Seasonal variations in reproductive activity and biochemical composition of the cockle Fulvia mutica (Reeve) from the eastern coast of China.
Article Type: Report
Subject: Seasons (Influence)
Shellfish (Physiological aspects)
Shellfish (Sexual behavior)
Shellfish (Environmental aspects)
Body composition (Environmental aspects)
Biochemistry (Research)
Authors: Liu, Wenguang
Li, Qi
Yuan, Yundang
Zhang, Shaohua
Pub Date: 04/01/2008
Publication: Name: Journal of Shellfish Research Publisher: National Shellfisheries Association, Inc. Audience: Academic Format: Magazine/Journal Subject: Biological sciences; Zoology and wildlife conservation Copyright: COPYRIGHT 2008 National Shellfisheries Association, Inc. ISSN: 0730-8000
Issue: Date: April, 2008 Source Volume: 27 Source Issue: 2
Topic: Event Code: 310 Science & research
Product: Product Code: 0913000 Shellfish; 8521210 Biochemistry NAICS Code: 114112 Shellfish Fishing; 54171 Research and Development in the Physical, Engineering, and Life Sciences SIC Code: 0913 Shellfish
Geographic: Geographic Scope: China Geographic Code: 9CHIN China
Accession Number: 179387583
Full Text: ABSTRACT Seasonal variations in condition index and biochemical composition of the cockle Fulvia mutica (Reeve) were studied from March 2004 to February 2005 in eastern coast of China in relation to reproductive cycle. The condition index declined during gametogenesis and spawning, recovered when the gonad was in resting phase. Histological analysis and measurements of protein, glycogen and lipid levels and RNA:DNA ratio from gonad-visceral mass, mantle, adductor muscle, and foot of F. mutica were performed. Gametogenesis took place during winter and spring at the expense of reserves (glycogen in various organs, protein in the foot, lipid in the adductor muscle), which were accumulated previously during summer and autumn. Spawning occurred in May to June when water temperature was higher and food availability was abundant. The RNA:DNA ratio is a good indicator of sexual maturity in the gonad-visceral mass; the increasing RNA:DNA ratio in the gonad-visceral mass appears to show the rising synthetic activity of vitellin within the gonad. The results demonstrated that F. mutica may be considered a conservative species in gametogenic pattern. The useful information obtained in this study can be applied for management of populations and to initiate aquaculture activities in this species.

KEY WORDS: cockle Fulvia mutica, biochemical composition, reproductive cycle


The reproductive cycles of marine bivalves are strongly related to the energy storage-utilization cycles. Seasonal metabolic activities of marine bivalves are the consequence of complex interactions between available food, environment conditions, growth, and reproduction (Gabbott 1983, Berthelin et al. 2000). When food is abundant, reserves accumulate prior to gametogenesis in the form of glycogen, lipid and protein substrates, and subsequently are used in the production of gametes when metabolic demand is high (Barber & Blake 1981; Brokordt & Guderley 2004; Mathieu & Lubet 1993). The specifics of which substrates are important, and how the timing of their consumption is related to gametogenesis vary between species as well as between populations of the same species. According to the classification of Bayne (1976), one group, called opportunistic species, uses the recently ingested energy from seston such as Tellina tenuis (Da Costa) and Abra alba (Wood), and another group, conservative species, uses the energy stored in various organs through feeding prior to its gametogenesis such as Chlamys opercularis (Linne) (Taylor & Venn 1979), Argopecten irradians concentricus (Barber & Blake 1981) and A. purpuratus (Martinez 1991). In others such as Placopecten magellanicus (Gmelin), it comes from a combination of stored reserves and ingested food (Thompson 1977).

