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Histological Characteristics and Development of the Retina in the Japanese Sardine Sardinops Melanostictus*

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Histological Characteristics and Development of the Retina in the Japanese Sardine Sardinops Melanostictus* Fisheries Science 65(2), 224-229 (1999) Histological Characteristics and Development of the Retina in the Japanese Sardine Sardinops melanostictus* Masanobu Matsuoka•õ Seikai National Fisheries Research Institute, Kokubu, Nagasaki 850-0951, Japan (Received July 27, 1998) Histological characteristics and the distribution pattern of the visual cells, single cones, twin cones, and rods in the retina of the eye of wild adult Japanese sardine Sardinops melanostictus were investigat ed. The developmental process of the visual cells was also examined in the reared and wild larvae. In the specialized part (area temporalis) of the adult retina, slender twin cones were regularly distributed in a square mosaic pattern with central single cones. In the unspecialized part, twin cones with stout ellip soids were regularly distributed and many rods were recognizable. A newly-hatched larva had develop ing lens and undifferentiated retinal cells. The retinal differentiation proceeded rapidly, with the pig ment epithelial cells and visual cells already formed in a 31.5 hour-old larva. In a 79.5 hour-old larva at the first-feeding stage, the visual cell layer consisted of only single cones. A so-called pure-cone retina was still recognized in a larva of 18.6 mm standard length (SL). In a 20.9 mm. SL larva, rod-like cells with thin ellipsoids and outer segments appeared and twin cones also observed. In larvae greater than about 20 mm SL, the rods and twin cones rapidly increased in number. The retina of a 35.6 mm SL juvenile basically did not differ from the adult one. Key words: Japanese sardine, Sardinops melanostictus, retina, development, single cone, twin cone, rod The Japanese sardine Sardinops melanostictus is one of larval stages of the Clupeiformes such as the northern an the most important commercial fishes in Japan. Many in chovy E. mordax,15) the pilchard Sardina pilchardus,9) and vestigations have been conducted into the population dy the herring Clupea harengus,16,17) although Sardinops has namics of this species (see Kuroda11)), but biological not yet been examined. In contrast, the leptocephalus of knowledge, particularly regarding its developmental biolo the European eel Anguilla anguilla and the deep-sea larva gy, is insufficient.2) Recently, Matsuoka3,4) reported the de of the Macruridae have only rods as visual receptors.9) velopment of bony and lateral muscular systems of this The rods usually appear well after hatching and often as species, but more information of other organs is required late as metamorphosis. As it is relatively difficult to ob- to clarify larval survival strategy. serve the rods directly under light microscope, the number The eye is one of the most important sense organs for of cones is compared with that of the prominent nuclei of feeding and predator avoidance. The detailed structure of the outer nuclear layer.17) This indirect counting technique the eye of adult clupeoid fish has been investigated in the to examine the differentiation of rods has been used in Pacific sardine Sardinops caerulea, the northern anchovy many studies. 10-12,14-19)The twin cones are formed by the Engraulis mordax, the American shad Alosa sapidissima, combination of two single cones. They usually appear just and the deep-bodied anchovy Anchoa compressa by before or during metamorphosis.20) It is important to clari O'Connell,5) although there has been no information on fy the differentiation of rods and twin cones by species, rel that of S. melanostictus. The retina of the fish eye usually ative to their morphological and ecological development. includes three types of visual cells, single cones, twin The present study clarifies histological characteristics and cones, and rods. The cones are involved in color vision the distribution pattern of visual cells in adult S. and visual acuity, and the rods in dim light vision. The melanostictus, and the developmental processes of their twin cones are peculiar to teleosts,6) and Kawamura and visual cells are also investigated. Tamura7) suggested that they are functional in dim light en vironment. Materials and Methods In the early larval stages of many teleosts, including salmon Oncorhynchus spp., the haddock Melanogrammus Specimens aeglefinus, the sand goby Pomatoschistus minutus, the red An adult specimen, 190 mm in standard length (SL), seabream Pagrus major, the sole Solea solea, the flounder was caught at night in the waters off southern Kyushu by Paralichthys olivaceus, and the marble goby Oxyeleotris angling. Of the specimens examined, 27 larvae were labora marmoratus, a pure-cone retina without rods has been ob- tory-reared, using wild