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Seasonal variations in biochemical composition and reproductive activity of Venus clam Cyclina sinensis (Gmelin) from the yellow river delta in northern China in relation to environmental factors.

ABSTRACT The seasonal variations in biochemical composition and reproductive activity of the venus clam Cyelina sinensis (Gmelin) from the Yellow River delta in China were investigated from April 2007 to March 2008 in relation to environmental factors. According to histological observations, gametogenesis began in January when the water temperature was low. Gametes matured mainly in June and July when the condition index (CI) and mean oocyte diameter peaked. Spawning occurred primarily in August when the temperature was highest, and coincided with phytoplankton bloom. The CI and oocyte diameter decreased sharply after spawning occurred, as mostly larger, mature gametes have been released. In autumn, the plentiful phytoplankton and higher water temperature were fit for the larvae to grow. Biochemical analysis indicated that gametogenesis took place at the expense of reserves accumulated in the various tissues previously during winter. A slight increase in lipid and protein content in female gonad-visceral mass during sexual maturation was observed, demonstrating that lipid and protein would be accumulated as vitellin in oocytes. Conversely, the lipid and protein content in the male gonad-visceral mass decreased during sexual maturation. The biochemical compositions in the adductor muscle and mantle varied during the study period, suggesting that they could support reproduction and growth. Seasonal variation in the RNA-to-DNA ratio suggests that it cannot reflect the situation of gonad development in this species.

KEY WORDS: Venus clam, Cyclina sinensis, biochemical composition, reproductive cycle, environmental factors


The venus clam Cyclina sinensis (Gmelin), class Veneroida, is commonly found in intertidal zones of muddy sand beaches along the north and south coasts of China, as well as in Japan and Korea. It is one of the wild, exploited bivalve species for human consumption, with a rapid growth rate and delicious flesh, and it can tolerate wide temperature and salinity ranges. The overexploitation of natural populations and growing market demand enhance the need of aquaculture in this species. So far, most of the seeds used in C. sinensis farming have relied on collections from nature. Culture of this species is limited by the scarcity and irregular supplies of the seeds (Zhou et al. 2006). Since the late 1980s, much effort has been exerted to develop and improve techniques for the artificial seed breeding of C. sinensis, either on a pilot or commercial scale (Sun et al. 1985, Lu et al. 1992, Liu et al. 2002, Zhou et al. 2006). However, the commercial hatchery production of C. sinensis seeds is rare. To be able to improve the efficiency of collecting seed from the wild and help hatchery managers to determine the best strategy for producing large quantities of C. sinensis eggs and larval of good quality, detailed knowledge of its reproductive strategy in a given area is fundamental.

The reproductive cycles of marine bivalves involve the storage and utilization of nutrients, and they are often closely related to local environmental parameters such as water temperature and food availability (Bayne 1976, Pazos et al. 1997, Berthelin et al. 2000, Kang et al. 2000, Ojea et al. 2004, Dridi et al. 2007, Liu et al. 2008). Gametogenesis represents a period of particularly high-energy demand when both reproduction and maintenance costs must be satisfied by the food supply and reserves accumulated in the tissues prior to gametogenesis, or a combination of both. Several authors have discussed the relative contribution of energy reserves versus food intake to meet the metabolic demands of growth and gonadal development in bivalves (Robinson et al. 1981, Epp et al. 1988, Barber & Blake 2006). However, no pattern has yet been established because these processes are highly dependent on several exogenous and endogenous factors. In general, most species are capable of storing energy reserves in the form of lipid, glycogen, and protein substrates when food is abundant, which are subsequently mobilized together with the available food when metabolic demand is high (Brokordt & Guderley 2004). The particular importance of these substrates, where they are stored and the timing of their use, differs among species and exhibit geographical variation within a single species (Bayne 1976). The reproductive cycle and seasonal changes in reserves storage utilization of marine bivalves may reveal its reproductive strategy in relation to local environmental factors.

In this study we examined the reproductive cycle and seasonal changes in the biochemical compositions of separate organs of C. sinensis from the Yellow River delta of northern China in relation to environmental factors. Knowledge of the specific role of various biochemical components in different tissues as well as evaluation of their role in reproduction is essential for a complete understanding of reproductive strategy in this species.


