The majority of holocephalans live in the mesopelagic zone of the deep ocean, where there is little or no sunlight, but some species migrate to brightly lit shallow waters to reproduce. This study compares the retinal morphology of two species of deep-sea chimaeras, the Pacific spookfish (Rhinochimaera pacifica) and the Carpenter’s chimaera (Chimaera lignaria), with the elephant shark (Callorhinchus milii), a vertical migrator that lives in the mesopelagic zone but migrates to shallow water to reproduce. The two deep-sea chimaera species possess pure rod retinae with long photoreceptor outer segments that might serve to increase visual sensitivity. In contrast, the retina of the elephant shark possesses rods, with an outer-segment length significantly shorter (a mean of 34 µm) than in the deep-sea species, and cones, and therefore the potential for color vision. The retinal ganglion cell distribution closely follows that of the photoreceptor populations in all three species, but there is a lower peak density of these cells in both deep-sea species (215–275 cells/mm2 vs. 769 cells/mm2 in the elephant shark), which represents a significant increase in the convergence of visual information (summation ratio) from photoreceptors to ganglion cells. It is evident that the eyes of deep-sea chimaeras have increased sensitivity to detect objects under low levels of light, but at the expense of both resolution and the capacity for color vision. In contrast, the elephant shark has a lower sensitivity, but the potential for color discrimination and a higher visual acuity.

Journal Section:
Editor's choice
Keywords:
Chimaera, Visual ecology, Ganglion cell, Photoreceptor, Spatial resolving power, Retinal summation, R Project for Statistical Computing
1.
Baddeley A, Turner R (2005): spatstat: An R package for analyzing spatial point patterns. J Stat Softw 12: 1–42.
2.
Barlow HB (1953): Summation and inhibition in the frog’s retina. J Physiol 119: 69–88.
3.
Beatty DD (1969): Visual pigments of three species of cartilaginous fishes. Nature 222: 285.
4.
Bergstad OA, Wik AD, Hildre O (2003): Predator-prey relationships and food sources of the Skagerrak deep-water fish assemblage. J Northw Atl Fish Sci 31: 165–180.
5.
Boycott BB, Wässle H (1974): The morphological types of ganglion cells of the domestic cat’s retina. J Physiol 240: 397–419.
6.
Bozzano A (2004): Retinal specialisations in the dogfish Centroscymnus coelolepis from the Mediterranean deep-sea. Sci Mar 68: 185–195.
7.
Bozzano A, Collin SP (2000): Retinal ganglion cell topography in elasmobranchs. Brain Behav Evol 55: 191–208.
8.
Bozzano A, Murgia R, Vallerga S, Hirano J, Archer SN (2001): The photoreceptor system in the retinae of two dogfishes, Scyliorhinus canicula and Galeus melastomus: possible relationship with depth distribution and predatory lifestyle. J Fish Biol 59: 1258–1278.
9.
Carter GSS (1948): Colour and colour vision in animals. Nature 4120: 439–440.
10.
Coimbra JP, Marceliano ML V, Andrade-da-Costa BLD, Yamada ES (2006): The retina of tyrant flycatchers: topographic organization of neuronal density and size in the ganglion cell layer of the great kiskadee Pitangus sulphu­ratus and the rusty margined flycatcher Myiozetetes cayanensis (Aves: Tyrannidae). Brain Behav Evol 68: 15–25.
11.
Coimbra JP, Trevia N, Marceliano ML V, Andrade-Da-Costa BLD, Picanco-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.
12.
Collin SP (1999): Behavioural ecology and retinal cell topography; in Archer SN, Djamgoz MBA, Loew ER, Partridge JC, Vallerga S (eds): Adaptive Mechanisms in the Ecology of Vision, pp 509–535.
13.
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.
14.
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.
15.
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.
16.
Collin SP, Pettigrew JD (1988b): Retinal topography in reef teleosts II. Some species with prominent horizontal streaks and high-density areae. Brain Behav Evol 31: 283–295.
17.
Collin SP (2008): A Web-based archive for topographic maps of retinal cell distribution in vertebrates: invited paper. Clin Exp Optom 91: 85–95.
18.
Compagno LJ V (2001): Sharks of the World: An Annotated and Illustrated Catalogue of Shark Species Known to Date. 2. Carcharhiniformes. Rome, FAO Food and Agriculture Organization of the United Nations.
19.
Compagno LJ V, Dando M, Fowler S (2005): Sharks of the World. Princeton, Princeton University Press.
20.
Crescitelli F (1969): The visual pigment of a chimaeroid fish. Vision Res 9: 1407–1414.
21.
Davies WL, Carvalho LS, Tay BH, Brenner S, Hunt DM, Venkatesh B (2009): Into the blue: gene duplication and loss underlie color vision adaptations in a deep-sea chimaera, the elephant shark Callorhinchus milii. Genome Res 19: 415–426.
22.
De Busserolles F, Marshall NJ (2017): Seeing in the deep-sea: visual adaptations in lanternfishes. Phil Trans R Soc B 372: 20160070.
23.
