Influence of seasonality and gonad development on the nutritional quality and safety of the razor clam Sinonovacula constricta (Lamarck 1818)
DOI:
https://doi.org/10.5327/fst.128022Keywords:
razor clam, seasonal variation, the gametogenic cycle, physicochemical variation, microbiological qualityAbstract
Understanding the reproductive activity or seasonal variation in comprehensive evaluations of the nutritional quality and safety of the razor clam Sinonovacula constricta (Lamarck) is important for improving product quality and economic benefits. The contents of moisture (from 80.12±0.38 to 84.98±0.40%), protein (from 53.14±0.06 to 63.12±0.69% DW), lipid (from 4.55±0.19 to 5.69±0.35% DW), glycogen (from 5.40±1.11 to 16.13±1.55% DW), and ash (from 12.03±0.33 to 19.86±0.56% DW) varied significantly at different gonadal development cycles or seasons. Glycogen, lipid, and protein variations were closely associated with gonadal development, with the lowest levels of lipid and protein in the spawning period. Moreover, S. constricta consistently had a well-balanced essential amino acid profile throughout the year, indicating that it is a source of high-quality protein. The predominant free amino acids in S. constricta were taurine, glycine, lysine, and alanine, which are important contributors to the flavor. S. constricta was defined as lean fat throughout the gonad cycle with polyunsaturated fatty acid accounting for the majority in the active and maturing stages. Microbiological quality and total volatile basic nitrogen were associated with the alteration of seasons. The optimal harvesting time of S. constricta was the inactive stage of most gonads in spring (from March to April in Taizhou, Zhejiang Province, China).
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Association of Official Analytical Chemists (AOAC). (2005). Official Methods of Official Analytical Chemists International (16th ed.). Association of Official Analytical Chemists.
Ayache, N., Hmida, L., Cardoso, J. F. M. F., Haouas, Z., Costa, F., & Romdhane, M. S. (2016). Reproductive cycle of the razor clam Solen marginatus (Pulteney,1799) in the southern Mediterranean Sean (Gulf of Gabes, South Tunaisia). Journal of Shellfish Research, 35(2), 389-397. https://doi.org/10.2983/035.035.0213
Bermudez, R., Franco, D., Carballo, J., Sentadreu, M. A., & Lorenzo, J. M. (2014). Influence of muscle type on the evolution of free amino acids and sarcoplasmic and myofibrillar proteins through the manufacturing process of Celta dry-cured ham. Food Research International, 56, 226-235. https://doi.org/10.1016/j.foodres.2013.12.023
Bethelin, C., Kellner, K., & Mathieu, M. (2000). Storage metabolism in the Pacifc oyster (Crassostrea gigas) in relation to summer mortalities and reproductive cycle (west coast of France). Comparative Biochemistry and Physiology, Part B, 125(3), 359-369. https://doi.org/10.1016/s0305-0491(99)00187-x
Bi, S. J., Xue C. H., Wen, Y. Q., Du, X., Xue, Q., Li, Z., & Liu, H. (2023). Effects of cooling rates during depuration on the quality of Pacific oysters (Crassostrea gigas) at anhydrous preservation stage. Food Chemistry, 17, 100606. https://doi.org/10.1016/j.fochx.2023.100606
Bongiorno, T., Iacumin, L., Tubaro, F., Marcuzzo, E., Sensidoni, A., & Tulli, F. (2015). Seasonal changes in technological and nutritional quality of mytilus galloprovincialis from suspended culture in the gulf of Trieste (northadriatic sea). Food Chemistry, 173, 355-362. https://doi.org/10.1016/j.foodchem.2014.10.029
Burkhardt, W., Watkins, W. D., & Rippey, S. R. (1992). Seasonal effects on accumulation of microbial indicator organisms by Mercenaria mercenaria. Applied and Environmental Microbiology, 58(3), 826-831. https://doi.org/10.1128%2Faem.58.3.826-831.1992
Celik, M. Y., Çulha, S. T., Çulha, M., Yildiz, H., Acarli, S., Celik, I., & Celik, P. (2014). Comparative study on biochemical composition of some edible marine mollusks at Canakkale coasts, Turkey. Indian Journal of Marine Science, 43, 601-606.
