Oogenesis and sexual maturation in Meretrix lusoria (Roding 1798) (Bivalvia: Veneridae) in western Korea.
KEY WORDS: Meretrix lusoria, germ cell differentiation, oogenesis, size at first sexual maturity
The hard clam, Meretrix lusoria (Roding 1798) is a commercially important bivalve in East Asian countries, including Korea, Japan, and China. On the west coast of Korea, this species is mainly found in silty sand in the tidal fiats and subtidal zone (Yoo 1976, Kwon et al. 1993), up to 10-15 m in depth (Ikuta 1988a, Ikuta 1988b). Recently the production levels per year of this species were recorded as 4,315 M/Ts in 1996, 1,799 M/Ts in 1999, and 1,704 M/Ts in 2002 (Ministry of Maritime Affairs and Fisheries, Republic of Korea 2004). Because of past over-harvesting, it has been denoted as a fisheries resource that should be managed using a more reasonable fishing regimen. For the propagation and management of a living natural resource, it is important that we understand its reproductive biology with regard to germ cell differentiation during oogenesis and sexual maturation.
Many studies have been conducted to investigate aspects of reproductive ecology, including artificial gamete discharge (Iwata 1948), artificial fertilization and development (Choi & Song 1974), early embryonic development and growth (Choi 1975, Hur 1994), the reproductive cycle (Lee 1997) and spawning season (Taki 1949, Choi & Song 1974), aspects of ecology; including propagation (Tanaka 1969), habitat and distribution (Yoo 1976; Kwon et al. 1993) and production (Chun et al. 1981), aspects of physiology, including an environmental survey of cultivation ground (Lee & Kim 1991), acute toxicity tests on some heavy metals (Ikuta 1988a, Ikuta 1988b), morphological and cytological characteristics of hemocytes (Park et al. 2002), effects of some hazardous substances (Lee 1991), and trematode parasite infection (Chun & Lee 1976) of M. lusoria. However, there is still disagreement in our knowledge regarding reproductive biology. Little information is available on the ultra-structures of germ cell differentiation and follicle cells during oogenesis and size at first sexual maturity of Meretrix lusoria. Understanding of the reproductive cycle and spawning period of this species will provide information needed for the determination of age and recruitment period. Additional information on the size at sexual maturity can determine a prohibitory size (50% of size at sexual maturity) for adequate natural resources management. Therefore, the purpose of this study is to describe vitellogenesis during oogenesis, the reproductive cycle, and the size at sexual maturity for M. lusoria using cytological, histological, and morphometric procedures. Results will be used for improved fisheries management of this species.
MATERIALS AND METHODS
Specimens of Meretrix lusoria were collected monthly by dredging to water depths of 10-20 m at the intertidal and subtidal zones of Simpo, on the west coast of Korea (Fig. 1), for two years from January 2002 to December 2003. After the live clams were transported to the laboratory, shell lengths and heights were measured by a Vernier caliper, and total weights were obtained using a top-loading electric balance (Casbee MW-120). Seawater temperatures were measured daily at 10:00 AM by the Kunsan Regional Maritime Affairs and Fisheries Office.
[FIGURE 1 OMITTED]
Ultrastructure of Germ Cells and Follicle Cells During Oogenesis and Oocyte Degeneration
For transmission electron microscope (TEM) observations, excised pieces of ovaries were cut into small pieces and fixed immediately in 2.5% paraformaldehyde-glutaraldehyde in 0.1 M phosphate buffer solution (pH 7.4) for 2 h at 4[degrees]C. After prefixation, the specimens were washed several times in the buffer solution and then postfixed in 1% osmium tetroxide solution in 0.2 M phosphate buffer solution (pH 7.4) for 1 hr at 4[degrees]C.
Specimens then were dehydrated in increasing concentrations of ethanol, cleared in propylene oxide, and embedded in an Epon-Araldite mixture. Ultrathin sections of Epon-embedded specimens were cut with glass knives on a Sorvall MT-2 microtome and a LKB ultramicrotome at a thickness of about 800-1000 [Angstrom]. Tissue sections were mounted on collodion-coated copper grids, doubly stained with uranyl acetate followed by lead citrate, and observed with a JEM 100CX-2 (80 kv) electron microscope.
