, Volume 616, Issue 1, pp 119–132 | Cite as

Stable isotope and fatty acid tracers in energy and nutrient studies of jellyfish: a review



Studies of the trophic ecology of gelatinous zooplankton have predominantly employed gut content analyses and grazing experiments. These approaches record only what is consumed rather than what is assimilated by the jellyfish, only provide evidence of recent feeding, and unless digestion rates of different prey are known, may provide biased estimates of the relative importance of different prey to jellyfish diets. Biochemical tracers, such as stable isotopes and fatty acids, offer several advantages because they differentiate between what is assimilated and what is simply ingested, they provide an analysis of diet that is integrated over time, and may be useful for identifying contributions from sources (e.g., bacteria) that cannot be achieved using gut content approaches. Stable isotope analysis has become more rigorous through recent advances that provide: (1) signature determination of microscopic organisms such as microalgae, (2) analysis of dissolved organic carbon, and (3) improved quantification of relative source contributions. The limitation that natural tracer techniques require different dietary sources to have unique signatures can potentially be overcome using pulse-chase isotope enrichment experiments. Trophic studies of gelatinous zooplankton would benefit by integrating several approaches. For example, gut content analyses may be used to identify potential dietary sources. Stable isotopes could then be used to determine which sources are assimilated and modeling could be used to quantify the contribution of different sources to the diet. Analysis of fatty acid profiles could be used to identify contributions of bacterioplankton to the diet and, potentially, to provide an alternative means of identifying dietary sources in situations where the isotopic signatures of different potential dietary sources overlap. In this review, we outline the application, advantages, and limitations of gut content analyses and stable isotope and fatty acid tracer techniques and discuss the benefits of using an integrated approach toward studies of the trophic ecology of gelatinous zooplankton.


Gelatinous zooplankton Trophic ecology Diet Gut contents 



We thank D. Hall and two anonymous reviewers who provided valuable feedback on this manuscript and R. Harvey for kindly providing Fig. 5.


  1. Båmstedt, U. & M. B. Martinussen, 2000. Estimating digestion rate and the problem of individual variability, exemplified by a scyphozoan jellyfish. Journal of Experimental Marine Biology and Ecology 251: 1–15.PubMedCrossRefGoogle Scholar
  2. Benstead, J. P., J. B. March, B. Fry, K. C. Ewel & C. M. Pringle, 2006. Testing isosource: stable isotope analysis of a tropical fishery with diverse organic matter sources. Ecology 87: 326–333.PubMedCrossRefGoogle Scholar
  3. Bodin, N., F. Le Loc’h & C. Hily, 2007. Effect of lipid renoval on carbon and nitrogen stable isotope ratios in crustacean tissues. Journal of Experimental Marine Biology and Ecology 341: 168–175.CrossRefGoogle Scholar
  4. Bosley, K. L. & S. C. Wainright, 1999. Effects of preservatives and acidification on the stable isotope ratios (15N:14N, 13C:12C) of two species of marine animals. Canadian Journal of Fisheries and Aquatic Sciences 56: 2181–2185.CrossRefGoogle Scholar
  5. Bouillon, S., M. Korntheuer, W. Baeyens & F. Dehairs, 2006. A new automated setup for stable isotope analysis of dissolved organic carbon. Limnology and Oceanography Methods 4: 216–226.Google Scholar
