Hostname: page-component-8448b6f56d-42gr6 Total loading time: 0 Render date: 2024-04-16T21:49:16.544Z Has data issue: false hasContentIssue false
  • English
  • Français

Potential dietary influence on the stable isotopes and fatty acid composition of migratory anchovy (Coilia mystus) around the Changjiang Estuary

Published online by Cambridge University Press:  04 September 2014

Ying Cui ,
Ying Wu ,
Zhao Li Xu  and
Jing Zhang
Ying Cui*
Affiliation:
State Key Laboratory of Estuarine and Coastal Research, East China Normal University, 3663 North Zhongshan Road, Shanghai 200062, China
Ying Wu
Affiliation:
State Key Laboratory of Estuarine and Coastal Research, East China Normal University, 3663 North Zhongshan Road, Shanghai 200062, China
Zhao Li Xu
Affiliation:
Key and Open Laboratory of Marine and Estuary Fisheries, Ministry of Agriculture of China, East China Sea Fisheries Research Institute, Chinese Academy of Fisheries Sciences, Shanghai 200090, China
Jing Zhang
Affiliation:
State Key Laboratory of Estuarine and Coastal Research, East China Normal University, 3663 North Zhongshan Road, Shanghai 200062, China
*
Correspondence should be addressed to: Y. Cui, State Key Laboratory of Estuarine and Coastal Research, East China Normal University, 3663 North Zhongshan Road, Shanghai 200062, China email: ycui@sklec.ecnu.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

The stable carbon and nitrogen isotopes and fatty acid composition of tapertail anchovy (Coilia mystus) at four migration stages collected around the Changjiang Estuary were analysed to investigate the variations in the trophic biomarkers during the fish migration. δ13 C and δ15N values of C. mystus ranged from −21.5 to −15.4‰ and from 6.9–15.8‰, respectively. Both δ13C and δ15N were enriched during migration. Polyunsaturated fatty acids were the dominant fatty acids and the major fatty acids found in C. mystus were C20:5n-3, C22:6n-3, C20:4n-6, C16:0, C18:0, C16:1n-7, C18:1(n-9, n-7) and C20:1 + C22:1. Significant changes among C. mystus at different migration stages were found both in the fatty acid composition and specific fatty acid concentration. Though the enrichment of stable isotopes may due to multiple factors (e.g. diet shift, environment and ontogeny), the dietary influence can be determined by the variation in fatty acid composition. Changes in the concentrations of benthic markers (C18:1n-7 and C20:4n-6) and pelagic markers (C18:1n-9 and C20:1 + C22:1) in C. mystus during the migration may suggest that benthic and pelagic food sources alternately dominated the anchovies' diet during different migration stages. It seems that application of multiple biomarkers in the trophic study of migratory fish will elevate the reliability of the analysis.

Keywords

migratory fishdiet sourceestuarymultiple biomarkers
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 95 , Issue 1 , February 2015 , pp. 193 - 205
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ahlgren, G., Vrede, T. and Goedkoop, W. (2009) Fatty acid ratios in freshwater fish, zooplankton and zoobenthos—are there specific optima? In Arts, M.T., Brett, M.T. and Kainz, M.J. (eds) Lipids in aquatic ecosystems. New York: Springer, pp. 147–177.Google Scholar
Alfaro, A.C. (2008) Diet of Littoraria scabra, while vertically migrating on mangrove trees: Gut content, fatty acid, and stable isotope analyses. Estuarine, Coastal and Shelf Science 79, 718–726.Google Scholar
Alfaro, A.C., Thomas, F., Sergent, L. and Duxbury, M. (2006) Identification of trophic interactions within an estuarine food web (northern New Zealand) using fatty acid biomarkers and stable isotopes. Estuarine, Coastal and Shelf Science 70, 271–286.CrossRefGoogle Scholar
Bacha, M. and Amara, R. (2009) Spatial, temporal and ontogenetic variation in diet of anchovy (Engraulis encrasicolus) on the Algerian coast (SW Mediterranean). Estuarine, Coastal and Shelf Science 85, 257–264.Google Scholar
