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Seasonal changes in food uptake by the sea cucumber Apostichopus japonicus in a farm pond: Evidence from C and N stable isotopes

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Abstract

This study investigated the seasonal changes in carbon (C) and nitrogen (N) stable isotope values of several typical food sources of Apostichopus japonicus in a farm pond, including particulate organic matter (POM), macroalgae, benthic microalgae and animals such as nematode and copepod. The stable isotope technique was used to quantify relative contributions of various sources to the food uptake by A. japonicus. The results showed that significant changes occurred in the C and N stable isotope values of sea cucumber food sources due to the seasonality of micro- or macroalgae prosperity and the fluctuation of environmental conditions. The sea cucumber A. japonicus exhibited corresponding alterations in feeding strategy in response to the changes in food conditions. Calculation with a stable isotope mixing model showed that macroalgae was the principal food source for A. japonicus throughout the 1-yr investigation, with the relative contribution averaging 28.1%–63.2%. The relative contributions of other food sources such as copepod and nematode, POM, benthic microalgae to the total food uptake by sea cucumber averaged 22.6%–39.1%, 6.3% -22.2%, 2.8%–6.5%, and 2.8%–4.2%, respectively. Together these results indicated that the seasonal changes in food sources led to the obvious temporal differences in the relative contribution of various food sources utilized by A. japonicus. Such findings provide the basic scientific information for improving the aquaculture techniques of A. japonicus, particularly for optimizing the food environment of A. japonicus culture in farm ponds.

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References

  • Akin, S., and Winemiller, K. O., 2006. Seasonal variation in food web composition and structure in a temperate tidal estuary. Estuaries and Coasts, 29: 552–567.

    Google Scholar 

  • Franco, M. D. A., Vanaverbeke, J., Van Oevelen, D., Soetaert, K., Costa, M. J., Vincx, M., and Moens, T., 2010. Respiration partitioning in contrasting subtidal sediments: seasonality and response to a spring phytoplankton deposition. Marine Ecology, 31: 276–290.

    Article  Google Scholar 

  • Bao, J., Dong, S. L., Tian, X. L., Wang, F., Gao, Q. F., and Dong, Y. W., 2010. Metabolic rates and biochemical compositions of Apostichopus japonicus (Selenka) tissue during periods of inactivity. Chinese Journal of Oceanology and Limnlology, 28(2): 218–223.

    Article  Google Scholar 

  • Canuel, E. A., Cloern, J. E., Ringelberg, D. B., Guckert, J. B., and Rau, G. H., 1995. Molecular and isotopic tracers used to examine source of organic matter and its incorporation into the food webs of San Francisco Bay. Limnology and Oceanography, 40: 67–81.

    Article  Google Scholar 

  • Chen, J. X., 2004. Present status and prospects of sea cucumber industry in China. In: Advances in Sea Cucumber Aquaculture and Management (ASCAM), 463. Lovatelli, A., et al., eds., FAO, Rome, Italy, 25–38.

    Google Scholar 

  • Couch, C. A., 1988. A procedure for extracting large numbers of debris-free, living nematodes from muddy marine systems. Transactions of the American Microscopical Society, 107: 96–100.

    Article  Google Scholar 

  • Couch, C. A., 1989. Carbon and nitrogen isotopes of meiobenthos and their food resources. Estuarine, Coastal and Shelf Science, 28: 433–411.

    Article  Google Scholar 

  • Currin, C. A., Newell, S. Y., and Paerl, H. W., 1995. The role of standing dead Spartina alterniflora and benthic microalgae in sail marsh food webs: considerations based on multiple stable isotope analysis. Marine Ecology Progress Series, 121: 99–116.

    Article  Google Scholar 

  • Debes, H. H., and Eliasen, K., 2006. Seasonal abundance, reproduction and development of four key copepod species on the Faroe shelf. Marine Biology Research, 2: 249–259.

    Article  Google Scholar 

  • Dong, Y. W., Ji, T. T., Meng, X. L., Dong, S. L., and Sun, W. M., 2010. Difference in thermo-tolerance between green and red color variants of the Japanese sea cucumber, Apostichopus japonicus Selenka: Hsp70 and heat-hardening effect. Biological Bulletin, 218: 87–94.

    Google Scholar 

  • Fong, P., and Zedler, J. B., 1993. Temperature and light effects on the seasonal succession of algal communities in shallow coastal lagoons. Journal of Experimental Marine Biology and Ecology, 171: 259–272.

    Article  Google Scholar 

  • Fry, B., and Sherr, E. B., 1984. δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Contributions in Marine Science, 27: 13–47.

    Google Scholar 

  • Fry, B., and Wainright, S. C., 1991. Diatom sources of 13C-rich carbon in marine food webs. Marine Ecology Progress Series, 76: 149–157.