  6. Brodeur, R. D., H. Sugisaki & G. L. Hunt Jr., 2002. Increases in jellyfish biomass in the Bering Sea: implications for the ecosystem. Marine Ecology Progress Series 233: 89–103.CrossRefGoogle Scholar
  7. Browne, J. G. & M. J. Kingsford, 2005. A commensal relationship between the scyphozoan medusae Catostylus mosaicus and the copepod Paramachronchiron maximum. Marine Biology 146: 1157–1168.CrossRefGoogle Scholar
  8. Budge, S. M. & C. C. Parrish, 1998. Lipid biogeochemistry of plankton, settling matter 1 and sediments 2 in Trinity Bay, Newfoundland. II. Fatty acids. Organic Geochemistry 29: 1547–1559.CrossRefGoogle Scholar
  9. Bunn, S. E., N. R. Loneragan & M. A. Kempster, 1995. Effects of acid washing on stable isotope ratios of C and N in penaeid shrimp and seagrass: implications for food web studies using multiple stable isotopes. Limnology and Oceanography 40: 622–625.Google Scholar
  10. Burkhardt, S., U. Riebesell & I. Zondervan, 1999. Effects of growth rate, CO2 concentration, and cell size on the stable carbon isotope fractionation in marine phytoplankton. Geochimica et Cosmochimica Acta 63: 3729–3741.CrossRefGoogle Scholar
  11. Carli, A., L. Pane & T. Valente, 1991. Lipid and protein content of jellyfish from the Ligurian Sea. First results. In UNEP (United Nations Action Plan), Jellyfish Blooms in the Mediterranean. Proceedings of the II Workshop on Jellyfish in the Mediterranean Sea. Mediterranean Action Plan Technical Reports Series No. 47, UNEP, Athens: 236–240.Google Scholar
  12. Connolly, R. M., M. Guest, A. J. Melville & J. Oakes, 2004. Sulfur stable isotopes separate producers in marine food-web analysis. Oecologia 138: 161–167.PubMedCrossRefGoogle Scholar
  13. Copeman, L. A. & C. C. Parrish, 2003. Marine lipids in a cold coastal ecosystem: Gilbert Bay, Labrador. Marine Biology 143: 1213–1227.CrossRefGoogle Scholar
  14. Costanzo, S. D., J. Udy, B. Longstsaff & A. Jones, 2005. Using nitrogen stable isotope ratios (δ15N) of macroalgae to determine the effectiveness of sewage upgrades: changes in the extent of sewage plumes over four years in Moreton Bay, Australia. Marine Pollution Bulletin 51: 212–217.PubMedCrossRefGoogle Scholar
  15. Dalsgaard, J., M. St. John, G. Kattner, D. Muller-Navarra & W. Hagen, 2003. Fatty acid trophic markers in the pelagic marine environment. Advances in Marine Biology 46: 225–340.PubMedCrossRefGoogle Scholar
  16. De Niro, M. J. & S. Epstein, 1977. Mechanism of isotope carbon fractionation associated with lipid síntesis. Science 197: 261–263.CrossRefGoogle Scholar
  17. De Souza, L. M., M. Iacomini, P. A. J. Gorin, R. S. Sari, M. A. Haddad & G. L. Sassaki, 2007. Glyco- and sphingophosphonolipids from the medusa Phyllorhiza punctata: NMR and ESI-MS/MS fingerprints. Chemistry and Physics of Lipids 145: 85–96.PubMedCrossRefGoogle Scholar
  18. Falkowski, P. G., 1991. Species variability in the fractionation of 13C and 12C by marine phytoplankton. Journal of Plankton Research 13(supplement): 21–28.Google Scholar
  19. Falk-Petersen, S., T. M. Dahl, C. L. Scott, J. R. Sargent, B. Gulliksen, S. Kwasniewski, H. Hop & R.-M. Millar, 2002. Lipid biomarkers and trophic linkages between ctenophores and copepods in Svalbard waters. Marine Ecology Progress Series 227: 187–194.CrossRefGoogle Scholar
  20. Fancett, M. S. & G. P. Jenkins, 1988. Predatory impact of scyphomedusae on ichthyoplankton and other zooplankton in Port Phillip Bay. Journal of Experimental Marine Biology and Ecology 116: 63–77.CrossRefGoogle Scholar
