Skip to main content
Log in

Fractionation of the stable carbon isotope ratio of essential fatty acids in zebrafish Danio rerio and mud snails Bellamya chinensis

  • Ecosystem ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Fractionation of stable carbon (C) isotopes in the essential fatty acids 18:2n-6, 18:3n-3, 20:4n-6, 20:5n-3, and 22:6n-3 was investigated in the zebrafish Danio rerio and the mud snail Bellamya chinensis fed the same two diets. These diets differed in essential fatty acid compositions: (1) TetraMin contained all five fatty acids, and (2) Chlorella contained only two, 18:2n-6 and 18:3n-3. On average, the isotopic fractionation was −0.5 ± 0.9 ‰ for 18:2n-6 and 18:3n-3 for all experiments, indicating that the fractionation of these essential fatty acids was negligible. However, the isotopic fractionation of 20:4n-6, 20:5n-3, and 22:6n-3 varied greatly between species and between diets. The isotopic fractionation of the Chlorella diet was −0.2 and −6.9 ‰ for zebrafish and mud snail, but 4.2 and −1.3 ‰, respectively, when these consumers were fed TetraMin. This variation could be explained by the different amount of assimilation and the biosynthesis of these fatty acids from their precursors (i.e., 18:2n-6 and 18:3n-3). These results indicate that the isotopic composition of C20 and C22 essential fatty acids was strongly influenced by the fatty acid composition in the diets. Thus the stable C isotope ratios of C18 essential fatty acids in consumers are more useful as dietary tracers in food web studies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abdulkadir S, Tsuchiya T (2008) One-step method for quantitative and qualitative analysis of fatty acids in marine animal samples. J Exp Mar Biol Ecol 354(1):1–8

    Article  CAS  Google Scholar 

  • Ahlgren G, Vrede T, Goedkoop W (2009) Fatty acid ratios in freshwater fish, zooplankton and zoobenthos—are there specific optima? In: Arts MT, Brett MT, Kainz MJ (eds) Lipid in aquatic ecosystems. Springer, New York, pp 147–178

    Chapter  Google Scholar 

  • Bell MV, Henderson RJ, Sargent JR (1986) The role of polyunsaturated fatty acids in fish. Comp Biochem Physiol 83B:711–719

    CAS  Google Scholar 

  • Budge SM, Wooller MJ, Springer AM, Iverson SJ, McRoy CP, Divoky GJ (2008) Tracing carbon flow in an arctic marine food web using fatty acid-stable isotope analysis. Oecologia 157:117–129

    Article  CAS  PubMed  Google Scholar 

  • Bunn SE, Leigh C, Jardine TD (2013) Diet-tissue fractionation of δ15N by consumers from streams and rivers. Limnol Oceanogr 58:765–773

    Article  CAS  Google Scholar 

  • Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol 46:443–453

    Article  CAS  Google Scholar 

  • Chamberlain PM, Bull ID, Black HIJ, Ineson P, Evershed RP (2004) Lipid content and carbon assimilation in Collembola: implications for the use of compound-specific carbon isotope analysis. Oecologia 139:325–335

    Article  PubMed  Google Scholar 

  • Chikaraishi Y, Ogawa NO, Kashiyama Y, Takano Y, Suga H, Tomitani A, Miyashita H, Kitazato H, Ohkouchi N (2009) Determination of aquatic food-web structure based on compound-specific nitrogen isotopic composition of amino acids. Limnol Oceanogr Methods 7:740–750

    Article  CAS  Google Scholar 

  • Dalsgaard J, John MS, Kattner G, Muller-Navarra D, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mari Biol 46:225–340

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Fry B, Arnold C (1982) Rapid 13C/12C turnover during growth of brown shrimp (Penaeus aztecus). Oecologia 54:200–204

    Article  Google Scholar 

  • Gaye-Siessegger J, Focken U, Abel H, Becker K (2004) Dietary lipid content influences the activity of lipogenic enzymes in the liver and on whole body delta C-13 values of Nile tilapia, Oreochromis niloticus (L.). Isotop Environ Health Stud 40:181–190

    Article  CAS  Google Scholar 

  • Gladyshev MI, Sushcik NN, Kalachova GS, Makhutova ON (2012) Stable isotope composition of fatty acids in organisms of different trophic levels in the Yensei River. PLoS One 7:e34059. doi:10.1371/journal.pone.0034059

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Graham C, Oxtoby L, Wang SW, Budge SM, Wooller MJ (2014) Sourcing fatty acids to juvenile polar cod (Boreogadus saida) in the Beaufort Sea using compound-specific stable carbon isotope analyses. Polar Biol 37:697–705

