792
Views
72
CrossRef citations to date
0
Altmetric
Stable Isotopes in Mammals

The effects of sex, tissue type, and dietary components on stable isotope discrimination factors (Δ13C and Δ15N) in mammalian omnivoresFootnote

, , &
Pages 307-321 | Received 05 Sep 2013, Accepted 06 Feb 2014, Published online: 30 Apr 2014

References

  • Ben-David M, Flaherty E. Stable isotopes in mammalian research: a beginner's guide. J Mammal. 2012;93:312–328. doi: 10.1644/11-MAMM-S-166.1
  • Martínez del Rio C, Wolf N, Carleton S, Gannes LZ. Isotopic ecology ten years after a call for more laboratory experiments. Biol Rev Camb Philos Soc. 2009;84:91–111. doi: 10.1111/j.1469-185X.2008.00064.x
  • Kurle CM. 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. 2002;80:902–909. doi: 10.1139/z02-069
  • Pearson S, Levey D, Greenberg C, Martínez del Rio C. Effects of elemental composition on the incorporation of dietary nitrogen and carbon isotopic signatures in an omnivorous songbird. Oecologia. 2003;135:516–523.
  • Vanderklift MA, Ponsard S. Sources of variation in consumer–diet δ15N enrichment: a meta-analysis. Oecologia. 2003;136:169–182. doi: 10.1007/s00442-003-1270-z
  • Robbins CT, Felicetti L, Florin S. The impact of protein quality on stable nitrogen isotope ratio discrimination and assimilated diet estimation. Oecologia. 2010;162:571–579. doi: 10.1007/s00442-009-1485-8
  • Parng E, Crumpacker A, Kurle CM. Variation in the stable carbon and nitrogen isotope discrimination factors from diet to fur in four felid species held on different diets. J Mammal. 2014;95:151–159. doi: 10.1644/13-MAMM-A-014.1
  • Poupin N, Box C, Mariotti F, Huneau J, Tome D, Fouillet H. The nature of the dietary protein impacts the tissue-to-diet 15N discrimination factors in laboratory rats. PLOS One. 2011;6:e28046.
  • Robbins CT, Felicetti L, Sponheimer M. The effect of dietary protein quality on nitrogen isotope discrimination in mmmals and birds. Oecologia. 2005;144:534–540. doi: 10.1007/s00442-005-0021-8
  • Bearhop S, Waldron S, Votier S, Furness R. Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers. Physiol Biochem Zool. 2002;75:451–458. doi: 10.1086/342800
  • Bond A, Diamond A. Recent Bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors. Ecol Appl. 2011;21:1017–1023. doi: 10.1890/09-2409.1
  • Phillips D. Converting isotope values to diet composistion – the use of mixing models. J Mammal. 2012;93:342–352. doi: 10.1644/11-MAMM-S-158.1
  • Caut S, Angulo E, Courchamp F. Discrimination factors (Δ15N and Δ13C) in an omnivorous consumer: effect of diet isotopic ratio. Funct Ecol. 2008;22:255–263. doi: 10.1111/j.1365-2435.2007.01360.x
  • Felicetti L, Schwartz C, Rye R, Harlodson M, Gunther K, Phillips D, Robbins C. Use of sulfur and nitrogen stable isotopes to determine the importance of whitebark pine nuts to Yellowstone grizzly bears. Can J Zool. 2003;81: 763–770. doi: 10.1139/z03-054
  • Hildebrand GV, Farley SD, Robbins CT, Hanley TA, Titus K, Servheen C. Use of stable isotopes to determine diets of living and extinct bears. Can J Zool. 1996;74:2080–2088. doi: 10.1139/z96-236
  • Caut S, Angulo E, Courchamp F. Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol. 2009;46:443–453. doi: 10.1111/j.1365-2664.2009.01620.x
  • Perga M, Grey J. Laboratory measures of isotope discrimination factors: comments on Caut, Angulo, and Courchamp. J Appl Ecol. 2010;47:942–947. doi: 10.1111/j.1365-2664.2009.01730.x
  • Auerswald K, Wittmer M, Zazzo A, Schaufele R, Schnyder H. Biases in the analysis of stable isotope discrimination in food webs. J Appl Ecol. 2010;47:936–941. doi: 10.1111/j.1365-2664.2009.01764.x
  • Focken U. 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. 2001;37:199–211. doi: 10.1080/10256010108033296
  • Koch PL. Isotopic study of the biology of modern and fossil vertebrates. In: Michener R, Lajtha K, editors. Stable isotopes in ecology and environmental science. 2nd ed. Boston: Blackwell Publishing; 2007. p. 99–154.
