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Development of the retina in the cuttlefish Sepia esculenta.

ABSTRACT To provide morphological bases for functional studies, the development of the photoreceptor cells in the retina of the cuttlefish Sepia esculenta from newly hatched juveniles to the adults was examined by light and electron microscopy. Four layers were distinguished in the retina: the rhabdomeric layer, subrhabdomeric layer, inner segmental layer, and plexiform layer. With the development of the retina, the structure of the plexiform layer becomes stronger. Morphometric data on the rhabdomeric microvilli from the newly hatched to the adult retinas are presented. The thickness of the rhabdomeric layer and the total surface area of the rhabdomeric microvilli present beneath a unit surface area of the retina show an exponential increase with developmental days; the diameter of the lens shows a linear increase with days. The results of our research show that the visual acuity and sensitivity of S. esculenta continuously increased with development.

KEY WORDS: cephalopod, Sepia esculenta, development, retina, photoreceptor, histology, ultrastructure

INTRODUCTION

The cephalopod has a pair of well-developed eyes of the camera type, which resemble vertebrate eyes as the result of convergent evolution (Packard 1972). The retina in the eye of the adult cephalopod provides important material for the study of visual mechanisms in invertebrates and has become increasingly interesting in recent years. It has been extensively examined from biochemical, physiological, morphological, and behavioral standpoints (Hara & Hara 1972, Hamdorf 1979, Messenger 1981).

The ultrastructural studies of adult cephalopod retinas have been reported by Zonana (1961), Yamamoto et al. (1965), Tonosaki (1965), Gray (1970), Cohen (1973a, 1973b), Saibil (1982), Kataoka and Yamamoto (1983), Yamamoto and Takasu 0984), and Yamamoto and Yoshida (1984). The cephalopod retina is composed of photoreceptor cells, supporting cells, and glial cells (Young 1971). The receptor cell body is divided into the outer and the inner segments by a narrow neck that passes through the basal lamina. The distal (vitreal) end of the outer segment elongates to form a process (the apical process) that bears 2 sets of microvilli, making up 2 opposite rhabdomeres. The inner segment contains a nucleus and sends out an axon from the proximal (sclerad) end toward the optic lobe. Because these structures are arranged in layers, it is convenient to recognize four layers in the retina: (1) the rhabdomeric layer, (2) the subrhabdomeric layer, (3) the inner segmental layer, and (4) the plexiform layer. The supporting cells are localized in the subrhabdomeric layer. The plexiform layer consists of the axons from receptor cells, efferent nerve fibers originating in the optic lobe, and the glial cells.

Morphogenetic processes of photoreceptor cells in the cephalopod during ontogeny have been briefly described in cuttlefish Sepia officinalis (Lemaire and Richard 1978) and Sepiellajaponica (Yamamoto 1985). Its relatively large size and simple architecture offer the opportunity to study the process of the acquisition of photoreceptive function during development. Developmental processes of cephalopod eyes have been described by some studies using conventional techniques (Meister 1972; for review, see Arnold 1971), but to our knowledge, the ontogeny of the visual system using modern techniques in S. esculenta from newly hatched juveniles to adults has not been published. Our goal is to provide functional morphology regarding the morphogenesis of photoreceptor cells from newly hatched to adult S. esculenta via light and electron microscopic observations.

MATERIALS AND METHODS

Experimental Animals

Five adults and 2,376 cuttlefish eggs were obtained from local fishermen in Lanshan Rizhao City in the Shandong Province of China in June 2006. These adults were caught using beach seines. The fertilized eggs were obtained with manmade spawning substrate. The eggs were then transferred to an aquafarm in Rushan Weihai City of the Shandong Province to incubate. The hatchling larvae were fed ad libitum on live mysids and on young shrimp from 1 to 30 days after hatching. The larvae from 30-88 days after hatching were fed live young fish and bigger shrimp caught from the nearby sea. Size of the diet increased as cuttlefish size increased. Enough prey was offered twice daily at 9:00 AM and 3:00 PM.

