Skip to main content
SpringerLink
Log in

Does lipid-correction introduce biases into isotopic mixing models? Implications for diet reconstruction studies

  • Concepts, Reviews and Syntheses
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Carbon isotopes are commonly used in trophic ecology to estimate consumer diet composition. This estimation is complicated by the fact that lipids exhibit a more depleted carbon signature (δ13C) than other macromolecules, and are often found at different concentrations among individual organisms. Some researchers argue that lipids bias diet reconstructions using stable isotopes and should be accounted for prior to analysis in food web mixing models, whereas others contend that removing lipids may result in erroneous interpretations of the trophic interactions under study. To highlight this disagreement on best practices for applying δ13C in food web studies, we sampled the recent literature to determine the frequency and method of lipid-correction. We then quantified the potential magnitude and source of bias in mixing model results from a theoretical example and case study of diet reconstruction. The literature was split nearly evenly as to whether lipid-correction was applied to δ13C data in mixing model estimates of diet composition. Comparative mixing model scenarios demonstrated that lipid-correction can substantially alter the estimated diet composition and interpretation of consumer foraging habits. Given the lack of consensus on whether or not to lipid-correct prey and/or consumers, and the associated variation in mixing model results, we call for the establishment of a unified framework that will guide diet reconstruction in stable isotope ecology. Uncertainty in the prevalence of direct routing versus de novo synthesis of lipids across ecosystems, taxa, and trophic levels must be resolved to better guide treatment of lipids in isotope studies using carbon.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ambrose SH, Norr L (1993) Carbon isotopic evidence for routing of dietary protein to bone collagen, and whole diet to bone apatite carbonate: purified diet growth experiments. In: Lambert JB, Grupe G (eds) Molecular archaeology of prehistoric human bone. Springer, Berlin, pp 1–37

    Google Scholar 

  • Arts MT, Achman RG, Holub BJ (2001) “Essential fatty acids” in aquatic ecosystems: a crucial link between diet and human health and evolution. Can J Fish Aquat Sci 58:122–137

    CAS  Google Scholar 

  • Babar A, Jayawant MS, Pawar SP (2017) Nutritional profile of the freshwater edible bivalve Lamellidens corrianus (Lea 1834) and its relation to water quality in the Bhatsa River, India. Asian Fish Sci 30:52–69

    Google Scholar 

  • Beukema JJ (1997) Caloric values of marine invertebrates with an emphasis on the soft parts of marine bivalves. Oceanogr Mar Biol 35:387–414

    Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    CAS  Google Scholar 

  • Boecklen WJ, Yarnes CT, Cook BA, James AC (2011) On the use of stable isotopes in trophic ecology. Annu Rev Ecol Evol Syst 42:411–440

    Google Scholar 

  • Bond AL, Diamond AW (2011) Recent Bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors. Ecol Appl 21:1017–1023

    PubMed  Google Scholar 

  • Brett MT (2014) Resource polygon geometry predicts Bayesian stable isotope mixing model bias. Mar Ecol Prog Ser 514:1–12

    Google Scholar 

  • Brett MT, Müller-Navarra DC (1997) The role of highly unsaturated fatty acids in aquatic foodweb processes. Freshw Biol 38:483–499

    CAS  Google Scholar 

  • Brett MT, Müller-Navarra DC, Ballantyne AP, Ravet JL, Goldman CR (2006) Daphnia fatty acid composition reflects that of their diet. Limnol Oceanogr 51:2428–2437

    CAS  Google Scholar 

  • Buchheister A, Latour RJ (2010) Turnover and fractionation of carbon and nitrogen stable isotopes in tissues of a migratory coastal predator, summer flounder (Paralichthys dentatus). Can J Fish Aquat Sci 67:445–461

    CAS  Google Scholar 

  • Cherry SG, Derocher AE, Hobson KA, Stirling I, Thiemann GW (2011) Quantifying dietary pathways of proteins and lipids to tissues of a marine predator. J Appl Ecol 48:373–381

