Oecologia

, Volume 144, Issue 4, pp 534–540

The effect of dietary protein quality on nitrogen isotope discrimination in mammals and birds

  • Charles T. Robbins
  • Laura A. Felicetti
  • Matt Sponheimer
Stable Isotopes Issue

Abstract

We tested the competing hypotheses that (1) nitrogen discrimination in mammals and birds increases with dietary nitrogen concentration or decreasing C:N ratios and, therefore, discrimination will increase with trophic level as carnivores ingest more protein than herbivores and omnivores or (2) nitrogen discrimination increases as dietary protein quality decreases and, therefore, discrimination will decrease with trophic level as carnivores ingest higher quality protein than do herbivores. Discrimination factors were summarized for five major diet groupings and 21 different species of birds and mammals. Discrimination did not differ between mammals and birds and decreased as protein quality (expressed as biological value) increased with trophic level (i.e., herbivores to carnivores). Relationships between discrimination factors and dietary nitrogen concentration or C:N ratios were either the opposite of what was hypothesized or non-significant. Dietary protein quality accounted for 72% of the variation in discrimination factors across diet groupings. We concluded that protein quality established the baseline for discrimination between dietary groupings, while other variables, such as dietary protein intake relative to animal requirements, created within-group variation. We caution about the care needed in developing studies to understand variation in discrimination and subsequently applying those discrimination factors to estimate assimilated diets of wild animals.