    Article  Google Scholar 

  • Hastings N, Agaba M, Tocher DR, Leaver MJ, Dick JR, Sargent JR, Teale AJ (2001) A vertebrate fatty acid desaturase with Δ5 and Δ6 activities. PNAS 98:14304–14309

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hayes JM, Freeman KH, Popp BN, Hoham CH (1990) Compound-specific isotopic analyses: a novel tool for reconstruction of ancient biogeochemical precesses. Adv Organ Geochem 16:1115–1128

    Article  CAS  Google Scholar 

  • Klein Breteler WCM, Grice K, Schouten S, Kloosterhuis HT, Sinninghe Damste JS (2002) Stable carbon isotope fractionation in the marine copepod Temora longicornis: unexpectedly low δ13C value of faecal pellets. Mar Ecol Prog Ser 240:195–204

    Article  CAS  Google Scholar 

  • McCutchan JH Jr, Lewis WM Jr, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen and sulfur. Oikos 102:378–390

    Article  CAS  Google Scholar 

  • Mfilinge PL, Meziane T, Bachok Z, Tsuchiya M (2005) Litter dynamics and particulate organic matter outwelling from a subtropical mangrove in Okinawa Island, South Japan. Estuar Coast Shelf Sci 63:301–313

    Article  CAS  Google Scholar 

  • 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 42:1135–1140

    Article  Google Scholar 

  • Napolitano GE (1999) Fatty acids as trophic and chemical markers in freshwater ecosystems. In: Arts MT, Wainman BC (eds) Lipids in freshwater ecosystems. Springer, New York, pp 21–44

    Chapter  Google Scholar 

  • Napolitano GN, Pollero RJ, Gayoso AM, Macdonald BA, Thompson RJ (1997) Fatty acids as trophic markers of phytoplankton blooms in the Bahia Blanca Estuary (Buenos Aires, Argentina) and in Trinity Bay (Newfoundland, Canada). Biochem Syst Ecol 25:739–755

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Prado P, Carmichael RH, Watts SA, Cebrian J, Heck KL Jr (2012) Diet-dependent δ13C and δ15N fractionation among sea urchin Lytechinus variegatus tissues: implications for food web models. Mar Ecol Prog Ser 462:175–190

    Article  CAS  Google Scholar 

  • Semenina EE, Tiunov AV (2011) Trophic fractionation (δ15N) in Collembola depends on nutritional status. A laboratory experiment and mini-review. Pedobiologia 54:101–109

    Article  CAS  Google Scholar 

  • Suzuki KW, Kasai A, Nakayama K, Tanaka M (2005) Differential isotopic enrichment and half-life among tissues in Japanese temperate bass (Lateolabrax japonicas) juveniles: implications for analyzing migration. Can J Fish Sci 62:671–678

    Article  Google Scholar 

  • Tieszen LL, Boutton TW, Tesdahl KG, Slade NA (1983) Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 57:32–37

    Article  Google Scholar 

  • Tocher DR (2010) Fatty acid requirements in ontogeny of marine and freshwater fish. Aquacult Res 41:717–732

    Article  CAS  Google Scholar 

  • Torres-Ruiz M, Wehr JD, Perrone AA (2007) Trophic relations in a stream food web: importance of fatty acids for macroinvertebrate consumers. J N Am Benthol Soc 26:509–522

    Article  Google Scholar 

  • Vander Zanden JB, Rasmussen JB (2001) Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web. Limnol Oceanogr 46:2031–2066

    Google Scholar 

  • Xu Q, Yang H (2007) Food sources of three bivalves living in two habitats of Jiaozhou Bay (Qingdao, China): indicated by lipid biomarkers and stable isotope analysis. J Shell Res 26:561–567

    Article  Google Scholar 

  • Yokoyama H, Tamaki A, Harada K, Shimoda K, Koyama K, Ishihi Y (2005) Variability of diet-tissue isotope fractionation in estuarine macrobenthos. Mar Fcol Prog Ser 296:115–128

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Erik Sperfeld for improving the English and Aya Takasawa for assisting with the feeding experiments. We also would like to thank two reviewers for their valuable comments.

Author contribution statement

M. F. and M. O. originally formulated the idea; M. F. and M. O. conducted all experiments and chemical analyses; O. N. gave advice on the experimental design; M. F. wrote the manuscript; O. N. and M. O. provided editorial advice.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Megumu Fujibayashi.

Additional information

Communicated by Joel Trexler.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fujibayashi, M., Ogino, M. & Nishimura, O. Fractionation of the stable carbon isotope ratio of essential fatty acids in zebrafish Danio rerio and mud snails Bellamya chinensis . Oecologia 180, 589–600 (2016). https://doi.org/10.1007/s00442-015-3486-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-015-3486-0

Keywords

Navigation