, Volume 136, Issue 2, pp 169–182 | Cite as

Sources of variation in consumer-diet δ15N enrichment: a meta-analysis

  • Mathew A. VanderkliftEmail author
  • Sergine Ponsard
Stable Isotope Ecology


Measurements of δ15N of consumers are usually higher than those of their diet. This general pattern is widely used to make inferences about trophic relationships in ecological studies, although the underlying mechanisms causing the pattern are poorly understood. However, there can be substantial variation in consumer-diet δ15N enrichment within this general pattern. We conducted an extensive literature review, which yielded 134 estimates from controlled studies of consumer-diet δ15N enrichment, to test the significance of several potential sources of variation by means of meta-analyses. We found patterns related to processes of nitrogen assimilation and excretion. There was a significant effect of the main biochemical form of nitrogenous waste: ammonotelic organisms show lower δ15N enrichment than ureotelic or uricotelic organisms. There were no significant differences between animals feeding on plant food, animal food, or manufactured mixtures, but detritivores yielded significantly lower estimates of enrichment. δ15N enrichment was found to increase significantly with the C:N ratio of the diet, suggesting that a nitrogen-poor diet can have an effect similar to that already documented for fasting organisms. There were also differences among taxonomic classes: molluscs and crustaceans generally yielded lower δ15N enrichment. The lower δ15N enrichment might be related to the fact that molluscs and crustaceans excrete mainly ammonia, or to the fact that many were detritivores. Organisms inhabiting marine environments yielded significantly lower estimates of δ15N enrichment than organisms inhabiting terrestrial or freshwater environments, a pattern that was influenced by the number of marine, ammonotelic, crustaceans and molluscs. Overall, our analyses point to several important sources of variation in δ15N enrichment and suggest that the most important of them are the main biochemical form of nitrogen excretion and nutritional status. The variance of estimates of δ15N enrichment, as well as the fact that enrichment may be different in certain groups of organisms should be taken into account in statistical approaches for studying diet and trophic relationships.


Stable isotopes Fractionation Trophic level Nitrogen Nitrogen excretion 



We gratefully acknowledge T. Adams, M. Ben-David, A. Dittel, U. Focken, E. Gorokhova, C. Harvey, S. Herzka, R. Hesslein, G. Hilderbrand, K. Hobson, K. Kurata, K. Oelbermann and J. Pinnegar for providing us with additional data. G. Kendrick and A.J. Smit provided comments that greatly improved the manuscript.