Bardonnet, A. and Riera, P. (2005) Feeding of glass eels (Anguilla anguilla) in the course of their estuarine migration: new insights from stable isotope analysis. Estuarine, Coastal and Shelf Science 63, 201–209.Google Scholar
Brett, M.T., Müller-Navarra, D.C. and Persson, J. (2009) Crustacean zooplankton fatty acid composition. In Arts, M.T., Brett, M.T. and Kainz, M.J. (eds) Lipids in aquatic ecosystems. New York: Springer, pp. 115–146.CrossRefGoogle Scholar
Budge, S.M., Iverson, S.J. and Koopman, H.N. (2006) Studying trophic ecology in marine ecosystems using fatty acids: a primer on analysis and interpretation. Marine Mammal Science 22, 759–801.CrossRefGoogle Scholar
Budge, S.M., Parrish, C.C. and Mckenzie, C.H. (2001) Fatty acid composition of phytoplankton, settling particulate matter and sediments at a sheltered bivalve aquaculture site. Marine Chemistry 76, 285–303.Google Scholar
Budge, S.M., Wooller, M.J., Springer, A.M., Iverson, S.J., McRoy, C.P. and Divokyet, G.J. (2008) Tracing carbon flow in an arctic marine food web using fatty acid-stable isotope analysis. Oecologia 157, 117–129.Google Scholar
Ciancio, J.E., Pascual, M.A., Botto, F., Amaya-Santi, M., O'Neal, S., Riva Rossi, C. and Iribarne, O. (2008) Stable isotope profiles of partially migratory salmonid populations in Atlantic rivers of Patagonia. Journal of Fish Biology 72, 1708–1719.Google Scholar
Clarke, K.R. (1993) Non-parametric multivariate analysis of changes in community structure. Australian Journal of Ecology 18, 117–143.Google Scholar
Copeman, L.A. and Parrish, C.C. (2003) Marine lipids in a cold coastal ecosystem: Gilbert Bay, Labrador. Marine Biology 143, 1213–1227.Google Scholar
Cui, Y., Wu, Y., Zhang, J. and Wang, N. (2012) Potential dietary influence on the stable isotopes and fatty acid compositions of jellyfishes in the Yellow Sea. Journal of the Marine Biological Association of the United Kingdom 92, 1325–1333.Google Scholar
Graeve, M., Kattner, G., Wiencke, C. and Karsten, U. (2002) Fatty acid composition of Arctic and Antarctic macroalgae: indicator of phylogenetic and trophic relationship. Marine Ecology Progress Series 231, 67–74.CrossRefGoogle Scholar
Graeve, M., Lundberg, M., Böer, M., Kattner, G., Hop, H. and Petersen, S.F. (2008) The fate of dietary lipids in the Arctic ctenophore Mertensia ovum (Fabricius 1780). Marine Biology 153, 643–651.Google Scholar
Gu, B., Schelske, C.L. and Hoyer, M.V. (1996) Stable isotopes of carbon and nitrogen as indicators of diet and trophic structure of the fish community in a shallow hypereutrophic lake. Journal of Fish Biology 49, 1233–1243.Google Scholar
Hall, D., Lee, S.Y. and Meziane, T. (2006) Fatty acids as trophic tracers in an experimental estuarine food chain: tracer transfer. Journal of Experimental Marine Biology and Ecology 336, 42–53.CrossRefGoogle Scholar
Hall, J.M., Parrish, C.C. and Thompson, R.J. (2002) Eicosapentaenoic acid regulates scallop (Placopecten magellanicus) membrane fluidity in response to cold. Biological Bulletin. Marine Biological Laboratory, Woods Hole 202, 201–203.Google Scholar
Harrod, C., Grey, J., McCarthy, T.K. and Morrissey, M. (2005) Stable isotope analyses provide new insights into ecological plasticity in a mixohaline population of European eel. Oecologia 144, 673–683.CrossRefGoogle Scholar
He, W.P., Li, Z.J., Liu, J.S., Li, Y.X., Murphy, B.R. and Xie, S.G. (2008) Validation of a method of estimating age, modelling growth, and describing the age composition of Coilia mystus from the Yangtze Estuary, China. ICES Journal of Marine Science 65, 1655–1661.Google Scholar
Hebert, C.E., Arts, M.T. and Weseloh, D.V.C. (2006) Ecological tracers can quantify food web structure and change. Environmental Science and Technology 40, 5618–5623.Google Scholar
