Germ cell differentiation and sexual maturation of the hanging cultured female scallop Patinopecten yessoensis on the east coast of Korea.

ABSTRACT Gonadosomatic index, germ cell differentiation, ovarian cycle and first sexual maturity in female Patinopecten yessoensis were studied by histologic and cytologic observations. In the early vitellogenic oocyte, the Golgi complex, mitochondria and endoplasmic reticulum were involved in the formation of lipid droplets. In the late vitellogenic oocyte, exogenous substances, namely, glycogen particles and lipid granular substances appeared in the germinal epithelium passed into the ooplasm through the microvilli of the vitelline envelope. Yolk granules and multivesicular bodies were involved in the formation of proteid yolk granules in the late vitellogenic oocyte. Vitellogenesis occurs by endogenous autosynthesis and exogenous heterosynthesis. The auxiliary cells function as nutritive cells in the formation and development of the previtellogenic and early vitellogenic oocytes in their early stages. Monthly changes in the gonadosomatic index were closely associated with ovarian developmental phases. The annual ovarian cycle of this species can be classified into 5 stages; early active stage (September to October), late active stage (November to February), ripe stage (March to May), spawning stage (April to June) and spent/inactive stage (June to September). The percentage of first sexual maturity was 56.3% in individuals of 61.0-70.9 mm in shell height, and 100% in those >81.0 mm.

KEY WORDS: Patinopecten yessoensis, germ cell differentiation, reproductive cycle, first sexual maturity, scallop 

INTRODUCTION

The scallop, Patinopecten yessoensis, is one of the important edible bivalves in East Asian countries including Korea, China and Japan (Yoo 1976, Kwon et al. 1993). In the east coast of Korea, this species is mainly found in fine sand in the subtidal zone of Jumunjin, Kangwondo, Korea (Yoo 1976, Kwon et al. 1993) and inhabits up to 20-30 m in depth. Because of the recent sharp reduction in the standing stock, which has been declining as a consequence of reckless overharvesting for commercial purpose (Park 1998), it has been denoted as a target and fisheries resource that should be managed using a more reasonable fishing regimen by hanging culture that can maintain an optimal population size. For the propagation and management of a living natural resource, it is important to understand its population characteristics with regard to oogenesis and ovarian development.

Previously, there have been many studies on aspects of reproductive ecology including reproductive cycle (Yamamoto 1943, 1950; Maru, 1976, 1978; Mori et al. 1977, Kawamata et al. 1981, Kawamata 1983, Chang et al. 1985, 1997), propagation and rearing (Ishihara 1966) and larval distribution and growth (Drew 1906, Yamamoto 1956, Ito et al. 1988, Yoo & Imai 1968, Yoo 1969, Maru 1972, Yoo & Park 1979, Yoo et al. 1981), on aspects of aquaculture including environmental condition of aquaculture (Yamamoto 1943, Imai 1977, Pyen & Rho 1978, Kang et al. 1982, Park et al. 2000) and aquaculture (Wildish et al. 1987, Kang et al. 1996, Wildish & Saulnier 1992, Yamamoto 1964, Lee & Chang 1977, Ventilla 1982, Tomita et al. 1982), on aspects of physiology including the digestive diverticula (Chang et al. 1989), tolerance (Yamamoto 1957, Maru 1985b), artificial insemination (Yamamoto & Nishioka 1943) and mortality (Yamamoto 1960), on ecology (Maru 1985a, Bower & Meyer 1990) and on morphology (Jorgensen 1946, Bourne et al. 1989) of P. yessoensis. However, there is still disagreement in our knowledge regarding reproductive biology. Especially, little information is available on ultrastructural study of germ cell differentiation (during oogenesis) and first sexual maturity of Patinopecten yessoensis. Understanding the reproductive cycle and the spawning period of this species will provide necessary information for natural and artificial spat collections or the recruitment period and age determination for aquaculture of this population. In addition, data on first sexual maturity and reproductive strategy of this population would be very useful information for natural resource management. However, reproduction studies involving examination of gonad samples from natural populations of Patinopecten yessoensis are very limited in Korea. Therefore, the main aim of this study is to describe the female germ cell differentiation during vitellogenesis, the ovarian cycle, spawning period and first sexual maturity of the scallop.

