Abstract
Gelatinous zooplankton are important predators, prey, and nutrient conduits within marine ecosystems. Information obtained from jellyfish stable isotope compositions can be invaluable to biological and environmental research and management. Protocols for best practice in preparing jellyfish for stable isotope analysis, however, require standardisation to provide consistently comparable data, with ecologically significant changes in values due to freezing reported in the literature. Jellyfish are easily sampled during standard marine fieldwork, and usually frozen before analysis. Here, mesoglea from freshly caught moon jelly, Aurelia aurita, were treated by thorough washing and/or freezing, and compared with untreated sections from the same individuals. Jellyfish were captured in July 2013 from Buckler’s Hard Marina in southern UK (latitude: 50.801, longitude: − 1.423). Isotope and element ratio changes of carbon and nitrogen composition due to the treatment of the mesoglea were quantified. Both washing and freezing elevated δ15N values, with washing also decreasing the variance observed in these values. Untreated mesoglea showed the lowest δ13C values. Carbon-to-nitrogen elemental ratio increased with both washing and freezing. These results imply the presence of a water-soluble, isotopically depleted nitrogenous component in fresh jellyfish mesoglea. The concentration of this component varies among individuals, and thorough washing or freezing are recommended to ensure consistent stable isotope analyses of jellyfish mesoglea. This study describes a methodology aimed at improving the consistency and repeatability of stable isotope analyses of jellyfish.
Similar content being viewed by others
References
Arai MN (2005) Predation on pelagic coelenterates: a review. J Mar Biol Assoc UK 85:523–536. doi:10.1017/S0025315405011458
Barrow LM, Bjorndal KA, Reich KJ (2008) Effects of preservation method on stable carbon and nitrogen isotope values. Physiol Biochem Zool 81:688–693. doi:10.1086/588172
Bischof JC, Wolkers WF, Tsvetkova NM et al (2002) Lipid and protein changes due to freezing in Dunning AT-1 cells. Cryobiology 45:22–32
Brodeur R (1998) In situ observations of the association between juvenile fishes and scyphomedusae in the Bering Sea. Mar Ecol Prog Ser 163:11–20. doi:10.3354/meps163011
Burgess KB, Bennett MB (2017) Effects of ethanol storage and lipid and urea extraction on δ15N and δ13C isotope ratios in a benthic elasmobranch, the bluespotted maskray Neotrygon kuhlii. J Fish Biol 90:417–423. doi:10.1111/jfb.13164
Cardona L, Álvarez de Quevedo I, Borrell A et al (2012) Massive consumption of gelatinous plankton by mediterranean apex predators. PLoS ONE 7:e31329. doi:10.1371/journal.pone.0031329
Casciotti KL (2009) Inverse kinetic isotope fractionation during bacterial nitrite oxidation. Geochim Cosmochim Acta 73:2061–2076. doi:10.1016/j.gca.2008.12.022
Casciotti KL, Sigman DM, Ward BB (2003) Linking diversity and stable isotope fractionation in ammonia-oxidizing bacteria. Geomicrobiol J 20:335–353. doi:10.1080/01490450303895
Condon RH, Steinberg DK, del Giorgio PA et al (2011) Jellyfish blooms result in a major microbial respiratory sink of carbon in marine systems. Proc Natl Acad Sci USA 108:10225–10230. doi:10.1073/pnas.1015782108
Condon RH, Duarte CM, Pitt KA et al (2013) Recurrent jellyfish blooms are a consequence of global oscillations. Proc Natl Acad Sci USA 110:1000–1005. doi:10.1073/pnas.1210920110
Costello J (1991) Complete carbon and nitrogen budgets for the hydromedusa Cladonema californicum (Anthomedusa: cladonemidae)*. Mar Biol 108:119–128