Herbeck, L.S. (2011) Ecological impact of land-derived anthropogenic nutrients and organic matter on tropical estuarine and coastal systems of Hainan, China. PhD dissertation. University of Bremen, Germany.Google Scholar
Hessen, D.O. and Leu, E. (2006) Trophic transfer and trophic modification of fatty acids in high Arctic lakes. Freshwater Biology 51, 1987–1998.Google Scholar
Iverson, S.J. (2008) Tracing aquatic food webs using fatty acids: from qualitative indicators to quantitative determination. In Arts, M.T., Brett, M.T. and Kainz, M.J. (eds) Lipids in aquatic ecosystems. New York: Springer, pp. 281–307.Google Scholar
Jennings, S., Pinnegar, J.K., Polunin, N.V.C. and Warr, K.J. (2002) Linking size-based and trophic analyses of benthic community structure. Marine Ecology Progress Series 226, 77–85.Google Scholar
Ji, H.H. and Ye, S.F. (2006) Ecological distribution characteristics of zooplankton and its relationship with environmental factors in the Changjiang River estuary. Marine Sciences 30, 23–30.Google Scholar
Kattner, G. and Hagen, W. (2008) Lipids in marine copepods: latitudinal characteristics and perspective to global warming. In Arts, M.T., Brett, M.T. and Kainz, M.J. (eds) Lipids in aquatic ecosystems. New York: Springer, pp. 257–280.Google Scholar
Koussoroplis, A.M., Bec, A., Perga, M.E., Koutrakis, E., Bourdier, G. and Desvilettes, C. (2011) Fatty acid transfer in the food web of a coastal Mediterranean lagoon: evidence for high arachidonic acid retention in fish. Estuarine, Coastal and Shelf Science 91, 450–461.Google Scholar
Letourneur, Y., Galzin, R. and Harmelin-Vivien, M. (1997) Temporal variations in the diet of the damselfish Stegastes nigricans (Lacepède) on a Réunion fringing reef. Journal of Experimental Marine Biology and Ecology 217, 1–18.Google Scholar
Li, X.C., Fan, X., Han, L.J., Yan, X.J. and Lou, Q.X. (2002) Fatty acids of common marine macrophytes from the Yellow and Bohai Seas. Oceanologia and Limnologia Sinica 33, 215–224.Google Scholar
Li, Z.Y., Zuo, T., Dai, F.Q., Jin, X.S. and Zhuang, Z.M. (2009) Study on feeding habits of organisms from Changjiang Estuary and adjacent Southern Yellow Sea in spring with stable isotope technology. Journal of Fisheries of China 33, 784–789.Google Scholar
Liu, K., Zhang, M.Y., Xu, D.P. and Shi, W.G. (2004) Studies on resource change and MSY of Coilia mystus in the Yangtze River estuary. Journal of Shanghai Fisheries University 13, 298–303.Google Scholar
Liu, S.H. and Xu, Z.L. (2011) Comparison of zooplankton lists between Coilia mystus food contents and collections from the Yangtze River Estuary and Hangzhou Bay. Acta Ecologica Sinica 31, 2263–2271.Google Scholar
Loseto, L.L., Stern, G.A., Connelly, T.L., Deibel, D., Gemmill, B., Prokopowicz, A., Fortier, L. and Ferguson, S.H. (2009) Summer diet of beluga whales inferred by fatty acid analysis of the eastern Beaufort Sea food web. Journal of Experimental Marine Biology and Ecology 374, 12–18.CrossRefGoogle Scholar
Luo, B.Z., Wei, S. and Dou, S.Z. (1997) Study on food web and trophic structure of fish in the Changjiang River Estuary. Studia Marina Sinica 38, 143–153.Google Scholar
Maazouzi, C., Masson, G., Izquierdo, M.S. and Pihan, J.C. (2007) Fatty acid composition of the amphipod Dikerogammarus villosus: feeding strategies and trophic links. Comparative Biochemistry and Physiology Part A 147, 868–875.CrossRefGoogle ScholarPubMed
Malej, A., Faganeli, J. and Pezdifi, J. (1993) Stable isotope and biochemical fractionation in the marine pelagic food chain: the jellyfish Pelagia noctiluca and net zooplankton. Marine Biology 116, 565–570.Google Scholar
Mandima, J.J. (2000) Spatial and temporal variations in the food of the sardine Limnothrissa miodon (Boulenger, 1906) in Lake Kariba, Zimbabwe. Fisheries Research 48, 197–203.CrossRefGoogle Scholar
Mercado-Silva, N., Helmus, M.R. and Vander Zanden, M.J. (2009) The effects of impoundment and invasive species on a river food web in Mexico's central plateau. River Research and Applications 25, 1090–1108.Google Scholar