Celik, M. Y., Karayucel, S., Karayucel, I., Ozturk, R., & Eyuboglu, B. (2012). Meat yield, condition index, and biochemical composition of mussels (mytilus galloprovincialis Lamarck, 1819) in sinop, south of the blacksea. Journal of Aquatic Food Product Technology, 21(3), 198-205. https://doi.org/10.1080/10498850.2011.589099
Chen, J. N., Huang, X. H., Zheng, J., Sun, Y.-H., Dong, X.-P., Zhou, D.-Y., Zhu, B.-W., & Qin, L. (2021). Comprehensive metabolomic and lipidomic profiling of the seasonal variation of blue mussels (mytilus edulis l.): free amino acids, 5′-nucleotides, and lipids. Food Science and Technology, 149, 111835. https://doi.org/10.1016/j.lwt.2021.111835
Chen, Y. H., Chen, Y. K., Tao, L., Du, X., Dong, Z., Niu, D., & Li, J. (2022). Genetic parameters and genotype by environment interaction for growth traits of razor clam Sinonovacula constricta, from outdoor pond and semi-natural environment. Aquacult Report, 24, 101173. https://doi.org/10.1016/j.aqrep.2022.101173
Chen, Z. Y., Yang, W. Y., Luo, M. Z., Meng, H. O., Zhang, J. J., Lin, C. H., Jin, X. L. (2008). Meat products-Determination of total sugars content (GB/T 9695.31-2008).
Chung, W. H., Howieson, J., & Chaklader, R. (2021). The ameliorative effects of low-temperature pasteurization on physicochemical and microbiological quality of raw akoya pearl oyster (pinctada fucata). Food Control, 129, 108241. https://doi.org/10.1016/j.foodcont.2021.108241
Cotter, E., Malham, S. K., O’Keeffe, S., Lynch, S.A., Latchford, J. W., King, J. W., Beaumont, A. R., & Culloty, S. C. (2010). Summer mortality of the Pacific oyster, Crassostrea gigas, in the Irish Sea: The influence of growth, biochemistry and gametogenesis. Aquaculture, 303(1-4), 8-21. https://doi.org/10.1016/j.aquaculture.2010.02.030
Darriba, S., San Juan, F., & Guerra, A. (2004). Reproductive cycle of the razor clam Ensis arcuatus (Jeffreys, 1865) in northwest spain and its relation to environmental conditions. Journal of Experimental Marine Biology and Ecology, 311(1), 101-115. https://doi.org/10.1016/j.jembe.2004.05.004
Dridi, S., Romdhane, M. S., & Elcafsi, M. (2007). Seasonal variation in weight and biochemical composition of the Pacific oyster, Crassostrea gigas in relation to the gametogenic cycle and environmental conditions of the Bizert lagoon, Tunisia. Romdhane, Elcafsi M. Aquaculture, 263(1-4), 234-248. https://doi.org/10.1016/j.aquaculture.2006.10.028
Fernandez, A., Grienke, U., Soler-Vila, A., Guihéneuf, F., Stengel, D. B., & Tasdemir, D. (2015). Seasonal and geographical variations in the biochemical composition of the blue mussel (Mytilus edulis L.) from Ireland. Food Chemistry, 177, 43-52. https://doi.org/10.1016/j.foodchem.2014.12.062
Food and Agriculture Organization of the United Nation (FAO). (2022). The State of Word Fisheries and Aquaculture. Food and Agriculture Organization.
Food and Agriculture Organization of the United Nations (FAO) & World Health Organization (WHO). (2017). Food Standards Programme, Codex Committee on Nutrition and Foods for Special Dietary Uses, 39 session. FAO/WHO.
Gao, J. X., Zhang, Y. Y., Huang, X. H., Liu, R., Dong, X. P., Zhu, B. W., & Qin, L. (2021). Comparison of amino acid, 5′-nucleotide and lipid metabolism of oysters (Crassostrea gigas Thunberg) captured in different seasons. Food Research International, 147, 110560. https://doi.org/10.1016/j.foodres.2021.110560
Gulusan, E., Duygu, K. (2009). Microbiological quality of carpet shell clam during harvesting period in izmir Bay. Advances in Food Sciences, 31, 222-225.
Horikoshi, H. (1958). Glycogen. Chemical Field, 34, 36-39.
Ibarra, A. M., Roberto, A. M., & Raminrez, J. L. (2017). Performance of Diploid and Triploid Crassostrea gigas (Thunberg, 1793) Grown in Tropical Versus Temperate Natural Environmental Conditions. Journal of Shellfish Research, 36(1), 119-139. https://doi.org/10.2983/035.036.0113
Isono, C., Maruta, H., Ma, Y., Ganeko, N., Miyake, T., & Yamashita, H. (2020). Seasonal variations in major components of Crassostrea gigas from Seto Inland Sea. Fisheries Science, 86, 1087-1099.