eggs collected with a plankton served.") A pure-cone retina has been also reported in the net.2) They were from 3.6 mm in notochord length (NL) * Contribution from Seikai National Fisheries Research Institute, No. 570. •õ Present Address: National Research Institute of Fisheries and Environment of Inland Sea, Ohno, Hiroshima 739-0452, Japan. Retinal Histology and Development in Sardine 225 (newly-hatched) to 9.65 mm NL (12 days old) in 1989 and quarters of the retina showed almost the same histological from 3.75 mm NL to 11.2 mm NL (16 days old) in 1991. features, called the unspecialized part here. Twin cones These larvae were reared at 17.0-17.5•Ž and fed on small with stout ellipsoids were regularly distributed and type rotifers after the first-feeding stage. In addition, 20 numerous very thin rods were recognizable among them, wild specimens, from 6.1 mm NL to 35.6 mm SL collected although single cones were not observed (Fig. 1A, B). The with a plankton net and a scoop net using a fish lamp, were outer nuclear layer was thick, indicating the existence of examined. numerous rod nuclei (Fig. 1B). The ventro-temporal quarter of the retina included the Histology specialized area, area temporalis, which contained densely The adult specimen was fixed in Bouin's solution. The re cones. Slender twin cones were regularly distributed in a tina was dissected out, cut into four quarters, dorso-nasal, square mosaic pattern with central single cones. Few rods ventro-nasal, dorso-temporal, and ventro-temporal, and were detected in this part (Fig. IC, D). The outer nuclear embedded in paraffin. Transverse and tangential sections layer of the area temporalis was thinner than that of the un- 4 Mm thick were cut with a microtome and stained with Al specialized retina (Fig. 1D). cian blue-Hematoxylin-Eosin. Larvae and juveniles were mainly fixed in Bouin's solu Retinal Development tion and partly in Zenker's solution. Transverse sections In a 3.5 hour-old larva of 3.6 mm NL, the lens was com- 4-6 ƒÊm thick were cut and stained with Alcian blue- posed of two layers, the inner fibrous layer and the outer Hematoxylin-Eosin. Sections were observed under a light single cell layer. The retinal cells were not yet differentiat microscope. ed (Fig. 2A). In a 31.5 hour-old larva of 4.75 mm NL, the differentiation of the retinal cells had rapidly proceeded, Results and the pigment epithelium and visual cell layer were formed (Fig. 2B). In a 53 hour-old larva of 4.85 mm NL, Retinal Structure of Adult the oculomotor muscles were formed and pale pigmenta The dorso-nasal, ventro-nasal, and dorso-temporal tion appeared (Fig. 2C). Fig. 1. Histological sections of the retina in the adult Japanese sardine Sardinops melanostictus. A: tangential section of unspecialized part showing regularly distributed twin cones with stout ellipsoids and very thin rods. B: transverse sec tion of unspecialized part showing thick outer nuclear layer with many rod nuclei. C: tangential section of specialized part (area temporalls) show ing slender twin cones regularly distributed in a square mosaic pattern with central single cones. D: transverse section of specialized part showing a relatively thin outer nuclear layer. ONL, outer nuclear layer; PEL, pigment epithelial layer; R, rod; SC, single cone; TC, twin cone. Scale bars indicate 50 ƒÊm. 226 Matsuoka In a 79.5 hour-old larva of 5.15 mm NL at the first-feed- stage. ing stage, the pigment epithelial layer was fully pigmented Figure 3A shows the visual cells of the unspecialized (Fig. 2D). The visual cell layer consisted of only single area of the retina in an 18.6 mm SL larva. Many darkly cones and the ratio of cellular nuclei of the outer nuclear stained small nuclei were observed in the basal part of the layer to cone ellipsoids was 1:1 (Fig. 2E). Figure 2F indi outer nuclear layer. The ratio of cellular nuclei to cone el cates a pure-cone retina of a 12 day-old larva of 8.9 mm lipsoids was about 2:1, although the rod ellipsoid or outer NL. It appeared similar to the retina of the first-feeding segment was not recognizable. The tangential section Fig. 2. Histological sections of the eye and retina in the early larval Japanese sardine Sardinops melanostictus (all transverse sections) . A: a 3.5-hour-old larva of 3.6 nun in notochord length (NL) showing the developing lens and undifferentiated retinal cells (arrows). B: a 31.5- hour-old larva of 4.75 mm NL showing differentiated pigment epithelium and visual cell layer. C: a 53-hour-old larva of 4 .85 mm NL showing pale pigmentation. D: a 79.5-hour-old larva of 5.15 mm NL at the first-feeding stage showing a thick pigment epithelial layer. E: enlargement of D showing a pure-cone retina. F: a 12-day-old larva of 8.9 mm NL showing a pure-cone retina. L, lens; N, nucleus of visual cell; OM , oculomotor muscle; PE, pigment epithelium; PEL, pigment epithelial layer; SC, single cone; V, visual cell layer.
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