  1. Adams TS, Sterner RW (2000) The effect of dietary nitrogen content on trophic level 15N enrichment. Limnol Oceanogr 45:601–607Google Scholar
  2. Ambrose SH, DeNiro MJ (1986) The isotopic ecology of East African mammals. Oecologia 69:395–406Google Scholar
  3. Ambrose SH, DeNiro MJ (1987) Bone nitrogen isotope composition and climates. Nature 325:201Google Scholar
  4. Bearhop S, Thompson DR, Waldron S, Russell IC, Alexander G, Furness RW (1999) Stable isotopes indicate the extent of freshwater feeding by cormorants Phalacrocorax carbo shot at inland fisheries in England. J Appl Ecol 36:75–84CrossRefGoogle Scholar
  5. Ben-David M (1996) Seasonal diets of mink and martens: effects of spatial and temporal changes in resource abundance. PhD thesis, University of Alaska, FairbanksGoogle Scholar
  6. Ben-David M, Flynn RW, Schell DM (1997) Annual and seasonal changes in diets of martens: evidence from stable isotope analysis. Oecologia 111:280–291CrossRefGoogle Scholar
  7. Checkley DM Jr, Entzeroth LC (1985) Elemental and isotopic fractionation of carbon and nitrogen by marine, planktonic copepods and implications to the marine nitrogen cycle. J Plankton Res 7:553–568Google Scholar
  8. Cormie AB, Schwartcz HP (1996) Effects of climate on deer bone δ15N and δ13C: lack of precipitation effects on δ15N for animals consuming low amounts of C4 plants. Geochim Cosmochim Acta 60:4161–4166CrossRefGoogle Scholar
  9. Curtis PS, Wang X (1998) A meta-analysis of elevated CO2 effects on woody plant mass, form, and physiology. Oecologia 113:299–313CrossRefGoogle Scholar
  10. DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351Google Scholar
  11. Dittel AI, Epifanio CE, Cifuentes LA, Kirchman DL (1997) Carbon and nitrogen sources for shrimp postlarvae fed natural diets from a tropical mangrove system. Estuar Coast Shelf Sci 45:629–637CrossRefGoogle Scholar
  12. Dittel AI, Epifanio CE, Schwalm SM, Fantle MS, Fogel ML (2000) Carbon and nitrogen sources for juvenile blue crabs Callinectes sapidus in coastal wetlands. Mar Ecol Prog Ser 194:103–112Google Scholar
  13. Downing JA, Osenberg CW, Sarnelle O (1999) Meta-analysis of marine nutrient-enrichment experiments: variation in the magnitude of nutrient limitation. Ecology 80:1157–1167Google Scholar
  14. Eggers T, Jones TH (2000) You are what you eat... or are you? Trends Ecol Evol 15:265–266Google Scholar
  15. Estep MLF, Vigg S (1985) Stable carbon and nitrogen isotope tracers of trophic dynamics in natural populations and fisheries of the Lahontan Lake System, Nevada. Can J Fish Aquat Sci 42:1712–1719Google Scholar
  16. Fantle MS, Dittel AI, Schwalm SM, Epifanio CE, Fogel ML (1999) A food web analysis of the juvenile blue crab, Callinectes sapidus, using stable isotopes in whole animals and individual amino acids. Oecologia 120:416–426CrossRefGoogle Scholar
  17. Focken U (2001) Stable isotopes in animal ecology: the effect of ration size on the trophic shift of C and N isotopes between feed and carcass. Isot Environ Health Stud 37:199–211Google Scholar
  18. Gaebler OH, Vitti TG, Vukmirovich R (1966) Isotope effects in metabolism of 14N and 15N from unlabeled dietary proteins. Can J Biochem 44: 1249–1257PubMedGoogle Scholar
  19. 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 78:1271–1276Google Scholar
  20. Gorokhova E, Hansson S (1999) An experimental study on variations in stable carbon and nitrogen isotope fractionation during growth of Mysis mixta and Neomysis integer. Can J Fish Aquat Sci 56:2203–2210CrossRefGoogle Scholar
  21. Gurevitch J, Hedges LV (1993) Meta-analysis: combining the results of independent experiments. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Chapman and Hall, New York, pp 378–398Google Scholar
  22. Gurevitch J, Hedges LV (1999) Statistical issues in ecological meta-analyses. Ecology 80:1142–1149Google Scholar
  23. Hare PE, Fogel ML, Stafford TW Jr, Mitchell AD, Hoering TC (1991) The isotopic composition of carbon and nitrogen in individual amino acids isolated from modern and fossil proteins. J Archaeol Sci 18:277–292Google Scholar
  24. 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 59:115–124CrossRefGoogle Scholar
  25. Hedges LV, Olkin I (1985) Statistical methods for meta-analysis. Academic Press, OrlandoGoogle Scholar
  26. Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156Google Scholar