    CAS  Google Scholar 

  • Cummings BM, Schindler DE (2013) Depth variation in isotopic composition of benthic resources and assessment of sculpin feeding patterns in an oligotrophic Alaskan lake. Aquat Ecol 47:403–414

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Erhardt EB, Wolf BO, Ben-David M, Bedrick EJ (2014) Stable isotope sourcing using sampling. Open J Ecol 4:289–298

    Google Scholar 

  • Felip O, Ibarz A, Fernández-Borrás J, Beltrán M, Martín-Pérez M, Planas JV, Blasco J (2012) Tracing metabolic routes of dietary carbohydrate and protein in rainbow trout (Oncorhynchus mykiss) using stable isotopes ([13C] starch and [15N] protein): effects of gelatinization of starches and sustained swimming. Br J Nutr 107:834–844

    CAS  PubMed  Google Scholar 

  • Fernandes R, Millard AR, Brabec M, Nadeau M-J, Grootes P (2014) Food reconstruction using isotopic transferred signals (Fruits): a Bayesian model for diet reconstruction. PLoS One 9:e87436

    PubMed  PubMed Central  Google Scholar 

  • Fernandes R, Larsen T, Knipper C, Feng F, Wang Y (2017) IsoMemo.com: a database of isotopic data for ecology, archaeology, and environmental science. http://www.isomemo.com Accessed 12 July 2018.

  • Fry B (2006) Stable isotope ecology. Springer, New York

    Google Scholar 

  • Fry B, Baltz DM, Benfield MC, Fleeger JW, Gace A, Haas HL, Quinones-Rivera ZJ (2003) Stable isotope indicators of movement and residency for brown shrimp (Farfantepenaeus aztecus) in coastal Louisiana marshscapes. Estuaries 26:82–97

    Google Scholar 

  • Galloway AWE, Eisenlord ME, Dethier MN, Holtgrieve GW, Brett MT (2014) Quantitative estimates of isopod resource utilization using a Bayesian fatty acid mixing model. Mar Ecol Prog Ser 507:219–232

    Google Scholar 

  • Garcés R, Mancha M (1993) One-step lipid extraction and fatty acid methyl esters preparation from fresh plant tissues. Anal Biochem 211:139–143

    PubMed  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 δ13C values of Nile tilapia, Oreochromis niloticus (L.). Isot Environ Health Stud 40:181–190

    CAS  Google Scholar 

  • Gelman A, Carlin JB, Stern HS, Dunson DB, Vehtari A, Rubin DB (2013) Bayesian data analysis, 3rd edn. CRC Press, Boca Raton

    Google Scholar 

  • Gende SM, Quinn TP, Willson MF (2001) Consumption choice by bears feeding on salmon. Oecologia 127:372–382

    CAS  PubMed  Google Scholar 

  • Gende SM, Quinn TP, Hilborn R, Hendry AP, Dickerson B (2004) Brown bears selectively kill salmon with higher energy content but only in habitats that facilitate choice. Oikos 104:518–528

    Google Scholar 

  • Goetz F, Rosauer D, Sitar S, Goetz G, Simchick C, Roberts S, Johnson R, Murphy C, Bronte CR, Mackenzie S (2010) A genetic basis for the phenotypic differentiation between siscowet and lean lake trout (Salvelinus namaycush). Mol Ecol 19:176–196

    PubMed  Google Scholar 

  • Goulden CE, Place AR (1990) Fatty acid synthesis and accumulation rates in daphniids. J Exp Zool 256:168–178

    CAS  Google Scholar 

  • Haramis GM, Nichols JD, Pollock KH, Hines JE (1986) The relationship between body mass and survival of wintering canvasbacks. Auk 103:506–514

    Google Scholar 

  • Harvey CJ, Hanson PC, Essington TE, Brown PB, Kitchell JF (2002) Using bioenergetics models to predict stable isotope ratios in fishes. Can J Fish Aquat Sci 59:115–124