  • Macko S, Fogel Estep M, Engel M, Hare P. Kinetic fractionation of stable nitrogen isotopes during amino acid transamination. Geochim Cosmochim Acta. 1986;50:2143–2146. doi: 10.1016/0016-7037(86)90068-2
  • McCutchan J, Lewis W, Kendall C, McGrath C. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos. 2003;102:378–390. doi: 10.1034/j.1600-0706.2003.12098.x
  • Sponheimer M, Robinson T, Roeder B, Passey B, Ayliffe L, Cerling T, Dearing M, Ehleringer J. An experimental study of nitrogen flux in llamas: is 14N preferentially excreted? J Archaeol Sci. 2003;30:1649–1655. doi: 10.1016/S0305-4403(03)00066-9
  • Roth J, Hobson KA. Stable carbon and nitrogen isotopic fractionation between diet and tissue of captive red fox: implications for dietary reconstruction. Can J Zool. 2000;78:848–852. doi: 10.1139/z00-008
  • Hobson KA, Clark RG. Assessing avian diets using stable isotopes II. Factors influenceing diet–tissue fractionation. Condor. 1992;94:181–188. doi: 10.2307/1368807
  • DeNiro MJ, Epstein S. Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta. 1978;42:495–506. doi: 10.1016/0016-7037(78)90199-0
  • Dobush G, Ankney C, Krementz D. The effect of apparatus, extraction time, and solvent type on lipid extractions of snow geese. Can J Zool. 1985;63:1917–1920. doi: 10.1139/z85-285
  • Doucette J, Wissel B, Somers C. Effects of lipid extraction and lipid normalization on stable carbon and nitrogen isotope ratios in double-crested cormorants: implications for food web studies. Waterbirds. 2010;33:273–284. doi: 10.1675/063.033.0302
  • Kurle CM, Sinclair E, Edwards A, Gudmundson C. Temporal and spatial variation in the δ15N and δ13C values of fish and squid from Alaskan waters. Mar Biol. 2011;158:2389–2404. doi: 10.1007/s00227-011-1741-4
  • Arneson L, MacAvoy S. Carbon, nitrogen, and sulfur diet–tissue discrimination in mouse tissues. Can J Zool. 2005;83:989–995. doi: 10.1139/z05-083
  • MacAvoy S, Macko S, Arneson L. Growth versus metabolic tissue replacement in mouse tissues determined by stable carbon and nitrogen isotope analysis. Can J Zool. 2005;83:631–641. doi: 10.1139/z05-038
  • Tieszen LL, Fagre T. Effect of diet quality and composition on the isotopic composition of respiratory CO2, bone collagen, bioapatite, and soft tissues. In: Lambert J, Grupe G, editors. Prehistoric human bone: archaeology at the molecular level. Berlin: Springer Verlag; 1993. p. 121–155.
  • Ambrose SH, Norr L. Carbon isotopic evidence for routing of dietary protein to bone collagen, and whole diet to bone apatite carbonate: purified diet growth experiments. In: Lambert J, Grupe G, editors. Molecular archaeology of prehistoric human bone. Berlin: Springer; 1993. p. 1–37.
  • Vander Zanden MJ, Rasmussen J. Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnol Oceanogr. 2001;46:2061–2066. doi: 10.4319/lo.2001.46.8.2061
  • MacAvoy S, Arneson L, Bassett E. Correlation of metabolism with tissue carbon and nitrogen turnover rate in small mammals. Oecologia. 2006;150:190–201. doi: 10.1007/s00442-006-0522-0
  • Bodwell C, Satterlee L, Hackler L. Protein digestibility of the same protein preparations by human and rat assays and by in vitro enzymic digestion methods. Am J Clin Nutr. 1980;33:677–686.