  27. Herzka SZ, Holt GJ (2000) Changes in isotopic composition of red drum (Sciaenops ocellatus) larvae in response to dietary shifts: potential applications to settlement studies. Can J Fish Aquat Sci 57:137–147CrossRefGoogle Scholar
  28. Hesslein RH, Hallard KA, Ramlal P (1993) Replacement of sulfur, carbon, and nitrogen in tissue of growing broad whitefish (Coregonus nasus) in response to a change in diet traced by δ34S, δ13C, and δ15N. Can J Fish Aquat Sci 50:2071–2076Google Scholar
  29. Hilderbrand GV, Farley SD, Robbins CT, Hanley TA, Titus K, Servheen C (1996) Use of stable isotopes to determine diets of living and extinct bears. Can J Zool 74:2080–2088Google Scholar
  30. Hobson KA (1993) Trophic relationships among high Arctic seabirds: insights from tissue-dependent stable-isotope models. Mar Ecol Prog Ser 95:7-18Google Scholar
  31. Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes II: Factors influencing diet-tissue fractionation. Condor 94:189–197Google Scholar
  32. 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 84:9-18Google Scholar
  33. Hobson KA. Alisauskas RT, Clark RG (1993) Stable-nitrogen isotope enrichment in avian tissues due to fasting and nutritional stress: implications for isotopic analysis of diet. Condor 95:388–394Google Scholar
  34. Hobson KA, Schell DM, Renouf D, Noseworthy E (1996) Stable carbon and nitrogen isotopic fractionation between diet and tissues of captive seals: implications for dietary reconstructions involving marine mammals. Can J Fish Aquat Sci 53:528–533CrossRefGoogle Scholar
  35. Hughes TP, Baird AH, Dinsdale EA, Harriot VJ, Moltschaniwskyj NA, Pratchett MS, Tanner JE, Willis BJ (2002) Detecting regional variation using meta-analysis and large-scale sampling: latitudinal patterns in recruitment. Ecology 83:436–451Google Scholar
  36. Kurata K, Minami H, Kikuchi E (2001) Stable isotope analysis of food sources for salt marsh snails. Mar Ecol Prog Ser 223:167–177Google Scholar
  37. Kurle CM (2002) Stable-isotope ratios of blood components from captive northern fur seals (Callorhinus ursinus) and their diet: applications for studying the foraging ecology of wild otariids. Can J Zool 80:902–909CrossRefGoogle Scholar
  38. Laird NM, Mosteller F (1990) Some statistical methods for combining experimental results. Int J Technol Assess Health C 6:5-30Google Scholar
  39. Lesage V, Hammill MO, Kovacs KM (2002) Diet-tissue fractionation of stable carbon and nitrogen isotopes in phocid seals. Mar Mammal Sci 18:182–193Google Scholar
  40. Macko SA, Lee WY, Parker PL (1982) Nitrogen and carbon isotope fractionation by two species of marine amphipods: laboratory and field studies. J Exp Mar Biol Ecol 63:145–149Google Scholar
  41. Markow TA, Anwar S, Pfeiler E (2000) Stable isotope ratios of carbon and nitrogen in natural populations of Drosophila species and their hosts. Funct Ecol 14:261–266CrossRefGoogle Scholar
  42. 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 48:1135–1140Google Scholar
  43. Mizutani H, Fukuda M, Kabaya Y (1992) δ13C and δ15N enrichment factors of feathers of 11 species of adult birds. Ecology 73:1391–1395Google Scholar
  44. Oelbermann K, Scheu S (2002) Stable isotope enrichment (δ15N and δ13C) in a generalist predator (Pardosa lugubris, Araneae: Lycosidae): effects or prey quality. Oecologia 130:337–344CrossRefGoogle Scholar
  45. Ostrom PH, Colunga-Garcia M, Gage SH (1997) Establishing pathways of energy flow for insect predators using stable isotope ratios: field and laboratory evidence. Oecologia 109:108–113CrossRefGoogle Scholar
  46. Owens NJP (1987) Natural variations in 15N in the marine environment. Adv Mar Biol 24:389–451Google Scholar
  47. Phillips DL (2001) Mixing models in analyses of diet using multiple stable isotopes: a critique. Oecologia 127:166–170CrossRefGoogle Scholar
  48. Phillips DL, Gregg JW (2001) Uncertainty in source partitioning using stable isotopes. Oecologia 127:171–179CrossRefGoogle Scholar
  49. Phillips DL, Koch PL (2002) Incorporating concentration dependence in stable isotope mixing models. Oecologia 130:114–125Google Scholar
  50. Pinnegar JK, Polunin NVC (1999) Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions. Funct Ecol 13:225–231CrossRefGoogle Scholar
  51. Ponsard S, Amlou M (1999) Effects of several preservation methods on the isotopic content of Drosophila samples. C R Acad Sci Paris 322:35–41CrossRefPubMedGoogle Scholar