Sampling Procedure

A subsample of 5 animals was taken at 1, 3, 5, 7, 14, 21, 28, 38, 48, 58, 68, 78, and 88 days after hatching, respectively. Early stages (younger than 14 days after hatching) were whole fixed in Bouin's solution for 24 h and then transferred to 70% EtOH for preservation. The bigger ones (more than 21 days after hatching) were sacrificed by decapitation. The eyes were dissected, enucleate& and bisected under a dissecting microscope (SMZ2645; Nikon, Tokyo, Japan). The eyes were then fixed in Bouin's solution for 24 h and transferred to 70% EtOH for preservation.

Histological Methods

For light microscopy, the preserved samples were dehydrated and then embedded in paraffin. The 6-[micro]m-thick sections were stained with hematoxylin--eosin stain, and were examined, analyzed, and photographed under a light microscope (Eclipse LV100POL; Nikon, Tokyo, Japan).

For electron microscopy, small pieces of the retina were fixed in 2.5% glutaraldehyde in 0.1 M sodium cacodylate buffer (pH, 7.4) for 2 h, washed, and minced under a dissecting microscope. Postfixation was made in 1% osmium tetroxide in the same buffer for 3 h. Sectioning was made in an LKB Bromma 2088 Ultrotome V (Leica Instruments, Bannockburn, IL). Semithin to thin (approximately 1-[micro]m-thick) sections were stained with 1% methylene blue, whereas ultrathin sections were stained with uranyl acetate and lead citrate, and were examined using a transmission electron microscope (H-7000; Hitachi, Tokyo, Japan).

Morphometry

The total membrane area of the rhabdomeric microvilli present beneath a unit surface area of the retina was estimated in the central part of the retina around the main axis of the eye. The procedure for the estimation follows that of Weibel et al. (1966): The mean volume of the rhabdomeres per unit volume of the rhabdomeric layer of the retina (Vv) was estimated stereologically by differential point counting (Weibel et al. 1966) on the electron micrographs covering the entire zone from the proximal to the distal margin of the rhabdomeric layer. The height of the rhabdomeric layer (H) was directly measured by light microscopy of semithin sections of the epoxy-embedded retinas cut longitudinally along the receptor cells. The total volume (V) of rhabdomeres present beneath a unit surface area of the retina was obtained as

V = H Vv.

The mean diameter of the rhabdomeric microvilli (D) was estimated on the electron micrographs by randomly choosing portions where the microvilli were cut at right angles to their long axes. The cross-profiles of microvilli were also counted on the same portions, and the mean number of profiles per unit area (Na) was calculated. By assuming that each microvillus is a cylinder, the collective membrane area of the microvilli contained in the unit volume of the rhabdomere (Sv) was calculated as

Sv = [pi]D Na.

The total membrane area of the microvilli present beneath the unit surface area of the retina (S) was then calculated as

S = Sv V = [pi]D H Na Vv.

Statistical Analysis

All data are expressed as mean [+ or -] SD. These statistical analyses were performed using SPSS 11.5 (SPSS, Inc., Gary, NC) statistical software and Microsoft Excel 2003 (Microsoft, Redmond, WA).

RESULTS

Histological Features of Eye Development

The development of the retina can be observed with the light microscope during early life history (Plate 1). The fundamental structure of the retina was almost the same from newly hatched juveniles to the adults (Plate 1). By light microscopy, 4 layers were distinguished in the wall of the eyeball. Proceeding centripetally, these layers are (1) the rhabdomeric layer, (2) the subrhabdomeric layer, (3) the inner segmental layer, and (4) the plexiform layer (Plate 1). The rhabdomes and supporting cells cover much of the internal surface of the eye; but, near to the cornea, the rhabdomes are absent. In this region there are pigmented cells and mucous cells (Platel-1). The [FIGURE OMITTED] layer and the inner segmental layer rapidly increased in height after hatching (Plate 1).

