory Processing in Aquatic Environments. New York, Springer.
39.
Matthiessen L (1880): Untersuchungen über den Aplanatismus und die Periscopie der Krystalllinsen in den Augen der Fische. Pflügers Arch Eur J Physiol 21:287-307.
40.
McComb DM, Kajiura SM (2008): Visual fields of four batoid fishes: a comparative study. J Exp Biol 211:482-490.
41.
McGowan DW, Kajiura SM (2009): Electroreception in the euryhaline stingray, Dasyatis sabina. J Exp Biol 212:1544-1552.
42.
Meredith TL, Kajiura SM (2010): Olfactory morphology and physiology of elasmobranchs. J Exp Biol 213:3449-3456.
43.
O'Shea OR, Thums M, Van Keulen M, Kempster RM, Meekan MG (2013): Dietary partitioning by five sympatric species of stingray (Dasyatidae) on coral reefs. J Fish Biol 82:1805-1820.
44.
Packer O, Hendrickson AE, Curcio CA (1989): Photoreceptor topography of the retina in the adult pigtail macaque (Macaca nemestrina). J Comp Neurol 288:165-183.
45.
Pankhurst PM, Hilder PE (1998): Effect of light intensity on feeding of striped trumpeter Latris lineata larvae. Mar Freshwater Res 49:363-368.
46.
Peterson EH, Rowe MH (1980): Different regional specializations of neurons in the ganglion cell layer and inner plexiform layer of the California horned shark, Heterodontus francisci. Brain Res 201:195-201.
47.
Platell ME, Potter IC, Clarke KR (1998): Resource partitioning by four species of elasmobranchs (Batoidea: Urolophidae) in coastal waters of temperate Australia. Mar Biol 131:719-734.
48.
Puckridge M, Last PR, White WT, Andreakis N (2012): Phylogeography of the Indo-West Pacific maskrays (Dasyatidae, Neotrygon): a complex example of chondrichthyan radiation in the Cenozoic. Ecol Evol 3:217-232.
49.
R Core Team (2012): R: A Language and Environment for Statistical Computing. Vienna, R Foundation for Statistical Computing.
50.
Rosenberger LJ (2001): Phylogenetic relationships within the stingray genus Dasyatis (Chondrichthyes: Dasyatidae). Copeia 3:615-627.
51.
Schieber NL, Collin SP, Hart NS (2012): Comparative retinal anatomy in four species of elasmobranch. J Morphol 273:423-440.
52.
Schiviz AN, Ruf T, Kuebber-Heiss A, Schubert C, Ahnelt PK (2008): Retinal cone topography of artiodactyl mammals: influence of body height and habitat. J Comp Neurol 507:1336-1350.
53.
Sivak JG (1978): Refraction and accommodations of the elasmobranch eye; in Hodgson ES, Mathewson RF (eds): Sensory Biology of Sharks, Skates and Rays. Arlington, Technical Information Division, Naval Research Laboratory.
54.
Stell WK, Witkovsky P (1973): Retinal structure in the smooth dogfish, Mustelus canis: general description and light microscopy of giant ganglion cells. J Comp Neurol 148:1-31.
55.
Templeton AR (1981): Mechanisms of speciation - a population genetic approach. Annu Rev Ecol Syst 12:23-48.
56.
Theiss SM, Lisney TJ, Collin SP, Hart NS (2007): Colour vision and visual ecology of the blue-spotted maskray, Dasyatis kuhlii Müller and Henle, 1814. J Comp Physiol A 193:67-79.
57.
Toyoda J-I, Saito T, Kondo H (1978): Three types of horizontal cells in the stingray retina: their morphology and physiology. J Comp Neurol 179:569-579.
58.
Warrant EJ (1999): Seeing better at night: life style, eye design and the optimum strategy of spatial and temporal summation. Vision Res 39:1611-1630.
59.
West-Eberhard MJ (1986). Alternative adaptations, speciation, and phylogeny (a review). Proc Natl Acad Sci USA 83:1388-1392.
60.
White WT, Platell ME, Potter IC (2004): Comparisons between the diets of four abundant species of elasmobranchs in a subtropical embayment: implications for resource partitioning. Mar Biol 144:439-448.
61.
White WT, Potter IC (2004): Habitat partitioning among four elasmobranch species in nearshore, shallow waters of a subtropical embayment in Western Australia. Mar Biol 145:1023-1032.
62.
Yokoyama S, Yokoyama R (1996): Adaptive evolution of photoreceptors and visual pigments in vertebrates. Annu Rev Ecol Syst 27:543-567.
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