Sample Collection

Seventy to 80 adult venus clams (C. sinensis) were collected monthly from April 2007 to March 2008 from a natural tidal fiat situated in the Yellow River delta, Shandong Province, China. The shell length varied between 3.32 cm and 3.68 cm, shell height between 3.38 cm and 3.71 cm, and shell width between 1.89 cm and 3.65 cm. The clams were immediately transported live to the laboratory, then the flesh of about 60 clams was dissected to obtain gonad-visceral mass, adductor muscles, and mantles. The gonad-visceral mass was analyzed as a unit because of the physical difficulty in separating the organs. The tissues were then frozen and stored at -80[degrees]C until used.

Temperature and salinity of the surface seawater were measured in situ during sampling with a mercury bulb thermometer and portable refractometer. The concentration of chlorophyll a at the sampling site (at a depth of 0-1 m) was determined according to Dai and Lu (1997) in laboratory.

Condition Index (CI)

The CI of the venus clam was calculated as the ratio of the dry weight of the soft parts divided by dry weight of the shell multiplied by 100 (Walne 1976).

Histological Procedures

Four-millimeter-thick gonad-visceral tissue from each clam was fixed in Bouin's fluid for 24-28 h, dehydrated in a graded series of alcohol, and embedded in paraffin. Sections with a 6-[micro]m thickness were prepared, stained with hematoxylin, and counterstained with eosin according to routine histological techniques. The sections were examined microscopically to assess the sex and stage of gonadal development using an Olympus BX50 microscope equipped with an image analyzing system (Olympus DP70, Tokyo, Japan). The diameter of 100 oocytes per animal for 5 animals (500 oocytes in total) was measured microscopically to determine the degree of maturity every month. Six stages of sexual maturity were identified according to Drummond et al. (2006). During stage 0, sex was indeterminable, with the gonad predominantly composed of connective tissue (Fig. 1-0). During stage 1, previtellogenic oocytes and spermatocytes were identified in females and males, respectively. Sex was just identifiable, with very little gonadal development, and gametogenesis only just began (Fig. 1-1). Stage 2 represented a period of moderate gonadal development (Fig. 1-2). At this stage, the follicles and acini began to distend, and germinal cells in all phases of gametogenesis coexisted. During stage 3, gametogenesis was complete, but spawning had not yet occurred or only just began (Fig. 1-3). Follicles and acini were predominantly composed of mature gametes. Ripe oocytes free in the follicles had a polygonal-shape profile as a result of packing in the female. Free sperm manifested as streaks, and the layer of spermatocytes was greatly thinner than that of mature sperm in males. During stage 4, the gonads were partly spent. In females, empty spaces were observed in follicles, and ripe oocytes were of a lower density (Fig. 14). In male, acini lost the radial arrangement of sperm. During stage 5, the follicles and acini appeared broken, scattered, and were relatively empty; only residual spermatozoa and oocytes were found in acini, and were undergoing resorption (Fig. 1-5).



Biochemical Determination

For the biochemical characterization of the body components, the quantity of lipid, glycogen, protein, and nucleic acids was estimated. Each determination of biochemical compounds was carried out in triplicate on pooled tissues of 5 individuals. The glycogen content was determined with minor modifications to the anthrone-sulfuric acid method described by Horikoshi (1958). The powdered, freeze-dried samples were suspended in 60 volumes of 30% KOH, and saponified by heating to 100[degrees]C for 30 min. After cooling, a portion of the saponified mixture was treated with the cold 0.2% anthrone-sulfuric acid solution for 10 min. Absorbance of the resulting colored complex was measured at the wavelength of 620 nm. The lipid concentration was determined using the gravimetric method, and extraction was made in diethyl ether by using an automatic Buchi extraction system (B-811; Buchi Co., Flawil, Sweden). Determination of soluble protein was carried out according to Bradford (1976), using bovine serum albumin as a reference protein. The saline crude extract sample was mixed with the dye reagent, Brilliant Blue G, and then the absorbance values at 595 nm were read. After the samples were homogenized in 20 volumes of distilled water, 1 mL of each homogenate was used for determination of nucleic acid (DNA and RNA) contents according to the modification of the Schmidt-Thammhauser-Schnerder method by Nakano (1988). Nucleic acids were precipitated with ethanol and washed with a mixture of ethanol and ether. RNA was separated by alkaline hydrolysis, and DNA was hydrolyzed with perchloric acid. DNA and RNA contents were determined by measuring their absorbance at 260 nm.



Statistical Analysis

One-way analysis of variance followed by a mean comparisons post hoc Tukey test was used to assess significant differences in the CI and oocyte diameter between months. Student's t-test was used to test for differences in biochemical composition between mean values for males and females. Significance was set at P < 0.05 in all cases. Pearson's correlation coefficient was used to determine the degree of association between CI, mean oocyte diameter, and environmental factors. The software SPSS 13.0 was used for analyses.