Ivell, R. (1979). The biology and ecology of brackish lagoon bivalve, Cerastoderma galucum Bruguiere, in an English lagoon, the Wide water, Sussex. Journal of Molluscan Study, 45(3), 383-400. https://doi.org/10.1093/oxfordjournals.mollus.a065513
Kachele, R., Zhang, M., Gao, Z., & Adhikari, B. (2017). Effect of vacuum packaging on the shelf-life of silver carp (Hypophthalmichthys molitrix) fillets stored at 4 ℃. LWT-Food Science and Technology, 80, 163-168. https://doi.org/10.1016/j.lwt.2017.02.012
Khan, M. A., Parrish, C. C., & Shahidi, F. (2005). Quality indicators of cultured newfound land blue mussels (Mytilus edulis) during storage on ice Microbial growth, pH, lipid oxidation, chemical composition characteristics, and microbial fatty acid contents. Journal of Agricultural and Food Chemistry, 53(18), 7067-7073. https://doi.org/10.1021/jf050082g
Kim, H. W., Jang, J. J., Kim, N. H., Lee, N. Y., Cho, T. J., Kim, S. H., & Rhee, M. S. (2018). Factors that determine the microbiological quality of ready-to-use salted napa cabbage (brassicapekinensis): season and distribution temperature. Food Control, 87, 1-8. https://doi.org/10.1016/j.foodcont.2017.12.009
Li, Q., Liu, W.G., Shirasu, K., Chen, W., & Jiang, S. (2006). Reproductive cycle and biochemical composition of the Zhe oyster Crassostrea plicatula Gmelin in an eastern coastal bay of China. Aquaculture, 261(2), 752-759. https://doi.org/10.1016/j.aquaculture.2006.08.023
Lira, G. M., Pascoal, J. C. M., Torres, E. A. F. S., Soares, R. A. M., Mendonça, S., Sampaio, G. R., Correia, M. S., Cabral, C. C. V. Q., Cabral Júnior, C. R., & López, A. M. Q. (2013). Seasonality on the chemical composition of oysters (Crassostrea rhizophorae). Food Chemistry, 138(1-2), 786-790. https://doi.org/10.1016/j.foodchem.2012.11.088
Liu, C., Meng, F., Tang, X., Wang, A., & Pan, Z. (2018). Comparison of nonvolatile taste active compounds of wild and cultured mud crab Scylla paramamosain. Fisheries Science, 84(14), 897-907. https://doi.org/10.1007/s12562-018-1227-0
Liu, C. S., Gu, Z. F., Lin, X. X., Wang, Y., Wang, A., Sun, Y., & Shi, Y. (2022). Effects of high hydrostatic pressure (hhp) and storage temperature on bacterial counts, color change, fatty acids and non-volatile taste active compounds of oysters (crassostrea ariakensis). Food Chemistry, 372, 131247. https://doi.org/10.1016/j.foodchem.2021.131247
Liu, C. S., Ji, W.Z., Jiang, H. Z., Shi, Y., He, L., Gu, Z., & Zhu, S. (2020). Comparison of biochemical composition and non-volatile taste active compounds in raw, high hydrostatic pressure-treated and steamed oysters Crassostrea hongkongensis. Food Chemistry, 344, 128632. https://doi.org/10.1016/j.foodchem.2020.128632
Liu, S., Li, L., Wang, W., Li, B., & Zhang, G. (2020). Characterization, fluctuation and tissue differences in nutrient content in the Pacific oyster (Crassostrea gigas) in Qingdao, northern China. Aquaculture Research, 51(4), 1353-1364. https://doi.org/10.1111/are.14463
Liu, W. G., Li, Q., Yuan, Y. D., Zhang, S. (2008). Seasonal variation in reproductive activity and biochemical composition of the cockle Fulvia mutica (Reeve) from the eastern coast of China. Journal of Shellfish Research, 27(2), 405-411. https://doi.org/10.2983/0730-8000(2008)27[405:SVIRAA]2.0.CO;2
Liu, Y. X., Zhang, Y. Y., Zheng, J., Chen, J.-N., Huang, X.-H., Dong, X.-P., Zhu, B.-W., & Qin, L. (2021). Seasonal variations in free aminoacid,5′-nucleotide, and lipid profiles of scallop (Patinopecten yessoensis) revealed by targeted and untargeted metabolomic approaches. Food Science and Technology, 154, 112881. https://doi.org/10.1016/j.lwt.2021.112881
Lopez-Caballero, M., Pérez-Mateos, M., Montero, P., & Borderías, A. J. (2000). Oyster preservation by high-pressure treatment. Journal of Food Protection, 63(2), 196-201. https://doi.org/10.4315/0362-028x-63.2.196
Marshall, R., Mckinley, R. S., & Pearce, C. M. (2012). Effect of temperature on gonad development of the Pacific geoduck clam Panopea generosa (Gould, 1850). Aquaculture, 338-341, 264-273. https://doi.org/10.1016/j.aquaculture.2012.01.004
