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Preservation methods alter stable isotope values in gelatinous zooplankton: implications for interpreting trophic ecology

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Abstract

Jellyfish are increasingly topical within studies of marine food webs. Stable isotope analysis represents a valuable technique to unravel the complex trophic role of these long-overlooked species. In other taxa, sample preservation has been shown to alter the isotopic values of species under consideration, potentially leading to misinterpretation of trophic ecology. To identify potential preservation effects in jellyfish, we collected Aurelia aurita from Strangford Lough (54o22′44.73″N, 5o32′53.44″W) during May 2009 and processed them using three different methods prior to isotopic analysis (unpreserved, frozen and preserved in ethanol). A distinct preservation effect was found on δ15N values: furthermore, preservation also influenced the positive allometric relationship between individual size and δ15N values. Conversely, δ13C values remained consistent between the three preservation methods, conflicting with previous findings for other invertebrate, fish and mammalian species. These findings have implications for incorporation of jellyfish into marine food webs and remote sampling regimes where preservation of samples is unavoidable.

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References

  • Arai MN (2005) Predation on pelagic coelenterates: a review. J Mar Biol Assoc UK 85:523–536

    Article  Google Scholar 

  • Båmstedt U, Martinussen MB (2000) Estimating digestion rate and the problem of individual variability, exemplified by a scyphozoan jellyfish. J Exp Mar Biol Ecol 251:1–15

    Article  Google Scholar 

  • Barrow LM, Bjorndal KA, Reich KJ (2008) Effects of preservation method on stable carbon and nitrogen isotope values. Physiol Biochem Zoo 81:688–693

    Article  Google Scholar 

  • Bosley KL, Wainwright SC (1999) Effects of preservation and acidification on the stable isotope ratios (15N:14N, 13C:12C) of two marine species of marine animals. Can J Fish Aquat Sci 56:2181–2185

    Article  Google Scholar 

  • Carabel S, Godínez-Domínguez E, Verísimo P, Fernández L, Freire J (2006) An assessment of sample processing methods for stable isotope analyses of marine food webs. J Exp Mar Biol Ecol 336:254–261

    Article  CAS  Google Scholar 

  • Carabel S, Verísimo P, Freire J (2009) Effects of preservatives on stable isotope analyses of four marine species. Estuar Coast Shelf S 82:348–350

    Article  CAS  Google Scholar 

  • Davenport SR, Bax NJ (2002) A trophic study of a marine ecosystem off southeastern Australia using stable isotopes of carbon and nitrogen. Can J Fish Aquat Sci 59:514–530

    Article  Google Scholar 

  • DeNiro M, Epstein S (1977) Mechanism of carbon isotope fractionation associated with lipid synthesis. Science 197:261–263

    Article  CAS  Google Scholar 

  • DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506

    Article  CAS  Google Scholar 

  • DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351

    Article  CAS  Google Scholar 

  • Doyle TK, Houghton JDR, Buckley SM, Hays GC, Davenport J (2007a) The broad-scale distribution of five jellyfish species across a temperate coastal environment. Hydrobiologia 579:29–39

    Article  Google Scholar 

  • Doyle TK, Houghton JDR, McDevitt R, Davenport J, Hays GC (2007b) The energy density of jellyfish: estimates from bomb-calorimetry and proximate-composition. J Exp Mar Biol Ecol 343:239–252

    Article  Google Scholar 

  • Doyle TK, De Haas H, Cotton D, Dorshell B, Cummins V, Houghton JDR, Davenport J, Hays GC (2008) Widespread occurrence of the jellyfish Pelagia noctiluca in Irish coastal and shelf waters. J Plankton Res 30:963–968

    Article  Google Scholar 

  • Feuchtmayr H, Grey J (2003) Effect of preparation and preservation procedures on carbon and nitrogen stable isotope determinations from zooplankton. Rapid Commun Mass Spectrom 17:2605–2610

    Article  CAS  Google Scholar 

  • Gannes LZ, O’Brien DM, Martínez Del Rio C (1997) Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments. Ecology 78:1271–1276

    Article  Google Scholar 

  • Goldstein DB, Chin JH (1981) Interaction of ethanol with biological membranes. Fed Proc 40(7):2073–2076

    CAS  PubMed  Google Scholar 

  • Hansson LJ, Norrman B (1995) Release of dissolved organic carbon (DOC) by the scyphozoan jellyfish Aurelia aurita and its potential influence on the production of planktonic bacteria. Mar Biol 121:527–532

    Article  CAS  Google Scholar 

  • Harrod C, Grey J, McCarthy TK, Morrissey M (2005) Stable isotope analyses provide new insights into ecological plasticity in a mixohaline population of European eel. Oecologia 144:673–683

    Article  Google Scholar 

  • Hobson KA, Welch HE (1992) Determination of trophic relationships within a high Arctic marine food web using δ13C and δ15N analysis. Mar Ecol Prog Ser 84:9–18