D’Ambra I, Carmichael RH, Graham WM (2014) Determination of δ13C and δ15N and trophic fractionation in jellyfish: implications for food web ecology. Mar Biol 161:473–480. doi:10.1007/s00227-013-2345-y
de Lafontaine Y, Leggett WC (1988) Predation by jellyfish on larval fish: an experimental evaluation employing in situ enclosures. Can J Fish Aquat Sci 45:1173–1190. doi:10.1139/f88-140
R Development Core Team R (2011) R: a language and environment for statistical computing. R Found Stat Comput 1:409
Dodge KL, Logan JM, Lutcavage ME (2011) Foraging ecology of leatherback sea turtles in the Western North Atlantic determined through multi-tissue stable isotope analyses. Mar Biol 158:2813–2824. doi:10.1007/s00227-011-1780-x
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. doi:10.1002/rcm.1227
Fisk AT, Tittlemier SA, Pranschke JL, Norstrom RJ (2002) Using anthropogenic contaminants and stable isotopes to assess the feeding ecology of Greenland sharks. Ecology 83:2162–2172. doi:10.1890/0012-9658(2002)083[2162:UACASI]2.0.CO;2
Fleming NEC, Houghton JDR, Magill CL, Harrod C (2011) Preservation methods alter stable isotope values in gelatinous zooplankton: implications for interpreting trophic ecology. Mar Biol 158:2141–2146. doi:10.1007/s00227-011-1714-7
Fleming NEC, Harrod C, Newton J, Houghton JDR (2015) Not all jellyfish are equal: isotopic evidence for inter- and intraspecific variation in jellyfish trophic ecology. PeerJ 3:e1110. doi:10.7717/peerj.1110
Gambini C, Abou B, Ponton A, Cornelissen AJM (2012) Micro- and macrorheology of jellyfish extracellular matrix. Biophys J 102:1–9. doi:10.1016/j.bpj.2011.11.4004
Gomez-Guillen MC, Martinez-Alvarez O, Montero P (2003) Functional and thermal gelation properties of squid mantle proteins affected by chilled and frozen storage. J Food Sci 68:1962–1967. doi:10.1111/j.1365-2621.2003.tb07002.x
Hoehn DP (2017) Population variability in Aurelia aurita. University of Southampton Doctoral Thesis, pp 182
Hussey NE, MacNeil MA, Fisk AT (2010) The requirement for accurate diet-tissue discrimination factors for interpreting stable isotopes in sharks. Hydrobiologia 654:1–5. doi:10.1007/s10750-010-0361-1
Jarman SN, McInnes JC, Faux C et al (2013) Adélie penguin population diet monitoring by analysis of food DNA in scats. PLoS ONE 8:e82227. doi:10.1371/journal.pone.0082227
Jesus FM, Pereira MR, Rosa CS et al (2015) Preservation methods alter carbon and nitrogen stable isotope values in crickets (Orthoptera: grylloidea). PLoS ONE 10:e0137650. doi:10.1371/journal.pone.0137650
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
Kogovšek T, Tinta T, Klun K, Malej A (2014) Jellyfish biochemical composition: importance of standardised sample processing. Mar Ecol Prog Ser 510:275–288. doi:10.3354/meps10959
Lebrato M, Pitt KA, Sweetman AK et al (2012) Jelly-falls historic and recent observations: a review to drive future research directions. Hydrobiologia 690:227–245. doi:10.1007/s10750-012-1046-8
Li Y, Zhang Y, Hussey NE, Dai X (2016) Urea and lipid extraction treatment effects on δ15N and δ13C values in pelagic sharks. Rapid Commun Mass Spectrom 30:1–8. doi:10.1002/rcm.7396
Logan JM, Jardine TD, Miller TJ et al (2008) Lipid corrections in carbon and nitrogen stable isotope analyses: comparison of chemical extraction and modelling methods. J Anim Ecol 77:838–846
MacKenzie KM, Longmore C, Preece C et al (2014) Testing the long-term stability of marine isoscapes in shelf seas using jellyfish tissues. Biogeochemistry 121:441–454. doi:10.1007/s10533-014-0011-1