MATERIALS AND METHODS

Sampling

Specimens of the scallop, Patinopecten yessoensis were collected monthly from hanging culture at the subtidal zone (shellfish farm) of Jumunjin on the East Sea of Korea, for 1 year from January 1997 to December 1998 (Fig. 1). The scallops ranging from 41.4-129.7 mm in shell height were used for this study. After the scallops were transported alive to the laboratory, shell heights and total body weights were immediately measured.

[FIGURE 1 OMITTED]

Gonadosomatic Index

A total of 252 individuals was used to calculate the gonadosomatic index (GSI). Monthly changes in the mean GSI were calculated by the following equation:

GSI = Gonad weight (g) x 100/Meat weight (g)

Ultrastructure of Germ Cell by Electron Microscopic Observation

For electron microscope observations, excised pieces of the gonads were cut into small pieces and immediately fixed in 2.5% paraformaldehyde-glutaraldehyde in 0.1 M phosphate buffer (pH 7.4) for 2 h at 4[degrees]C. After prefixation, the specimens were washed several times with the same buffer and then postfixed in 1% osmium tetroxide dissolved in 0.2 M phosphate buffer solution (pH 7.4) for 1 h at 4[degrees]C. Specimens were then dehydrated in a series of increasing concentrations of ethanol, cleared in propylene oxide and embedded in Epon-Araldite mixture. Ultrathin sections of Epon-embedded specimens were cut with glass knives with a Sorvall MT-2 microtone and an LKB ultramicrotome at a thickness of about 800-1,000 [Angstrom]. Tissue sections were mounted on collodion-coated copper grids, doubly stained with uranyl acetate followed by lead citrate and examined with a JEM 100 CX-2 (80 kv) electron microscope.

Ovarian Cycle and First Sexual Maturity by Light Microscopy Observation

For light microscopic examination of histologic preparations, 216 female gonad tissues were removed from shells and preserved in Bouin fixative for 24 h and then washed with running tap water for 24 h. Tissues were then dehydrated in alcohol and embedded in paraffin molds. Embedded tissues were sectioned at 5-7-[micro]m thickness using a rotary microtome. Sections were mounted on glass slides, stained with Hansen hematoxylin-0.5% eosin, Mallory triple stain and PAS stain and examined using a light microscope.

For the study of first sexual maturity, 101 female individuals (41.4-129.7 mm in shell height) were histologically examined to certify shell heights that reached maturation and participated in reproduction from March to July.

RESULTS

Position and Morphology of the Ovary 

The scallop Patinopecten yessoensis was a dioecious organism composed of well-define male and female individuals (Fig. 2). The gonad is separated from digestive diverticula and the midintestinal gland. As the gonads were getting mature, they were extended to the adductor muscle near digestive diverticula. The gonads were composed of a number of follicles. As maturation progresses the external features of the sex of clams can be easily distinguishable, because the ovary shows light pink and the testis yellowish white in color. At this stage, if they are slightly scratched with a razor, ripe eggs flow out readily. Therefore, their sexes could be easily distinguishable by visual observation and dissection. After spawning, the gonads degenerated, and it became difficult to distinguish their sexes by external color or dissection.

[FIGURE 2 OMITTED]

Monthly Changes in the Gonadosomatic Index and Water Temperature

Monthly gonadosomatic index GSI changes in females were shown in Fig. 3. In 1997, the GSI values slowly increased between February and March. Their values reached the maximum (mean 22.5) in April when seawater temperature gradually increased. Then, the GSI rapidly decreased from May to July when higher water temperatures were maintained and spawning occurred. Thereafter, the value temporarily reached the minimum in October (mean 2.5) when spawning was completely finished. Monthly GSI changes in 1998 showed a similar result to those in 1997.

[FIGURE 3 OMITTED]

Ultrastructure of Germ Cells During Oogenesis

Based on ultrastructural observations, the germ cell developmental phases during oogenesis can be classified into 4 phases: (1) oogonial phase; (2) previtellogenic phase; (3) vitellogenic phase and (4) mature phase. Characteristic features in each phase were as follows:

Oogonial Phase

Oogonia that propagated on the follicle wall were 10 [micro]m in diameter. They were a single or formed a cluster on the germinal epithelium. Each oogonium had a large nucleus with chromatin, several mitochondria and the endoplasmic reticulum in the cytoplasm (Fig. 4A).