Keywords

Assimilated diet Discrimination Nitrogen Stable isotopes Trophic level 

References

  1. ARC (1965) The nutrient requirements of farm livestock. No. 2 Ruminants. Agricultural Research Council, LondonGoogle Scholar
  2. Bearhop S, Waldron S, Votier SC, Furness RW (2002) Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers. Physiol Biochem Zool 75:451–458PubMedCrossRefGoogle Scholar
  3. Ben-David M, Schell DM (2001) Mixing models in analyses of diet using multiple stable isotopes: a response. Oecologia 127:180–184CrossRefGoogle Scholar
  4. DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351CrossRefGoogle Scholar
  5. 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
  6. Felicetti, LA, Robbins CT, Shipley LA (2003a) Dietary protein content alters energy expenditure and composition of the mass gain in grizzly bears (Ursus arctos horribilis). Physiol Biochem Zool 76:256–261PubMedCrossRefGoogle Scholar
  7. Felicetti LA, Schwartz CC, Rye RO, Haroldson MA, Gunther KA, Phillips DL, Robbins CT (2003b) Use of sulfur and nitrogen stable isotopes to determine the importance of whitebark pine nuts to Yellowstone grizzly bears. Can J Zool 81:763–770CrossRefGoogle Scholar
  8. Gaye-Siessegger J, Focken U, Muetzel S, Abel H, Becker K (2004) Feeding level and individual metabolic rate affect δ13C and δ15N values in carp: implications for food web studies. Oecologia 138:175–183PubMedCrossRefGoogle Scholar
  9. Hands ES (2000) Nutrients in foods. Lippincott Williams and Wilkins, BaltimoreGoogle Scholar
  10. Haramis GM, Jorde DG, Macko SA, and Walker JL (2001) Stable-isotope analysis of canvasback winter diet in Upper Chesapeake Bay. Auk 118:1008–1017CrossRefGoogle Scholar
  11. 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 74:2080–2088CrossRefGoogle Scholar
  12. Hobson KA, Bairlein F (2003) Isotopic fractionation and turnover in captive Garden Warblers (Sylvia borin): implications for delineating dietary and migratory associations in wild passerines. Can J Zool 81:1630–1635CrossRefGoogle Scholar
  13. Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes II: factors influencing diet-tissue fractionation. Condor 94:189–197CrossRefGoogle Scholar
  14. 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 84:9–18CrossRefGoogle Scholar
  15. 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 52:528–533CrossRefGoogle Scholar
  16. Izhaki I (1993) Influence of nonprotein nitrogen on estimation of protein from total nitrogen in fleshy fruits. J Chem Ecol 19:2605–2615CrossRefGoogle Scholar
  17. Jacoby ME, Hilderbrand GV, Servheen C, Schwartz CC, Arthur SM, Hanley TA, Robbins CT, Michener R (1999) Trophic relations of brown and black bears in several western North American ecosystems. J Wildl Manage 63:921–929CrossRefGoogle Scholar
  18. Jenkins SG, Partridge ST, Stephenson TR, Farley SD, Robbins CT (2001) Nitrogen and carbon isotope fractionation between mothers, neonates, and nursing offspring. Oecologia 129:336–341Google Scholar
  19. Kellems RO, Church DC (2002) Livestock feeds and feeding, 5th edn. Prentice Hall, New JerseyGoogle Scholar
  20. Lesage V, Hammill MO, Kavacs KM (2002) Diet-tissue fractionation of stable carbon and nitrogen isotopes in phocid seals. Mar Mamm Sci 18:182–193CrossRefGoogle Scholar
  21. Lewis LD, Morris ML Jr (1983) Small animal clinical nutrition. Mark Morris Associates, Topeka, KSGoogle Scholar
  22. 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 102:378–390CrossRefGoogle Scholar
  23. McDonald P, Edwards RA, Greenhalgh JFD (1973) Animal nutrition, 2nd edn. Longman, LondonGoogle Scholar
  24. 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 48:1135–1140CrossRefGoogle Scholar
  25. Mitchell HH (1924) Nutritive value of proteins. Physiol Rev 4:424–478Google Scholar
  26. Mitchell HH, Burroughs W, Beadles JR (1936) The significance and accuracy of biological values of proteins computer from nitrogen metabolism data. J Nutr 11:257–274Google Scholar
  27. NAS (1971) Atlas of nutritional data on United States and Canadian feeds. National Academy of Sciences, WashingtonGoogle Scholar
  28. Ogden LJE, Hobson KA, Lank DB (2004) Blood isotopic (δ13C and δ15N) turnover and diet-tissue fractionation factors in captive dunlin (Calidris alpine pacifica). Auk 121:170–177CrossRefGoogle Scholar
  29. Pearson SF, Levey DJ, Greenberg CH, Martinez del Rio C (2003) Effects of elemental composition on the incorporation of dietary nitrogen and carbon isotopic signatures in an omnivorous songbird. Oecologia 135:516–523PubMedGoogle Scholar
  30. Peoples AD, Lochmiller RL, Leslie DM Jr, Boren JC, Engle DM (1994) Essential amino acids in Northern bobwhite foods. J Wildl Manage 58:167–175CrossRefGoogle Scholar
  31. Phillips DL, Koch PL (2002) Incorporating concentration dependence in stable isotope mixing models. Oecologia 130:114–125Google Scholar
  32. Ponsard S, Averbuch P (1999) Should growing and adult animals fed on the same diet show different δ15N values. Rapid Commun Mass Spectrom 13:1305–1310PubMedCrossRefGoogle Scholar
  33. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718CrossRefGoogle Scholar
  34. Pritchard GT, Robbins CT (1990) Digestive and metabolic efficiencies of grizzly and black bears. Can J Zool 68:1645–1651CrossRefGoogle Scholar
  35. Robbins CT (1993) Wildlife feeding and nutrition. Academic, New YorkGoogle Scholar
  36. Robbins CT, Hilderbrand GV, Farley SD (2002) Incorporating concentration dependence in stable isotope mixing models: a response to Phillips and Koch (2002) Oecologia 133:10–13CrossRefGoogle Scholar
  37. Robinson TF, Sponheimer M, Roeder BL, Passey B, Cerling TE, Dearing MD, Ehleringer JR (2005) Digestibility and nitrogen retention in llamas and goats fed alfalfa, C3 grass, and C4 grass hays. Small Rum Res (in press)Google Scholar
  38. 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
  39. SAS Institute Inc (1998) Using StatView. SAS Institute Inc. Cary, NCGoogle Scholar
  40. Sponheimer M, Robinson T, Ayliffe L, Roeder B, Hammer J, Passey B, West A, Cerling T, Dearing D, Ehleringer J (2003a) Nitrogen isotopes in mammalian herbivores: hair δ15N values from a controlled feeding study. Int J Osteoarchaeol 13:80–87CrossRefGoogle Scholar
  41. Sponheimer M, Robinson TF, Roeder BL, Passey BH, Ayliffe LK, Cerling TE, Dearing MD, Ehleringer JR (2003b) An experimental study of nitrogen flux in llamas: is 14N preferentially excreted? J Archaeol Sci 30:1649–1655CrossRefGoogle Scholar
  42. 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
  43. Stirling I, McEwan EH (1975) The caloric value of whole ringed seals (Phoca hispica) in relation to polar bear (Ursus maritimus) ecology and hunting behavior. Can J Zool 53:1021–1027PubMedGoogle Scholar
  44. Van Soest PJ (1994) Nutritional ecology of the ruminant, 2nd edn. Cornell University Press, IthacaGoogle Scholar
  45. Vanderklift MA, Ponsard S (2003) Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136:169–182PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Charles T. Robbins
    • 1
  • Laura A. Felicetti
    • 2
  • Matt Sponheimer
    • 3
  1. 1.Department of Natural Resource Sciences and School of Biological SciencesWashington State UniversityPullmanUSA
  2. 2.Zoological Society of San DiegoSan DiegoUSA
  3. 3.Department of AnthropologyUniversity of Colorado at BoulderBoulderUSA

Personalised recommendations