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Morphometry of Rhabdomeres

Morphometric data on the rhabdomeres and the lens in both adult and newly hatched juvenile retinas are presented in Table 1. The rhabdomere data were obtained from the central area of each retina. The rhabdomeric layer increased in height during development, attaining, at the time of hatching, about a fifth of that of the adult retina. From 1-88 days after hatching, the thickness of the rhabdomeric layer (H) shows an exponential increase with days (d) (H - 34.117Ln(d) + 31.752, [r.sup.2] = 0.9404, n = 65). The relationship is very strong, but the volume fraction occupied by rhabdomeres in the rhabdomeric layer, the numerical density of the microvilli in the rhabdomere, and the diameter of each microvillus show an inconspicuous growth. These parameters obtained from 1 88 days old are almost the same as those in the adult retinas. The diameter of lens (DL) shows a linear increase with days (d) (DL = 0.0735 d + 0.31, [r.sup.2] = 0.9723, n = 65) with a very strong relationship as well. Calculated from these parameters, the total surface area of the rhabdomeric microvilli present beneath a unit surface area of the retina (S) shows an exponential increase with developmental days (d) (S = 119.54Ln(d) + 151.87, [r.sup.2] = 0.9548, n = 65), demonstrating a strong relationship.

UItvastructure of the Developing Retina

The ultrastructural features of the developing retina are almost constant over a wide range of the central area, but are somewhat different between the central and the marginal areas of the retina. The following descriptions are limited to the central area of the retina.

The rhabdomeric layer increases in thickness from about 49.9 [micro]m at 1 day old to 196.4 [micro]m at 88 days old to 247.7 [micro]m in the adult. On the lateral surface of the growing apical processes, microvilli increased in length and regularity (Plate 2 and Plate 3-20, 3-21). In longitudinal sections of the apical processes, the microvilli are arranged at right angles to the long axis of each apical process (Plate 3-20, 3-21). The top of the apical process is often free from microvilli. In cross-sections, the microvilli arise radially in all directions from the round circumference of the apical process (Plate 2). At early stages, the microvilli are short but more or less regular in shape; they are cylindrical, with a narrow neck at each base (Plate 3-22); with the development of the retina, the microvilli become slender and more regular in shape (Plate 3-20, 3-21). In some profiles, the microvilli arise in a radial fashion, but in others, the circumferences are partly free from microvilli (Plate 2). From the cross-sectional profiles of the apical processes, we can easily see that the 2 long sides of the rectangle give off microvilli in opposite directions. The short sides are usually free from the microvilli. Thus, at least within a small region, the microvilli are classified into 2 groups arranged perpendicular to each other (Plate 2). The microvilli from contiguous apical processes are opposed, tip to tip, or are arranged in perpendicular fashion. Thus, the basic pattern of a square rhabdome composed of rhabdomeres from 4 contiguous cells can be seen even in the retinas of newly hatched juveniles.

From the cross-sectional profiles of the apical processes, the shape of the apical processes are various, such as round, spindle, linear, trigonal, and so on (Plate 2). The apical processes contain pigment granules and small vesicles. Small vesicles of various shapes--flat, tubular, and round (Plates 24)--coming from microvilli, contain some pigment granules and then release the pigment granules when they get to the apical processes. Usually the pigment granules are crowded near the distal end and base of the process, then gradually increase in number and often form a large aggregation (Plate 3-21). As more and more vesicles come from microvilli, some microvilli degenerate (Plate 4-24). With the number of the pigment granules increasing, the apical process becomes nonelectron lucent. In addition, unlike other cephalopods, the size of the pigment granules is too small and it is difficult to measure their diameter.

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The subrhabdomeric layer shows an irregular increase during development. According to the measure, the thickness of the subrhabdomeric layer fluctuates between 5.5 [micro]m at 38 days old and 22.9 [micro]m at 5 days old. The cytoplasmic features in the subrhabdomeric layer are similar to those in the apical process. There exist numerous pigment granules, sparsely scattered small vesicles of various shapes, mitochondria, Golgi apparatuses, and myeloid bodies (Plate 5). Mitochondria and Golgi apparatuses are rare, but increase somewhat in number near the distal end (Plate 5). Myeloid bodies are very few in number and are small stacks of lamellae made of juxtaposed paired membranes, measuring about 0.5-1 [micro]m in width, increasing in size and number thereafter with development (Plate 5-29, 5-30). Between the myeloid bodies, the rough-surfaced endoplasmic reticulum is usually observed (Plate 5-31). In addition, we can observe that the number of the nuclei in the subrhabdomeric layer of juveniles between 1 day and 28 days old is very large, but decreases with age. After 68 days, there are nearly no nuclei found in the inner segment. Nuclei in the subrhabdomeric layer ceaselessly pass through the basal lamina into the inner segment with development (Plate 1 and Plate 6-32), become a little slender than those of the nuclei in inner segment cells, and have very electron-dense nucleoplasm with many patches of heterochromatin (Plate 6-32). The supporting cells increase in number and send out very long microvilli into the rhabdomeric layer (Plate 5-28, 29). Meanwhile, the electron-lucent of the whole sub- rhabdomeric layer is increasing (Plate 5-28, 29).