Mondol, M. R., Kim, C.W., Kang, C. K., Park, S. R., Noseworthy, R. G., & Choi, K.-S. (2016). Growth and reproduction of early grow-out hardened juvenile Pacific oysters, Crassostrea gigas in Gamakman Bay, off the south coast of Korea. Aquaculture, 463, 224-233. https://doi.org/10.1016/j.aquaculture.2016.05.047
Murata, Y., Touhata, K., & Miwa, R. (2020). Correlation of extractive components and body index with taste in oyster Crassostrea gigas brands. Fisheries Science, 86(3), 561-572. https://doi.org/10.1007/s12562-020-01417-1
Normand, J., Marcel, L. P., & Pierre, B. (2008). Comparative histological study of gametogenesis in diploid and triploid Pacific oysters (Crassostrea gigas) reared in an estuarine farming site in France during the 2003 heat wave. Aquaculture, 282(1-4), 124-129. https://doi.org/10.1016/j.aquaculture.2008.06.026
Park, M. S., Kang, C. K., & Lee, P. Y. (2001). Reproductive cycle and biochemical composition of the ark shell Scapharca broughtonii (Schrenck) in a southern coastal bay of Korea. Journal of Shellfish Research, 20(1), 177-184.
Parsons, T. R., Maita, Y., & Lalli, C. M. A. (1984). Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon Press.
Prato, E., Biandolino, F., Parlapiano, I., Papa, L., Denti, G., Fanelli, G. (2019). Seasonal changes of commercial traits, proximate and fatty acid compositions of the scallop Flexopecten glaber from the Mediterranean Sea (Southern Italy). PeerJournal, 7, e5810. https://doi.org/10.7717/peerj.5810
Qin, P., Li, X. Y., Li, J., Zhou Y. Y., Xiang Z. M., Ma, H. T., Noor, Z. H. B., Mo, R. G., Zhang, Y. H., Yu, Z. N. (2021). Seasonal variation in biochemical composition and nutritional quality of Crassostrea honkongensis, in relation to the gametogenic cycle. Food Chemistry, 356, 129736.
Ran, Z. S., Chen, H., Ran, Y., Yu, S., Li, S., Xu, J., Liao, K., Yu, X., Zhong, Y., Ye, M., & Ran, Y. (2017a). Fatty acid and sterol changes in razor clam sinonovacula constricta (Lamarck 1818) reared at different salinities. Aquaculture, 473, 493-500. https://doi.org/10.1016/j.aquaculture.2017.03.017
Ran, Z. S., Li, S., Li, S., Zhang, R., Xu, J., Liao, K., Yu, X., Zhong, Y., Ye, M., Yu, S., Ran, Y., Huang, W., & Yan, X. (2017b). Proximate, amino acid and lipid compositions in Sinonovacula constricta (Lamarck) reared at different salinities. Jouranl of the Science Food and Agriculture, 97(13), 4476-4483. https://doi.org/10.1002/jsfa.8311
Ren, J., Marsden, I. H., Ross, A. R., & Schiel, D. (2003). Seasonal variation in the reproductive activity and biochemical composition of the Pacifc oyster (Crassostrea gigas) from the Marlborough Sounds, New Zealand. New Zealand Journal of Marine & Freshwater Research, 37(1), 171-182. https://doi.org/10.1080/00288330.2003.9517155
Santos, S., Cardoso, J., Carvalho, C., Luttikhuizen, P. C., & van der Veer, H. W. (2011). Seasonal variability in somatic and reproductive investment of the bivalve scrobicularia plana (da costa, 1778) along a latitudinal gradient. Estuarine, Coastal and Shelf Science, 92(1), 19-26. https://doi.org/10.1016/j.ecss.2010.12.005
Shen, H. D., Liu, G., Fang, L., & Li, J. (2013). Effect of microalgae and temperature on absorption efficiency of razor clam (Sinonovacula constricta Lamark, 1818). Aquaculture Research, 44(10), 1524-1530. https://doi.org/10.1111/j.1365-2109.2012.03159.x
Songsaeng, S., Sophanodora, P., Kaewsrithong, J., & Ohshima, T. (2010). Quality changes in oyster (Crassostrea belcheri) during frozen storage as affected by freezing and antioxidant. Food Chemistry, 123(2), 286-290. https://doi.org/10.1016/j.foodchem.2010.04.033
Tan, K., Ma, H., Liand, S., & Zhang, H. P. (2019). Bivalves as future source of sustainable natural omega-3 polyunsaturated fatty acids. Food Chemistry, 311, 125907. https://doi.org/10.1016/j.foodchem.2019.125907
Woyewoda, A. D., Shaw, S. J., Ke, P. J., & Burns, B. G. (1986). Recommended laboratory methods for assessment of fish quality (pp. 1-5). Canadian Technical Report of Fisheries and Aquatic Science, No. 1448. Fisheries and Oceans.
