AbstractAbstract

Morphological characteristics of the retina of a deep-water shark of the order Morphological characteristics of the retina of a deep-water shark of the order Squaliformes were compared to three epipelagic sharks (one carcharhinoid and two Squaliformes were compared to three epipelagic sharks (one carcharhinoid and two lamnoids) to investigate visual adaptations in elasmobranchs living at different lamnoids) to investigate visual adaptations in elasmobranchs living at different depths. The three epipelagic species (depths. The three epipelagic species (Alopias vulpinusAlopias vulpinus, , Isurus oxyrinchusIsurus oxyrinchus, and , and Prionace glaucaPrionace glauca) have well-developed eyes, with retinas composed of both rod and ) have well-developed eyes, with retinas composed of both rod and cone photoreceptors in ratios of 13:1, 12:1, and 14:1, respectively, whereas cone photoreceptors in ratios of 13:1, 12:1, and 14:1, respectively, whereas CentrophorusCentrophorus cf. cf. uyatouyato, a mesobenthic species found at depths greater than 400 m, , a mesobenthic species found at depths greater than 400 m, has a retina composed solely of rods. The rod-rich, relatively cone-poor retinas of has a retina composed solely of rods. The rod-rich, relatively cone-poor retinas of these four elasmobranchs yield low visual acuity and rather high sensitivity, enabling these four elasmobranchs yield low visual acuity and rather high sensitivity, enabling them to detect an object against contrasting background in dim light. Further them to detect an object against contrasting background in dim light. Further histologic investigations into eight different regions of the retinas, four central and histologic investigations into eight different regions of the retinas, four central and four peripheral, exhibited no indication of intraretinal variation within each species in four peripheral, exhibited no indication of intraretinal variation within each species in terms of photoreceptor abundance, distribution, outer-segment length, inner-segment terms of photoreceptor abundance, distribution, outer-segment length, inner-segment length, or width, suggesting that there is no specific area of increased visual acuity or length, or width, suggesting that there is no specific area of increased visual acuity or sensitivity in the retinas of these species. As expected, interspecific variation in these sensitivity in the retinas of these species. As expected, interspecific variation in these characteristics was observed between the deep-water squaloid and the three epipelagic characteristics was observed between the deep-water squaloid and the three epipelagic sharks, whereas little variation was observed between the ecologically and sharks, whereas little variation was observed between the ecologically and taxonomically related taxonomically related AA. . vulpinusvulpinus and and II. . oxyrinchusoxyrinchus. These variations in retinal . These variations in retinal structure are discussed in terms of the ecologic and taxonomic relationships of these structure are discussed in terms of the ecologic and taxonomic relationships of these sharks.sharks.

Histological Comparison of the Retinal Structure of Deep-Water and Epipelagic SharksHistological Comparison of the Retinal Structure of Deep-Water and Epipelagic Sharks

MethodsMethods

• Species used (N = 3): Species used (N = 3): CentrophorusCentrophorus cf. cf. uyato uyato were obtained with horizontal longline were obtained with horizontal longline gear at depths ranging from 400-913 meters from the Cayman Trench, Jamaica, West gear at depths ranging from 400-913 meters from the Cayman Trench, Jamaica, West Indies; Indies; Alopias vulpinus, Isurus oxyrinchusAlopias vulpinus, Isurus oxyrinchus and and Prionace glaucaPrionace glauca were obtained from were obtained from specimens collected by rod and reel off of the south shore of Long Island, NY.specimens collected by rod and reel off of the south shore of Long Island, NY.• Retinas were divided into eight regions: dorsal-central, dorsal-peripheral, posterior –Retinas were divided into eight regions: dorsal-central, dorsal-peripheral, posterior – central, posterior-peripheral, ventral-central, ventral-peripheral, anterior-central orcentral, posterior-peripheral, ventral-central, ventral-peripheral, anterior-central or anterior-peripheral.anterior-peripheral.• Retinas were fixed in 10% neutral buffered formalin at pH 7.2, dehydrated through a Retinas were fixed in 10% neutral buffered formalin at pH 7.2, dehydrated through a graded series of ethanol (80%, 95% & 100%) and embedded in paraffin wax. graded series of ethanol (80%, 95% & 100%) and embedded in paraffin wax. • Embedded specimens were sectioned between 4μm and 6μm. Embedded specimens were sectioned between 4μm and 6μm. • Measurements and counts were collected from digital photographs at 200x and 400x. Measurements and counts were collected from digital photographs at 200x and 400x. • The within species and between species differences were determined using one-way The within species and between species differences were determined using one-way repeated measures analysis of variance (ANOVA) and the Student-Newman-Keuls post repeated measures analysis of variance (ANOVA) and the Student-Newman-Keuls post hoc test. hoc test.