The knowledge of the reproductive cycle of economic marine bivalves is essential for management of populations and to initiate aquaculture activities. The cockle Fulvia mutica (Reeve) classified to Cardiidae is distributed from north of the Yellow Sea in China, south of Mutsu Bay to Kyushu in Japan, and the Korean Peninsula coastal waters and inhabits from intertidal to muddy-sand bottoms at a depth of 50 m buried in bottom sands and gravels. Fulvia mutica is a functional hermaphrodite bivalve species, with a short lifespan, rapid growth rates, and can reach commercial size (5-6 cm) in a short time (Li et al. 1994). Fulvia mutica is commercially important, but nowadays the exploitation is based solely on natural population, and indiscriminate harvesting has resulted in its depletion. Decline in the supply of wild caught F. mutica enhance the need for their artificial culture. To produce oocytes and spermatozoa of the best quality, which will develop into strong and viable larvae, it has been essential to understand the seasonal behavior of F. mutica from wild population. Despite the biological and commercial importance in F. mutica, information on its biology is limited (Li et al. 1994), and investigation on the biochemical composition and its reproductive cycle has not been performed.

This study investigated the seasonal variation in biochemical composition and reproductive cycle of F. mutica in eastern coast of China. The objective of this work is to observe the seasonal cycles of energy storage and depletion in different organs in relation to the reproductive cycle and to establish the gametogenic pattern.


Animal Collection

Thirty cockles were collected monthly from March 2004 to February 2005 in Weihai (36[degrees]41'-37[degrees]36'N and 121[degrees]11'-121[degrees]42'E), Shandong Province, eastern coast China. They were transported live to the laboratory where the fresh weight, shell weight, and linear dimension (length, height, and width) were determined then they were dissected to obtain mantles, adductor muscles, foot, and gonad-visceral mass (including digestive system, labial palps, nerve ganglia, and kidney-pericardium region). 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 of the seawater was measured in situ during sampling, and chlorophyll a (from 0-1 m of depth) at the site of sampling was determined according to Parsons et al. (1984).

Condition Index

The condition index of the cockle (CI) was calculated as the ratio of the dry weight of the soft parts/dry weight of shell x 100 (Walne 1976).

CI = (Dry weight of the soft parts/Dry weight of shell) x 100


Fifteen individuals from each sample were used for histological examination. A transverse cut was made across the basal part of the foot, which contained the gonad-visceral mass of the cockle and a 5-mm-thick piece was fixed in Bouin solution. It was then routinely processed for histology and 6-[micro]m paraffin-embedded sections were stained with Mayer hematoxylin and eosin. The specimens were examined microscopically to develop a profile of gametogenesis, and the diameter of 100 oocytes was microscopically measured in sections from five animals to determine the degree of maturity every month.

Five gametogenic stages were classified according to a scale of maturity (Gallucci & Gallucci 1982). Undifferentiated stage: this stage is characterized by a total absence of gametes; the connective tissue occupies almost all of the space (Fig. 1A). At the developing stage in the female there were rounded oocytes along with oocytes attached to the follicle wall. Some detached oocytes occurred; in the male, varying quantities of spermatogenic cells were present (Fig. 1B). At the ripe stage in the female most oocytes were free within the follicles, but some oocytes attached to the follicle wall. In the male, follicles filled by spermatozoa arranged in characteristic bands (Fig. 1C). At the partially spawned in the female large spaces inside the follicles and between free oocytes were present. Some follicles were completely devoid of oocytes. In the male, a marked decrease in the quantity of spermatozoa was observed. Large spaces inside the follicles occurred. In some follicles, only a few residual spermatozoa were present (Fig. 1D). At the spent stage, some unspawned oocytes and spermatozoa were observed within follicles (Fig. 1E).


Biochemical Analysis

For the biochemical characterization of the body components, the levels of protein, glycogen, lipid, and nucleic acids were estimated. Total protein was determined by the Kjeldahl method. The dried, powdered samples were catalytically digested with sulphuric acid and analyzed by an automatic Kjeldahl analysis instrument (Kjeltec 2300; Foss Tecator, Sweden). The amount of N was multiplied by 6.25 to estimate the amount of proteins (Stephen 1980). For determining the lipid levels, extractions were made in ethyl ether using a soxhlet apparatus (Folch et al. 1957). 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 wave length of 620 nm. After the samples were homogenized in 20 volumes of distilled water, one milliliter 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 absorbances at 260 nm.