For light microscopic examination of histologic preparations, female ovarian tissues were removed from shells and preserved in Bouin fixative for 24 h and then washed with running tap water for 24 h. Tissue 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. After histologic preparations produced by histolocal methods mentioned earlier, (1) the gonad index; (2) the ovarian cycle; and (3) the size at sexual maturity were analyzed by histologic preparations. The methods for their studies in detail were as follows:
Gonad Index and the Ovarian Cycle by Light Microscopic Observation
To identify the spawning period, a total of 422 ovarian histologic preparations (60.2-96.4 mm in shell length) were examined for determination of the GI from January 2002 to December 2003. The mean GI was calculated using a modification of Mann's methods (1979). Each histological section of ovarian tissue was also examined in detail to assess the stage of ovarian development and was scored on a 1-5 scale to describe five stages of ovarian activity: 1 = spent/inactive stage (S1); 2 = partially spawned stage (S2); 3 = early active stage (S3); 4 = late active stage (S4); and 5 = ripe stage ($5). The mean GI was obtained by multiplying the number of female clams in each stage by the numerical ranking of that stage (NRVs) and dividing the resulting value by the total number of clams in the sample. The arithmetic mean of the individual scores of the whole samples was recorded as the G| for each month. The following formula was used to determine the GI.
GI = (NRVS 1) + (NRVS2) + (NRVS3) + (NRVS4) + (NRVS5)/ Total N observed by month
The high average values of GI coincide with gonadal maturity. Minimal average values following high average values are considered an indication of spawning (Chung et al. 1998).
For the study of the ovarian cycle with the ovarian developmental stages, a total of 422 ovarian histologic preparations (60.2 96.4 mm in shell length) were histologically examined for determination of ovarian developmental stages from January 2002 to December 2003.
Size at First Sexual Maturity by Light Microscopic Observation
For the study of the size at first sexual maturity, a total of 221 ovarian preparations (26.3-96.4 mm in shell length) were histologically examined for evidence of maturation and spawning from May to October 2002. The size equivalent to 50% of size at sexual maturity was estimated to be the biological minimum size for natural resource management.
Position and Morphology of the Ovary
The hard clam, Meretrix lusoria, is a dioecious organism. The ovary is located between the digestive diverticula and the outer fibromuscular layers, which are compacted by the fibrous connective tissues and muscle fibers. It is composed of a number of oogenic follicles. In our findings, as the ovary matured, it extended to the lowest part of the muscular layers around the foot. Mature ovaries were of the same pinkish-white color as mature testes. Therefore, the sex of individuals could not be easily distinguished by external features. However, if the ripe ovary was slightly scratched with a razor, a number of ripe yellowish brown eggs flowed out readily. Therefore, sex could be easily distinguished by dissection. After spawning, the ovary degenerated, and it became difficult to distinguish sex by external color or dissection.
Monthly Changes in the Gonad Index
The gonad index gradually increased between March and April. Values reached a maximum (mean 4.7) in May, when seawater temperature increased sharply. The GI then gradually decreased from June to October when spawning occurred. Monthly GI changes in 2003 showed a similar trend to those in 2002. Monthly variations in the GI showed a close relationship with ovarian development (Fig. 2).
[FIGURE 2 OMITTED]
Ultrastracture of Germ Cells and the Follicle Cells Daring Oogenesis and Oocyte Degeneration
Based on ultrastructural observations, ovarian activity and morphological characteristics of germ cells during oogenesis can be classified into four phases (Eckelbarger & Davis 1996): (1) oogonia; (2) previtellogenic oocytes; (3) vitellogenic oocytes; and (4) mature oocytes. In addition, ultrastructural characteristics in each phase of the oocytes including oocyte degeneration were as follows:
The stem cells, which constituted the boundaries of the follicles, gave rise to the primary oogonia (about 10-11 [micro]m), which are characterized by a high nuclear-cytoplasmic ratio. The primary oogonia were observed individually or formed a cluster on the germinal epithelium. The primary oogonia divided mitotically to produce the secondary oogonia, which were observed individually or formed a cluster in the follicle. Each primary and secondary oogonia had a large nucleus with chromatin, a few mitochondria, and the Golgi complex appeared in the cytoplasm (Fig. 3A).
