Skip to main content

Advertisement

SpringerLink
Log in

Annual variations of biogenic element contents of manila clam (Ruditapes philippinarum) bottom-cultivated in Jiaozhou Bay, China

  • Published:
Journal of Ocean University of China Aims and scope Submit manuscript

Abstract

Manila clam (Ruditapes philippinarum) was monthly sampled from its benthic aquaculture area in Jiaozhou Bay from May 2009 to June 2010. The annual variations of major elemental composition, organic content, fatness and element ratio of Manila clam were examined. The element removal effect of clam farming in Jiaozhou Bay was analyzed based on natural mortality and clam harvest. The results indicated that the variation trend of carbon content in shell (C shell) was similar to that in clam (C clam). Such a variation was higher in summer and autumn than in other seasons, which ranged from 9.10 ± 0.13 to 10.38 ± 0.09 mmol g−1 and from 11.28 ± 0.29 to 12.36 ± 0.06 mmol g−1, respectively. Carbon content of flesh (C flesh) showed an opposite variation trend to that of shell in most months, varying from 29.42 ± 0.05 to 33.64 ± 0.62 mmol g−1. Nitrogen content of shell (N shell) and flesh (N flesh) changed seasonally, which was relatively low in spring and summer. N shell and N flesh varied from 0.07 ± 0.009 to 0.14 ± 0.009 mmol g−1 and from 5.46 ± 0.12 to 7.39 ± 0.43 mmol g−1, respectively. Total nitrogen content of clam ranged from 0.50 ± 0.003 to 0.76 ± 0.10 mmol g−1 with a falling tend except for a high value in March 2010. Phosphorus content of clam (N clam) fluctuated largely, while phosphorus content of shell (P shell) was less varied than that of flesh (P flesh). P shell varied from 0.006 ± 0.001 to 0.016 ± 0.001 mmol g−1; while P flesh fluctuated between 0.058 ± 0.017 and 0.293 ± 0.029 mmol g−1. P clam ranged from 0.015 ± 0.002 to 0.041 ± 0.006 mmol g−1. Carbon and nitrogen content were slightly affected by shell length, width or height. Elemental contents were closely related to the reproduction cycle. The removal amounts of carbon, nitrogen and phosphorus from clam harvest and natural death in Jiaozhou Bay were 2.92×104t, 1420 t and 145 t, respectively. The nutrient removal may aid to reduce the concentrations of nitrogen and phosphorus, the main causes of eutrophication, and to maintain the ecosystem health of Jiaozhou Bay.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Bartoli, M., Nizzoli, D., Viaroli, P., Turolla, E., Castaldelli, G., Fano, E. A., and Rossi, R., 2001. Impact of Tapes philippinarum farming on nutrient dynamics and benthic respiration in the Sacca di Goro. Hydrobiologia, 455: 203–212.

    Article  Google Scholar 

  • Berthelin, C., Kelhner, K., and Mathieu, M., 2000. Storage metabolism in the Pacific oyster (Crassostrea gigas) in relation to summer mortalities and reproductive cycle (west coast of France). Comparative Biochemistry and Physiology, 125(3): 359–369.

    Article  Google Scholar 

  • Birkely, S. R., Grahl-Nielsen, O., and Gulliksen, B., 2003. Temporal variations and anatomical distributions of fatty acids in the bivalve Mya truncata, L. 1758, from Isfjorden. Spitsbergen, 26(2):83–92.

    Google Scholar 

  • Carré, M., Bentaleb, I., Bruguier, O., Ordinola, E., Barrett, N. T., and Fontugne, M., 2006. Calcification rate influence on trace element concentrations in aragonitic bivalve shells: evidences and mechanisms. Geochimica et Cosmochimica Acta, 70(19): 4906–4920.

    Article  Google Scholar 

  • Chong, K., and Wang, W. X., 2001. Comparative studies on the biokinetics of Cd, Cr, Zn in the green mussel Perna viridis and Manila clam Ruditapes philippinarum. Environmental Pollution, 115: 107–121.

    Article  Google Scholar 

  • Chopin, T., Buschmann, A. H., Halling, C., Troell, M., Kautsky, N., Neori, A., Kraemer, G. P., Zertuche-Gonzalez, J. A., Yarish, C., and Neefus, C., 2001. Integrating seaweeds into marine aquaculture systems: a key towards sustainability. Journal of Phycology, 37: 975–986.