    Google Scholar 

  • Hoffman JC, Sierszen ME, Cotter AM (2015) Fish tissue lipid-C: N relationships for correcting values and estimating lipid content in aquatic food-web studies. Rapid Commun Mass Spectrom 29:2069–2077

    CAS  PubMed  Google Scholar 

  • Hopkins CA (1950) Studies on cestode metabolism. I. Glycogen metabolism in Schistocephalus solidus in vivo. J Parasitol 26:384–390

    Google Scholar 

  • Janjua MY, Gerdeaux D (2011) Evaluation of food web and fish dietary niches in oligotrophic Lake Annecy by gut content and stable isotope analysis. Lake Reserv Manag 27:115–127

    Google Scholar 

  • Kelly LJ, Martínez del Rio C (2010) The fate of carbon in growing fish: an experimental study of isotopic routing. Physiol Biochem Zool 83:473–480

    PubMed  Google Scholar 

  • Kilborn L, Macleod J (1920) Observation on the glycogen content of certain invertebrates and fishes. Exp Physiol 12:317–330

    Google Scholar 

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

    CAS  Google Scholar 

  • Layman CA, Araujo MS, Boucek R, Hammerschlag-Peyer CM, Harrison E, Jud ZR, Matich P, Rosenblatt AE, Vaudo JJ, Yeager LA, Post DM, Bearhop S (2012) Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biol Rev 87:545–562

    PubMed  Google Scholar 

  • Lincoln AE, Quinn TP (2018) Optimal foraging or surplus killing: selective consumption and discarding of salmon by brown bears. Behav Ecol 30:202–212

    Google Scholar 

  • Logan JM, Jardine TD, Miller TJ, Bunn SE, Cunjak RA, Lutcavage ME (2008) Lipid corrections in carbon and nitrogen stable isotope analyses: comparison of chemical extraction and modeling methods. J Anim Ecol 77:838–846

    PubMed  Google Scholar 

  • Martínez del Rio C, Wolf N, Carleton S, Gannes LZ (2009) Isotopic ecology ten years after a call for more laboratory experiments. Biol Rev 84:91–111

    Google Scholar 

  • Mayntz D, Raubenheimer D, Salomon M, Toft S, Simpson SJ (2005) Nutrient-specific foraging in invertebrate predators. Science 307:111–113

    CAS  PubMed  Google Scholar 

  • Mayntz D, Nielsen VH, Sørensen A, Toft S, Raubenheimer D, Hejlesen C, Simpson SJ (2009) Balancing of protein and lipid intake by a mammalian carnivore, the mink, Mustela vison. Anim Behav 77:349–355

    Google Scholar 

  • McConnaughey T, McRoy CP (1979) Food-web structure and the fractionation of carbon isotopes in the Bering Sea. Mar Biol 53:257–262

    CAS  Google Scholar 

  • Mohan JA, Smith SD, Connelly TL, Attwood ET, McClelland JW, Herzka SZ, Walther BD (2016) Tissue-specific isotope turnover and discrimination factors are affected by diet quality and lipid content in an omnivorous consumer. J Exp Mar Biol Ecol 479:35–45

    CAS  Google Scholar 

  • Moore JW, Semmens BX (2008) Incorporating uncertainty and prior information into stable isotope mixing models. Ecol Lett 1:470–480

    Google Scholar 

  • Morrison RIG, Davidson NC, Wilson JR (2007) Survival of the fattest: body stores on migration and survival in red knots Calidris canutus islandica. J Avian Biol 38:479–487

    Google Scholar 

  • Newsome SD, Wolf N, Peters J, Fogel ML (2014) Amino acid analysis shows flexibility in the routing of dietary protein and lipids to the tissue of an omnivore. Integr Comp Biol 54:890–902

    CAS  PubMed  Google Scholar 

  • Nithirojpakdee P, Beamish FWH, Boonphakdee T (2014) Diet diversity among five co-existing fish species in a tropical river: integration of dietary and stable isotope data. Limnology 15:99–107