The inner segmental layer increases more regularly than the subrhabdomeric layer, but not as regularly as the rhabdomeric layer. The inner segmental layer fluctuates between 39.8 [micro]m at age 21 days and 117.2 [micro]m in the adult. The inner segmental layers are rich in membranous organelles such as Golgi apparatus and cisternae of rough endoplasmic reticulum, in addition to the previously mentioned myeloid bodies (Plate 6-33, 6-34). The cytoplasm also contains microtubules and numerous free ribosomes. Mitochondria increase in number remarkably. The nuclei in the inner segmental layer increase in number as they ceaselessly arrive from the subrhabdomeric layer, become somewhat irregular in outline, and mostly distribute in the proximal half of the plexiform layer (Plate l). Heterochromatin of the nucleus becomes more conspicuous after the nucleus enters into the inner segments (Plate 6-33, 6-34).

The plexiform layer consists of the receptor cell axons, efferent nerve fibers, mitochondria, Golgi apparatuses, and glial cells. With the development of the retina, the structure of plexiform layer becomes stronger (Plate 6-35).

In addition that previously mentioned, at the bottom of the rhabdomeric layer a tissuelike ink is often observed that has not been described in other cephalopod retinas (Plate 7-36, 7-37). We speculate it is a vestigial nerve board, and no suggestion can be made here regarding functionality of this structure.

Finally, the schematic three-dimensional reconstruction of the S. esculenta retina can be drawn on the basis of our findings based on both light and electron microscopy (Plate 8; modified from Yamamoto et al. 1965).

DISCUSSION

The histology of the retina of S. esculenta agrees closely with that shown in decapod cephalopods (Young 1936), Octopus vulgaris (Cazal & Bogoraze 1944, Yamamoto et al. 1965), and Sepiellajaponica (Yamamoto 1985). The basic structure of the eye at hatching is almost the same as that of the adult, containing lens, iris, cornea, and retina (Plate 1-1). Four layers can be distinguished in the wall of the retina (Plate 1). Proceeding centripetally, these layers are: (1) the rhabdomeric layer, (2) the subrhabdomeric layer, (3) the inner segmental layer, and (4) the plexiform layer. This structure is different from the vertebrate retina, which contains 10 layers: (1) retinal pigment epithelium, (2) cone and rod layer, (3) outer limiting membrane, (4) outer nuclear layer, (5) outer plexiform layer, (6) inner nuclear layer, (7) inner plexiform layer, (8) ganglion cell layer, (9) nerve fiber layer, and (10) inner limiting membrane (Blaxter & Janes 1967). Obviously, the number of layers distinguishable in the cephalopod retina is much less than that in vertebrate retinas, and the order of the retina layer in the cephalopod is opposite that of the vertebrate retina. Maybe these differences could be explained by the result of convergent evolution (Packard 1972). Otherwise, different species may have different structures. For example, both Nautilus and S. esculenta belong to Cephalopoda and Mollusca; however, there are no ocular muscles that would allow the eye to move or accommodate in the eye of Nautilus, and no lens or cornea--merely a "pinhole" aperture of narrow diameter to admit light (Barber 1967).

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Morphogenetic data on the rhabdomeres in the development of the retina have been briefly described in cuttlefish by several authors (Yoshida et al. 1976, Lemaire & Richard 1978, Yamamoto 1985). Their results are mostly confirmed by the current report. In this study, we find that there are no significant differences in the volume fraction occupied by rhabdomeres in the rhabdomeric layer, the density of the microvilli in the rhabdomere, and the diameter of each microvillus during the development (Table 1). Our morphogenetic data will be useful as a structural basis for further analyses of the development of the cephalopod visual system.