    Article  Google Scholar 

  • Delgado, M., Camacho, A. P., Labarta, U., and Fernández-Reiriz, M. J., 2004. The role of lipids in the gonadal development of the clam Ruditapes decussatus (L.). Aquaculture, 241(1–4): 395–411.

    Article  Google Scholar 

  • Du, R., 2009. Biostatistics. 3rd edition. Higher Education Press, Beijing, 104–118, 173–181.

    Google Scholar 

  • Dumbauld, B. R., Ruesink, J. L., and Rumrill, S. S., 2009. The ecological role of bivalve shellfish aquaculture in the estuarine environment: A review with application to oyster and clam culture in West Coast (USA) estuaries. Aquaculture, 290(3–4): 196–223.

    Article  Google Scholar 

  • Editorial Board of Annals of Bays in China, 1993. Annals of Bays in China, Series 4. China Ocean Press, Beijing, 159–168 (in Chinese).

    Google Scholar 

  • Elser, J. J., Acharya, K., Kyle, M., Cotner, J., Makino, W., Markow, T., Watts, T., Hobbie, S., Fagan, W., Schade, J., Hood, J., and Sterner R. W., 2003. Growth rate-stoichiometry couplings in diverse biota. Ecology Letters, 6: 936–943.

    Article  Google Scholar 

  • Elser, J. J., Dobberfuhl, D., MacKay, N. A., and Schampel, J. H., 1996. Organism size, life history, and N:P stoichiometry: towards a unified view of cellular and ecosystem processes. BioScience, 46: 674–684.

    Article  Google Scholar 

  • Fan, D. J., Liu, S. F., Zhang A. B., Yu, Z. S., and Wang, W. Z., 2005. Comparison study on the shell mineralogy of 9 species of modern bivalves living in Yellow Sea. Acta Sedimentological Sincia, 23(3): 475–482 (in Chinese with English abstract).

    Google Scholar 

  • FAO, 2011. Fishery and Aquaculture Statistics 2009. Food and Agriculture Organization of the United Nations, Rome, 107pp.

    Google Scholar 

  • Fishery Bureau, Ministry of Agriculture of China, 2011. China Fisheries Yearbook. China Agriculture Press, Beijing, 180–187 (in Chinese).

    Google Scholar 

  • Forrest, B. M., Keeley, N. B., Hopkins, G. A., Webb, S. C., and Clement, D. M., 2009. Bivalve aquaculture in estuaries: review and synthesis of oyster cultivation effects. Aquaculture, 298(1–2): 1–15.

    Article  Google Scholar 

  • Fukunaga, A., and Anderson, M. J., 2011. Bioaccumulation of copper, lead and zinc by the bivalves Macomona liliana and Austrovenus stutchburyi. Journal of Experimental Marine Biology and Ecology, 396(2): 244–252.

    Article  Google Scholar 

  • Goulletquer, P., and Wolowicz, M., 1989. The shell of Cardium edule, Cardium glaucum and Ruditapes philippinarum: organic content, composition and energy value, as determined by different methods. Journal of the Marine Biological Association of the United Kingdom, 69: 563–572.

    Article  Google Scholar 

  • Hickson, J. A., Johnson, A. L. A., Heaton, T. H. E., and Balson, P. S., 1999. The shell of the Queen Scallop Aequipecten opercularis (L.) as a promising tool for palaeoenvironmental reconstruction: Evidence and reasons for equilibrium stableisotope incorporation. Palaeogeography, Palaeoclimatology, Palaeoecology, 154(4): 325–337.

    Article  Google Scholar 

  • Kaspar, H. F., Gillespie, P. A., Boyer, I. C., and MacKenzie, A. L., 1985. Effects of mussel aquaculture on the nitrogen cycle and benthic communities in Kenepuru Sound, Marlborough Sounds, New Zealand. Marine Biology, 85: 127–136.

    Article  Google Scholar 

  • Kim, S. K., Rosenthal, H., Clemmesen, C., Park, K. Y., Kim, D. H., Choi, Y. S., and Seo, H. C., 2005. Various methods to determine the gonadal development and spawning season of the purplish Washington clam, Saxidomus purpuratus (Sowerby). Journal of Applied Ichthyology, 21: 101–106.