[FIGURE 3 OMITTED]
As the secondary oogonia entered into the first prophase of meiosis, they developed into previtellogenic oocytes. Previtellogenic oocytes were small and oval in shape, having a large nucleolus in the nucleus. With cytoplasmic growth, a number of mitochondria and the rough endoplasmic reticulum were concentrated around the perinuclear region in the cytoplasm. The nucleus and cytoplasm of the previtellogenic oocyte increased in volume. The nucleus and oocyte diameters were 4-5 [micro]m and 15-25 [micro]m, respectively (Fig. 3B).
As the further development of previtellogenic oocytes proceeded, the oocytes developed into early vitellogenic oocytes. The early vitellogenic oocyte was partially surrounded by follicle cells, which maintained intimate contact with the smooth oolemma of the oocyte. At this time, follicle cells measuring 4-5 [micro]m in diameter migrated from the periphery of the follicular wall. The follicle cells possessed a dense chromatin and marginal chromatin in the nucleus, and contained the endoplasmic reticulum and mitochondria in the cytoplasm. In the early vitellogenic oocytes several lipid droplets and mitochondria appeared in the cytoplasm, especially with the initiation of yolk formation (Fig. 3C). The Golgi product in the Golgi complex was present in the perinuclear region, and several lipid droplets, numerous vacuoles, and vesicles appeared near the Golgi complex (Fig. 3D).
A number of lipid droplets and the mitochondria appeared near the oolemma (Fig. 3 E). At the same stage, lipid droplets that were surrounded by the mitochondria and well-developed rough endoplasmic reticulum appeared near the cortical granules and exogenous substances. These substances represent many glycogen particles that were passed into the ooplasm from the outside of the oolemma (Fig. 3F).
When the early vitellogenic oocytes began to form microvilli on the oolemma, the initial contours of the microvilli were oval or slightly long in shape. Several coated vesicles by endocytosis appeared at the basal region of the oolemma of the oocyte. Uptake of nutritive material in the coated vesicle appeared through the formation of coated pits on the oolemma during vitellogenesis (Fig. 4A). In the late vitellogenic oocytes, exogenous substances, viz. many glycogen particles appeared outside the oolemma, and the cortical granules appeared at the cortical region. In particular, proteinaceous yolk granules appeared among the yolk precursors (yolk granules), the mitochondria, and the lipid droplets in the cytoplasm (Fig. 4B). At the same stage, as oocyte volume increased, the ooplasm of the stalked region was filled with a number of proteinaceous yolk granules, lipid droplets, and mitochondria. At this time, the follicle cells contained a few lipid droplets and mitochondria in the cytoplasm, but they gradually lost their intimate association with the entire oocyte surface, and the microvilli appeared along the vitelline coat where the follicle cells had withdrawn (Fig. 4C). In the late stages of oogenesis, proteinaceous yolk granules containing several different components were intermingled and became immature yolk granules in the cytoplasm (Fig. 4D).
[FIGURE 4 OMITTED]
In the mature oocytes, the thick vitelline coat of the mature oocyte was slightly separated from the germinal epithelium. In the cytoplasm of the mature oocyte, small immature yolk granules were continuously mixed with each other and became large mature yolk granules. The mature yolk granules were composed of three components; (1) a crystalline core, (2) an electron-lucent cortex, and (3) a limiting membrane (Figs. 4D). The vitelline coat of the mature oocyte was about 0.30-[micro]m thick and was surrounded by a jelly coat (Fig. 4E).
Ultrastructure of Degenerated Oocytes
The degenerating oocytes appeared slightly irregular or polyhedric near the follicle cells, and were deformed by compression in the follicle. A number of vacuoles, degenerating yolk granules, distended endoplasmic reticulum, a few phagosomes (lysosomes), and lipid droplets appeared in the ooplasm of the degenerating oocyte. At this stage, especially in the follicle cells, a few phagosomes (lysosomes), a number of vacuoles, myelin-like organelles, and a small number of lipid droplets appeared in the cytoplasm of the follicle cell, whereas glycogen particles decreased in the cytoplasm of the follicle cells, which were attached to the degenerated oocyte (Fig. 4F).
