Oecologia

, Volume 162, Issue 3, pp 571–579 | Cite as

The impact of protein quality on stable nitrogen isotope ratio discrimination and assimilated diet estimation

  • Charles T. Robbins
  • Laura A. Felicetti
  • Scott T. Florin
Physiological ecology - Original Paper

Abstract

Accurately predicting isotopic discrimination is central to estimating assimilated diets of wild animals when using stable isotopes. Current mixing models assume that the stable N isotope ratio (δ15N) discrimination (∆15N) for each food in a mixed diet is constant and independent of other foods being consumed. Thus, the discrimination value for the mixed diet is the combined, weighted average for each food when consumed as the sole diet. However, if protein quality is a major determinant of ∆15N, discrimination values for mixed diets may be higher or lower than the weighted average and will reflect the protein quality of the entire diet and not that of the individual foods. This potential difference occurs because the protein quality of a mixed diet depends on whether, and to what extent, the profiles and amounts of essential amino acids in the individual foods are complementary or non-complementary to each other in meeting the animal’s requirement. We tested these ideas by determining the ∆15N of several common foods (corn, wheat, alfalfa, soybean, and fish meal) with known amino acid profiles when fed singly and in combination to laboratory rats. Discrimination values for the mixed diets often differed from the weighted averages for the individual foods and depended on the degree of complementation. ∆15N for mixed diets ranged from 1.1‰ lower than the weighted average for foods with complementary amino acid profiles to 0.4‰ higher for foods with non-complementary amino acid profiles. These differences led to underestimates as high as 44% and overestimates as high as 36% of the relative proportions of fish meal and soybean meal N, respectively, in the assimilated mixed diets. We conclude that using isotopes to estimate assimilated diets is more complex than often appreciated and will require developing more biologically based, time-sensitive models.