Ni, Y. (1999) Fishery resources conservation for Coilia maystus in the Changjiang estuary. Journal of Fishery Sciences of China 6, 75–77.Google Scholar
Ni, Y., Wang, Y.L., Jiang, M. and Chen, Y.Q. (1999) Biological characteristics of Coilia mystus in the Changjiang estuary. Journal of Fishery Sciences of China 6, 69–71.Google Scholar
Nybakken, J.W. (1997) Marine biology: an ecological approach. Reading: Addison-Wesley Longman, pp. 109–111.Google Scholar
Overman, N.C. and Parrish, D.L. (2001) Stable isotope composition of walleye: 15N accumulation with age and area-specific differences in δ13C. Canadian Journal of Fisheries and Aquatic Sciences 58, 1253–1260.Google Scholar
Parrish, C.C., Abrajano, T.A., Budge, S.M., Helleur, R.J., Hudson, E.D., Pulchan, K. and Ramos, C. (2000) Lipid and phenolic biomarkers in marine ecosystems: analysis and applications. In Wangersky, P. (ed.) The handbook of environmental chemistry, Volume 5, Part D: marine chemistry. Berlin: Springer, pp. 193–223.Google Scholar
Petursdottir, H., Gislason, A., Falk-Petersen, S., Hop, H. and Svavarsson, J. (2008) Trophic interactions of the pelagic ecosystem over the Reykjanes Ridge as evaluated by fatty acid and stable isotope analyses. Deep-Sea Research Part II 55, 83–93.Google Scholar
Pinnegar, J.K. and Polunin, N.V.C. (1999) Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions. Functional Ecology 13, 225–231.Google Scholar
Pitt, K.A., Connolly, R.M. and Meziane, T. (2009) Stable isotope and fatty acid tracers in energy and nutrient studies of jellyfish: a review. Hydrobiologia 616, 119–132.CrossRefGoogle Scholar
Pond, D.W., Bell, M.V., Harris, R.P. and Sargent, J.R. (1998) Microplanktonic polyunsaturated fatty acid markers: a mesocosm trial. Estuarine, Coastal and Shelf Science 46, 61–67.Google Scholar
Post, D.M. (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703–718.Google Scholar
Prigge, E., Malzahn, A.M., Zumholz, K. and Hanel, R. (2012) Dietary effects on fatty acid composition in muscle tissue of juvenile European eel, Anguilla Anguilla (L.). Helgoland Marine Research 66, 51–61.Google Scholar
Rossi, S., Sabatés, A., Latasa, M. and Reyes, E. (2006) Lipid biomarkers and trophic linkages between phytoplankton, zooplankton and anchovy (Engraulis encrasicolus) larvae in the NW Mediterranean. Journal of Plankton Research 6, 551–562.Google Scholar
Rossi, S., Youngbluth, M.J., Jacoby, C.A., Pagès, F. and Garrofé, X. (2008) Fatty acid trophic markers and trophic links among seston, crustacean zooplankton and the siphonophore Nanomia cara in Georges Basin and Oceanographer Canyon (NW Atlantic). Scientia Marina 72, 403–416.Google Scholar
Saddler, J.B., Koski, K.V. and Cardwell, R.D. (1972) Fatty acid alterations during migration and early sea water growth of Chum Salmon (Oncorhynchus keta). Lipids 7, 90–95.Google Scholar
Schafer, L.N., Platell, M.E., Valesini, F.J. and Potter, I.C. (2002) Comparisons between the influence of habitat type, season and body size on the dietary compositions of fish species in nearshore marine waters. Journal of Experimental Marine Biology and Ecology 278, 67–92.Google Scholar
Steffy, L.Y. and Kilham, S.S. (2004) Elevated delta N-15 in stream biota in areas with septic tank systems in an urban watershed. Ecological Applications 14, 637–641.Google Scholar
Stowasser, G., Mcaallen, R., Pierce, G.J., Collins, M.A., Moffat, C.F., Priede, I.G. and Pond, D.W. (2009a) Trophic position of deep-sea fish—assessment through fatty acid and stable isotope analyses. Deep-Sea Research Part I 56, 812–826.Google Scholar
Stowasser, G., Pond, D.W. and Collins, M.A. (2009b) Using fatty acid analysis to elucidate the feeding habits of Southern Ocean mesopelagic fish. Marine Biology 156, 2289–2302.Google Scholar