    Article  Google Scholar 

  • Klein, R. T., Lohmann, K. C., and Thayer, C. W., 1996. Sr/Ca and 13C/12C ratios in skeletal calcite of Mytilus trossulus: covariation with metabolic rate, salinity, and carbon isotopic composition of seawater. Geochimica et Cosmochimica Acta, 60(21): 4207–4221.

    Article  Google Scholar 

  • Lan, B. J., 2002. A study on the use of Vanadium-Ammonium molybdate colorimetric method to estimate the phosphorus content in the Manganese Ore. China’s Manganese Industry, 20(3): 43–46 (in Chinese with English abstract).

    Google Scholar 

  • Li, N., 2006. Distribution, source of organic carbon and carbon-nitrogen-phosphors interaction in Changjing River estuary and Jiaozhou Bay waters. PhD thesis. Graduate University of Chinese Academy of Sciences, 77–83 (in Chinese with English abstract).

    Google Scholar 

  • Liu, S. F., Fan, D. J., Shi, X. F., and Zhang, A. B., 2008. Accumulation regularities of Ca, Mg, Mr, Fe and Sr elements in clam shell during its growing process. Marine Science Bulletin, 27(2): 43–51 (in Chinese with English abstract).

    Google Scholar 

  • Lodeiros, C. J., Rengel, J. J., Guderley, H. E., Nusetti, O., and Himmelman, J. H., 2001. Biochemical composition and energy allocation in the tropical scallop Lyropecten (Nodipecten) nodosus during the months leading up to and following the development of gonads. Aquaculture, 199(1–2): 63–72.

    Article  Google Scholar 

  • Makino, W., Cotner, J. B., Sterner, R. W., and Elser, J. J., 2003. Are bacteria more like animals than plants? Growth rate and resource dependence of bacterial C:N:P stoichiometry. Functional Ecology, 17: 121–130.

    Article  Google Scholar 

  • Martinez, G., 1991. Seasonal variation in biochemical composition of three size classes of the chilean scallop Argopecten purpuratus Lamarck, 1819. Veliger, 34(4): 335–343.

    Google Scholar 

  • Martínez-Pita, I., Sánchez-Lazo, C., Ruíz-Jarabo, I., Herrera, M., and Mancera, J. M., 2012. Biochemical composition, lipid classes, fatty acids and sexual hormones in the mussel Mytilus galloprovincialis from cultivated populations in south Spain. Aquaculture, 358–359: 274–283.

    Article  Google Scholar 

  • Nakamura, Y., 2001. Filtration rates of the Manila clam, Ruditapes philippinarum: Dependence on prey items including bacteria and picocyanobacteria. Journal of Experimental Marine Biology and Ecology, 266: 181–192.

    Article  Google Scholar 

  • Nakamura, Y., and Kerciku, F., 2000. Effects of filter-feeding bivalves on the distribution of water quality and nutrient cycling in a eutrophic coastal lagoon. Journal of Marine Systems, 26(2): 209–221.

    Article  Google Scholar 

  • Narváez, M., Freites, L., Guevara, M., Mendoza, J., Guderley, H., Lodeiros, C. J., and Salazar, G., 2008. Food availability and reproduction affects lipid and fatty acid composition of the brown mussel, Perna perna, raised in suspension culture. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 149(2): 293–302.

    Article  Google Scholar 

  • Navarrete-Mier, F., Sanz-Lázaro, C., and Marín, A., 2010. Does bivalve mollusc polyculture reduce marine fin fish farming environmental impact?. Aquaculture, 306(1–4): 101–107.

    Article  Google Scholar 

  • Navarro, J. M., and Thompson, R. J., 1997. Biodeposition by the horse mussel Modiolus modiolus (Dillwyn) during the spring diatom bloom. Journal of Experimental Marine Biology and Ecology, 209(1–2): 1–13.

    Article  Google Scholar 

  • Neori, A., Chopin, T., Troell, M., Buschmann, A. H., Kraemer, G. P., Halling, C., Shpigel, M., and Yarish, C., 2004. Integrated aquaculture: rationale, evolution and state of the art emphasizing seaweed biofiltration in modern mariculture. Aquaculture, 231: 361–391.

    Article  Google Scholar 

  • Neori, A., Ragg, N. L. C., and Shpigel, M., 1998. The integrated culture of seaweed, abalone, fish and clams in modular intensive land-based systems: II. Performance and nitrogen partitioning within an abalone (Haliotis tuberculata) and macroalgae culture system. Aquacultural Engineering, 17(4): 215–239.