[FIGURE 4 OMITTED]

Previtellogenic Phase

With cytoplasmic growth, several small mitochondria, well-developed endoplasmic reticulum and several vacuoles were concentrated around the nucleus in the cytoplasm of the previtellogenic oocyte. The Golgi apparatus scattered from the perinuclear region to the cortical region of the oocyte. At this time many vacuoles formed by the Golgi apparatus appeared in the endoplasmic reticulum and some mitochondria and auxiliary ceils were present around the vitelline envelop of the previtellogenic oocyte.

At this stage, auxiliary cells migrated from the periphery of the follicle, establishing an intimate contact with the previtellogenic oocytes. The attached auxiliary cells also showed cytologic modifications as their cytoplasmic volume increased. The mitochondria, endoplasmic reticulum, lipid-like granules, small number of vacuoles and myelin figures appeared in the cytoplasm of the auxiliary cells (Fig. 4B)

Vitellogenic Phase

In the early vitellogenic oocyte, especially with the initiation of yolk formation, lipid droplets were found in the vacuoles formed by the Golgi complex in the perinuclear region (Fig. 4C). The plasma membrane changed as the oocyte became peduncular.

The oocyte detached from the auxiliary cells at the end of their peduncular stage. Close contact was maintained with the auxiliary cell. Near the adherence zone, several vacuoles and myelin figures appeared, indicative of membrane breakdown in the cytoplasm of the auxiliary cells. Endocytotic figures may be seen between the vitellogenic oocyte and the auxiliary cell, indicating a transfer of nutrients. Lipid droplets diffused toward the cortical layer, and then, lipid yolk granules appeared around a well-developed cortical region of early vitellogenic oocytes. Well-developed endoplasmic reticulum and annulus lamella were present around the mitochondria and the multivesicular body that was formed by the modified mitochondria and appeared in the cytoplasm (Fig. 4D). In the late vitellogenic oocyte, accumulation of lipid droplets by the Golgi complex, which is composed of the Golgi sac, Golgi vacuole and Golgi vesicle began in the vacuoles and vesicles (Fig. 5A). Exogenous lipid granular substances and glycogen particles in the germinal epithelium were passed into the ooplasm of the oocyte through the microvilli of the vitelline envelope. At this time, a number of multivesicular bodies (which was formed by the modified mitochondria) and yolk granules were involved in the formation of proteid yolk granules (Figs. 5B-5D). Yolk precursors, such as glycogen particles (carbohydrate yolk precursor), lipid yolk granules and proteid yolk granules were accumulated in the cytoplasm. Eventually, their yolk granules consisting of several different components were intermingled and became a small immature yolk granule (Fig. 5E).

[FIGURE 5 OMITTED]

Mature Phase

In the mature oocyte, small immature yolk granules were continuously mixed with each other and became large mature yolk granules in the cytoplasm. A mature yolk granule is composed of 3 components; (1) main body (central core); (2) superficial layer and (3) a limiting membrane (Fig. 5F).

Ovarian Cycle with Gonad Developmental Stages

Based on histologic observation of the germ cells and other surrounding cells, the gonad developmental stages were classified into five successive stages (Fig. 6). The criteria in defining each stage are as follows:

[FIGURE 6 OMITTED]

Early Active Stage

The gonadal volume was small, and the follicles occupied approximately 25% of the gonad. The follicular walls were thick. At this stage, several oogonia of 10 [micro]m in diameter were present along the follicular walls of the ovary, and the previtellogenic oocytes appeared. Previtellogenic oocytes of 15-25 [micro]m in diameter formed an egg-stalk attached to the follicle wall, and many attached auxiliary cells and undifferentiated mesenchymal cells appeared at this stage (Fig. 7A). In 1997 and 1998, the individuals in the early active stage were found from September to October when seawater temperatures were gradually decreased.