Ovarian Cycle with Gonad Developmental Stages
Based on the morphological features of the germ cells and other surrounding cells, the gonad developmental stages were classified into five successive stages (Fig. 5). The criteria in defining each stage are as follows:
[FIGURE 5 OMITTED]
Early Active Stage
The early active stage was characterized by the expansion of the oogenic follicle, and the appearance of oogonia and well-defined previtellogenic oocytes propagated along the follicular wall of the ovary. At this stage, the early vitellogenic oocytes appeared near the previtellogenic oocytes, and follicular walls were relatively thick. The sizes of the oogonia, previtellogenic and early vitellogenic oocytes were about 9-11 [micro]m, 15-20 [micro]m, and 25-40 [micro]m in diameter, respectively. No free oocytes were present in the lumen of the follicle (Fig. 6A). In 2002 and 2003, the individuals in the early active stage were found from January to March, when seawater temperatures were gradually decreased.
[FIGURE 6 OMITTED]
Late Active Stage
This stage is characterized by the presence of early vitellogenic oocytes. Follicular walls of oogenic follicles were slightly thin. Several early vitellogenic oocytes, 25-40 [micro]m in diameter, appeared in the oogenic follicles. When the late vitellogenic oocytes grew to 40-60 [micro]m in diameter, each oocyte attached to the follicular wall (germinal epithelium) through each egg-stalk. Some fully ripe oocytes were free in the lumen of the follicle, but accounted for less than half of the total number of oocytes in the follicles (Fig. 6B). In 2002 and 2003, the individuals in the late active stage appeared from February to May, when seawater temperatures increased gradually.
The majority of ripe ova (60-70 [micro]m in diameter) became round or oval in shape, and ripe ova were located in the center of the lumen. At this time, the follicular walls became very thin. Ripe ova measured about 70-75 [micro]m in diameter, and were surrounded by gelatinous membranes. The cytoplasm of the mature oocytes contained a large number of yolk granules (Fig. 6C). In 2002 and 2003, mature and ripe ovaries were found from April to August, when seawater temperatures were relatively high (15-26.5[degrees]C).
Partially Spawned Stage
During this stage, the lumen of the oogenic follicle appeared mostly empty because approximately 50-60% of ripe ova in the lumen were discharged. Some oocytes underwent cytolysis. Spawned ovaries were characterized by the presence of a few ripe, undischarged oocytes and very young oocytes in the lumen (Fig. 6D). In 2002 and 2003, the individuals in the partially spawned stage appeared from June to September, and peak spawning occurred between July and August, when seawater temperatures were higher than 20[degrees]C.
After spawning, each oogenic follicle was contracted, and degeneration or resorption of residual oocytes occurred. Thereafter, the connective tissues and a few oogonia appeared on the newly formed follicular walls (Figs. 6E, F). In 2002 and 2003, the individuals in this stage were found from September to February, when seawater temperatures gradually decreased.
Size at First Sexual Maturity
Clams of different size that reached first sexual maturity are summarized in Table 1. The breeding season of Meretarix lusoria was found to occur from May to October. In the case of some individuals undergoing ovarian development during the late active stage, it is assumed that maturity can usually be reached, except for in individuals in the early active stage during the breeding season. Sexual maturity was 0% in female clams of 26.3-30.0 mm in shell length if they were at the early active stage during the breeding season, as small numbers of oogonia and previtellogenic oocytes were present in the follicle of the ovary. The percentage of female clams 30.1-35.0 mm in shell length that were at sexual maturity was 21.7%, but most individuals were still in the early active stage during the breeding season. The percentage of individuals 40.0-45.0 mm in shell length that were in the late active, ripe, or partially spawned stage was 54.8%. Sexual maturity was 100% for clams over 50.0 mm in shell length. Shell length at 50% of sexually mature clams (rate of sexual maturity, R[M.sub.50]) was fit to an exponential equation, and was determined to be 41.0 mm (Fig. 7).