Mackie IM (1993) The effects of freezing on flesh proteins. Food Rev Int 9:575–610. doi:10.1080/87559129309540979
Makri M (2010) The biochemical, textural and sensory properties of king scallop (Pecten maximus) meats frozen at different characteristic freezing times. African J Biotechnol 9:4374–4385
Malej A, Faganeli J, Pezdič J (1993) Stable isotope and biochemical fractionation in the marine pelagic food chain: the jellyfish Pelagia noctiluca and net zooplankton. Mar Biol Int J Life Ocean Coast Waters 116:565–570. doi:10.1007/BF00355475
Martínez Del Rio C, Wolf N, Carleton SA, Gannes LZ (2009) Isotopic ecology ten years after a call for more laboratory experiments. Biol Rev 84:91–111. doi:10.1111/j.1469-185X.2008.00064.x
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. doi:10.1007/s00442-008-1052-8
Matsakis S (1992) Ammonia excretion rate of Clytia spp. hydro-medusae (Cnidaria, Thecata): effects of individual dry weight, temperature and food availability. Mar Ecol Prog Ser 87:55–63
Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta 48:1135–1140. doi:10.1016/0016-7037(84)90204-7
Nagata R, Moreira M, Pimentel C, Morandini A (2015) Food web characterization based on δ15N and δ13C reveals isotopic niche partitioning between fish and jellyfish in a relatively pristine ecosystem. Mar Ecol Prog Ser 519:13–27. doi:10.3354/meps11071
O’Rorke R, Lavery SD, Wang M et al (2015) Phyllosomata associated with large gelatinous zooplankton: hitching rides and stealing bites. ICES J Mar Sci 72:i124–i127. doi:10.1093/icesjms/fsu163
Ozcelikkale A, Han B (2016) Thermal destabilization of collagen matrix hierarchical structure by freeze/thaw. PLoS ONE 11:e0146660. doi:10.1371/journal.pone.0146660
Paredi ME, Roldan HA, Crupkin M (2006) Changes in myofibrillar proteins and lipids of squis (Illex argentinus) during frozen storage. J Food Biochem 30:604–621. doi:10.1111/j.1745-4514.2006.00088.x
Paredi ME, Pagano MR, Crupkin M (2010) Biochemical and physicochemical properties of actomyosin and myofibrils from frozen stored flounder (Paralichthys patagonicus) fillets. J Food Biochem 34:983–997. doi:10.1111/j.1745-4514.2010.00344.x
Pikitch EK, Santora C, Babcock EA et al (2004) Ecosystem-based fishery management. Science 305:346–347. doi:10.1126/science.1098222
Pitt KA, Clement A-L, Connolly RM, Thibault-Botha D (2008) Predation by jellyfish on large and emergent zooplankton: implications for benthic–pelagic coupling. Estuar Coast Shelf Sci 76:827–833. doi:10.1016/j.ecss.2007.08.011
Pitt KA, Connolly RM, Meziane T (2009a) Stable isotope and fatty acid tracers in energy and nutrient studies of jellyfish: a review. Hydrobiologia 616:119–132. doi:10.1007/s10750-008-9581-z
Pitt KA, Welsh DT, Condon RH (2009b) Influence of jellyfish blooms on carbon, nitrogen and phosphorus cycling and plankton production. Hydrobiologia 616:133–149. doi:10.1007/s10750-008-9584-9
Pitt KA, Duarte CM, Lucas CH et al (2013) Jellyfish body plans provide allometric advantages beyond low carbon content. PLoS ONE 8:1–10. doi:10.1371/journal.pone.0072683
Post DM, Layman CA, Arrington DA et al (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189. doi:10.1007/s00442-006-0630-x
Purcell JE (2003) Predation on zooplankton by large jellyfish, Aurelia labiata, Cyanea capillata and Aequorea aequorea, in Prince William Sound, Alaska. Mar Ecol Prog Ser 246:137–152. doi:10.3354/meps246137
Purcell JE, Arai MN (2001) Interactions of pelagic cnidarians and ctenophores with fish: a review. Hydrobiologia 451:27–44. doi:10.1023/A:1011883905394