  52. Ponsard S, Averbuch P (1999) Should growing and adult animals fed on the same diet show different δ15N values? Rapid Commun Mass Spectrom 13:1305–1310Google Scholar
  53. Ponsard S, Arditi R (2000) What can stable isotopes (δ15N and δ13C) tell about the food web of soil macro-invertebrates? Ecology 81:852–864Google Scholar
  54. Ponsard S, Arditi R (2001) Detecting omnivory with δ15N. Trends Ecol Evol 16:20–21CrossRefGoogle Scholar
  55. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718Google Scholar
  56. Post DM, Pace ML, Hairston NG (2000) Ecosystem size determines food-chain length in lakes. Nature 405:1047–1049PubMedGoogle Scholar
  57. Rieutord M (1999) Physiologie animale, vol 2. Les grandes fonctions. Masson, ParisGoogle Scholar
  58. Robinson D (2001) δ15N as an integrator of the nitrogen cycle. Trends Ecol Evol 16:153–162PubMedGoogle Scholar
  59. Roth JD, Hobson KA (2000) Stable carbon and nitrogen isotopic fractionation between diet and tissue of captive red fox: implications for dietary reconstruction. Can J Zool 78:848–852CrossRefGoogle Scholar
  60. Schmidt O, Scrimgeour CM, Curry JP (1999) Carbon and nitrogen stable isotope ratios in body tissue and mucus of feeding and fasting earthworms (Lumbricus festivus). Oecologia 118:9-15CrossRefGoogle Scholar
  61. Schoeninger MJ, DeNiro MJ (1984) Nitrogen and carbon isotopic composition of bone collagen from marine and terrestrial animals. Geochim Cosmochim Acta 48:625–639Google Scholar
  62. Scrimgeour CM, Gordon SC, Handley LL, Woodford JAT (1995) Trophic levels and anomalous δ15N of insects on raspberry (Rubus idaeus L.). Isot Environ Health Stud 31:107–115Google Scholar
  63. Sealy JC, VanDerMerwe NJ, Lee Thorp JA, Lanham JL (1987) Nitrogen isotopic ecology in southern Africa: implications for environmental and dietary tracing. Geochim Cosmochim Acta 51:2707–2717Google Scholar
  64. Smit AJ (2001) Source identification in marine ecosystems: food web studies using δ13C and δ15N. In: Unkovich MJ, Pate JS, McNeil AM, Gibbs J (eds) Stable isotope techniques in the study of biological processes and functioning of ecosystems. Kluwer Academic, Dordrecht, pp 219–245Google Scholar
  65. Steele KW, Daniel RM (1978) Fractionation of nitrogen isotopes by animals: a further complication to the use of variations in the natural abundance of 15N for tracer studies. J Agric Sci 90:7-9Google Scholar
  66. Szepanski MM, Ben-David M, Van Ballenberghe V (1999) Assessment of anadromous salmon resources in the diet of the Alexander Archipelago wolf using stable isotope analysis. Oecologia 120:327–335CrossRefGoogle Scholar
  67. Thoman ES, Ingall ED, Davis DA, Arnold CR (2001) A nitrogen budget for a closed, recirculating mariculture system. Aquacult Eng 24:195–2111CrossRefGoogle Scholar
  68. Toda H, Wada E (1990) Use of 15N/14N rations [sic] to evaluate the food source of the mysid, Neomysis intermedia Czerniawsky, in a eutrophic lake in Japan. Hydrobiologia 194:85-90Google Scholar
  69. Vander Zanden MJ, Rasmussen JB (2001) Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnol Oceanogr 46:2061–2066Google Scholar
  70. Vander Zanden MJ, Shuter B, Lester NP, Rasmussen JB (2000) Within- and among-population variation in the trophic position of a pelagic predator, lake trout (Salvelinus namaycush). Can J Fish Aquat Sci 57:725–731CrossRefGoogle Scholar
  71. Webb SC, Hedges REM, Simpson SJ (1998) Diet quality influences the δ13C and δ15N of locusts and their biochemical components. J Exp Biol 201:2903–2911PubMedGoogle Scholar
  72. Yoneyama T, Ohta Y, Ohtani T (1983) Variations of natural 13C and 15N abundances in the rat tissues and their correlation. Radioisotopes 32:330–332PubMedGoogle Scholar
  73. Yoneyama T, Handley LL, Scrimgeour CM, Fisher, Raven JA (1997) Variations of the natural abundances of nitrogen and carbon isotopes in Triticum aestivum, with special reference to phloem and xylem exudates. New Phytol 137:205–213CrossRefGoogle Scholar
  74. Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice Hall, New JerseyGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  1. 1.Department of BotanyUniversity of Western AustraliaNedlandsAustralia
  2. 2.Laboratoire Dynamique de la Biodiversité (UMR CNRS 5552) - Batiment 4R3Université P. Sabatier—Toulouse IIIToulouse Cedex 04France
  3. 3.Centre for Ecosystem ManagementEdith Cowan UniversityJoondalupAustralia

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