  21. Flynn, B. A. & M. J. Gibbons, 2007. A note on the diet and feeding of Chrysaora hyoscella in Walvis Bay Lagoon, Namibia, in September 2003. African Journal of Marine Science 29: 303–307.CrossRefGoogle Scholar
  22. Frazer, T. K., R. M. Ross, L. B. Quetin & J. P. Montoya, 1997. Turnover of carbon and nitrogen during growth of larval krill, Euphausia superba Dana: a stable isotope approach. Journal of Experimental Marine Biology and Ecology 212: 259–275.CrossRefGoogle Scholar
  23. Fry, B., 2006. Stable Isotope Ecology. Springer Verlag, New York, USA.Google Scholar
  24. Fry, B. & C. Arnold, 1982. Rapid 13C/12C turnover during growth of brown shrimp (Penaeus aztecus). Oecologia 54: 200–204.CrossRefGoogle Scholar
  25. Fukuda, Y. & T. Naganuma, 2001. Potential dietary effects on the fatty acid composition of the common jellyfish Aurelia aurita. Marine Biology 138: 1029–1035.CrossRefGoogle Scholar
  26. Gee, J. M., 1989. An ecological and economic review of meiofauna as food for fish. Journal of the Linnean Society 96: 253–261.CrossRefGoogle Scholar
  27. Gorokhova, E. & S. Hansson, 1999. An experimental study on variations in stable carbon and nitrogen isotope fractionation during growth of Mysis mixta and Neomysis integer. Canadian Journal of Fisheries and Aquatic Sciences 56: 2203–2210.CrossRefGoogle Scholar
  28. Graeve, M., G. Kattner, C. Wiencke & U. Kartsen, 2002. Fatty acid composition of Arctic and Antarctic macroalgae: indicator of phylogenetic and trophic relationship. Marine Ecology Progress Series 231: 67–74.CrossRefGoogle Scholar
  29. Graeve, M., M. Lundberg, M. Böer, G. Kattner, H. Hop & S. Falk-Petersen, 2008. The fate of dietary lipids in the Arctic ctenophore Mertensia ovum (Fabricius 1780). Marine Biology 153: 643–651.CrossRefGoogle Scholar
  30. Gribsholt, B., H. T. S. Boschker, E. Struyf, M. Andersson, A. Tramper, L. De Brabandere, S. van Damme, N. Brion, P. Meire, F. Dehairs, J. J. Middelburg & C. H. R. Heip, 2005. Nitrogen processing in a tidal freshwater marsh: a whole-ecosystem N-15 labelling study. Limnology and Oceanography 50: 1945–1959.Google Scholar
  31. Hall, D., S. Y. Lee & T. Meziane, 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
  32. Hamilton, S. K., S. J. Sippel & S. E. Bunn, 2005. Separation of algae from detritus for stable isotope or ecological stoichiometry studies using density fractionation in colloidal silica. Limnology and Oceanography Methods: 3: 149–157.Google Scholar
  33. Hansson, L. J., O. Moeslund, T. Kiørboe & H. U. Riisgård, 2005. Clearance rates of jellyfish and their potential predation impact on zooplankton and fish larvae in a neritic ecosystem (Limfjorden, Denmark). Marine Ecology Progress Series 304: 117–131.CrossRefGoogle Scholar
  34. Harland, A. D., D. P. Spencer & L. M. Fixter, 1992. Lipid content of some Caribbean corals in relation to depth and light. Marine Biology 113: 357–361.CrossRefGoogle Scholar
  35. Heaton, T. H. E., 1986. Isotopic studies of nitrogen pollution in the hydrosphere and atmosphere: a review. Chemical Geology (Isotope Geoscience Section) 59: 87–102.CrossRefGoogle Scholar
  36. Heeger, T. & H. Möller, 1987. Ultrastructural observations on prey capture and digestion in the scyphomedusa Aurelia aurita. Marine Biology 96: 391–400.CrossRefGoogle Scholar
  37. Hesslein, R. H., K. A. Hallard & P. Ramlal, 1993. Replacement of sulfur, carbon, and nitrogen in tissue of growing broad whitefish (Coregonus nasus) in response to a change in diet traced by δ34C, δ13C, and δ15N. Canadian Journal of Fisheries and Aquatic Sciences 50: 2071–2076.CrossRefGoogle Scholar