Yamamoto (1985) divided the development of the Sepiella japonica retina into 4 phases--from embryo to adult--on the basis of the morphological differentiation of the receptor cells. Accordingly, the development of the S. esculenta retina is attributed to the fourth phase. During this phase, the receptor cells have completed their specific differentiation when they hatch, and the apical processes continue to grow gradually. Wolken (1958) first described the rhabdome of the eyes of Octopus and Sepia as being formed from the radial arrangement of 4 retinula cells, which are separated from each other by pigment cells. This interpretation is questionable, inasmuch as Moody and Parriss (1961) and Zonana (1961), working with Octopus and Loligo, respectively, have shown that the rhabdome is made up of the tubule-bearing surfaces of the distal ends of 4 pigment-laden retinula cells. The closely packed tubules that make up the light receptor unit are oriented perpendicularly to the process from which they extend and show a uniquely regular pattern. Our own observations on the retina agree with those of the later workers.

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Yoshida et al. (1976) have suggested that the microvilli elongate by invagination, not by stretching of the plasma membrane. The formation of the microvilli, at any rate, requires the addition of new membrane to the cell surface. At the time of daily renewal of rhabdomeres in some arthropods, new microvilli are assembled in situ from sheets of endoplasmic reticulum (Itaya 1976, Stowe, 1980). In the frog photoreceptor, Besharse and Pfenninger (1980) have suggested that cytoplasmic vesicles are the precursors of the photoreceptive membranes and fuse with the plasma membrane adjacent to the connecting cilium. Previously, Kataoka and Yamamoto (1983) have proposed as a process of daily formation of rhabdomeric microvilli in adult Octopus ocellatus that large cytoplasmic cysts come into contact with the base of microvilli and form a group of closed microvilli, which then become open microvilli with constricted bases. Rhabdome formation during development is a more gradual process than the daily renewal. In the developing eyes of the crayfish Palinuridae (Hafner et al. 1982) and the moth (White et al. 1983), smooth endoplasmic reticular vacuoles or cisternae, which occur near the base of differentiating rhabdomeres, are presumed to be the source of the rhabdomere membrane. If we assume that membrane addition in the receptor cell of the cephalopod embryo occurs in the vicinity of growing, the only candidate for the source of membrane are irregularly shaped smooth vesicles that occur in clusters at the time of rapid elongation of the apical process. No clear continuity, however, has been found between these vesicles and the plasma membrane. Smooth vesicles are also present in high density in the distal cytoplasm of the apical processes of adult cephalopods (Yamamoto et al. 1965, Cohen 1973a). However, the formation of the microvilli in our research is not clear.

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In cross-sections through the rhabdomeric layer of the adult retina, rectangular profiles of the receptor cells are arranged in a rectilinear grid. The microvilli arising from contiguous cells are perpendicular to each other (Zonana 1961, Cohen, 1973a, Saibil, 1982). Such an ordered arrangement is consistent with the capacity to discriminate planes of polarized light, which has been revealed behaviorally (Moody & Parriss 1961) and electrophysiologically (Tasaki & Karita 1966, Saidel et al. 1983). Jander et al. (1963) have reported in 2 sepiolid cephalopods, Euprymna and Sepiotheuthis, that juveniles show polarotaxis in a vertical light beam. The rectilinear arrangement of the receptor cells and the crossed pattern of the rhabdomeric microvilli are established during development. The interesting question of how the capability of detecting polarized light depends on the orderliness of the rhabdomeric microvilli may be explained by taking advantage of the sensitivity to polarized light of early cephalopod development.

Yamamoto (1985) reported the ontogeny of the visual system in the embryonic cuttlefish S.japonica and found that the nucleus begins to pass through the basal lamina by constricting itself into the inner segments at stage 33 (about 20 days after fecundation). He also found that this phenomenon in the nucleus becomes less and less frequent with development. Our observations strongly sustain these results. The nucleus in the subrhabdomeric layer ceaselessly passes through the basal lamina into the inner segment with development. The number of nuclei in the subrhabdomeric layer of juveniles between 1 day and 28 days is very large, but decrease much with age. There are nearly no nuclei found in the inner segment after 68 days. We speculate that the migration of the nucleus may have a relation to the perfection of the visual organ.

