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Vision in Elasmobranchs: Histology of the Retina And

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Vision in Elasmobranchs: Histology of the Retina And VISION IN ELASMOBRANCHS: HISTOLOGY OF THE RETINA AND ERG SPECTRAL SENSITIVITY by Joel L. Cohen f A thesis submitted in partial fulfillment of the requirements for the degree of Master of Arts in the Department of Biology California State University, Fresno August, 1972 I1U LWOU'l IA LULLI CP LIE KMC TABLE OF CONTENTS PAGE LIST OF TABLES vi ' LIST OF FIGURES vi ' ' INTRODUCTION 1 I Purpose Function of the Retina 5 EIasmobranch Visual Cells METHODS AND MATERIALS ... 6 Animals Optics and Stimulation 9 Ca I ibration 9 Procedure u. , . 10 Histology RESULTS 12 I 2 Hexanchus griseus a. , 12 Histology I 5 Electrophysiology Triakis semifasciata ^ 4- , 20 Histology 20 Electrophysiology 25 Rhinobatos productus Histology 2^ 32 Electrophysiology V i TABLE OF CONTENTS (Continued) PAGE DISCUSSION 35 Histology 33 Electrophysiology 3^ CONCLUSIONS 42 LITERATURE CITED 43 V i i LIST OF TABLES TABLE PAGE 1. Comparison of The Thicknesses of each layer for The fundus and side of the retina 18 2. Comparison of cell ratios 19 V i i i LIST OF FIGURES FIGURE PAGE 1. Optical system number one 7 2. Optical system number two 8 3. Cross section of the retina of Flexanchus griseus stained with hematoxylin and eosin 13 4. Spectral sensitivity curve of Hexanchus griseus 16 5. Amp Iitude-i ntensity curve of Hexanchus griseus 17 6. Cross section of the retina of Triakis semifasciata stained with hematoxylin and eosin 21 7. Spectral sensitivity curve of Triakis semifasciata 23 8. Amp Iitude-intensity curve of Triakis semifasciata 24 9. Cross section of the retina of Rhinobatos productus stained with PTAH 26 10. Rods and cones in the retina of Rhinobatos productus stained with hematoxylin and eosin 28 11. Horizontal section of the retina of Rhinobatos productus at the level of the cone el Iipsoids stained with PTAH 30 12. Spectral sensitivity curve of Rhinobatos productus 33 13. Amplitude intensity curve of Rhinobatos productus 34 14. Relative spectral distribution of solar energy in , XQ different types of sea water INTRODUCTION Purpose The eyes of vertebrates have adapted to their habitat to such an extent that Detweiler (1947) stated "So closely correlated is the mode of life of the animal with the structure of the retina, that, from a histological section, one can predict something of the habits of the animal, as well as its visual acuity." Vision plays an important role in the life of a shark. Experimen­ tal evidence shows that although olfactory cues initiates an advance toward an object, the final phase of the approach is controlled by vision (Hobson, 1963). McLaughlin and O'Gower (1971) have shown that the heterodont shark, Heterodontus portusjacksoni, gives evidence of a homing ability. They suggested this homing ability probably is dependent on vision. The early studies on elasmobranch vision were primarily histologi­ cal in approach (Franz, 1905, 1913; Rochon-Duvigneaud, 1943; Verrier, 1929, 1930). Although most recent studies are physiologically oriented, the need for continued histological studies is evidenced by the appear­ ance of articles in the literature which refute the older findings (Gruber et al. 1963, Plamaski and Gruber, 1965; Stell, 1972). Many of the recent physiological studies have concentrated on determining the spectral sensitivity of the retina, using electro­ physiological techniques. Kobayashi (1962) was the first to study electrophysiological re­ sponse in the retina of eIasmobranchs. He used eyecup preparations and oriented his findings to ecological questions. Using the dogfish 2 i-iuste I us manazo and the batoid rays and skates PI atyrh ina, Dasyat i s, Ra ja, Na rka, and Ho I orhinus, he determined their respective spectral sensitivity and the properties of their eIectroretinograms. From these data, he con­ cluded that the dogfish eye was well adapted for an open ocean existence and the eye of rays and skates for a bottom dwelling habit. O'Gower and Mathewson (1967) using living intact animals determined the spectral sensitivity of the lemon shark Negaprion brevirostris. Hamasaki et al. (1967), also using intact living animals, determined the properties of the e I ectroreti nogram of the lemon shark, Negaprion brevirostris, the nurse shark, GingIymostoma cirratum, and the stingray, Dasyatis sayi. Using microeIectrodes, Tamura et al. (1966) and Tamura and Niwa (1967) determined the spectral sensitivity of Dasyatis akajei and Heterodontus japonicus. To interpret the findings of physiologists, behavioral experiments must be done to determine the actual visual capabilities of elasmobranchs. At present few behavioral studies have been performed (Clark, 1961; Tester and Kato, 1966; and Gruber, 1969). This thesis is concerned with the retinal histology and scotopic (dark adapted) spectral sensitivity of three species of elasmobranch as determined by electroreti nography. The cellular make up of the retinas of each species of elasmobranch will be discussed as well as a deter­ mination of rod to bipolar cell and rod to ganglion cell ratios. The purpose will be to determine whether the retinal histology and spectral response appears adaptive to the species' habitat. 