Environmental Parameters

The environmental conditions of the sampling area are described in Figure 2. A seasonal cycle in water temperature was observed, with the maximum value in summer (30.0[degrees]C in August 2007), decreasing gradually until winter (2.0[degrees]C in February 2008). Salinity remained relatively stable throughout the year, varying from 31.0-34.1 [per thousand]. The concentration of chlorophyll a exhibited a clear seasonal pattern characterized by 2 unequal-size peaks. The small one was seen in June 2007 (22.07 [micro]g/L), whereas the large one was seen in September 2007 (24.35 [micro]g/L). Chlorophyll a concentration was low during winter.


Condition Index and Gametogenesis

Significant differences (Tukey test, P < 0.05) were observed for the CI throughout the year (Fig. 3). It increased from 7.3 in April, reached the highest value in June (14.4), decreased gradually afterward until reaching its lowest value in September (5.6), and then recovered.

Gametogenesis of venus clam was characterized by a clear seasonal pattern (Fig. 4). The mean oocyte diameter increased from 17.4 [micro]m in April, attained a maximum value of 55.1 gm in July, and decreased markedly after July, showing significant differences among months (P < 0.05). A positive correlation between the mean oocyte diameter and water temperature was observed during the study period (Pearson's r = 0.613, P < 0.05). Gametogenesis began during January, after a period of a sexual inactivity in December. In February, 92.1% of the individuals were at stage 1. In May, 80.0% of the clams were at stage 2. Gonads became ripe beginning in June. The main spawning activity was observed in August (66.1% of the clams). By December, 68.8 % of the clams were at stage 0. Therefore, we could characterize the gametogenic cycle of C. sinensis in the Yellow River delta by 2 distinctive phases: a resting phase in December and gametogenesis during the rest of the year, including ripeness and spawning.

Biochemical Composition

Seasonal changes in the lipid content of the gonad-visceral mass, adductor muscle, and mantle of C. sinensis are shown in Figure 5. In the female gonad-visceral mass, the lipid content increased from 10.5% in April to a maximum value of 12.3% in July, followed by a decrease when spawning gradually occurred, and then reached a minimum value of 7.6% in September. In contrast, the lipid content of the male gonad-visceral mass decreased beginning in April and was significantly lower than that of the female gonad-visceral mass (P < 0.05) during sexual maturation, showing the lowest value (7.5%) in September. The lipid content showed the lower values from September through December both in female and male gonad-visceral mass, and then increased from January onward. The lipid content of the adductor muscles attained the highest value in September (10.0% in the females and 11.5% in the males), and then decreased slightly, showing the minimum values in January (6.8% in females and 6.3% in males). The lipid content of the mantles decreased from 10.5 % in May, attained a lower value of 8.8% in July, and then increased, showing a maximum value of 11.3 % in September in females. The lipid content of the mantles decreased from 12.2% in May, reached a minimum value of 7.5% in August, and then recovered in males.

The glycogen content of the female gonad-visceral mass decreased from 35.7% in April to a minimum value of 12.7% in July, and then increased. In male gonad-visceral mass, a similar pattern was observed during sexual maturation, although significant differences were present (P < 0.05) in February between females and males (Fig. 6). In the adductor muscles of each sex, the glycogen content showed no marked change throughout the year. The glycogen content in the mantles of each sex decreased beginning in August, and then recovered after September. The glycogen content of the mantles in females was significantly higher than that of the males during January through March (P < 0.05).

In female gonad-visceral mass, the protein content decreased from 61.2 mg/g in July and reached its lowest level of 28.5 mg/g in September, then gradually increased, showing the highest value (83.7 mg/g) in February (Fig. 7). In male gonad-visceral mass, the protein content decreased beginning in May, reached a minimum value of 25.4 mg/g in August, and then increased. The protein content of the gonad-visceral mass showed significant differences between females and males throughout the year. In females, the protein content of adductor muscles increased beginning in April until a higher value (36.0 mg/g) was reached in July, and then gradually decreased. Beginning in August, the protein content of the adductor muscles recovered, then reached the highest value (41.1 mg/g) in October. In the males, a similar pattern was observed. The protein content increased slightly in mantles during spring (March through May) and decreased beginning in August until minimum values (24.1 mg/g in females and 20.0 mg/g in males) were reached in September, and then recovered until the maximum values (80.1 mg/g in females and 83.4 mg/g in males) were observed in October.