Statistical Analysis

One-way ANOVA followed by mean comparisons post hoc Tukey test was made to assess significant differences in biochemical composition and indices among months. The software SPSS 11.5 was used for analyses.



Environment Parameters and Biometric Measurements

Monthly water temperature for the coast of Weihai in eastern China is given in Figure 2. A seasonal cycle of water temperature was observed, with the maximum value in summer (29.5[degrees]C in August 2004), decreasing gradually until winter (1.8[degrees]C in January 2005). The concentration of chlorophyll a exhibited a clear seasonal pattern characterized by two unequally sized peaks (Fig. 2). The small one was seen in April 2004 (17.7 [micro]g/L), whereas the large one was seen in September 2004 (25.8 [micro]g/L). During winter chlorophyll a concentration was low. Biometric measurements are displayed in Table 1. Mean shell height ranged from 4.70 to 6.05 cm, mean shell length from 4.15 to 5.41 cm, mean shell width from 2.81 to 3.65 cm, mean dry shell weight from 10.68 to 21.40 g, and mean wet flesh weight from 10.82 to 19.56 g.

Condition Index and Gametogenesis

Significant differences (Tukey test, P < 0.01) were observed for condition index throughout the year, which varied between 5.89 and 11.34 (Fig. 3). The maxima were in September to October, decreased gradually afterwards until reaching its lowest value in June (5.89), and it recovered after July. The reproductive cycle of F. mutica is characterized by a clear seasonal pattern (Fig. 3). The mean oocyte diameter showed significant differences among months (Tukey test, P < 0.01), increased from November (20.80 [micro]m), reached a maximum value of 68.63 [micro]m in May, and then decreased after June. From July to October, the gonad of F. mutica was spent, and thus the oocyte diameter was not estimated.

Gonad development started in November and peaked during March to May. Ripe gonads were found from February to June (Fig. 3). It was estimated from the histological observations that F. mutica spawned between May and June. After spawning, there was a sexual resting period from July to October. According to histological observations F. mutica is a functional hermaphroditism. In the male and female acinis, the gametes were in the same developmental stage.

Biochemical Composition

Gonad-visceral Mass

The glycogen content showed a clearly seasonal pattern (Fig. 4). The lower values were observed from December to June. An obvious increase was observed from July, and the highest values were attained in August (25.45%) followed by a decrease from September. The lipid content showed a gradual increase during sexual maturation (December to March), decreased during April and May and increased sharply from June, then decreased again from August to December (Fig. 4). The lipid content in the gonad-visceral mass was higher than that in the other parts of the soft body. The protein content showed maximum values in May (73.10%), decreased significantly in June, then increased slightly from July to November (Fig. 4). The RNA:DNA ratio showed maximum value in May and decreased afterwards, similar to the changes of the protein content in the gonad-visceral mass (Fig. 4).


The glycogen content had maximum value (17.04%) in August, then decreased from September to June, showing significant differences among months (Tukey test, P < 0.01) (Fig. 5). The lipid content fluctuated between 3.60% and 4.95%, and did not change markedly throughout the year (Fig. 5). Proteins were the major biochemical constituents of the mantle of F. mutica, and showed less changes annually (63.25% to 68.94%) (Fig. 5). The RNA:DNA ratio showed no clear annual change (3.64% to 4.08%) (Fig. 5).


Adductor Muscle

The glycogen content showed lower values from March to May, increased sharply in June, and then decreased gradually afterwards, showing significant differences among months (Tukey test, P < 0.01) (Fig. 6). The lower lipid content occurred from March to June, increased gradually from June, reached the highest values in November, then decreased from December (Fig. 6). The protein content fluctuated between 69.30% and 76.66%, showing no seasonal change (Fig. 6). The RNA:DNA ratio showed no seasonal fluctuation (4.37% to 5.34%) (Fig. 6).