Denton EJ, Nicol JAC (1964): The chodioidal tapeta of some cartilaginous fishes (Chondrichthyes). J Mar Biol Assoc UK 44: 219–258.
24.
Denton EJ, Shaw T (1963): The visual pigments of some deep-sea elasmobranchs. J Mar Biol Assoc UK 43: 65–70.
25.
Didier DA (2004): Phylogeny and classification of extant Holocephali; in Carrier JC, Musick JA, Heithaus MR (eds): Biology of Sharks and Their Relatives. Boca Raton, CRC Press, pp 115–136.
26.
Didier DA (1998): The leopard Chimaera, a new species of chimaeroid fish from New Zealand (Holocephali, Chimaeriformes, Chimaeridae). Ichthyol Res 5: 281–289.
27.
Didier DA, Kemper JM, Ebert DA (2012): Phylogeny, biology and classification of extant holocephalans; in Carrier JC, Musick JA, Heithaus MR (eds): Biology of Sharks and Their Relatives, ed 2. Boca Raton, CRC Press, pp 97–123.
28.
Douglas RH (2010): Vision: vertebrates; in Breed MD, Moore J (eds): Encyclopedia of Animal Behavior. Oxford, Academic Press, pp 525–542.
29.
Douglas RH, Partridge JC, Hope AJ (1995): Visual and lenticular pigments in the eyes of demersal deep-sea fishes. J Comp Physiol A 177: 111–122.
30.
Dunn MR, Griggs L, Forman J, Horn P (2010): Feeding habits and niche separation among the deep-sea chimaeroid fishes Harriotta raleighana, Hydrolagus bemisi and Hydrolagus novaezealandiae. Mar Ecol Ser 407: 209–225.
31.
Ebert DA (ed) (2003): Sharks, Rays, and Chimaeras of California. Los Angeles, University of California Press.
32.
Franz V (1905): Zur Anatomie, Histologie und funktionellen Gestaltung des Selachierauges. Jena Z Naturw 40: 697–840.
33.
Fritsches KA, Marshall NJ, Warrant EJ (2003): Retinal specializations in the blue marlin: eyes designed for sensitivity to low light levels. Mar Freshw Res 54: 333–341.
34.
Fröhlich E, Negishi K, Wagner H-J (1995): Patterns of rod proliferation in deep-sea fish retinae. Vision Res 35: 1799–1811.
35.
Garcia VB, Lucifora LO, Myers RA (2008): The importance of habitat and life history to extinction risk in sharks, skates, rays and chimaeras. Proc R Soc B Biol Sci 275: 83–89.
36.
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.
37.
Gonzalez C, Teruel J, López E, Paz X (2007): Feeding habits and biological features of deep-sea species of the northwest Atlantic: large-eyed rabbitfish (Hydrolagus mirabilis), narrownose chimaera (Harriotta raleighana) and black dogfish (Centroscyllium fabricii). Northwest Atlantic Fisheries Organization Scientific Council Meeting, Dartmouth, NS, Canada, doc. 07/63 (9 pages).
38.
Gruber SH, Gulley RL, Brandon J (1975): Duplex retina in seven elasmobranch species. Bull Mar Sci 25: 353–358.
39.
Hart NS (2002): Vision in the peafowl (Aves: Pavo cristatus). J Exp Biol 205: 3295–3935.
40.
Hart NS, Lisney T, Collin SP (2006): Visual communication in elasmobranchs; in Ladich F, Collin SP, Moller P, Kapoor BG (eds): Communication in Fishes. Enfield, Science Publishers, pp 337–392.
41.
Hart NS, Lisney T, Marshall NJ, Collin SP (2004): Multiple cone visual pigments and the potential for trichromatic colour vision in two species of elasmobranch. J Exp Biol 207: 4587–4594.
42.
Hart NS, Theiss SM, Harahush BK, Collin SP (2011): Microspectrophotometric evidence for cone monochromacy in sharks. Naturwissenschaften 98: 193–201.
43.
Herring PJ (1977): Bioluminescence of marine organisms. Nature 267: 788–793.
44.
Herring PJ (2000): Bioluminescent signals and the role of reflectors. J Pure Appl Opt 2:R29–R38.
45.
Hueter RE (1991): Vision in elasmobranchs – introduction. J Exp Zool 256: 1–2.
46.
Hughes A (1975): A comparison of retinal ganglion cell topography in the plains and tree kangaroo. J Physiol 244: 61P.
47.
Hughes A (1977): The topography of vision in mammals of contrasting life style: comparative optics and retinal organization; in Crescitelli F (ed): The Visual System in Vertebrates. Berlin, Springer, pp 613–756.
48.
Inoue JG, Miya M, Lam K, Tay BH, Danks JA, Bell J, et al (2010): Evolutionary origin and phylogeny of the modern holocephalans (Chondrichthyes: Chimaeriformes): a mitogenomic perspective. Mol Biol Evol 27: 2576–2586.
49.
Kuchnow KP (1971): The elasmobranch pupillary response. Vision Res 11: 1395–1406.
50.