Sugisaki, H. and Tsuda, A. (1995) Nitrogen and carbon stable isotopic ecology in the ocean: the transportation of organic materials through the food web. In Sakai, H. and Nozaki, Y. (eds) Biogeochemical processes and ocean flux in the Western Pacific. Tokyo: Terra Scientific Publishing Company, pp. 307–317.Google Scholar
Vander Zanden, M.J. and Fetzer, W.W. (2007) Global patterns of aquatic food chain length. Oikos 116, 1378–1388.Google Scholar
Vander Zanden, M.J. and Vadeboncoeur, Y. (2002) Fishes as integrators of benthic and pelagic food webs in lakes. Ecology 83, 2152–2161.Google Scholar
Volkman, J.K., Barrett, S.M., Blackburn, S.I., Mansour, M.P., Sikes, E.L. and Gelin, F. (1998) Microalgal biomarkers: a review of recent research developments. Organic Geochemistry 29, 1163–1179.CrossRefGoogle Scholar
Wan, R.J., Wu, Y., Huang, L., Zhang, J., Gao, L. and Wang, N. (2010) Fatty acids and stable isotopes of a marine ecosystem: study on the Japanese anchovy (Engraulis japonicus) food web in the Yellow Sea. Deep-Sea Research Part II 57, 1047–1057.Google Scholar
Wang, N. (2008) Application of fatty acids biomarker in marine food web research: a case in the Yangtze River Estuary Sea Area. MSc dissertation. East China Normal University, Shanghai, China.Google Scholar
Würzberg, L., Peters, J., Schüller, M. and Brandt, A. (2011) Diet insights of deep-sea polychaetes derived from fatty acid analyses. Deep-Sea Research Part II 58, 153–162.CrossRefGoogle Scholar
Xu, J., Zhang, M. and Xie, P. (2007) Size-related shifts in reliance on benthic and pelagic food webs by lake anchovy. Ecoscience 2, 170–177.Google Scholar
Xu, Z.L. and Shen, X.Q. (2005) Zooplankton biomass and its variation in water near Changjiang Estuary. Resources and Environment in the Yangtze Basin 14, 282–286.Google Scholar
Xu, Z.L., Wang, Y.L., Chen, Y.Q. and Shen, H.T. (1995) An ecological study on zooplankton in maximum turbid zone of estuarine area of Changjiang (Yangtze) river. Journal of Fishery Sciences of China 2, 39–48.Google Scholar
Xue, Y., Jin, X.S., Zhang, B. and Liang, Z.L. (2004) Diet composition and seasonal variation in feeding habits of small yellow croaker Pseudosciaena polyactis Bleeker in the central Yellow Sea. Journal of Fishery Sciences of China 11, 237–243.Google Scholar
Xue, Y., Xu, B.D., Gao, T.X., Xu, H. and Lin, L.S. (2010) Preliminary study on the feeding habit of Lophius litulon during autumn in the North Yellow Sea. Journal of Ocean University of China 40, 39–44.Google Scholar
Yuan, C.B. and Qin, A.L. (1984) Ecological habits and distribution of Coilia along the Chinese coast and its changes of output. Marine Sciences 5, 35–37.Google Scholar
Zeng, Q. and Dong, F.Y. (1993) Study on the biological characteristics and factor correlation of Coilia mystus propagating population. Journal of Lake Sciences 2, 164–170.Google Scholar
Zhang, B. (2004) Feeding habit and ontogenetic diet shift of hairtail fish (Trichiurus leprurus) in East China Sea and Yellow Sea. Marine Fisheries Research 25, 6–12.Google Scholar
Zhang, B., Jin, X.S. and Dai, F.Q. (2008) Feeding habits of the two sciaenid fishes near the Changjiang estuary. Acta Zoologica Sinica 54, 209–217.Google Scholar
Zhou, Y.D., Xu, L.J. and Xu, K.D. (2004) A study on biological characteristics of Coilia mystus (Linnaeus) offshore of Zhoushan. Journal of Modern Fisheries Information 19, 19–21.Google Scholar
Zhu, Q.Q. (1988) An investigation on the ecology of zooplankton in Changjiang Estuary and Hangzhou Bay. Journal of Fisheries of China 12, 111–123.Google Scholar
Zhu, Y.Z., Liu, L.S., Zheng, B.H. and Wang, Y. (2011) Relationship between spatial distribution of zooplankton and environmental factors in the Changjiang Estuary and its adjacent waters in spring. Marine Sciences 35, 59–65.Google Scholar
Zhuang, P., Luo, G., Zhang, T., Zhang, L.Z., Liu, J., Feng, G.P. and Hou, J.L. (2010) Food comparison among juvenile Acipenser sinensis and other six economic fishes in the Yangtze estuary. Acta Ecologica Sinica 30, 5544–5554.Google Scholar