    Article  Google Scholar 

  • Gannes, L. Z., Martínez del Rio, C., and Koch, P., 1998. Natural abundance variations in stable isotopes and their potential uses in animal physiological ecology. Comparative Biochemistry and Physiology — Part A: Molecular and Integrative Physiology, 119: 725–737.

    Article  Google Scholar 

  • Gao, Q. F., Paul, K. S. S., Lin, G. H., Chen, S. P., and Cheung, S. G., 2006. Stable isotope and fatty acid evidence for uptake of organic waster by green-lipped mussels Perna viridis in a polyculture fish farm system. Marine Ecology Progress Series, 317: 273–283.

    Article  Google Scholar 

  • Gao, Q. F., Wang, Y. S., Dong, S. L., and Sun, Z. L., 2011. Absorption of different food sources by sea cucumber Apostichopus japonicus (Selenka) (Echinodermata: Holothuroidea): evidence from carbon stable isotope. Aquaculture, 319: 272–276.

    Article  Google Scholar 

  • Gu, M., Ma, H. M., Mai, K. S., Zhang, W. B., Bai, N., and Wang, X. J., 2011. Effects of dietary beta-glucan, mannan oligosaccharide and their combinations on growth performance, immunity and resistance against Vibrio splendidus of sea cucumber, Apostichopus japonicus. Aquaculture, 31: 303–309.

    Google Scholar 

  • Hamm, C. E., Merkel, R., Springer, O., Jurkojc, P., Maier, C., Prechtel, K., and Smetacek, V., 2003. Architecture and mate rial properties of diatom shells provide effective mechanical protection. Nature, 421: 841–843.

    Article  Google Scholar 

  • Hua, H. F., 1989. The ecological habit of the sea cucumber Apostichopus japonicus. Aquaculture Overseas, 2: 5–8 (in Chinese with English abstract).

    Google Scholar 

  • Hobson, K. A., and Welch, H. E., 1992. Determination of trophic relationships within a high Artic marine food web using δ13C and δ15N analysis. Marine Ecology Progress Series, 84: 9–18.

    Article  Google Scholar 

  • Jiang, Z. H., Chen, R. S., and Wang, J., 2007. Species composition and biomass of microphytobenthos in intertidal zone of Hongdao Island, Jiaozhou Bay. Marine Fisheries Research, 28: 74–81 (in Chinese with English abstract).

    Google Scholar 

  • Kharlamenko, V. I., Kiyashko, S. I., Rodkina, S. A., and Imbs, A. B., 2008. Determination of food sources of marine invertebrates from a subtidal sand community using analyses of fatty acids and stable isotopes. Russian Journal of Marine Biology, 34: 101–109.

    Article  Google Scholar 

  • Lehane, C., and Davenport, J., 2002. Ingestion of mesozooplankton by three species of bivalves: Mytilus edulis, Cerastoder-ma edule and Aequipecten opercularis. Journal of the Marine Biological Association of the United Kingdom, 82: 615–619.

    Article  Google Scholar 

  • Li, Q., Chen, L., and Kong, L., 2009. A genetic linkage map of the sea cucumber, Apostichopus japonicus (Selenka), based on AFLP and microsatellite markers. Animal Genetics, 40: 678–685.

    Article  Google Scholar 

  • Liao, Y., 1980. The Aspidochirote holothurians of China with erection of a new genus. In: Echinoderms: Present and Past. Proceeding of European Colloquium on Echinoderms, Brussels. Jangoux, M. ed., Balkema, A. A., Rotterdam, Netherlands, 115–120.

    Google Scholar 

  • Liu, Y., Dong, S. L., Tian, X. L., Wang, F., and Gao, Q. F., 2009. Effects of dietary sea mud and yellow soil on growth and energy budget of the sea cucumber Apostichopus japonicus (Selenka). Aquaculture, 286: 266–270.

    Article  Google Scholar 

  • Lorrain, A., Savoye, N., Chauvaud, L., Paulet, Y. M., and Naulet, N., 2003. Decarbonation and preservation method for the analysis of organic C and N contents and stable isotope ratios of low-carbonated suspended particulate material. Analytica Chimica Acta, 491: 125–133.

    Article  Google Scholar 

  • Mangion, P., Taddel, D., Frouin, P., and Conand, C., 2004. Feeding Rate and Impact of Sediment Reworking by Two Deposit Feeders Holothuria leucospilota and Holothuria atra on a Fringing Reef (Reunion Island, Indian Ocean), Echinoderms. Nebelsick, J. H., and Heinzeller, T., eds, Taylor and Francis Group, London, 311–317.

    Google Scholar 

  • McClelland, J. W., and Valiela, I., 1998. Changes in food web structure under the influence of increased anthropogenic nitrogen inputs to estuaries. Marine Ecology Progress Series, 186: 259–271.