[FIGURE 7 OMITTED]
Vitellogenesis of the Oocyte
The process of vitellogenesis of oocytes during oogenesis of Meretaix lusoria is summarized in Figure 8. Although many authors suggested the formation of lipid droplets in several species, no clear morphological evidence has been shown for the processes involved in lipid droplet formation thus far (Pipe 1987, Dorange & Le Pennec 1989, Gaulejac et al. 1995). In our present study, however, lipid droplets appeared among the Golgi complex, well-developed endoplasmic reticulum, and mitochondria in the early vitellogenic oocytes. Therefore, it is assumed that they may be involved in the formation of lipid droplets (Chung et al. 2002, Chung et al. 2005, Chung et al. 2006). Jong-Brink et al. (1983) distinguished three categories of oocyte--follicle cell relationships according to the number and arrangement of the follicle cells. In the first type, the oocyte is completely surrounded by increasing numbers of follicle cells; in the second type, the oocyte is surrounded by a small, distinct number of follicle cells; and in the third type, a small number of follicle cells surround the oocyte only during the early stages of oogenesis. In the present study, an oocyte of M. lusoria was surrounded by a small number of follicle cells during the early and late stages of oogenesis. Therefore, this species shows the second type of oocyte--follicle cell relationship. As shown in Figure 8, vitellogenesis showed a possibility of autosynthetic and heterosynthetic yolk formation. The process of yolk formation by endogenous autosynthesis and exogenous heterosynthesis of M. lusoria was similar to those of Crassostrea virginica (Eckelbarger & Davis 1996) and Mytilus edulis (Pipe 1987).
[FIGURE 8 OMITTED]
Induction of Oocyte Degeneration and Resorption by the Follicle Cells
According to our observations, the follicle cells and degenerated oocytes showed the characteristics of cells that play a functional role in hydrolytic enzyme activity. A number of degenerating yolk granules showed lysosomal enzyme activity, and lipid droplets appeared in the ooplasm of the degenerating oocytes in Meretrix lusoria. At the same time, phagosomes (or lysosomes) and lipid droplets, in particular, increased in the cytoplasm of the follicle cells, which are attached to the degenerated oocytes. However, the number of glycogen particles decreased in the cytoplasm of the follicle cells, as reported in Mytilus edulis (Pipe 1987) and Pecten maximus (Dorange & Le Pennec 1989). In this study, morphologically similar phagosomes, which were easily observed in the cytoplasm of degenerated oocytes, also appeared in the follicle cells. Thus, the follicle cells appeared to play an integral role in vitellogenesis and oocyte degeneration. Regarding functions of the follicle cells during the period of oocyte degeneration, Gaulejac et al. (1995) stated that in Pinna nobilis, the functions of the follicle cells are phagocytosis and intracellular digestion of products originating from the degeneration of oocytes. Judging from the observations of the follicle cells, as shown in Figure 8, they probably perform a function associated with the induction of oocyte degeneration, and it is assumed that they also function in the resorption of phagosomes from the degenerated oocyte because morphologically similar degenerating phagosomes (various lysosomes), which were observed in the degenerated oocytes, appeared in the follicle cells. In the present study, lipid granules gradually increased, whereas glycogen contents decreased in the follicle cell with gametogenesis. This function can permit a transfer of yolk precursors necessary for vitellogenesis, and allows the accumulation of reserves in the cytoplasm, in the form of glycogen and lipids, which can be used by vitellogenic oocytes (Gaulejac et al. 1995). Therefore, it is assumed that the follicle cells, which are attached to degenerated oocytes, may be involved in the induction of oocyte degeneration and the resorption of degenerating phagosomes (lysosomes) by the lysosomal system.
The gonad index of M. lusoria increased in spring months and reached a maximum in May, when the water temperature rapidly increased. Because of spawning, the GI values then showed a gradual decrease with the increase of water temperatures. Chung et al. (1998) stated that the high average values of the GI coincided with gonadal maturity, and the minimal average values following high average values were considered an indication of spawning. Accordingly, variations in the GI showed a close relationship with ovarian development and ovarian activity.