    CAS  Google Scholar 

  • O’Neill SM, Ylitalo GM, West JE (2014) Energy content of Pacific salmon as prey of northern and southern resident killer whales. Endanger Species Res 25:265–281

    Google Scholar 

  • Park R, Epstein S (1961) Metabolic fractionation of C13 and C12 in plants. Plant Physiol 36:133–138

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS One 5:e9672

    PubMed  PubMed Central  Google Scholar 

  • Parrish FA, Martinelli-Liedtke TL (1999) Some preliminary findings on the nutritional status of the Hawaiian spiny lobster (Panulirus marginatus). Pac Sci 53:361–366

    Google Scholar 

  • Patterson HK, Carmichael RH (2016) The effect of lipid extraction on carbon and nitrogen stale isotope ratios in oyster tissues: implications for glycogen-rich species. Rapid Commun Mass Spectrom 30:2594–2600

    CAS  PubMed  Google Scholar 

  • Pauli JN, Newsome SD, Cook JA, Harrod C, Steffan SA, Baker CJO, Ben-David M, Bloom D, Bowen GJ, Cerling TE, Cicero C, Cook C, Dohm M, Dharampal PS, Graves G, Gropp R, Hobson KA, Jordan C, MacFadden B, Birch SP, Poelen J, Ratnasignham S, Russell L, Stricker CA, Uhen MD, Yarnes CT, Hayden B (2017) Why we need a centralized repository for isotopic data. Proc Natl Acad Sci USA 114:2997–3001

    CAS  PubMed  Google Scholar 

  • Pecquerie L, Nisbet RM, Fablet R, Lorrain A, Koojiman SA (2010) The impact of metabolism on stable isotope dynamics: a theoretical framework. Phil Trans R Soc B 365:3455–3468

    PubMed  Google Scholar 

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

    Google Scholar 

  • Phillips DL, Gregg JW (2003) Source partitioning using stable isotopes: coping with too many sources. Oecologia 136:261–269

    PubMed  Google Scholar 

  • Phillips DL, Inger R, Bearhop S, Jackson AL, Moore JW, Parnell AC, Semmens BX, Ward EJ (2014) Best practices for use of stable isotope mixing models in food-web studies. Can J Zoo 92:823–835

    Google Scholar 

  • Podlesak DW, McWilliams SR (2007) Metabolic routing of dietary nutrients in birds: effects of dietary lipid concentration on δ13C of depot fat and its ecological implications. Auk 124:916–925

    Google Scholar 

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

    Google Scholar 

  • Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montaña CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189

    PubMed  Google Scholar 

  • Rau GH (1980) Carbon-13/carbon-12 variation in subalpine lake aquatic insects: food source implications. Can J Fish Aquat Sci 37:742–746

    CAS  Google Scholar 

  • Reimchen TE (2000) Some ecological and evolutionary aspects of bear-salmon interactions in coastal British Columbia. Can J Zool 78:448–457

    Google Scholar 

  • Reitan KI, Rainuzzo JR, Olsen Y (1994) Effect of nutrient limitation on fatty acid and lipid content of marine microalgae. J Phycol 30:972–979

    CAS  Google Scholar 

  • Rowe DK, Thorpe JE, Shanks AM (1991) Role of fat stores in the maturation of male Atlantic salmon (Salmo salar) parr. Can J Fish Aquat Sci 48:405–413

    Google Scholar 

  • Ryan C, McHugh B, Trueman CN, Harrod C, Berrow SD, O’Connor I (2012) Accounting for the effects of lipids in stable isotope (δ13C and δ15N values) analysis of skin and blubber of balaenopterid whales. Rapid Commun Mass Spectrom 26:2745–2754

    CAS  PubMed  Google Scholar 

  • Sanderson BL, Tran CD, Coe HJ, Pelekis V, Steel A, Reichert WL (2009) Nonlethal sampling of fish caudal fins yields valuable stable isotope data for threatened and endangered fishes. Trans Am Fish Soc 138:1166–1177

    Google Scholar 

  • Shine R, Madsen T (1997) Prey abundance and predator reproduction: rats and pythons on a tropical Australian floodplain. Ecology 78:1078–1086