[FIGURE 7 OMITTED]

Late Active Stage

This stage is characterized by the presence of early vitellogenic oocytes. Follicular walls of oogenic follicles were thin. Several early vitellogenic oocytes of 30-40-[micro]m in diameter were attached to the follicular walls through each egg-stalk. With yolk formation proceeds, there were numerous yolk granules in the cytoplasm of late vitellogenic oocytes of 45-50 [micro]m. Some fully ripe oocytes were free in the lumen of the follicle. At this stage, auxiliary cells (detached from the oocyte) gradually disappeared (Fig. 7B). The individuals in the late active stage appeared from November to February in 1997 and 1998.

Ripe Stage

Follicles occupied over 70% of the gonad, and follicular walls became thin. Mature oocytes growing up to 60-73-[micro]m diameter became polygonal in shape, and contained several mature yolk granules (Figs. 7C, D). In 1997 and 1998, ripe ovaries were found in March to May when seawater temperatures gradually increased.

Spawning Stage

The lumen of the oogenic follicle became considerably empty because approximately 50% to 60% of ripe oocytes in the lumen were discharged. Spawned ovaries were characterized by the presence of a few undischarged and young oocytes in the follicle (Fig. 7E). The individuals in the spawning stage appeared from April to June when seawater temperatures were greater than 20[degrees]C.

In 1997 and 1998, spawning occurred once a year from April to June, and the main spawning occurred between April and May when seawater temperatures are gradually increased.

Spent/Inactive Stage

After spawning, each follicle was contracted, and then degeneration or resorption of the oocytes occurred. Thereafter, the connective tissues and a few oogonia and oocytes appeared on the newly formed follicular walls (Fig. 7F). The individuals in the spent/inactive stage were found from June to September in 1997 and 1998.

First Sexual Maturity

During the breeding season, a total of 101 individuals (41.4-129.7 mm in shell height) were histologically examined to check whether they reached maturity and participated in reproduction. The rate of scallops of different size that reached first sexual maturity is summarized in Table 1. The breeding season of P. yessoensis was found to be from April to June. In the case of some individuals with ovarian developmental stage in the late active stage, it is supposed that they can reach maturity except for individuals in the early active stage during the breeding season. First sexual maturity was 0% in female scallops of 41.4-49.9 mm in shell height if they were at the early active stage during the breeding season, as small number of oogonia and the previtellogenic oocytes were present in the follicle of the ovary.

The percentage of first sexual maturity of female scallops of 50.0-59.9 mm in height was 26.7%: most of the individuals were still in the early active stage. The percentage of first sexual maturity in 60.0-69.9 mm in shell height were 56.3%, all of which were at the late active, ripe, partially spawned stages. First sexual maturity was 100% for scallops of 80.0 mm in height.

Shell Height of Sexually Mature Scallops

Shell height of sexually mature scallops (50% of rate of group maturity) that fitted to an exponential equation was 63.79 mm in shell height (Fig. 8).

[FIGURE 8 OMITTED]

DISCUSSION

Germ Cell Differentiation During Vitellogenesis

Lipid droplets often arise in the cytoplasm of the oocytes before proteinaceous yolk synthesis begins (Humphreys 1962). Reverberi (1971) reported that the Golgi complex present in the perinuclear region is involved in lipid droplet formation in Mytilus edulis. Chung and Ryou (2000) reported that in the vitellogenic oocytes of Mactra veneriformis, the Golgi complex and mitochondria in the perinuclear region are involved in lipid droplet and lipid granule formation. It is possible that the Golgi complex and mitochondria present in the perinuclear region may be involved in lipid droplet formation in the oocyte as observed in M. veneriformis. The yolk granules originate first in the cortical regions of the oocyte, and then fill the entire ooplasm of the oocyte. Yolk granules vary in different regions of the egg. Therefore, various cell organelles, namely, the Golgi apparatus, mitochondria, endoplasmic reticulum and vacuoles are believed to be involved in endogenous formation of yolk granules in the cytoplasm. Some mitochondria in late vitellogenic oocytes of P. yessoensis seem to undergo a process of transformation during late vitellogenesis, and some evidence affirms that the yolk precursor are derived from modified mitochondrial structure found in the cytoplasm. The endoplasmic reticulum and modified mitochondria are present near the proteid yolk granules, however, we did not find pinocytotic tubules, which are believed to be involved in yolk production as seen in the vitellogenic oocytes of Agriolimax reticulatus (Hill & Bowen 1976, Dohmen 1983). Accordingly, it is assumed that the endoplasmic reticulum and modified mitochondria are involved in the formation of proteid yolk granules (Taylor & Anderson 1969). Light microscope observations with the PAS stain showed a strong positive reaction at the site of the egg-stalk of the late active oocyte connected to the follicle wall (germinal epithelium). At this time, according to the results by electron microscope observation, lipid granular substances and glycogen particles in the germinal epithelium are passed into the ooplasm of the oocyte through the microvilli of the vitelline envelope. Therefore, we assume that some vitellogenic substances in the late vitellogenic oocyte are originated from exogenous substances in the germinal epithelium during vitellogenesis.