  38. Howell, K. L., D. W. Pond, D. S. M. Billett & P. A. Tyler, 2003. Feeding ecology of deep-sea seastars (Echinodermata: Asteroidea): a fatty-acid biomarker approach. Marine Ecology Progress Series 255: 193–206.CrossRefGoogle Scholar
  39. Ito, M. K. & K. L. Simpson, 1996. The biosynthesis of ω3 fatty acids from 18:2ω6 in Artemia spp. Comparative Biochemistry and Physiology 115B: 67–76.Google Scholar
  40. Ju, S.-J., K. Scolardi, K. L. Daly & H. R. Harvey, 2004. Understanding the trophic role of the Antarctic ctenophore, Callianira antarctica, using lipid biomarkers. Polar Biology 27: 782–792.CrossRefGoogle Scholar
  41. Lorrain, A., Y.-M. Paulet, L. Chauvaud, N. Savoye, A. Donval & C. Saot, 2002. Differential δ13C and δ15N signatures among scallop tissues: implications for ecology and physiology. Journal of Experimental Marine Biology and Ecology 275: 47–61.CrossRefGoogle Scholar
  42. Lucas, C. H., 1994. Biochemical composition of Aurelia aurita in relation to age and sexual maturity. Journal of Experimental Marine Biology and Ecology 183: 179–192.CrossRefGoogle Scholar
  43. Lynam, C. P., M. J. Gibbons, E. A. Bjørn, C. A. J. Sparks, B. G. Heywood & A. S. Brierley, 2006. Jellyfish overtake fish in a heavily fished ecosystem. Current Biology 16: R492–R493.PubMedCrossRefGoogle Scholar
  44. MacAvoy, S. E., S. A. Macko & G. C. Garman, 2001. Isotopic turnover in aquatic predators: quantifying the exploitation of migratory prey. Canadian Journal of Fisheries and Aquatic Sciences 58: 923–932.CrossRefGoogle Scholar
  45. Malej, A., J. Faganeli & J. Pezdic, 1993. Stable isotope and biochemical fractionation in the marine pelagic foodchain: the jellyfish Pelagia noctiluca and net zooplankton. Marine Biology 116: 565–570.CrossRefGoogle Scholar
  46. McCutchan, J. H. J. & W. M. J. Lewis, 2002. Relative importance of carbon sources for macroinvertebrates in a rocky mountain stream. Limnology and Oceanography 47: 742–752.Google Scholar
  47. McCutchan, J. H., W. M. Lewis, C. Kendall & C. C. McGrath, 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102: 378–390.CrossRefGoogle Scholar
  48. Melville, A. J. & R. M. Connolly, 2003. Spatial analysis of stable isotope data to determine primary sources of nutrition for fish. Oecologia 136: 499–507.PubMedCrossRefGoogle Scholar
  49. Melville, A. J. & R. M. Connolly, 2005. Food webs supporting fish over subtropical mudflats are based on transported organic matter not in situ microalgae. Marine Biology 148: 363–371.CrossRefGoogle Scholar
  50. Meziane, T., F. d’Agata & S. Y. Lee, 2006. Fate of mangrove organic matter along a subtropical estuary: small-scale exportation and contribution to the food of crab communities. Marine Ecology Progress Series 312: 15–27.CrossRefGoogle Scholar
  51. Meziane, T., S. Y. Lee, P. L. Mfilinge, P. K. S. Shin, M. H. W. Lam & M. Tsuchiya, 2007. Inter-specific and geographical variations in the fatty acid composition of mangrove leaves: implications for using fatty acids as a taxonomic tool and tracers of organic matter. Marine Biology 150: 1103–1113.CrossRefGoogle Scholar
  52. Meziane, T., M. C. Sanabe & M. Tsuchiya, 2002. Role of fiddler crabs of a subtropical intertidal flat on the fate of sedimentary fatty acids. Journal of Experimental Marine Biology and Ecology 270: 191–201.CrossRefGoogle Scholar
  53. Michener, R. H. & D. M. Schell, 1994. Stable isotope ratios as tracers in marine aquatic food webs. In Lajtha, K. & R. H. Michener (eds), Stable Isotopes in Ecology and Environmental Science. Oxford Blackwell Scientific Publications, London: 138–157.Google Scholar