    Google Scholar 

  • Smith RJ, Moore FR (2003) Arrival fat and reproductive performance in a long-distance passerine migrant. Oecologia 134:325–331

    PubMed  Google Scholar 

  • Stock BC, Semmens BX (2013) MixSIAR GUI User Manual. Version 3.1. https://github.com/brianstock/MixSIAR/. Accessed Dec 2018

  • Stock BC, Semmens BX (2016) Unifying error structures in commonly used biotracer mixing models. Ecology 97:2562–2569

    PubMed  Google Scholar 

  • Stock BC, Jackson AL, Ward EJ, Parnell AC, Phillips DL, Semmens BX (2018) Analyzing mixing systems using a new generation of Bayesian tracer mixing models. PeerJ 6:e5096

    PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Taipale SJ, Kainz MJ, Brett MT (2011) Diet-switching experiments show rapid accumulation and preferential retention of highly unsaturated fatty acids in Daphnia. Oikos 120:1674–1982

    Google Scholar 

  • Tarroux A, Ehrich D, Lecomte N, Jardine TD, Bêty J, Berteaux D (2010) Sensitivity of stable isotope mixing models to variation in isotopic ratios: evaluating consequences of lipid extraction. Methods Ecol Evol 1:231–241

    Google Scholar 

  • Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11:107–184

    CAS  Google Scholar 

  • van der Merwe NJ (1982) Carbon isotopes, photosynthesis, and archaeology. Am Sci 70:596–606

    Google Scholar 

  • Wessels FJ, Hahn DA (2010) Carbon 13 discrimination during lipid biosynthesis varies with dietary concentration of stable isotopes: implications for stable isotope analyses. Funct Ecol 24:1017–1022

    Google Scholar 

  • Wolf N, Newsome SD, Peters J, Fogel ML (2015) Variability in the routing of dietary proteins and lipids to consumer tissues influences tissue-specific isotopic discrimination. Rapid Commun Mass Spectrom 29:1448–1456

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Funding for this project was provided by the Achievement Rewards for College Scientists (ARCS) Foundation Seattle Chapter via the Barton family, Richard and Lois Worthington Endowment, H. Mason Keeler Endowment, Clarence H. Campbell Endowed Lauren Donaldson Scholarship in Ocean and Fishery Sciences, Richard T. Whiteleather Fisheries B.S. 1935 Endowed Scholarship, and Floyd E. Ellis Memorial Scholarship. We thank Thomas Quinn, Michael Brett, Joel Trexler, and three anonymous reviewers for critical feedback on the manuscript.

Author information

Author notes

  1. Martin C. Arostegui

    Present address: Applied Physics Laboratory, Air-Sea Interaction & Remote Sensing Department, University of Washington, Seattle, WA, 98105, USA

Authors and Affiliations

  1. School of Aquatic and Fishery Sciences, University of Washington, P. O. Box 355020, Seattle, WA, 98195, USA

    Martin C. Arostegui, Daniel E. Schindler & Gordon W. Holtgrieve

Authors
  1. Martin C. Arostegui
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniel E. Schindler
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gordon W. Holtgrieve
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MCA, DES, and GWH designed the study. MCA conducted the literature review, mixing model comparisons and wrote the first draft, after which DES and GWH contributed to the editing and refinement of the manuscript.

Corresponding author

Correspondence to Martin C. Arostegui.

Additional information

Communicated by Joel Trexler.

There is a lack of consensus in stable isotope ecology about whether to apply lipid-correction in diet reconstruction. We discuss implications for study design and assumptions violated by this method.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 84 kb)

Supplementary material 2 (DOCX 77 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Arostegui, M.C., Schindler, D.E. & Holtgrieve, G.W. Does lipid-correction introduce biases into isotopic mixing models? Implications for diet reconstruction studies. Oecologia 191, 745–755 (2019). https://doi.org/10.1007/s00442-019-04525-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-019-04525-7

Keywords

Search

Navigation