Jill A. Olin* and John F. MorrisseyJill A. Olin* and John F. MorrisseyDepartment of Biology, Hofstra University, Hempstead, NY 11549Department of Biology, Hofstra University, Hempstead, NY 11549

ResultsResults

• The retina of The retina of CC. cf. . cf. uyatouyato contained only rod photoreceptors in abundance of contained only rod photoreceptors in abundance of 6,000/mm, measuring approximately 686,000/mm, measuring approximately 68µm (Figure 1)µm (Figure 1). . • The retinas of The retinas of AA.. vulpinus vulpinus, , II. . oxyrinchus oxyrinchus and and PP.. glauca glauca contained both rod and contained both rod and cone photoreceptors in ratios of 13:1, 12:1, and 14:1 measuring approximatelycone photoreceptors in ratios of 13:1, 12:1, and 14:1 measuring approximately 54µm and 31µm, 53µm and 33µm, and 65µm and 22µm, respectively (Figure 54µm and 31µm, 53µm and 33µm, and 65µm and 22µm, respectively (Figure 2).2).• No differences were observed within species between the eight regions of the No differences were observed within species between the eight regions of the retina.retina.• Significant differences were observed between the species in photoreceptor Significant differences were observed between the species in photoreceptor composition, abundance and dimensions (Figures 3, 4, 5 and 6).composition, abundance and dimensions (Figures 3, 4, 5 and 6).• The retinas of the two lamnoid species exhibited significantly similar The retinas of the two lamnoid species exhibited significantly similar characteristics, for photoreceptor abundance, as well as rod and cone outer andcharacteristics, for photoreceptor abundance, as well as rod and cone outer and inner segment.inner segment.• The retina of The retina of PP. . glaucaglauca was observed to be the median between the lamnoids and was observed to be the median between the lamnoids and centrophoroid species containing significant similarities to both. centrophoroid species containing significant similarities to both.

ConclusionsConclusions

• These findings indicate clear variation in retinal compositions between These findings indicate clear variation in retinal compositions between mesobenthic (400-900m) and pelagic (0-400m) habitats .mesobenthic (400-900m) and pelagic (0-400m) habitats .

• The lack of differences within the retinas indicate that there are no adaptations The lack of differences within the retinas indicate that there are no adaptations associated with areas of high photoreceptor concentrations, as seen in other associated with areas of high photoreceptor concentrations, as seen in other elasmobranch species (Hueter 1991).elasmobranch species (Hueter 1991).

• As anticipated the retina of the centrophoroid species indicates an adaptation for As anticipated the retina of the centrophoroid species indicates an adaptation for scotopic vision with high sensitivity.scotopic vision with high sensitivity.

• The retinas of the two lamnoid species exhibit similarities and indicate The retinas of the two lamnoid species exhibit similarities and indicate adaptations for both scotopic and photopic vision. These data represent adaptations for both scotopic and photopic vision. These data represent similarities resulting from both taxonomic relations and habitat use.similarities resulting from both taxonomic relations and habitat use.

• The similarities of the carcharhinoid species to the other three species indicate a The similarities of the carcharhinoid species to the other three species indicate a retina adapted for both photopic and scotopic vision with high sensitivity.retina adapted for both photopic and scotopic vision with high sensitivity.