  54. Middelburg, J. J., C. Barranguet, H. T. S. Boschker, P. M. J. Herman, T. Moens & C. H. R. Heip, 2000. The fate of intertidal microphytobenthos carbon: an in situ del13C-labeling study. Limnology and Oceanography 45: 1224–1234.Google Scholar
  55. Minagawa, M. & E. Wada, 1984. Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochimica et Cosmochimica Acta 48: 1135–1140.CrossRefGoogle Scholar
  56. Moens, T., L. Verbeeck, A. de Maeyer, J. Swings & M. Vincx, 1999. Selective attraction of marine bacterivorous nematodes to their bacterial food. Marine Ecology Progress Series 176: 165–178.CrossRefGoogle Scholar
  57. Montoya, J. P., S. G. Horrigan & J. J. McCarthy, 1990. Natural abundance of 15N in particulate nitrogen and zooplankton in the Chesapeake Bay. Marine Ecology Progress Series 65: 35–61.CrossRefGoogle Scholar
  58. Mutchler, T., M. J. Sullivan & B. Fry, 2004. Potential of 14N isotope enrichment to resolve ambiguities in coastal trophic relationships. Marine Ecology Progress Series 266: 27–33.CrossRefGoogle Scholar
  59. Ng, J. S. S., T-C. Wai & G. A. Williams, 2007. The effects of acidification on the stable isotope signatures of marine algae and molluscs. Marine Chemistry 103: 97–102.CrossRefGoogle Scholar
  60. Nichols, P. D., K. T. Danaher & J. A. Koslow, 2003. Occurrence of high levels of tetracosahexaenoic acid in the jellyfish Aurelia sp. Lipids 38: 1207–1210.PubMedCrossRefGoogle Scholar
  61. Oakes, J. M., A. T. Revill, R. M. Connolly & S. I. Blackburn, 2005. Measuring carbon isotope ratios of microphytobenthos using compound-specific stable isotope analysis of phytol. Limnology and Oceanography Methods 3: 511–519.Google Scholar
  62. Palomares, M. L. D. & D. Pauly, 2008. The growth of jellyfishes. Hydrobiologia (this volume). doi:10.1007/s10750-008-9582-y.
  63. Papina, M., T. Meziane & R. Van Woesik, 2003. Symbiotic zooxanthellae provide the host-coral Montipora digitata with polyunsaturated fatty acids. Comparative Biochemistry and Physiology Part B 135: 533–537.CrossRefGoogle Scholar
  64. Pel, R., H. Hoogveld & V. Floris, 2003. Using the hidden isotopic heterogeneity in phyto- and zooplankton to unmask disparity in trophic carbon transfer. Limnology and Oceanography 48: 2200–2207.Google Scholar
  65. Phillips, D. L. & J. W. Gregg, 2001. Uncertainty in source partitioning using stable isotopes. Oecologia 127: 171–179.CrossRefGoogle Scholar
  66. Phillips, D. L. & J. W. Gregg, 2003. Source partitioning using stable isotopes: coping with too many sources. Oecologia 136: 261–269.PubMedCrossRefGoogle Scholar
  67. Phillips, D. L., S. D. Newsome & J. W. Gregg, 2005. Combining sources in stable isotope mixing models: alternative methods. Oecologia 144: 520–527.PubMedCrossRefGoogle Scholar
  68. Phleger, C. F., P. D. Nichols & P. Virtue, 1998. Lipids and trophodynamics of Antarctic zooplankton. Comparative Biochemistry and Physiology Part B 120: 311–323.CrossRefGoogle Scholar
  69. Pitt, K. A., A. L. Clement, R. M. Connolly & D. Thibault-Botha, 2008. Predation by jellyfish on large and emergent zooplankton: implications for benthic-pelagic coupling. Estuarine, Coastal and Shelf Science 76: 827–833.CrossRefGoogle Scholar
  70. Purcell, J. E., 1992. Effects of predation by the scyphomedusan Chrysaora quinquecirrha on zooplankton populations in Chesapeake Bay, USA. Marine Ecology Progress Series 87: 65–76.CrossRefGoogle Scholar
  71. Purcell, J. E., 1997. Pelagic cnidarians and ctenophores as predators: selective predation, feeding rates and effects on prey populations. Annales de l’Institut océanographique, Paris 73: 125–137.Google Scholar