    Article  Google Scholar 

  • Nizzoli, D., Bartoli, M., and Viaroli, P., 2006. Nitrogen and phosphorous budgets during a farming cycle of the Manila clam Ruditapes philippinarum: an in situ experiment. Aquaculture, 261(1): 98–108.

    Article  Google Scholar 

  • Nizzoli, D., Welsh, D. T., and Viaroli, P., 2011. Seasonal nitrogen and phosphorus dynamics during benthic clam and suspended mussel cultivation. Marine Pollution Bulletin, 62(6): 1276–1287.

    Article  Google Scholar 

  • Ojea, J., Pazos, A. J., Martínez, D., Novoa, S., Sánchez, J. L., and Abad, M., 2004. Seasonal variation in weight and biochemical composition of the tissues of Ruditapes decussatus in relation to the gametogenic cycle. Aquaculture, 238(1–4): 451–468.

    Article  Google Scholar 

  • Patrick, S., Faury, N., and Goulletquer, P., 2006. Seasonal changes in carbohydrate metabolism and its relationship with summer mortality of Pacific oyster Crassostrea gigas (Thunberg) in Marennes-Oléron Bay (France). Aquaculture, 252(2–4): 328–338.

    Article  Google Scholar 

  • Qi, X. H., Liu, S. M., Zhang, J., Ren, J. L., and Zhang, G. L., 2011. Cycling of phosphorus in the Jiaozhou Bay. Acta Oceanologica Sinica, 30(2): 62–74.

    Article  Google Scholar 

  • Qingdao Municipal Statistics Bureau, 2011. Qingdao Statistical Yearbook. China Statistical Press, Beijing, 219–220 (in Chinese).

    Google Scholar 

  • Ren, Y. P., 2006. The resources biology and conservation strategies of transplant enhanced Manila clam R. philippinarum in the Jiaozhou Bay. PhD thesis. Ocean University of China (in Chinese with English abstract).

    Google Scholar 

  • Riebesell, U., Schulz, K. G., Bellerby, R. G. J., Botros, M., Fritsche, P., Meyerhöfer, M., Neill, C., Nondal, G., Oschlies, A., Wohlers, J., and Zöllner, E., 2007. Enhanced biological carbon consumption in a high CO2 ocean. Nature, 450(7169): 545–548.

    Article  Google Scholar 

  • Riisgaard, H. U., Seerup, D. F., Jensen, M. H., Glob, E., and Larsen, P., 2004. Grazing impact of filter-feeding zoobenthos in a Danish fjord. Journal of Experimental Marine Biology and Ecology, 307(2): 261–271.

    Article  Google Scholar 

  • Robert, R., Trut, G., and Laborde, J. L., 1993. Growth, reproduction and gross biochemical composition of the Manila clam Ruditapes philippinarum in the Bay of Arcachon, France. Marine Biology, 116: 291–299.

    Article  Google Scholar 

  • Serdar, S., and Lök, A., 2009. Gametogenic cycle and biochemical composition of the transplanted carpet shell clam Tapes decussatus, Linnaeus 1758 in Sufa (Homa) Lagoon, Izmir, Turkey. Aquaculture, 293: 81–88.

    Article  Google Scholar 

  • Shen, G. Y., Huang, L. F., Guo, F., and Shi, B. Z., 2010. Marine Ecology. Third edition. Science Press, Beijing, 283–300 (in Chinese).

    Google Scholar 

  • Takesue, R. K., Bacon, C. R., and Thompson, J. K., 2008. Influences of organic matter and calcification rate on trace elements in aragonitic estuarine bivalve shells. Geochimica et Cosmochimica Acta, 72(22): 5431–5445.

    Article  Google Scholar 

  • Tan, Y. Q., Zhang, Z., Liang, C. J., and Wang, J. T., 2011. Distribution of organic carbon in the seawater of Qingdao and adjacent area. Advances in Earth Science, 26(4):426–432.

    Google Scholar 

  • Troell, M., Joyce, A., Chopin, T., Neori, A., Buschmann, A. H., and Fang, J. G., 2009. Ecological engineering in aquaculture-Potential for integrated multi-trophic aquaculture (IMTA) in marine offshore systems. Aquaculture, 297: 1–9.