Literature CitedLiterature Cited

Bozzano, A., R. Murgia, S. Vallerga, J. Hirano, and S. Archer. 2001. The Bozzano, A., R. Murgia, S. Vallerga, J. Hirano, and S. Archer. 2001. The photoreceptor system in the retinae of two dogfishes, photoreceptor system in the retinae of two dogfishes, Scyliorhinus caniculaScyliorhinus canicula and and Galeus melastomusGaleus melastomus: Possible relationship with depth distribution and : Possible relationship with depth distribution and predatory lifestyle. J. Fish Bio. 59: 1258 – 1278.predatory lifestyle. J. Fish Bio. 59: 1258 – 1278.Gruber, S.H., D.H. Hamasaki, and C.D.B. Bridges. 1963. Cones in the retina of Gruber, S.H., D.H. Hamasaki, and C.D.B. Bridges. 1963. Cones in the retina of the lemon shark (the lemon shark (Negaprion brevirostrisNegaprion brevirostris). Vis. Res. 3: 397-399. ). Vis. Res. 3: 397-399. Gruber, S.H., R.L. Gulley, J. Brandon. 1975. Duplex retina in seven Gruber, S.H., R.L. Gulley, J. Brandon. 1975. Duplex retina in seven elasmobranch species. Bull. Mar. Sci. (25) 3: 353-358. elasmobranch species. Bull. Mar. Sci. (25) 3: 353-358. Gruber, S.H. and J.L. Cohen. 1985. Visual system of the white shark, Gruber, S.H. and J.L. Cohen. 1985. Visual system of the white shark, Carcharodon carchariasCarcharodon carcharias, with emphasis on retinal structure. Memoir #9 , with emphasis on retinal structure. Memoir #9 S. California Academy of Science. 9: 61-72. S. California Academy of Science. 9: 61-72. Hamasaki, D.I. and S.H. Gruber. 1965. The photoreceptors of the nurse shark, Hamasaki, D.I. and S.H. Gruber. 1965. The photoreceptors of the nurse shark, Ginglymostoma cirratumGinglymostoma cirratum and the sting ray, and the sting ray, Dasyatis sayiDasyatis sayi. Bull. Mar. Sci. 15 . Bull. Mar. Sci. 15 (4): 1051-1059. (4): 1051-1059. Hueter, R.E. 1991. Adaptations for spatial vision in sharks. J. Exp. Zool. Suppl. Hueter, R.E. 1991. Adaptations for spatial vision in sharks. J. Exp. Zool. Suppl. 5: 130 -141.5: 130 -141.Kohbara, J., H. Niwa, and M. Oguri. 1987. Comparative light microscopic Kohbara, J., H. Niwa, and M. Oguri. 1987. Comparative light microscopic studies on the retina of some elasmobranch fishes. Nipp. Suis. Gakka. 53 studies on the retina of some elasmobranch fishes. Nipp. Suis. Gakka. 53 (12): 2117- 2125.(12): 2117- 2125.Sillman, A.J., G.A. Letsinger, S. Patel, E.R. Loew, and A.P. Klimley. 1996. Sillman, A.J., G.A. Letsinger, S. Patel, E.R. Loew, and A.P. Klimley. 1996. Visual pigments and photoreceptors in two species of shark, Visual pigments and photoreceptors in two species of shark, Triakis Triakis semifasciatasemifasciata and and Mustelus henlei Mustelus henlei. J. Exp. Zool. 276: 1-10.. J. Exp. Zool. 276: 1-10.Stell, W.K. 1972. The structure and morphologic relations of rods and cones Stell, W.K. 1972. The structure and morphologic relations of rods and cones in the retina of the Spiny Dogfish, in the retina of the Spiny Dogfish, SqualusSqualus. Comp. Biochem. Physiol. 42A: . Comp. Biochem. Physiol. 42A: 141-151.141-151.Yew, D.T., Y.W. Chan, M. Lee, and S. Lam. 1984. A biophysical, Yew, D.T., Y.W. Chan, M. Lee, and S. Lam. 1984. A biophysical, morphological and morphometrical survey of the eye of the small shark morphological and morphometrical survey of the eye of the small shark ((Hemiscyllium plagiosumHemiscyllium plagiosum). Anat. Anz. 155: 355-363. ). Anat. Anz. 155: 355-363.

AcknowledgementsAcknowledgements

The authors acknowledge Hofstra University for providing partial funding for The authors acknowledge Hofstra University for providing partial funding for this research. Special thanks to all of the fellow graduate students, faculty, this research. Special thanks to all of the fellow graduate students, faculty, researchers and volunteers who donated their time to the success of this project.researchers and volunteers who donated their time to the success of this project.

IntroductionIntroduction

Fishes inhabit more diverse light environments than any other group of vertebrates. Fishes inhabit more diverse light environments than any other group of vertebrates. These different light environments present broadly different visual problems to their These different light environments present broadly different visual problems to their inhabitants. A relatively large amount of information on elasmobranch retinal structure inhabitants. A relatively large amount of information on elasmobranch retinal structure has been collected, however the emphasis has been placed on coastal and pelagic has been collected, however the emphasis has been placed on coastal and pelagic species (Gruber et al. 1963, 1975, 1985; Hamasaki and Gruber 1965; Sillman et al. species (Gruber et al. 1963, 1975, 1985; Hamasaki and Gruber 1965; Sillman et al. 1996; Yew et al. 1984) with modest attention paid to deep-sea forms (Bozzano et al. 1996; Yew et al. 1984) with modest attention paid to deep-sea forms (Bozzano et al. 2001; Kohbara et al. 1987; Stell and Witkovsky 1972, 1973). The deep sea, defined as 2001; Kohbara et al. 1987; Stell and Witkovsky 1972, 1973). The deep sea, defined as the area that lies below the level of effective light penetration, makes for a biologically the area that lies below the level of effective light penetration, makes for a biologically unique environment and the elasmobranchs living there practical research materials to unique environment and the elasmobranchs living there practical research materials to investigate retinal adaptations in comparison with pelagic and coastal elasmobranchs.investigate retinal adaptations in comparison with pelagic and coastal elasmobranchs.

Figure 1:Figure 1: Cross section of the retina of Cross section of the retina of CC. cf . cf uyatouyato depicting an all rod retina. depicting an all rod retina.

Figure 2:Figure 2: Rod and cone photoreceptors Rod and cone photoreceptors of of II. . oxyrinchusoxyrinchus..

Figure 3:Figure 3: Average Number of Rod Photoreceptors (0.1mm). Average Number of Rod Photoreceptors (0.1mm). Figure 4:Figure 4: Average Number of Cone Photoreceptors (0.1mm). Average Number of Cone Photoreceptors (0.1mm).

Figure 5:Figure 5: Average Length of Rod Photoreceptors. Average Length of Rod Photoreceptors. Figure 6:Figure 6: Average Length of Cone Photoreceptors. Average Length of Cone Photoreceptors.

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