Wu, H. X., Li, W.J., Shan, C. J., Zhang, Z.-Y., Lv, H.-B., Qiao, F., Du, Z.-Y., & Zhang, M.-L. (2021). Oligosaccharides improve the flesh quality and nutrition value of Nile tilapia fed with high carbohydrate diet. Food Chemistry: Molecular Sciences, 3, 100040. https://doi.org/10.1016/j.fochms.2021.100040
Xie, Z. M. (2003). Aquaculture Technology of Marine Economic Shellfishes. China Agriculture Press.
Xue, B. B., Meng, D.L., Li, H., Liang, W., Niu, D., Li, J., Shen, H. (2021). Determining the biological zero for gonadal development razor clams Sinonovacula constricta (lamarck 1818) in Zhejiang, China. Aquaculture and Fisheries, 6(1), 56-62. https://doi.org/10.1016/j.aaf.2019.05.006
Yan, H.W., Li, Q., Liu, W. G., Yu, R., & Kong, L. (2010). Seasonal changes inreproductive activity and biochemical composition of the razor clam Sinonovacula constricta (Lamarck 1818). Marine Biology Research, 6(1), 78-88. https://doi.org/10.1080/17451000903039756
Yang, J. H., Lin, H. C., & Mau, J. L. (2001). Non-volatile taste components of several commercial mushrooms. Food Chemistry, 72(4), 465-471. https://doi.org/10.1016/S0308-8146(00)00262-4
Yin, M. Y., Matsuoka, R., Yanagisawa, T. K. Y., Xi, Y., Zhang, L., & Wang, X. (2022). Effect of different drying methods on free amino acid and flavor nucleotides of scallop (patinopecten yessoensis) adductor muscle. Food Chemistry, 396, 133620. https://doi.org/10.1016/j.foodchem.2022.133620
Yue, J., Zhang, Y., Jin, Y., Deng, Y., & Zhao, Y. (2016). Impact of high hydrostatic pressure on non-volatile and volatile compounds of squid muscles. Food Chemistry, 194, 12-19. https://doi.org/10.1016/j.foodchem.2015.07.134
Zhang, L., Li, X., Lu, W., Shen, H., & Luo, Y. (2011). Quality predictive models of grass carp (Ctenopharyngodon idellus) at different temperatures during storage. Food Control, 22(8), 1197-1202. https://doi.org/10.1016/j.foodcont.2011.01.017
Zhang, N. L., Wang, W. L., Li, B., & Liu, Y. (2019). Non-volatile tasteactive compounds and umami evaluation in two aquacultured pufferfish (Takifugu obscurus and Takifugu rubripes). Food Bioscience, 32, 100468. https://doi.org/10.1016/j.fbio.2019.100468
Zhao, W., Li, Y., Wang, Y. H., Luo, X., Wu, Q., Huo, Z., Song, J., & Yan, X. (2022). Gonadal development and the reproductive cycle of the geoduck clam (Panopea japonica) in the Sea of Japan. Aquaculture, 548(part 1), 737606. https://doi.org/10.1016/j.aquaculture.2021.737606
Zhou, Z., Zhang, Y. Y., Gao, J. X., Ma, L.-X., Huang, X.-H., Zheng, J., Dong, X.-P., & Qin, L. (2021). Metabolomic approaches to analyze the seasonal variations of amino acid, 5’-Nucleotide, and lipid profile of clam (Ruditapes philippinarum). LWT-Food Science and Technology, 148, 111709. https://doi.org/10.1016/j.lwt.2021.111709