    Article  Google Scholar 

  • McCutchan, J. H., Lewis, W. M., Kendall, C., and McGrath, C. C., 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikis, 102: 378–390.

    Article  Google Scholar 

  • Ministry of Agriculture of China, 2009. China Fisheries Yearbook, 2008. China Agriculture Publisher, Beijing, China, 24–28 (in Chinese).

    Google Scholar 

  • Nadon, M. O., and Himmelman, J. H., 2006. Stable isotopes in subtidal food webs: have enriched carbon ratios in benthic consumers been misinterpreted? Limnology and Oceanography, 51: 2 828–2 836.

    Article  Google Scholar 

  • Paltzat, D. L., Pearce, C. M., Barnes, P. A., and McKinley, R. S., 2008. Growth and production of California sea cucumbers (Parastichopus californicus Stimpson) co-cultured with suspended Pacific oysters (Crassostrea gigas Thunberg). Aquaculture, 275: 124–137.

    Article  Google Scholar 

  • Peterson, B. J., 1999. Stable isotopes as tracers of organic matter input and transfer in benthic food webs: a review. Acta Oecologica, 20: 479–487.

    Article  Google Scholar 

  • Peterson, B. J., and Fry, B., 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics, 18: 293–320.

    Article  Google Scholar 

  • Phillips, D. L., and Gregg, J. W., 2003. Source partitioning using stable isotopes: coping with too many sources. Oecologia, 136: 261–267.

    Article  Google Scholar 

  • Ren, Y. C., Dong, S. L., Wang, F., Gao, Q. F., Tian, X. L., and Liu, F., 2010. Sedimentation and sediment characteristics in sea cucumber Apostichopus japonicus (Selenka) culture ponds. Aquaculture Research, 42: 14–21.

    Article  Google Scholar 

  • Riéra, P., Richard, P., Grémare, A., and Blanchard, G., 1996. Food source of intertidal nematodes in the Bay of Marennes-Oléron (France), as determined by dual stable isotope analysis. Marine Ecology Progress Series, 142: 303–309.

    Article  Google Scholar 

  • Riéra, P., and Hubas, C., 2003. Trophic ecology of nematodes from various microhabitats of the Roscoff Aber Bay (France): Importance of stranded macroalgae evidenced through δ13C and δ15N. Marine Ecology Progress Series, 260: 151–159.

    Article  Google Scholar 

  • Ruiz, J. F., Ibáñez, C. M., and Cáceres, C. W., 2007. Gut morphometry and feeding of the sea cucumber Athyonidium chilensis (Semper, 1868) (Echinodermata: Holothuroidea). Journal of Marine Biology and Oceanography, 42: 269–274 (in Spanish with English abstract).

    Google Scholar 

  • Seo, J. Y., and Lee, S. M., 2011. Optimum dietary protein and lipid levels for growth of juvenile sea cucumber Apostichopus japonicus. Aquaculture Nutrition, 17: e56–e61.

    Article  Google Scholar 

  • Schmidt, O., Scrimgeour, C. M., and Curry, J. P., 1999. Carbon and nitrogen stable isotope ratios in body tissue and mucus of feeding and fasting earthworms (Limbricus festivus). Oecologia, 118: 9–15.

    Article  Google Scholar 

  • Shimoda, K., Aramaki, Y., Nasuda, J., Yokoyama, H., Ishihi, Y., and Tamaki, A., 2007. Food sources for three species of Nihonotrypaea (Decapoda: Thalassinidea: Callianassidae) from western Kyushu, Japan, as determined by carbon and nitrogen stable isotope analysis. Journal of Experimental Marine Biology and Ecology, 342: 292–312.

    Article  Google Scholar 

  • Slater, M. J., and Carton, A. G., 2009. Effect of sea cucumber (Australostichopus mollis) grazing on coastal sediments impacted by mussel farm deposition. Marine Pollution Bulletin, 58: 1 123–1 129.

    Article  Google Scholar 

  • Slater, M. J., and Carton, A. G., 2010. Sea cucumber habitat differentiation and site retention as determined by intraspecific stable isotope variation. Aquaculture Research, 41: e695–e702.

    Google Scholar 

  • SPSS Inc., 2008. SPSS 16.0 Student Version for Windows. SPSS, Prentice Hall, Upper Saddle River, New Jersey.

    Google Scholar 

  • Strickland, J. D. H., and Parsons, T. R., 1977. A Practical Handbook of Seawater Analysis. Canadian Government Publishing Center, Ottawa, Canada, 330pp.