The RNA-to-DNA ratio of the female gonad-visceral mass increased slightly during March through June, and then decreased, followed by an increase during autumn (September through October; Fig. 8). The RNA-to-DNA ratio of the male gonad-visceral mass decreased from 36.7 in April until it reached its lowest level of 3.1 in September, and then increased. The RNA-to-DNA ratio of the adductor muscles and mantles showed the same tendency as that of the gonad-visceral mass.



The reproductive strategy of bivalves can be considered an adaptation to ambient environmental conditions, particularly temperature and food availability. The timing and duration of gametogenesis of bivalves are different between species because of the different locations or interspecific variations (Lango-Reynoso et al. 2000, Chavez-Villalba et al. 2002, Darriba et al. 2005, Li et al. 2006). In the current study, histological analysis demonstrated that C. sinensis displayed an annual reproductive cycle at the Yellow River delta. A new cycle of gametogenesis began in January when both water temperature and concentration of chlorophyll a were low, followed by the rapid development and proliferation of the gonad, accompanied by a rapid increase in CI during sexual maturation. The clams became ripe mainly in June and July, and spawned in August. A positive correlation between water temperature and mean oocyte diameter was observed during the study period, indicating that water temperature may have an important role in inducing gametogenesis and spawning of C. sinensis. The effect of temperature could be direct by affecting the metabolic rate of bivalves or indirect by affecting the availability of food. Previous study demonstrated that the spawning of C. sinensis occurred in September through November when water temperature ranged from 28.0[degrees]C to 24.0[degrees]C in Fujian (Zeng & Li 1991), and in July through September when water temperature was 22.0-27.0[degrees]C in Dalian (Bai et al. 2008). In this study, the spawning of C. sinensis took place mainly in August. The timing and duration of gametogenesis of C. sinensis is different in different regions of the China. Mann (1979) suggested that gametogenesis was dependent on both absolute temperature and the period of exposure.


The experimental manipulation of food supply altered the reproductive cycle of the mussel Perna perna (Velez & Epifanio 1981). Newell et al. (1982) observed that Mytilus edulis populations from North America cultured in nearly identical thermal environments exhibited distinct reproductive cycles. These differences were apparently related to temporal differences in food supply among locations. Therefore, food avail ability also plays an important role in the reproductive cycle of bivalves. For bivalves, phytoplankton is major food source. In the current study, spawning of C. sinensis coincided with phytoplankton bloom, ensuring that the amount of food in the water was sufficient when larvae are released, increasing the survival rate of larval.

The CI is generally considered to reflect reproductive activity (Massapina et al. 1999, Ojea et al. 2004, Liu et al. 2008). In our study, the CI showed clearly a seasonal cycle, increasing during gametogenesis and decreasing during spawning. The CI increased immediately after spawning, demonstrating a rapid recovery and an accumulation of reserves that may be used in the next gametogenesis cycle.

Lipid content has been considered to be one of the principal energy sources used by larvae during embryonic and early larval stages of bivalves (Gallager et al. 1986, Fraser 1989, Whyte et al. 1991, Couturier & Newkirk 1991), apart from their indispensable role as structural elements of all biological membranes in the metabolism of bivalves. Seasonal variation of its concentration is closely related to the reproductive cycles. In general, lipid content increases before mass spawning occurs, and then markedly decreases (Couturier & Newkirk 1991, Pazos et al. 1997, Racotta et al. 2003, Dridi et al. 2007, Liu et al. 2008, Colaco et al. 2009). In the current study, the lipid content of the female gonad-visceral mass increased steadily during gametogenesis, with a maximum value prior to spawning, indicating that the lipid was accumulated in ripening eggs and may be subsequently used by the larvae. In contrast, the lipid content of the male gonad-visceral mass decreased during spermatogenesis and was significantly lower than that of the female, suggesting that lipids provided a nutrient source and material for spermatogenesis, as has been reported for other species (Martinez 1991, Li et al. 2000). However, in the functional hermaphrodite pectinid Nodipecten (Lyropecten) subnodosus, it was suggested that the decrease of lipid in the testis portion may be the result of the transfer of lipid from the testis portion to the ovary portion during the ripening process for the accumulation in gametes as yolk (Arellano-Martinez et al. 2004). The adductor muscle lipid slightly increased in autumn when the phytoplankton concentration was at a higher level and subsequently decreased in October through January, suggesting that it might play an important role in supporting the energy costs when the available food was scarce. The lipid content of the mantles could have been transferred to the gonad during sexual maturation, because the decrease in the lipid content was observed.