  72. Purcell, J. E., 2003. Predation on zooplankton by large jellyfish, Aurelia labiata, Cyanea capillata, and Aequorea aequorea, in Prince William Sound, Alaska. Marine Ecology Progress Series 246: 137–152.CrossRefGoogle Scholar
  73. Purcell, J. E., F. P. Cresswell, D. G. Cargo & V. S. Kennedy, 1991. Differential ingestion and digestion of bivalve larvae by the scyphozoan Chrysaora quinquecirrha and the Ctenophore Mnemiopsis leidyi. Biological Bulletin 180: 103–111.CrossRefGoogle Scholar
  74. Quoy, J. R. C. & J. P. Gaimard, 1824. Voyage de l’Uranie. Traité Zool 4: 712.Google Scholar
  75. Rolff, C., 2000. Seasonal variation in δ13C and δ15N of size-fractionated plankton at a coastal station in the northern Baltic proper. Marine Ecology Progress Series 203: 47–65.CrossRefGoogle Scholar
  76. Sakano, H., E. Fujiwara, S. Nohara & H. Ueda, 2005. Estimation of nitrogen stable isotope turnover rate of Oncorhynchus nerka. Environmental Biology of Fishes 72: 13–18.CrossRefGoogle Scholar
  77. Sargent, J. R., R. J. Parkes, I. Muellere-Harvey & R. J. Henderson, 1987. Lipid biomarkers in marine ecology. In Sleigh, M. A. (ed.), Microbes in the Sea. Ellis Horwood Ltd, Chichester: 119–138.Google Scholar
  78. Schmidt, K., A. Atkinson, D. Stubing, J. W. McClelland, J. P. Montoya & M. Voss, 2003. Trophic relationships among Southern Ocean copepods and krill: some uses and limitations of a stable isotope approach. Limnology and Oceanography 48: 277–289.Google Scholar
  79. Stoecker, D. K., A. E. Michaels & L. H. Davis, 1987. Grazing by the jellyfish, Aurelia aurita, on microzooplankton. Journal of Plankton Research 9: 901–915.CrossRefGoogle Scholar
  80. Tarboush, R. A., S. E. MacAvoy, S. A. Macko & V. Connaughton, 2006. Contribution of catabolic tissue replacement to the turnover of stable isotopes in Danio rerio. Canadian Journal of Zoology 84: 1453–1460.CrossRefGoogle Scholar
  81. Tieszen, L. L., T. W. Boutton, K. G. Tesdahl & N. A. Slade, 1983. Fractionation and turnover of stable carbon isotopes in animal tissues: Implications for δ13C analysis of diet. Oecologia 57: 32–37.CrossRefGoogle Scholar
  82. Toonen, R. J. & R. Chia, 1993. Limitations of laboratory assessments of coelenterate predation: container effects on the prey selection of the limnomedusa, Proboscidactyla flavicirrata (Brandt). Journal of Experimental Marine Biology and Ecology 167: 215–235.CrossRefGoogle Scholar
  83. Towanda, T. & E. V. Thuesen, 2006. Ectosymbiotic behaviour of Cancer gracilis and its trophic relationships with its host Phacellophora camtschatica and the parasitoid Hyperia medusarum. Marine Ecology Progress Series 315: 221–236.CrossRefGoogle Scholar
  84. Van der Zanden, M. J. & J. B. Rasmussen, 2001. Variation in del15N and del13C trophic fractionation: implications for aquatic food web studies. Limnology and Oceanography 46: 2061–2066.CrossRefGoogle Scholar
  85. West, J. B., G. J. Bowen, T. E. Cerling & J. R. Ehleringer, 2006. Stable isotopes as one of nature’s ecological recorders. Trends in Ecology and Evolution 21: 408–414.PubMedCrossRefGoogle Scholar
  86. Winning, M. A., R. M. Connolly, N. R. Loneragan & S. E. Bunn, 1999. 15N enrichment as a method of separating the isotopic signatures of seagrass and its epiphytes for food web analysis. Marine Ecology Progress Series 189: 289–294.CrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  1. 1.Australian Rivers Institute – Coast and Estuaries, and Griffith School of EnvironmentGriffith UniversityGold CoastAustralia
  2. 2.Département Milieux et Peuplements AquatiquesUMR-CNRS 5178, Biologie des Organismes Marins et Ecosystèmes, MNHNParis cedex 05France

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