Gonad Development and Maturation
A wide range of exogenous factors has recently been suggested as controls for gonadal development and maturation in marine bivalves. Of these factors, water temperature and food availability seem to be particularly important. However, Sastry (1966, 1968) stated that these and other factors (salinity, day length, etc.) probably interact with endogenous factors (neuroendocrine activity) in a complex manner to control the initiation of gametogenesis. According to Sastry (1968, 1970), seawater temperature acts as a triggering stimulus for the initiation of the oocyte growth phase. The temperatures required for activating the growth of oocytes at the beginning of oogenesis and for attaining maturity ultimately limit the annual period of gonad activity and gametogenesis in the natural environment. In the present study, gamete differentiation of M. lusoria began in early spring, and reached maturity in the population in May, in conjunction with an increase in water temperature. Gonad activity and gametogenesis of this species occur under temperature conditions that allow nutrient mobilization to the gonads, after basic metabolic requirements are satisfied (Sastry 1966). The periods of food abundance and of gonad development of M. lusoria are nearly coincident: gonad growth and gametogenesis in spring coincided with peak food levels, although food concentrations remained high throughout the summer months (Kim 2005). It is assumed that if food and temperature criteria are met, growth of oocytes is initiated in conjunction with the transfer of nutrients from the digestive diverticula to the gonad. According to the results of the present study, development of gametes to maturity in M. lusoria was accelerated after gametogenesis has been initiated, and the development of gametes to maturation was dependent on water temperature. However, it is assumed that the amount of nutrients mobilized for the gonad maturation depends not only on the food level, but also on the water temperature and the basic metabolic requirements of the clams.
Size/Age at Sexual Maturity
Over 50% of individuals 40.0-45.0 mm in shell length were in the late active, ripe, and partially spawned stage; 100% of individuals over 50.0 mm in shell length were in the late active, ripe, partially spawned, and spent/inactive stage. Accordingly, most individuals reach maturity by September if they are larger than 50.1 mm in shell length. According to the growth curve for the mean shell length fitted to von Bertalanffy equation (Ryu et al. 2006), females ranging from 40.0 mm to 45.0 mm in shell length are approximately two years old. Therefore, it is assumed that female clams begin reproduction at about two years of age. This result suggests that harvesting clams <40.0 mm in shell length could potentially cause a drastic reduction in recruitment. Accordingly, a measure indicating a prohibitory fishing size should be taken for adequate fisheries management. Thus, information on size at sexual maturity is very important, and can determine a prohibitory fishing size for adequate natural resources management by 50% of the size at first sexual maturity.
Breeding Pattern and Spawning
According to histologic observations, on the west coast of Korea, spawning of Meretrix lusoria occurred from June to September in the Simpo coastal waters, and also occurred from June to August in Anmyun-do, Korea (Choi & Song 1974). Therefore, the spawning period showed a similar pattern to that of the clams from Anmyun-do, which is found in the waters off the west coast of Korea. In Japan, M. lusoria has been reported to spawn from June through October in Haneda and Chiba, Tokyo Bay, Japan (Taki 1949), and spawning occurred from June to August in Seto Inland Sea, Japan (Ikuta 1988a). Therefore, our results almost coincide with the results of Ikuta (1988a). However, the spawning period of the hard clam at Simpo, Korea was completed 20-30 days faster than those present in the Haneda and Chiba regions in Japan. The slight discrepancies in the spawning periods among these several studies might be related to geographic differences in environmental conditions such as water temperature and food availability, as reported for Mactra veneriformis (Chung & Ryou 2000).
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TABLE 1. Shell length at first sexual maturity in female Meretrix lusoria from May to October, 2002. Number of Individuals by Gonadal Stage * Total Mature Shell Length EA LA RI PS SP/IA Ind. (%) (mm) 26.3 ~ 30.0 21 21 0.0 30.0 ~ 35.0 18 3 2 23 21.7 35.0 ~ 40.0 16 3 6 1 26 38.5 40.0 ~ 45.0 14 4 10 3 31 54.8 45.0 ~ 50.0 4 5 16 3 1 29 86.2 50.0 ~ 55.0 2 14 5 2 23 100.0 55.0 ~ 60.0 1 12 4 4 21 100.0 60.0 ~ 70.0 12 2 2 16 100.0 70.0 ~ 80.0 2 9 2 1 12 100.0 80.0 ~ 90.0 7 2 2 11 100.0 90.0 ~ 96.4 6 2 8 100.0 Total 221 * Gonadal stage: EA, early active stage; LA, late active stage; RI, ripe stage; PS, partially spawned stage; SP/IA, spent/inactive stage.
School of Marine Life Science, Kunsan National University, Kunsan 573-701, Korea
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|Publication:||Journal of Shellfish Research|
|Date:||Apr 1, 2007|
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