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Lamellated membranes, called "myeloid bodies" by Zonana (1961) in squid material, were also found in the retinula cells of the eye of the cuttlefish we studied. Similar structures are present in the process-bearing cells of the S. esculenta body. Receptor cells in the adult cephalopod retina contain a large number of well-developed lamellated membranes (myeloid bodies), mainly in the inner segments (Yamamoto et al. 1965, Cohen 1973a). The myeloid bodies begin to develop later than the rhabdomeric microvilli, and are much smaller and fewer in the newly hatched juveniles than in the adult. In Octopus, Yamamoto et al. (1965) have demonstrated continuities of the lamellated membranes to the cisternae of rough endoplasmic reticulum, but in Loligo, Cohen (1973a) could not show such connections convincingly. The fact is that such connections are frequently found during the early phase of myeloid body formation.

Some scholars reported that the receptor cells of cuttlefish have cilia at early stages during development (Yamamoto et al. 1965, Cohen 1973a, Vanfleteren 1982). Eakin (1979) regarded such cilia as incidental and explained their presence by the developmental origin of the ocelli from the ectoderm, which is typically ciliated. Vanfleteren and Coomans (1976) have speculated that the ciliary structures induce the elaboration of photoreceptive plasma membranes and become more or less abortive (rhabdomeric type) or develop into a ciliary organelle (ciliary type) after they exert their inductive function. Salvini-Plawen and Mayer (1977) have postulated that photoreceptors evolved from primitive, nonspecialized cells that were provided with both simple cilia and some microvilli. In the our study, receptor cells completely lack ciliary structures. The fact is that many rhabdomeric photoreceptors possess cilia during embryonic or larval stages, and receptor cells of adult cephalopods completely lack ciliary structures (Yamamoto et al. 1965, Cohen 1973a). Ciliary induction of the rhabdomes seems to be improbable in the receptor cells of cuttlefish, because the cilia are always vestigial and they disappear from the receptor cells before the apical processes begin to be formed (Yamamoto 1985).

The presence of numerous pigment granules near the distal end and base of the process in S. esculenta can be observed, gradually increase in number, and often form a large aggregation (Plates 2-4). As observed by us, there are several obvious differences between the pigment granules of S. esculenta and that of the other described cephalopods (Young 1936, Cazal and Bogoraze 1944, Yamamoto et al. 1965, Yamamoto 1985). First, the pigment granules found in our study are much smaller in size and it is too difficult to measure their diameter and decide their shape. Second, some authors suggest that these pigment granules may come from supporting cells and could be used to alter the sensitivity of the cells by migration up or down the cell length, depending on light intensity (Young 1963). However, it is clearly seen that the pigment granules come from the vesicles. Whether they could be used to alter the sensitivity of the cells by migration up or down the cell length (depending on light intensity), as described in other cephalopods, is not revealed in the current study.

Except for the presence of pigment granules, there is a tissue-like ink observed very often throughout the development process at the bottom of the rhabdomeric layer, and to our knowledge, this has not been described in other cephalopod retinas. We speculate it is a vestigial nerve board, and no suggestion can be made here regarding functionality of this structure in the S. esculenta retina. Finally, based on our observations and measurements, we conclude that the visual acuity and sensitivity of S. esculenta continuously increases with development as a result of increasing total surface area of the rhabdomeric microvilli present beneath a unit surface area of the retina.

ACKNOWLEDGMENTS

The authors thank the staff of Key Laboratory of Mariculture, Ministry of Education, China, for their help with the experiment, and Dr. Nwafili, SA, of Ocean University of China for his comments on the manuscript. The authors are also grateful to the anonymous reviewers for the great elaboration of the manuscript through their critical reviewing and comments. This study was supported by funds from the National High Technology Research and Development Program ("863" Program) of China (grant no. 2006AA100303) and The Science & Technology Development Plans Projects of Qindao (grant no. 04-2-JZ-80).