    Google Scholar 

  • Sun, Z. L., Gao, Q. F., Dong, S. L., Shin, P. K. S., and Wang, F., 2012. Estimates of carbon turnover rates in the sea cucumber Apostichopus japonicus (Selenka) using stable isotope analysis: the role of metabolism and growth. Marine Ecology Progress Series, 457: 101–112.

    Article  Google Scholar 

  • Tieszen, L. L., Boutton, T. W., Tesdahl, K. G., and Slade, N. A., 1983. Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia, 57: 32–37.

    Article  Google Scholar 

  • Vanderklift, M. A., and Ponsard, S., 2003. Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia, 136: 169–182.

    Article  Google Scholar 

  • Wang, J. Y., Song, Z. D., Wang, S. X., Huang. B. S., Li. P. Y., and Zhang, L. M., 2009. The study on the protein requirement of the sea cucumber Apostichopus japonicus (Selenka) under different growth stages. Aquaculture Science and Technology Information, 36: 229–233 (in Chinese with English abstract).

    Google Scholar 

  • Wing, S. R., McLeod, R. J., Clark, K. L., and Frew, R., D., 2008. Plasticity in the diet of two echinoderm species across an ecotone: microbial recycling of forest litter and bottom-up forcing of population structure. Inter-Research Marine Ecology Progress Series, 360: 115–123.

    Article  Google Scholar 

  • Wong, W. H., and Cheung, S. G., 2001. Feeding rates and scope for growth of green mussels, Perna viridis (L.) and their relationship with food availability in Kat O, Hong Kong. Aquaculture, 193: 123–137.

    Article  Google Scholar 

  • Yang, E. J., Ju, S. J., and Choi, J. K., 2010. Feeding activity of the copepod Acartia hongi on phytoplankton and micro-zooplankton in Gyeonggi Bay, Yellow Sea. Estuarine, Coastal and Shelf Science, 88: 292–301.

    Article  Google Scholar 

  • Yang, H. S., Yuan, X. T., and Zhou, Y., 2005. Effects of body weight and water temperature on food consumption and growth in the sea cucumber Apostichopus japonicus (Selenka) with special reference to aestivation. Aquaculture Research, 36: 1 085–1 092.

    Article  Google Scholar 

  • Yuan, X. T., Yang, H. S., Wang, L. L., Zhou, Y., Zhang, T., and Liu, Y., 2007. Effects of aestivation on the energy budget of sea cucumber Apostichopus japonicus (Selenka) (Echinodermata: Holothuroidea). Acta Ecologica Sinica, 27: 3155–3161.

    Article  Google Scholar 

  • Yuan, X. T., Yang, H. S., Wang, L. L., Zhou, Y., and Gabr, H. R., 2009. Bioenergetic responses of sub-adult sea cucumber Apostichopus japonicus (Selenka) (Echinodermata: Holothuroidea) to temperature with special discussion regarding its southern most distribution limit in China. Journal of Thermal Biology, 34: 315–319.

    Article  Google Scholar 

  • Zamora, L. N., and Jeffs, A. G., 2011. Feeding, selection, digestion and absorption of the organic matter from mussel waste by juveniles of the deposit-feeding sea cucumber, Australostichopus mollis. Aquaculture, 317: 223–228.

    Article  Google Scholar 

  • Zar, J. H., 2009. Biostatistical analysis. 5th edition, Prentice Hall, Upper Saddle River, New Jersey, USA, 66–284.

    Google Scholar 

  • Zhang, B. L., Sun, D. Y., and Wu, Y. Q., 1995. Preliminary analysis on the feeding habit of Apostichopus janonicus in the rocky coast waters of Lingshan Island. Marine Science, 3: 11–13 (in Chinese with English abstract).

    Google Scholar 

  • Zhou, Y., Yang, H. S., Liu, S. L., Yuan, X. T., Mao, Y. Z., Liu, Y., Xu, X. L., and Zhang, F. S., 2006. Feeding and growth on bivalve biodeposits by the deposit feeder Stichopus japonicus Selenka (Echinodennata: Holothuroudea) co-cultured in lantern nets. Aquaculture, 256: 510–520.

    Article  Google Scholar 

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Authors and Affiliations

  1. Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, 266003, P. R. China

    Zhenlong Sun, Qinfeng Gao, Shuanglin Dong & Fang Wang

  2. Department of Biology and Chemistry and State Key Laboratory in Marine Pollution, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong, P. R. China

    Paul K. S. Shin

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  1. Zhenlong Sun
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Correspondence to Qinfeng Gao.

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Sun, Z., Gao, Q., Dong, S. et al. Seasonal changes in food uptake by the sea cucumber Apostichopus japonicus in a farm pond: Evidence from C and N stable isotopes. J. Ocean Univ. China 12, 160–168 (2013). https://doi.org/10.1007/s11802-012-1952-z

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  • DOI: https://doi.org/10.1007/s11802-012-1952-z

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