Function and Fate of the Auxiliary Cells with the Reproductive Cycle

In the early active stage, the auxiliary cells that appeared at the periphery of the follicle migrated the early developing germ cells and then the cells initially appeared close to the previtellogenic oocyte, thereafter, progressively surround the oocyte. At this stage, a small number of vacuoles and myelin-like bodies (myelin figures) were visible in the cytoplasm of the auxiliary cells near the adherence zone. By and by, the attached auxiliary cells appeared to have cytologic modifications as their cytoplasmic volume increased. In this study, several auxiliary cells attached to a previtellogenic oocyte appeared from the early active stage. However, in the late active stage (end of the vitellogenic phase), the vitellogenic oocytes, which attached to the auxiliary cells, were gradually detached from auxiliary cells. At the adherence zone of the auxiliary cells and vitellogenic oocyte, lipid droplets surrounded by the myelin figures, several vacuoles and a small number of myelin figures appeared in the cytoplasm of the auxiliary cell, indicative of membrane breakdown, as seen in Mytilus edulis (Pipe 1987). Endocytotic figures may be seen between the vitellogenic

********** oocyte and the auxiliary cell, indicating nutrient transfer. Similar ultrastructural changes have been observed in the auxiliary cells of Mytilus edulis (Pipe 1987). In the ripe stage, several auxiliary cells almost disappeared from the mature oocyte. Therefore, it is assumed that auxiliary cells function as nutritive cells in the formation and development of the germ ceils in their early stages.

Fate of the Gametes

After spawning gamete resorptions, common in the follicles of the ovary, are also observed in P. yessoensis. Regarding fate of the gametes, Morvan & Ansell (1988) and Paulet (1990) stated that the continuous production and resorption of gametes may be regarded as an adaptation to environmental temperature and food availability. If the reproductive energy allocated to production of gametes is too large, nutritive reserves may not be enough to allow all eggs to reach the critical size for spawning and fertilization. Under these conditions, the products of gamete atresia would be resorbed and the energy reallocated to still-developing oocytes or used for other metabolic purpose by the bivalves (Dorange & LePennec 1989, Mortavkine & Varaksine 1989). Therefore, it is assumed that the bivalve should have a reproductive mechanism to resorb and use the high nutritive substances, rather than releasing hopless gametes.

Breeding Pattern

Comparisons of spawning periods of P. yessoensis in different localities (latitude) are shown in Table 2. From this study by histologic observations, in case of Korea, spawning of P. yessoensis in Jumunjin, the East Sea of Korea, occurs from April to June and in the scallop from Gosung-gun, the East Sea is also from April to June (Chang et al. 1997). Therefore, our result about the spawning period shows a similar pattern to Gosung-gun, the East Sea of Korea. As shown in Table 2, the Japanese P. yessoensis has been reported to spawn once a year from April through May to June in Toni Bay and Funka Bay, Japan, and spawning occurs from May through June to July in Lake Saroma and Abashiri waters, Hokkaido, Japan. Therefore, our results coincide with the result of Mori et al. (1977) and Kawamata (1983). However, the spawning period of the scallop in Jumunjin, Korea is 20-30 days faster than that of Lake Saroma in Japan. Slight discrepancy in the spawning period between these several studies might be related to geographic differences in environmental conditions such as water temperature and food availability as reported in Mactra veneriformis (Chung & Ryou 2000).