The glycogen content of the gonad-visceral mass markedly decreased during both female and male gametogenesis, suggesting that glycogen is a major constituent for the development of gametes as an energy and material source. Similar results have been reported for other bivalves such as Argopecten irradians concentricus (Barber & Blake 1981), Crassostrea gigas (Li et al. 2000), and C. plicatula (Li et al. 2006). Seasonal variations in glycogen content of the female gonad-visceral mass are inversely related to lipid content in the current study. It has long been evident that glycogen and lipids are inversely correlated and that lipid loss accompanies spawning (Beninger & Lucas 1984, Beninger & Stephan 1985, Robert et al. 1993, Ojea et al. 2004). This relationship is usually attributed to the conversion of glycogen to lipids biosynthesized during the formation of gametes (Gabbott 1975, Holland 1978). However, significant increase associated with reproductive activity and a decrease in the spawning period were observed in other species such as N. subnodosus (Arellano-Martinez et al. 2004). In others, such as Modiolus barbatus (Mladineo et al. 2007) and Spisula solida (Joaquim et al. 2008), there are 2 periods: one with a consumption Of glycogen that is stored during the resting period and another during which the storage of reserves and gametogenesis took place simultaneously. In the current study, glycogen increased immediately after spawning, indicating an accumulation of it that may be used in the new reproductive cycle. The glycogen content of the adductor muscle did not change considerably, suggesting that the adductor muscle might not be used as a glycogen storage site. The glycogen content of the mantle during the resting stage was obviously higher than that during gametogenesis and spawning, indicating that glycogen of the mantle might be an important reserve source for reproductive activity.

In the current study, the protein content of the female gonad-visceral mass showed a slight increase during maturation and then decreased during spawning, indicating that protein would be accumulated as vitellin in oocytes. The strategy of accumulating protein in the gonad has also been observed in other species (Barber & Blake 1981, Epp et al. 1988, Park et al. 2001, Dridi et al. 2007), but the protein content does not increase during gametogenesis in Placopecten magellanicus (Couturier & Newkirk 1991) and Argopecten ventricosus (Ruiz-Verdugo et al. 2001). Both strategies have been found in other species such as N. subnodosus because of different locations (Racotta et al. 2003, Arellano-Martinez et al. 2004). Conversely, the protein content of the male gonad-visceral mass decreased during sexual maturation, suggesting that protein provided an energy and material source for spermatogenesis in C. sinensis after carbohydrate and lipid reserves were depleted. The protein content in the adductor muscle showed no clear seasonal change, indicating that this organ did not transfer protein to the gonad during ripening. The protein content in the mantle decreased during gametogenesis, suggesting that protein provided a nutrient source and material for reproduction in the clam after carbohydrate reserves were depleted.

Because RNA is an essential component of protein synthesis, its concentration in tissue often reflects the rate of protein synthesis (Garlick et al. 1976). The RNA-to-DNA ratio provides an index of protein synthetic capacity per cell because the amount of DNA per cell is assumed to be constant in sexually mature adults (Bulow 1987). In some marine animals, the RNAto-DNA ratio has been used as an index of growth rate (Clarke et al. 1989, Moss 1994), nutritional stress, and condition (Wright & Hetzel 1985, Chicharo & Chicharo 1995, Chicharo et al. 2001). Moreover, previous studies have proved that the RNA-to-DNA ratio can be used as a sensitive indicator of identifying the gonadal development state of oyster (Li et al. 2000), clam (Kim et al. 2005), and scallop (Robbins et al. 1981, Roddick et al. 1999). However, no relationship was observed between the RNA-to-DNA ratio in gonad-visceral mass and the reproductive cycle for C. sinensis. The RNA-to-DNA ratio of the 3 tissues increased during autumn when food abundant, indicating increasing protein synthetic activity.

In conclusion, C. sinensis from the Yellow River delta of northern China follows an annual reproductive cycle with precise periods of gonad maturation in June and July, and spawning in August. Gametogenesis took place in winter and spring at the expense of reserves accumulated previously. The data generated in this study provide useful information on reproductive strategies of C. sinensis populations in this area. This information can be applied not only for optimizing the aquaculture in this species, but also for management of C. sinensis populations.


The study was supported by grants from the Scientific and Technical Supporting Program (no. 2006BAD09A01), the National High Technology Research and Development Program (no. 2007AA09Z433), and the Chinese Ministry of Education (no. 707041).


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Author:Yan, Hongwei; Li, Qi; Yu, Ruihai; Kong, Lingfeng
Publication:Journal of Shellfish Research
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Geographic Code:9CHIN
Date:Apr 1, 2010
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