Purcell JE, Breitburg DL, Decker MB et al (2001) Pelagic cnidarians and ctenophores in low dissolved oxygen environments: A review. In: Rabalais NN, Turner RE (eds) Coastal Hypoxia: Consequences for Living Resources and Ecosystems. American Geophysical Union, Washington D.C, pp 77–100. doi:10.1029/CE058p0077
Purcell J, Uye S, Lo W (2007) Anthropogenic causes of jellyfish blooms and their direct consequences for humans: a review. Mar Ecol Prog Ser 350:153–174. doi:10.3354/meps07093
Schmid V, Bally A, Beck K et al (1991) The extracellular matrix (mesoglea) of hydrozoan jellyfish and its ability to support cell adhesion and spreading. Hydrobiologia 216–217:3–10. doi:10.1007/BF00026436
Shaposhnikova T, Matveev I, Napara T, Podgornaya O (2005) Mesogleal cells of the jellyfish Aurelia aurita are involved in the formation of mesogleal fibres. Cell Biol Int 29:952–958. doi:10.1016/j.cellbi.2005.08.008
Søreide J, Tamelander T, Hop H et al (2006) Sample preparation effects on stable C and N isotope values: a comparison of methods in Arctic marine food web studies. Mar Ecol Prog Ser 328:17–28. doi:10.3354/meps328017
Sotiropoulos MA, Tonn WM, Wassenaar LI (2004) Effects of lipid extraction on stable carbon and nitrogen isotope analyses of fish tissues: potential consequences for food web studies. Ecol Freshw Fish 13:155–160. doi:10.1111/j.1600-0633.2004.00056.x
Sweeting CJ, Polunin NVC, Jennings S (2006) Effects of chemical lipid extraction and arithmetic lipid correction on stable isotope ratios of fish tissues. Rapid Commun Mass Spectrom 20:595–601. doi:10.1002/rcm.2347
Sweetman AK, Smith CR, Dale T, Jones DOB (2014) Rapid scavenging of jellyfish carcasses reveals the importance of gelatinous material to deep-sea food webs. Proc Biol Sci 281:20142210. doi:10.1098/rspb.2014.2210
Syväranta J, Vesala S, Rask M et al (2007) Evaluating the utility of stable isotope analyses of archived freshwater sample materials. Hydrobiologia 600:121–130. doi:10.1007/s10750-007-9181-3
Syväranta J, Martino A, Kopp D et al (2011) Freezing and chemical preservatives alter the stable isotope values of carbon and nitrogen of the Asiatic clam (Corbicula fluminea). Hydrobiologia 658:383–388. doi:10.1007/s10750-010-0512-4
Towanda T, Thuesen EV (2006) Ectosymbiotic behavior of Cancer gracilis and its trophic relationships with its host Phacellophora camtschatica and the parasitoid Hyperia medusarum. Mar Ecol Prog Ser 315:221–236. doi:10.3354/meps315221
Ueng Y-E, Chow C-J (1998) Textural and histological changes of different squid mantle muscle during frozen storage. J Agric Food Chem 46:4728–4733. doi:10.1021/jf9803278
Acknowledgements
The authors would like to thank Ocean and Earth Science at the University of Southampton for funding this study. Many thanks also to David Locke and Joseph Jones for help with jellyfish collection.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Funding was provided to KMM by Ocean and Earth Science at the University of Southampton, and the authors have no conflict of interest. The experiments comply with the current laws of the country (UK) in which they were performed. The species collected is a very common jellyfish and is not protected throughout its range.
Additional information
Responsible Editor: S. Shumway.
Reviewed by P. Kremer and an undisclosed expert.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
MacKenzie, K.M., Trueman, C.N., Lucas, C.H. et al. The preparation of jellyfish for stable isotope analysis. Mar Biol 164, 219 (2017). https://doi.org/10.1007/s00227-017-3242-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-017-3242-6