The glycogen had a significantly higher concentration in July to August, decreased gradually from September to the minimum values in December (7.47%) (Fig. 7). The lipid content fluctuated between 3.79% and 4.68%, and did not change markedly throughout the year. The protein content was low from May to June, increased significantly from July, showed the highest value in September, then decreased afterwards (Fig. 7). The variations in the RNA:DNA ratio increased gradually from May to November and significantly decreased from December, similar to the changes of the protein content in the foot.


This paper is the first to report on seasonal variation in the reproductive cycle and biochemical composition of F. mutica. The results clearly indicate that the biochemical components of four body parts vary seasonally in accordance with the reproductive cycle. Similar characteristics have been observed in other bivalves such as Glyeymeris glycymeris (Linnaeus) (Galap et al. 1997), Ruditapes philippinarum (Adams & Reeve) (Robert et al. 1993) and Laternula elliptica (King & Broderip) (Ahn et al. 2003).


In F. mutica, the condition index showed clearly seasonal cycle, declined during gametogenesis and spawning and recovered in summer and autumn when the gonad was in the resting phase. The timing and duration of gametogenesis of bivalves was different in different regions of the world (Pazos et al. 1997, Dridi et al. 2007). In general, reproductive strategy can be considered an adaptation to ambient environmental conditions such as water temperature and food availability. The effect of the temperature could be direct, affecting the metabolic rate, or indirectly, affecting the availability of food (Taylor & Venn 1979, Park et al. 2001). In Crassostrea gigas and Ostrea edulis (Linnaeus), Mann (1979) found that initiation of gametogenesis and spawning was dependent on minimum absolute temperature. In our study, temperature was also the important factor that correlated with the reproductive cycle. Based on histological data, the gametogenesis of F. mutica occurred in November at water temperature close to 7.1[degrees]C, characterized by an average oocyte diameter close to 20.8 [micro]m, increased rapidly in spring, reaching a maximum value in May, spawning took place over a short period and may have been restricted to May and June when water temperature is higher (19.4[degrees]C to 23.6[degrees]C). After spawning, F. mutica had a resting phase in summer-autumn.


According to histological observation, F. mutica was hermaphroditic throughout the gametogenic period, with no sex reversal. According to Coe (1943), hermaphroditic conditions in bivalves were divided into 4 categories, according to the sequence of reproductive events: (1) functional hermaphroditism (eggs and sperm produced simultaneously); (2) consecutive sexuality (single sex-reversal, usually protandrous); (3) rhythmical sexuality (> 1 sex-reversal, usually protandrous); and (4) alternative sexuality (adults function seasonally as separate sexes). In the current study, consecutive sexuality and rhythmical sexuality, which can be subdivided, F. mutica was found to be a functional hermaphrodite. The male and female sections of the gonad increased simultaneously during gametogenesis, and the gametes of both sexes were spawned at about the same time. Similar phenomena have also been observed in Clinocardium nuttalli (Conrad) (Gallucci & Gallucci 1982). In contrast, a rhythmic consecutive sexuality has been observed in O. puelchana (Castro & Mattio 1987).

Food availability was considered another important factor affecting the reproductive cycle of bivalves (Ruiz et al. 1992a, Urrutia et al. 2001). The gametogenesis of F. mutica took place at the expense of the stored reserves because of the poor food quality in winter, indicated by the low chlorophyll a levels. Spawning of F. mutica coincided with the higher chlorophyll a concentrations, insuring that when larvae are released the amount of food in the water was high, increasing the possibility of larval success. This coincidence and its adaptive importance were described extensively by Start et al. (1990).