3 The three species studied are the sixgill shark, Hexanchus griseus (Bonnaterre), the leopard shark, Triakis semifasciata Girard, and the shove I nose guitarfish, Rhinobatos productus (Ayres). Hexanchus griseus is a primitive deep sea shark found in depths ranging from 75 fathoms to as deep as 3430 fathoms (Bigelow and Schroeder, 1948). I have caught specimens in depths ranging from 70 to 150 fathoms. Triakis semifasciata is found in rather shallow waters and in sloughs (Roedel, 1950). Rhinobatos productus inhabits the shal low waters of shores and bays (Barnhart, 1936). Function of the Retina The retina has evolved to perform one of two functions, acuity and sensitivity (Detwiler, 1943). Sensitivity of an eye means its ability to respond to weak stimuli. By acuity we mean the ability to continue to see separately and unblurred the details of the visual object as those details are made smaller and closer. Summation as discussed here is the gathering together of many rods to form bipolar cells and ganglion cells. This causes the response to stimulus to be additive (WalIs, 1942). Acuity in the retina is governed by three factors, the slenderness of the visual cells, their closeness of spacing and the number connected with one optic nerve fiber (Walls, 1942). Diurnal vertebrates have retinas designed for acuity. Their visual cells are slender and closely spaced. There are a great number of cone, bipolar cells and ganglion cells, so that in some cases, one cone is attached to one bipolar cell (Walls, 1942). On the other hand, nocturnal animals have evolved retinal character­ istics that enable them to have very sensitive eyes including enlargement 4 of the rod outer segment and summation. These animals have very long rod outer segments which enable them to contain more photosensitive material than a short one would allow. They have a large number of rods and fewer number of bipolar and ganglion cells, so that summation is extensive (Walls, 1942). In nocturnal animals, however, there is an area of the retina in which mostly cones are present and the number of secondary and tertiary neurons increases. This area is called the area centralis and gives an area of acuity in an eye designed for sensitivity (Walls, 1942). EIasmobranchs are considered to be nocturnal animals (Walls, 1942). As such they would be expected to have a retina that is designed for sensitivity. Verrier (1924), Franz (in Walls, 1942) and Kato (1962) have found mostly rod retinas and a high degree of summation in sharks. It should be expected that this summation would vary according to the habitat of the animal. Verrier (1929) found that ScyIIium had a rod: gang I ion ceII ratioof 8:1 and Acanthias 5:1. Franz (in Walls, 1942) found that the ratio in Etmopterus wa s 147:1 and in various sma II sha rks 20:1. In the blacktip shark, Carcharhinus melanopterus this ratio was found to be 77:1 and in the white tip shark, Triaenodon obesus it was 82:1 (Kato, 1962). Such large variations in these ratios point out the difficulty in microtechnique and counting methods. Elasmobranch Visual Cells It is generally thought that eIasmobranchs possess pure rot retinas. Flowever, cones have been found in Squatina and Muste I us (Franz 1905, 1913), in My Iiobatis (Verrier 1930), and in Lamna (Rochon-Duvignon, 1943). More recently Gilbert (1961) studied sixteen species of 5 elasmobranch and found cones only in Muste I us. Some of his findings were reversed when Gruber et al. (1963) found cones in the lemon shark, Negaprion brevirostris and in three other sharks (Carcharhinus springeri, C. falciformis and Sphyrna mokarran). Hamasaki and Gruber (1965) also found cones in the nurse shark, GingIymostoma cirratum and the stingray Dasyatis sayi . Gruber (1969), however, did not find cones in Mustel us sp. Stell (1972) recently found cones in SquaI us which was thought to have only rods. METHODS AND MATERIALS Anima I s Shove I nose guitarfish and leopard sharks were caught with a gill net in Elkhorn Slough, Monterey County, California. The Slough is about 20 feet deep at high tide. Sixgill sharks were caught in Monterey Bay, California, using large mesh gill net and long lines set in depths of 70 to 150 fathoms. Animals were placed in a large outdoor aquarium until needed. This varied from 24 hours to 4 weeks. The variation in time between capture and use did not seem to affect the results. Optics and Stimulation A six volt automobile spotlight (Westi nghouse) was used as the light source. The lamp was powered by two 12 volt automobile storage batteries connected in series, and underrun at 2.5 amps. Current was continually monitored by an ammeter and controlled by a variable resistor.
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