    Article  Google Scholar 

  • Vanni, M. J., Flecker, A. S., Hood, J. M., and Headworth, J. L., 2002. Stoichiometry of nutrient recycling by vertebrates in a tropical stream:linking biodiversity and ecosystem function. Ecology Letters, 5: 285–293.

    Article  Google Scholar 

  • Viaroli, P., Giordani, G., Bartoli, M., Naldi, M., Azzoni, R., Nizzoli, D., Ferrari, I., Comenges, J. M. Z., Bencivelli, S., Castaldelli, G., and Fano, E. A., 2006. The Sacca di Goro Lagoon and an arm of the Po River. The Handbook of Environmental Chemistry, 5(H): 197–232.

    Google Scholar 

  • Vittinghoff, E., Glidden, D. V., Shiboski, S. C., and McCulloch, C. E., 2010. Regression Methods in Biostatistics: Linear, Logistic, Survival, and Repeated Measures Models (Statistics for Biology and Health). Springer, 29–33.

    Google Scholar 

  • Walne, P. R., 1976. Experiments on the culture in the sea of the butterfish Venerupis decussata L. Aquaculture, 8(4): 371–381.

    Article  Google Scholar 

  • Walne, P. R., and Mann, R., 1975. Growth and biochemical composition in Ostrea edulis and Crassostrea gigas. In: Proceedings of the 9th European Marine Biological Symposium. Barnes, H. B., ed., Aberdeen University Press, Aberdeen, 587–607.

    Google Scholar 

  • Wang, G., 2009. Study on the pollutant of point source and mariculture fluxes flowing into Jiaozhou Bay. Master thesis. Ocean University of China, 14–31 (in Chinese with English abstract).

    Google Scholar 

  • Wu, Y. Q., and Pan, H. M., 1992. Resources and fishing prospects of Ruditapes philippinarum in the Jiaozhou Bay. China Fisheries, 3: 34–35 (in Chinese).

    Google Scholar 

  • Zarnoch, C. B., 2006. Studies on the physiological basis for over-winter mortality in juvenile aquacultured hard clams, Mercenaria mercenaria (Linnaeus, 1758). PhD thesis. The City University of New York.

    Google Scholar 

  • Zarnoch, C. B., and Schreibman, M. P., 2008. Influence of temperature and food availability on the biochemical composition and mortality of juvenile Mercenaria mercenaria (L.) during the over-winter period. Aquaculture, 274(2–4): 281–291.

    Article  Google Scholar 

  • Zhang, J. H., Fang, J. G., and Tang, Q. S., 2005. The contribution of shellfish and seaweed mariculture in China to the carbon cycle of coastal ecosystem. Advances in Earth Science, 20(3): 359–365 (in Chinese with English abstract).

    Google Scholar 

  • Zhang, J. H., Fang, J. G., and Wang, W., 2009. Progress in studies on ecological carrying capacity of mariculture for filter-feeding shellfish. Journal of Fishery Sciences of China, 16(4): 626–632 (in Chinese with English abstract).

    Google Scholar 

  • Zhang, J. H., Fang, J. G., Jin, X. S., and Liang, F. P., 2002. Effect of energy budget of short-necked clam Ruditapes philippinarum under low temperature. Journal of Fisheries of China, 26(5): 423–427 (in Chinese with English abstract).

    Google Scholar 

  • Zhang, Y., 2007. Research on total amount control method and application in bay. PhD thesis. Ocean University of China, 58–64 (in Chinese with English abstract).

    Google Scholar 

  • Zhou, Y., Yang, H. S., Hu, S. L., and Zhang, F. S., 2002. Chemical composition and net organic production of cultivated and fouling organisms in Sishili Bay and their ecological effects. Journal of Fisheries of China, 26(2): 21–27 (in Chinese with English abstract).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. College of Fisheries, Ocean University of China, Qingdao, 266003, P. R. China

    Xiaoxiao Zan, Binduo Xu, Chongliang Zhang & Yiping Ren

Authors
  1. Xiaoxiao Zan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Binduo Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chongliang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yiping Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yiping Ren.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zan, X., Xu, B., Zhang, C. et al. Annual variations of biogenic element contents of manila clam (Ruditapes philippinarum) bottom-cultivated in Jiaozhou Bay, China. J. Ocean Univ. China 13, 637–646 (2014). https://doi.org/10.1007/s11802-014-2140-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11802-014-2140-5

Key words

Search

Navigation