The present study demonstrated the seasonal changes in biochemical composition of gonad-visceral mass, adductor muscle, foot, and mantle in the cockle F. mutica. The analysis of body parts is often more instructive than analysis of the whole animal when studying biochemical composition in relation to reproductive cycles. In fact, measurement of the biochemical composition content of the different organs showed that they did not experience the same variation. In our study, we observed a decrease in the glycogen content during gametogenesis in all tissues of F. mutica, especially in the gonad-visceral mass, and its depletion was significantly correlated to increase in oocyte diameter, suggesting that the glycogen is the main source of energy for gametogenesis in F. mutica. Similar results have been reported for other bivalves such as G. glycymeris (Galap et al. 1997) and C. gigas (Ruiz et al. 1992b). It is generally accepted that glycogen reserves are the major energy source in bivalves (Beninger & Lucas 1984, Li et al. 2000, Park et al. 2001).

Glycogen can be transformed into lipid for the formation of gametes (Gabbott 1975, Kang et al. 2000). Lipid reserves are lost in spawning of adult bivalves (Gabbott 1983). The variation of lipid content in the gonad-visceral mass increased during gametogenesis and decreased when spawning took place, strongly supporting these hypotheses. This result corresponds to that previously observed in Scapharca Broughtonii and R. philippinarum (Park et al. 2001, Robert et al. 1993). Holland (1978) and Fraser (1989) demonstrated that lipid was the basic energetic reserves for sustaining embryonic and larval development of most species of marine bivalves. The lipid reserves in the adductor muscle decreased during gametogenesis, suggesting that they may have been used to provide energy when food was scarce. The lipid content in the mantle and foot did not clearly show seasonal variations, indicating that it was not the substrate used as energy reserves.


The protein content in the gonad-visceral mass increased during gametogenesis and decreased when spawning, showing that protein constitutes the major organic component of bivalve oocytes. Similar observations have been made in a number of marine bivalves (Park et al. 2001). The protein content in the mantle and adductor muscle showed no clearly seasonal change, indicating that this organ did not transfer protein to the gonad during ripening. The protein content in the foot decreased during gametogenesis, suggesting that the protein provided a nutrient source and material for reproduction in the cockle after carbohydrate reserves were depleted. The contribution of the muscle protein to gametogenesis has also been described for A. irradians concentricus (Barber & Blake 1981), A. ventricosus (Racotta et al. 1998), and A. irradians irradians (Epp et al. 1988).

RNA is necessary for protein synthesis and the concentration of RNA in tissue corresponds to the amount of protein being synthesized, whereas DNA levels per somatic cell is fairly constant, the RNA:DNA ratio therefore has been used as an index of cellular protein synthetic activity (Robbins et al. 1990, Nakata et al. 1994). The RNA:DNA ratio in the gonad-visceral mass exhibited a seasonal variation, which was synchronized with protein content. The peak of RNA:DNA ratio observed in May possibly corresponded to the increased number of vitellogenic oocytes present in the gonad (Li et al. 1998). Therefore, the results indicate that the RNA:DNA ratio is a valuable indicator of sexual maturation in the gonad and the increasing RNA:DNA ratio in the gonad appears to show the rising synthetic activity of vitellin as one of proteins produced within the gonad. The RNA:DNA ratio in the mantle and adductor muscle exhibited no change throughout the year, coinciding with the pattern of protein content in them. The RNA:DNA ratio in the foot was low during winter and spring, consistent with the protein content in the foot, suggesting a reduced protein synthetic activity.

The current study showed that gametogenesis in F. mutica occurred during winter-spring when food supply was scarce, and relied on previously stored reserves (glycogen in various organs, protein in the foot, and lipid in the adductor muscle), thus behaved as a conservative species (Bayne 1976). This finding is consistent with the previous data concerning other bivalves like C. gigas (Ruiz et al. 1992b) and S. broughtonii (Park et al. 2001) In contrast, the result obtained by Ruiz et al. (1992a) in O. edulis indicated that its reproductive activity depended on the available food in the environment. This discrepancy has be explained by various endogenous and exogenous parameters.