    Article  CAS  Google Scholar 

  • Hobson KA, Lisle Gibbs H, Gloutney ML (1997) Preservation of blood and tissue samples for stable-carbon and stable-nitrogen isotope analysis. Can J Zool 75:1720–1723

    Article  CAS  Google Scholar 

  • Houghton JDR, Doyle TK, Wilson MW, Davenport J, Hays GC (2006) Jellyfish aggregations and leatherback turtle foraging patterns in a temperate coastal environment. Ecology 87(8):1967–1972

    Article  Google Scholar 

  • Houghton JDR, Doyle TK, Davenport J, Lilley MKS, Wilson RP, Hays GC (2007) Stranding events provide indirect insights into the seasonality and persistence of jellyfish medusa (Cnidaria: Scyphozoa). Hydrobiologia 587:1–13

    Article  Google Scholar 

  • Ishii H, Tanaka F (2001) Food and feeding of Aurelia aurita in Tokyo Bay with an analysis of stomach contents and a measurement of digestion times. Hydrobiologia 451:311–320

    Article  Google Scholar 

  • Jiang ST, Hwang BS, Tsao C (1987) Protein denaturation and changes in nucleotides of fish muscle during frozen storage. J Agr Food Chem 35:22–27

    Article  CAS  Google Scholar 

  • Kaehler S, Pakhomov EA (2001) Effects of storage and preservation on the δ13C and δ15N signatures of selected marine organisms. Mar Ecol Prog Ser 219:299–304

    Article  CAS  Google Scholar 

  • Kaehler S, Pakhomov EA, McQuaid CD (2000) Trophic structure of the marine food web at the Prince Edward Islands (Southern Ocean) determined by δ13C and δ15N analysis. Mar Ecol Prog Ser 208:13–20

    Article  Google Scholar 

  • Kiljunen M, Grey J, Sinisalo T, Harrod C, Immonen H, Jones RI (2006) A revised model for lipid-normalising d13C values from aquatic organisms, with implications for isotope mixing models. J App Ecol 43:1213–1222

    Article  CAS  Google Scholar 

  • Kirby RR, Beaugrand G, Lindley JA (2009) Synergistic effects of climate and fishing in a marine ecosystem. Ecosystems 12:548–561

    Article  Google Scholar 

  • Knoff A, Hohn A, Macko S (2008) Ontogenetic diet changes in bottlenose dolphins (Tursiops truncatus) reflected through stable isotopes. Mar Mammal Sci 24(1):128–137

    Article  Google Scholar 

  • Lovelock JE (1957) The denaturation of Lipid-protein complexes as a cause of damage by freezing. Proc R Soc B Biol Sci 147:427–433

    Article  CAS  Google Scholar 

  • Lucas CH (2001) Reproduction and life history strategies of the common jellyfish, Aurelia aurita, in relation to its ambient environment. Hydrobiologia 451:229–246

    Article  Google Scholar 

  • Lynam CP, Hay SJ, Brierley AS (2004) Interannual variability in abundance of North Sea jellyfish and links to the North Atlantic oscillation. Limnol Oceanogr 49(3):637–643

    Article  Google Scholar 

  • Lynam CP, Heath MR, Hay SJ, Brierley AS (2005) Evidence for impacts by jellyfish on North Sea herring recruitment. Mar Ecol Prog Ser 298:157–167

    Article  Google Scholar 

  • Mackie IM (1993) The effects of freezing on flesh proteins. Food Rev Int 9(4):575–610

    Article  CAS  Google Scholar 

  • Makri M (2010) The biochemical, textural and sensory properties of king scallop (Pecten maxinus) meats frozen at different characteristic freezing times. Afr J Biotechnol 9(28):4374–4385

    CAS  Google Scholar 

  • Malej A, Faganeli J, Pezdic J (1993) Stable isotope and biochemical fractionation in the marine pelagic food chain: the jellyfish Pelagia noctiluca and net zooplankton. Mar Biol 116:565–570

    Article  CAS  Google Scholar 

  • Malej A, Turk V, Lučić D, Benović A (2007) Direct and indirect trophic interactions of Aurelia sp. (Scyphozoa) in a stratified marine environment (Mljet Lakes, Adriatic Sea). Mar Biol 151:827–841

    Article  Google Scholar 

  • Mateo MA, Serrano O, Serrano L, Michener RH (2008) Effects of sample preparation on stable isotope ratios of carbon and nitrogen in marine invertebrates: implications for food web studies using stable isotopes. Oecologia 157:105–115

    Article  Google Scholar 

  • Michener RH, Kaufman L (2007) Stable isotope ratios as tracers in marine food webs: an update. In: Michener RH, Lajtha K (eds) Stable isotopes in ecology and environmental science, 2nd edn. Wiley-Blackwell, London, pp 238–282

    Chapter  Google Scholar 

  • Mills CE (2001) Jellyfish blooms: are populations increasing globally in response to changing ocean conditions? Hydrobiologia 451:55–68

    Article  Google Scholar 

  • Olson MH (1996) Ontogenetic niche shifts in largemouth bass: variability and consequences for first-year growth. Ecology 77(1):179–190