LaMarca MJ (1964): The functional anatomy of the clasper and clasper gland of the yellow stingray, Urolophus jamaicensis (Cuvier). J Morphol 114: 303–323.
51.
Land MF (1981): Optics and vision in invertebrates; in Autrum H (ed): Handbook of Sensory Physiology. Berlin, Springer, pp 471–592.
52.
Last PR, Stevens JD (eds) (2009): Sharks and Rays of Australia, ed 2. Collingwood, CSIRO Publishing.
53.
Lisney T (2010): A review of the sensory biology of chimaeroid fishes (Chondrichthyes; Holocephali). Rev Fish Biol Fish 20: 571–590.
54.
Lisney T, Collin SP (2007): Relative eye size in elasmobranchs. Brain Behav Evol 69: 266–279.
55.
Lisney T, Collin SP (2008): Retinal ganglion cell distribution and spatial resolving power in elasmobranchs. Brain Behav Evol 72: 59–77.
56.
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.
57.
Lund R, Grogan ED (1997): Relationships of the Chimaeriformes and the basal radiation of the Chondrichthyes. Rev Fish Biol Fish 7: 65–123.
58.
Maddock RG, Nicol JAC (1978): Studies on the eyes of Hydrolagus (Pisces: Chimaeridae). Contrib Mar Sci 21: 77–87.
59.
Marques A, Porteiro F (2000): Hydrothermal vent mussel Bathymodiolus sp. (Mollusca: Mytilidae): diet item of Hydrolagus affinis (Pisces: Chimaeridae). Copeia 3: 806–807.
60.
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.
61.
Moura T, Figueiredo I, Bordalo-Machado P, Almeida C, Gordo LS (2005): A new deep-water chimaerid species, Hydrolagus lusitanicus n. sp., from off mainland Portugal with a proposal of a new identification key for the genus Hydrolagus (Holocephali: Chimaeridae) in the north-east Atlantic. J Fish Biol 67: 742–751.
62.
Muguruma K, Takei S, Yamamoto N (2013): Retinal ganglion cell distribution and spatial resolving power in the Japanese catshark Scyliorhinus torazame. Zool Sci 30: 42–52.
63.
Muguruma K, Stell, WK, Yamamoto N (2014): A morphological classification of retinal ganglion cells in the Japanese Catshark Scyliorhinus torazame. Brain Behav Evol 83: 199–215.
64.
Nicol JAC, Somiya H (1989): The Eyes of Fishes. NY, Oxford University Press.
65.
Nychka D, Furrer R, Sain S (2012): R: fields: Tools for spatial data (Internet). R Package Version 6. http://cran.r-project.org/package=fields.
66.
Partridge JC, Shand J, Archer SN, Lythgoe JN, Groningen-Luyben WAHM (1989): Interspecific variation in the visual pigments of deep-sea fishes. J Comp Physiol A 164: 513–529.
67.
Pettigrew JD, Dreher B, Hopkins CS, McCall MJ, Brown M (1988): Peak density and distribution of ganglion cells in the retinae of microchiropteran bats: implications for visual acuity. Brain Behav Evol 32: 39–56.
68.
R Core Team (2012): R: a language and environment for statistical computing (Internet). http://www.r-project.org/.
69.
R Studio (2012) (Internet). http://www.rstudio.org/.
70.
Schieber NL, Collin SP, Hart NS (2012): Comparative retinal anatomy in four species of elasmobranch. J Morphol 273: 423–440.
71.
Schneider CA, Rasband WS, Eliceiri KW (2012): NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671–675.
72.
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.
73.
Stone J (ed) (1981): The Whole Mount Handbook: A Guide to the Preparation and Analysis of Retinal Whole Mounts. London, Maitland Publications.
74.
Theiss SM, Lisney T, Collin SP, Hart NS (2007): Colour vision and visual ecology of the blue-spotted maskray, Dasyatis kuhlii Müller & Henle, 1814. J Comp Physiol A 193: 67–79.
75.
Theiss SM, Davies WIL, Collin SP, Hunt DM, Hart NS (2012): Cone monochromacy and visual pigment spectral tuning in wobbegong sharks. Biol Lett 8: 1019–1022.
76.
Vigh-Teichmann I, Szel A, Rohlich P, Vigh B (1990): A comparison of the ultrastructure and opsin immnocytochemistry of the pineal organ and retina of the deep-sea fish Chimaera monstrosa. Exp Biol 48: 361–371.
77.
Wagner HJ, Frohlich E, Negishi K, Collin SP (1998): The eyes of deep-sea fish II. Functional morphology of the retina. Prog Retin Eye Res 17: 637–685.
78.
Warrant EJ, Locket AN (2004): Vision in the deep sea. Biol Rev 79: 671–712.
79.
Wickham H (2009): ggplot2: Elegant graphics for data analysis (Internet). New York, Springer. http://had.co.nz/ggplot2/book.
80.
Wickham H (2012): stringr: Make it easier to work with strings (Internet). R Package. http://cran.r-project.org/package=stringr.
81.
Yopak KE, Montgomery JC (2008): Brain organization and specialization in deep-sea chondrichthyans. Brain Behav Evol 71: 287–307.
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