Keywords

Assimilated diet Isotope discrimination Nitrogen Protein quality Stable isotopes 

References

  1. Arneson LS, MacAvoy SE (2005) Carbon, nitrogen, and sulfur diet-tissue discrimination in mouse tissues. Can J Zool 83:989–995CrossRefGoogle 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 Bochem Zool 75:451–458CrossRefGoogle 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. Caut S, Angulo E, Courchamp F (2008a) Discrimination factors (∆15N and ∆13C) in an omnivorous consumer: effect of diet isotopic ratio. Funct Ecol 22:255–263CrossRefGoogle Scholar
  5. Caut S, Angulo E, Courchamp F (2008b) Caution on isotopic model use for analyses of consumer diet. Can J Zool 86:438–445CrossRefGoogle Scholar
  6. Cherel Y, Hobson KA, Hassani S (2005) Isotopic discrimination between food and blood and feathers of captive penguins: implications for dietary studies in the wild. Physiol Biochem Zool 78:106–115CrossRefPubMedGoogle Scholar
  7. Crawford K, Mcdonald RA, Bearhop S (2008) Applications of stable isotopes to the ecology of mammals. Mamm Rev 38:87–107CrossRefGoogle Scholar
  8. Darr RL, Hewitt DG (2008) Stable isotope trophic shifts in white-tailed deer. J Wildl Manage 72:1525–1531Google Scholar
  9. DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351CrossRefGoogle Scholar
  10. Elangovan A, Shim KF (2000) The influence of replacing fish meal partially in the diet with soybean meal on growth and body composition of juvenile tin foil barb (Barbodes altus). Aquaculture 189:133–144CrossRefGoogle Scholar
  11. 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
  12. Felicetti LA, Schwartz CC, Rye RO, Haroldson MA, Gunther KA, Phillips DL, Robbins CT (2003) 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
  13. Gaye-Siessegger J, Focken U, Muetzel S, Abel H, Becker K (2004) Feeding level and metabolic rate affect δ13C and δ15N values in carp: implications for food web studies. Oecologia 138:175–183CrossRefPubMedGoogle Scholar
  14. Gaye-Siessegger J, Focken U, Abel H, Becker K (2007) Starvation and low feeding levels result in an enrichment of C-13 in lipids and N-15 in protein of Nile tilapia Oreochromis niloticus L. J Fish Biol 71:90–100CrossRefGoogle Scholar
  15. Haramis GM, Jorde DG, Macko SA, Walker JL (2001) Stable-isotope analysis of canvasback winter diet in Upper Chesapeake Bay. Auk 118:1008–1017CrossRefGoogle Scholar
  16. 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
  17. Hobson KA, Clark RG (1992a) Assessing avian diets using stable isotopes. II. Factors influencing diet-tissue fractionation. Condor 94:189–197CrossRefGoogle Scholar
  18. Hobson KA, Clark RG (1992b) Turnover of 13C in cellular and plasma fractions of blood: implications for nondestructive sampling in avian dietary studies. Auk 110:638–641Google Scholar
  19. 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
  20. Hobson KA, Schell DM, Renouf D, Noseworthy E (1996) Stable carbon and nitrogen isotopic fractionation between diet and tissues of captive seals: implication for dietary reconstructions involving marine mammals. Can J Fish Aquat Sci 52:528–533CrossRefGoogle Scholar
  21. 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
  22. Klasing KC (1998) Comparative avian nutrition. CAB International, New YorkGoogle Scholar
  23. Kleinbaum DG, Kupper LL (1978) Applied regression analysis and other multivariable methods. Duxbury Press, MassachusettsGoogle Scholar
  24. Lesage V, Hammill MO, Kovacs KM (2002) Diet-tissue fractionation of stable carbon and nitrogen isotopes in phocid seals. Mar Mamm Sci 18:182–193CrossRefGoogle Scholar
  25. Lewis LD, Morris ML Jr (1983) Small animal clinical nutrition. Morris, TopekaGoogle Scholar
  26. Martinez del Rio C, Wolf N, Carleton SA, Gannes LZ (2009) Isotopic ecology ten years after a call for more laboratory experiments. Biol Rev 84:91–111CrossRefGoogle Scholar
  27. Miron MLL, Herrera MLG, Ramirez PN, Hobson KA (2006) Effect of diet quality on carbon and nitrogen turnover and isotopic discrimination in blood of a New World nectarivorous bat. J Exp Biol 209:541–548CrossRefGoogle Scholar
  28. Mitchell HH (1924) Nutritive value of proteins. Physiol Rev 4:424–478Google Scholar
  29. Murphy ME, Pearcy SD (1993) Dietary amino acid complementation as a foraging strategy for wild birds. Physiol Behav 53:689–698CrossRefPubMedGoogle Scholar
  30. National Research Council (NRC) (1994) Nutrient requirements of poultry. National Academy of Sciences, Washington, DCGoogle Scholar
  31. National Research Council (NRC) (1995) Nutrient requirements of laboratory animals. National Academy of Sciences, Washington, DCGoogle Scholar
  32. 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
  33. 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
  34. Phillips DL (2001) Mixing models in analyses of diet using multiple stable isotopes: a critique. Oecologia 127:166–170CrossRefGoogle Scholar
  35. Phillips DL, Gregg JW (2001) Uncertainty in source partitioning using stable isotopes. Oecologia 127:171–179CrossRefGoogle Scholar
  36. Phillips DL, Koch PL (2002) Incorporating concentration dependence in stable isotope mixing models. Oecologia 130:114–125Google Scholar
  37. Robbins CT (1993) Wildlife feeding and nutrition. Academic Press, New YorkGoogle Scholar
  38. Robbins CT, Hanley TA, Hagerman AE, Hjeljord O, Baker DL, Schwartz CC, Mautz WW (1987) Role of tannins in defending plants against ruminants: reduction in protein availability. Ecology 68:98–107CrossRefGoogle Scholar
  39. Robbins CT, Felicetti LA, Sponheimer M (2005) The effect of dietary protein quality on nitrogen isotope discrimination in mammals and birds. Oecologia 144:534–540CrossRefPubMedGoogle Scholar
  40. Robbins CT, Fortin JK, Rode KD, Farley SD, Shipley LA, Felicetti LA (2007) Optimizing protein intake as a foraging strategy to maximize mass gain in an omnivore. Oikos 116:1675–1682CrossRefGoogle Scholar
  41. Roth JD, Hobson KA (2000) Stable carbon and nitrogen isotopic fractionation between diet and tissue of captive red fox: implications for dietary consideration. Can J Zool 78:848–852CrossRefGoogle Scholar
  42. SAS (1998) SAS/STAT user’s guide, version 6.12. SAS Institute, CaryGoogle Scholar
  43. Simpson SJ, Sibly RM, Lee KP, Behmer ST, Raubenheimer D (2004) Optimal foraging when relating intake of multiple nutrients. Anim Behav 68:1299–1311CrossRefGoogle Scholar
  44. Sponheimer M, Robinson T, Ayliffe L, Roeder B, Hammer J, Passey B, West A, Cerling T, Dearing D, Ehleringer J (2003) Nitrogen isotopes in mammalian herbivores: hair δ15N values from a controlled feeding study. Int J Osteoarchaeol 13:80–87CrossRefGoogle Scholar
  45. 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 90:7–9CrossRefGoogle Scholar
  46. Thompson DR, Bury SJ, Hobson KA, Wassenaar LI, Shannon JP (2005) Stable isotopes in ecological studies. Oecologia 144:517–519CrossRefPubMedGoogle Scholar
  47. Tsahar E, Wolf N, Izhaki I, Arad Z, Martinez del Rio C (2008) Dietary protein influences the rate of 15N incorporation in blood cells and plasma of yellow-vented bulbuls (Pycnonotus xanthopygos). J Exp Biol 211:459–465CrossRefPubMedGoogle Scholar
  48. Van Soest PJ (1994) Nutritional ecology of the ruminant. Cornell University Press, IthacaGoogle Scholar
  49. Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice-Hall, New JerseyGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Charles T. Robbins
    • 1
  • Laura A. Felicetti
    • 1
  • Scott T. Florin
    • 2
  1. 1.Department of Natural Resource Sciences and School of Biological SciencesWashington State UniversityPullmanUSA
  2. 2.School of Biological SciencesWashington State UniversityPullmanUSA

Personalised recommendations