    Article  Google Scholar 

  • Paredi ME, Roldan HA, Crupkin M (2006) Changes in myofibrillar proteins and lipids of squid (Illex argentinus) during frozen storage. J Food Biochem 30:604–621

    Article  CAS  Google Scholar 

  • Paredi ME, Pagano MR, Crupkin M (2010) Biochemical and physicochemical properties of actomysin and myofibrils from frozen stored flounder (Paralichthys patagonicus) fillets. J Food Biochem 34(5):983–997

    Article  CAS  Google Scholar 

  • Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320

    Article  Google Scholar 

  • Pitt KA, Connolly CM, Meziane T (2009) Stable isotope and fatty acid tracers in energy and nutrient studies of jellyfish: a review. Hydrobiologia 616(1):119–132

    Article  CAS  Google Scholar 

  • Post DM (2002) Using stable isotopes to estimate trophic position: models, methods and assumptions. Ecology 83(3):703–718

    Article  Google Scholar 

  • Purcell JE, Arai MN (2001) Interactions of pelagic cnidarians and ctenophores with fish: a review. Hydrobiologia 451:27–44

    Article  Google Scholar 

  • Purcell JE, Fuentes V, Atienza D, Tilves U, Astorga D, Kawahara M, Hays GC (2010) Use of respiration rates of scyphozoan jellyfish to estimate their effects on the food web. Hydrobiologia 645(1):135–152

    Article  CAS  Google Scholar 

  • Reyes G, Finol H, Bello R (2009) Effect of freezing and cooking on the ultrastructure of arms of octopus (Octopus vulgaris). Acta Microscopia 18(2):76–80

    CAS  Google Scholar 

  • Russell FS (1970) The medusae of the British Isles II. Cambridge University Press, Cambridge

    Google Scholar 

  • Sarakinos HC, Johnson ML, Vander Zanden MJ (2002) A synthesis of tissue-preservation effects on carbon and nitrogen stable isotope signatures. Can J Zool 80(2):381–387

    Article  Google Scholar 

  • Syväranta J, Vesala S, Rask M, Ruuhijärvi J, Jones R (2008) Evaluating the utility of stable isotope analyses of archived freshwater sample materials. Hydrobiologia 600:121–130

    Article  Google Scholar 

  • Syväranta J, Martino A, Kopp D, Céréghino R, Santoul F (2011) Freezing and chemical preservatives alter the stable isotope values of carbon and nitrogen of the Asiatic clam (Corbicula fluminea). Hydrobiologia 658:383–388

    Article  Google Scholar 

  • Vander Zanden MJ, Rasmussen JB (2001) Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnol Oceanogr 46:2061–2066

    Article  CAS  Google Scholar 

  • Wada E, Terazaki M, Kabaya Y, Nemoto T (1987) 15N and 13C abundances in the Antarctic Ocean with emphasis on the biogeochemical structure of the food web. Deep Sea Res 34:829–841

    Article  CAS  Google Scholar 

  • Wallace BP, Avens L, Braun-McNeill J, McClellan CM (2009) The diet composition of immature loggerheads: insights on trophic niche, growth rates, and fisheries interactions. J Exp Mar Biol Ecol 373(1):50–57

    Article  Google Scholar 

  • Wroblowski B, Diaz JF, Heremans K, Engelborghs Y (1996) Molecular mechanisms of pressure induced conformational changes in BPTI. Proteins 25:446–455

    Article  CAS  Google Scholar 

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Acknowledgments

This study was supported by a Department of Education and Learning (DEL) PhD studentship awarded to NECF by the Northern Ireland Assembly. We are grateful to Phillip Johnston from Queen’s University, Belfast Marine Laboratory (QUML) for boat support and sample collection, and Michelle Thompson from the 14CHRONO centre, School of Geography, Archaeology and Palaeoecology, Queen’s University, Belfast for SIA processing. Thanks also go to Donal Griffin and Tony Lilley for help with sample processing.

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Authors and Affiliations

  1. School of Biological Sciences, Medical Biology Centre, Queen’s University, Belfast, 97 Lisburn Road, Belfast, BT9 7BL, UK

    Nicholas E. C. Fleming, Jonathan D. R. Houghton, Caroline L. Magill & Chris Harrod

  2. Queen’s University Marine Laboratory, 12–13 The Strand, Portaferry, Co. Down, BT22 1PF, UK

    Nicholas E. C. Fleming & Jonathan D. R. Houghton

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  1. Nicholas E. C. Fleming
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  2. Jonathan D. R. Houghton
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  3. Caroline L. Magill
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Correspondence to Nicholas E. C. Fleming.

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Communicated by U. Sommer.

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Fleming, N.E.C., Houghton, J.D.R., Magill, C.L. et al. Preservation methods alter stable isotope values in gelatinous zooplankton: implications for interpreting trophic ecology. Mar Biol 158, 2141–2146 (2011). https://doi.org/10.1007/s00227-011-1714-7

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  • DOI: https://doi.org/10.1007/s00227-011-1714-7

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