Spawning of P. yessoensis in Korea occurs from April to June, therefore, this species may be classified as a summer breeder, based on the criteria for classification of the breeding season of marine molluscs by Boolootian et al. (1962).

First Sexual Maturity

Percentage of first sexual maturity of female individuals of 61.0-70.9 mm in shell height was 56.3%, and 100% for scallop greater than 81.0 mm in shell height. According to the growth curves for the mean shell height fitted to yon Bertalanfy equation by Park (1998), ages and shell heights are as follows: age (years); mean shell height (mm) 0.5: 28.4, 1.0: 69.4, 1.5: 91.4, 2.0:113.2, 2.5: 127.0, 3.0:142.0

Therefore, individuals ranging from 61.0-70.9 mm (group maturity, 63.79 mm) in shell height are considered to be 1 year old. We assumed that this female population achieve maturity and begin reproduction at 1 year of age. In the aspect of natural resource management, this result suggests that catching scallops <63.79 mm in shell height will cause a drastic reduction of its recruitment. Therefore, catching shells <63.79 mm in shell height should be prohibited for adequate natural resource management.

ACKNOWLEDGMENTS

The authors thank Dr. John B. Burch of the University of Michigan for helpful comments on the manuscript. This research was supported in part by the fund (1997-1998) from the Gangnung Hatchery, East Sea Fisheries Research Institute.

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EE-YUNG CHUNG, (1) * YOUNG-JE PARK, (2) JEONG-YONG LEE (3) AND DONG-KI RYU (1)

(1) School of Marine Life Science, Kunsan National University, Kunsan 573-701, Korea; (2) West Sea Fisheries Research Institute, National Fisheries Research and Development Institute, Incheon 400-420, Korea; (3) Research Planning Department, National Fisheries Research and Development Institute, Busan 619-902, Korea

* Corresponding author. E-mail: [e-mail]

TABLE 1.
Shell height of first sexual maturity in female Patinopecten
yessoensis during the breeding season.

                    Number of Individuals by the Gonadal Stage *
Shell Height
(mm)           EA   LA   RI   PS   SP/IA   Total   Mature (%)

 41.4-49.9     10                            10        0
 50.0-59.9     11   2    2                   15       26.7
 60.0-69.9      6   3    5    2              16       56.3
 70.0-79.9      2   3    6    4      2       17       88.2
 80.0-89.9          2    7    4      1       14      100.0
 90.0-99.9               5    3      2       10      100.0
100.0-109.9              3    3      2        8      100.0
110.0-119.9              1    2      3        6      100.0
120.0-129.7              1    2      2        5      100.0
Total                                       101

* Gonadal stage: EA, early active stage; LA, late active stage; RI,
ripe stage; PS, partially spawned stage; SP/IA, spent/inactive
stage.

TABLE 2.
A comparison of spawning periods of Patinopecten yessoensis with
locality.

       Locality (latitude)          Culture Method   Spawning Periods

Juminjin, Kangwon-do, Korea
  (37[degrees]50'N)                    Hanging          April-June
Gosung-gun, Kangwon-do, Korea
  (38[degrees]20'N)                    Hanging          April-June
Toni Bay, Iwate Prefecture, Japan
  (39[degrees]N)                       Hanging          April-May
Funka Bay, Hokkaido, Japan
  (42[degrees]N)                        Sowing          April-June
Saroma Lake, Hokkaido, Japan
  (44[degrees]N)                       Hanging           May-June
Abashiri waters, Hokkaido, Japan
  (44[degrees]N)                        Sowing           May-July

       Locality (latitude)          References

Juminjin, Kangwon-do, Korea
  (37[degrees]50'N)                 Present study
Gosung-gun, Kangwon-do, Korea
  (38[degrees]20'N)                 Chang et al. 1997
Toni Bay, Iwate Prefecture, Japan
  (39[degrees]N)                    Mori et al. 1977
Funka Bay, Hokkaido, Japan          Kawamata et al. 1981;
  (42[degrees]N)                      Kawamata, 1983
Saroma Lake, Hokkaido, Japan
  (44[degrees]N)                    Maru 1978
Abashiri waters, Hokkaido, Japan
  (44[degrees]N)                    Chang et al. 1985