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ZHEN-LIN HAO, (1) XIU-MEI ZHANG, (l) * ([dagger]) HIDEAKI KUDO (2) AND MASAHIDE KAERIYAMA (2)

(1) Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao 266003, Shandong, China; (2) Laboratory of Strategic Studies on Marine Bioresource Conservation and Management, Hokkaido University, 3-1-1 Minato-cho, Hakodate, 041-8611, Hokkaido, Japan

* Corresponding author. E-mail: gaozhang@ouc.edu.cn.

([dagger]) Current address: Fisheries College, Ocean University of China, 5 Yushan Road, Qingdao 266003, PR China.
TABLE 1.
Quantitation of the rhabdomeres in the central area
of the retina.

                 Height of
                Rhabdomeric           Diameter of
Age (days)   Layer * ([micro]m)        Lens (mm)

 1            49.9 [+ or -] 3.8    0.32 [+ or -] 0.04
 3            68.7 [+ or -] 4.9    0.33 [+ or -] 0.03
 5            85.2 [+ or -] 1.9    0.41 [+ or -] 0.02
 7            97.1 [+ or -] 7.0    0.63 [+ or -] 0.20
14            99.8 [+ or -] 5.5    0.82 [+ or -] 0.11
21           110.8 [+ or -] 2.6    1.15 [+ or -] 0.04
28           142.4 [+ or -] 7.8    1.80 [+ or -] 0.04
38           157.5 [+ or -] 3.8    3.00 [+ or -] 0.05
48           163.4 [+ or -] 2.6    3.69 [+ or -] 0.04
58           176.7 [+ or -] 5.9    4.30 [+ or -] 0.10
68           184.5 [+ or -] 2.0    5.61 [+ or -] 0.18
78           186.8 [+ or -] 2.6    5.84 [+ or -] 0.26
88           196.4 [+ or -] 3.0    7.51 [+ or -] 1.39
Adult        247.7 [+ or -] 5.0   12.40 [+ or -] 1.14

                                  Density of Microvilli
                                   in the Rhabdomere *
                Diameter of        (n/[micro][m.sup.2]
Age (days)    Microvillif (nm)      of cross-section)

 1           65.0 [+ or -] 3.7    165.O [+ or -] 5.2
 3
 5           66.7 [+ or -] 13.2   166.3 [+ or -] 11.3
 7           63.2 [+ or -] 4.1    165.8 [+ or -] 8.7
14           65.9 [+ or -] 2.8    163.7 [+ or -] 14.9
21
28           64.8 [+ or -] 1.8    164.7 [+ or -] 25.6
38
48           64.8 [+ or -] 2.2    166.8 [+ or -] 5.6
58
68
78
88           65.9 [+ or -] 5.1    165.5 [+ or -] 9.3
Adult

                                     Total Surface Area of
                                         Microvilli > 1
                                     [micro]m ([dagger]) of
                Volume Fraction         Retinal Surface
             of Rhabdomeres in the     ([double dagger])
Age (days)    Rhabdomeric layer *      ([micro][m.sup.2])

 1           0.108 [+ or -] 0.011    181.5 [+ or -] 15.7
 3
 5           0.120 [+ or -] 0.021    356.8 [+ or -] 10. 9
 7           0.117 [+ or -] 0.013    373.7 [+ or -] 7.5
14           0.113 [+ or -] 0.017    387.5 [+ or -] 10.2
21
28           0.116 [+ or -] 0.017    553.9 [+ or -] 6.6
38
48           0.111 [+ or -] 0.019    616.9 [+ or -] 10.9
58
68
78
88           0.108 [+ or -] 0.013    729.7 [+ or -] 15.3
Adult

* Mean values obtained from 5 individuals [+ or -] SD.

([dagger]) Mean of 300 microvilli (60 from each individual)
[+ or -] SD.

([double dagger]) Mean values calculated separately in 5
individuals [+ or -] SD.
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Author:Hao, Zhen-Lin; Zhang, Xiu-Mei; Kudo, Hideaki; Kaeriyama, Masahide
Publication:Journal of Shellfish Research
Article Type:Report
Geographic Code:9CHIN
Date:Aug 1, 2010
Words:5746
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