In conclusion, our findings suggest that gametogenesis of F. mutica took place in winter-spring at the expense of reserves accumulated previously during the summering period. The results demonstrated that F. mutica may be considered a conservative species in gametogenic pattern. A single spawning occurred in early summer when water temperature was higher and chllorophyll a concentration was abundant. The data generated in this study provide useful information on reproductive cycle and the annual biochemical variation associated with the gametogenesis cycle of F. mutica. The information can be applied for management of populations and to initiate aquaculture activities in this species.


The study was supported by the grants from National High Technology Research and Development Program (2006AA10A409) and Scientific and Technical Supporting Program (2006BAD09A01).


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(1) Fisheries College, Ocean University of China, Qingdao 266003, China; (2) Oceanic and Fishery Administration of Huancui District, Weihai 264200, China

* Corresponding author. E-mail:
Biometric measurements of the cockle Fulvia mutica (mean [+ or -]
standard errors, n = 10) H, shell height, L, shell length, W, shell
width, SW, dry shell weight, FW, wet flesh weight.

Month-Year          H (cm)                  L (cm)

  Mar-05      4.96 [+ or -] 0.38      4.48 [+ or -] 0.36
  Apr-05      4.70 [+ or -] 0.25      4.15 [+ or -] 0.17
  May-05      4.92 [+ or -] 0.30      4.45 [+ or -] 0.25
  Jun-05      5.01 [+ or -] 0.36      4.54 [+ or -] 0.35
  Jul-05      4.75 [+ or -] 0.37      4.39 [+ or -] 0.28
  Aug-05      4.86 [+ or -] 0.27      4.48 [+ or -] 0.27
  Sep-05      5.15 [+ or -] 0.29      4.67 [+ or -] 0.26
  Oct-05      6.05 [+ or -] 0.42      5.41 [+ or -] 0.46
  Nov-05      4.91 [+ or -] 0.17      4.51 [+ or -] 0.21
  Dec-05      5.33 [+ or -] 0.36      4.70 [+ or -] 0.26
  Jan-06      5.07 [+ or -] 0.21      4.52 [+ or -] 0.21
  Feb-06      5.57 [+ or -] 0.32      4.96 [+ or -] 0.25

Month-Year          W (cm)                  SW (g)

  Mar-05      2.90 [+ or -] 0.24      12.07 [+ or -] 2.45
  Apr-05      2.85 [+ or -] 0.34      12.27 [+ or -] 2.17
  May-05      2.94 [+ or -] 0.21      12.36 [+ or -] 2.32
  Jun-05      3.00 [+ or -] 0.23      13.32 [+ or -] 2.32
  Jul-05      2.81 [+ or -] 0.21      11.16 [+ or -] 2.43
  Aug-05      2.94 [+ or -] 0.16      11.91 [+ or -] 2.13
  Sep-05      3.00 [+ or -] 0.16      12.99 [+ or -] 2.79
  Oct-05      3.65 [+ or -] 0.28      21.40 [+ or -] 4.52
  Nov-05      2.99 [+ or -] 0.35      10.68 [+ or -] 1.57
  Dec-05      2.99 [+ or -] 0.20      13.06 [+ or -] 2.95
  Jan-06      2.90 [+ or -] 0.10      12.56 [+ or -] 1.40
  Feb-06      3.20 [+ or -] 0.21      15.66 [+ or -] 2.48

Month-Year          FW (g)

  Mar-05      13.93 [+ or -] 3.06
  Apr-05      13.51 [+ or -] 2.74
  May-05      13.03 [+ or -] 3.06
  Jun-05      13.43 [+ or -] 1.60
  Jul-05      12.64 [+ or -] 2.22
  Aug-05      13.59 [+ or -] 1.64
  Sep-05      13.01 [+ or -] 2.61
  Oct-05      19.56 [+ or -] 5.42
  Nov-05      10.82 [+ or -] 2.07
  Dec-05      12.39 [+ or -] 1.93
  Jan-06      11.13 [+ or -] 1.17
  Feb-06      13.91 [+ or -] 2.92
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