  • Sarwar G, Peace R, Botting H, Brule D. Digestibility of protein and amino acids in selected foods as determined by a rat balance method. Plant Foods Hum Nutr. 1989;39:23–32. doi: 10.1007/BF01092398
  • Lecomte N, Ahlstrom O, Ehrich D, Fuglei E, Ims R, Yoccoz N. Intrapopulation variability shaping isotope discrimination and turnover: experimental evidence in arctic foxes. PLOS One. 2011;6:1–10. doi: 10.1371/journal.pone.0021357
  • Miller J, Millar J, Longstaffe F. Carbon- and nitrogen-isotope tissue–diet discrimination and turnover rates in deer mice, Peromyscus maniculatus. Can J Zool. 2008;86:685–691.
  • Fuller B, Fuller J, Sage N, Harris D, O'Connell T, Hedges R. Nitrogen balance and δ15N: why you're not what you eat during pregnancy. Rapid Commun Mass Spectrom. 2004;18:2889–2896. doi: 10.1002/rcm.1708
  • Awkerman J, Hobson KA, Anderson D. Isotopic (δ15N and δ13C) evidence for intersexual foraging differences and temporal variation in habitat use in waved albatrosses. Can J Zool. 2007;85:273–279. doi: 10.1139/z06-202
  • Kurle CM, Worthy GAJ. Stable isotope assessment of temporal and geographic differences in feeding ecology of northern fur seals (Callorhinus ursinus) and their prey. Oecologia. 2001;126:254–265. doi: 10.1007/s004420000518
  • Tieszen L, Boutton T, Tesdahl K, Slade N. Fractionation and turnover of stable carbon isotopes in animal tissues: implications for 13C analysis of diet. Oecologia. 1983;57:32–37. doi: 10.1007/BF00379558
  • Kurle CM, Finkelstein M, Smith K, George D, Ciani D, Koch P, Smith P. Discrimination factors for stable isotopes of carbon and nitrogen in blood and feathers from chicks and juveniles of the California condor. Condor. 2013;115: 492–500. doi: 10.1525/cond.2013.120107
  • Dale J, Wallsgrove N, Popp B, Holland K. Nursery habitat use and foraging ecology of the brown stingray Dasyatis lata determined from stomach contents, bulk and amino acid stable isotopes. Mar Ecol Prog Ser. 2011;433:221–236. doi: 10.3354/meps09171
  • Lorrain A, Graham B, Menard F, Popp B, Bouillon S, van Breugel P, Cherel Y. Nitrogen and carbon isotope values of individual amino acids: a tool to study foraging ecology of penguins in the Southern Ocean. Mar Ecol Prog Ser. 2009;391:293–306. doi: 10.3354/meps08215
  • Popp B, Graham B, Olson R, Hannides C, Lott M, Lopez-Ibara G, Galvan-Magana F, Fry B. Insight into the trophic ecology of yellowfin tuna, Thunnus albacares, from compound-specific nitrogen isotope analysis of protenaceous amino acids. In: Dawson T, Siegwolf R, editors. Stable isotopes as indicators of ecological change. New York, NY: Elsevier Academic Press; 2007. p. 173–190.
  • Hobson K, Welch H. Determination of trophic relationships within a high Arctic marine food web using δ13C and δ15N analysis. Mar Ecol Prog Ser. 1992;84:9–18. doi: 10.3354/meps084009
  • Kelly JF. Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can J Zool. 2000;78:1–27. doi: 10.1139/z99-165
  • Kurle CM. Interpreting temporal variation in omnivore foraging ecology via stable isotope modeling. Funct Ecol. 2009;23:733–744. doi: 10.1111/j.1365-2435.2009.01553.x
  • Federer R, Hollmen T, Esler D, Wooller M, Wang S. Stable carbon and nitrogen isotope discrimination factors from diet to blood plasma, cellular blood, feathers, and adipose tissue fatty acids in Spectacled Eiders (Somateria fisheri). Can J Zool. 2010;88:866–874. doi: 10.1139/Z10-052
  • Hobson KA, Schell D, Renouf D, Noseworthy E. 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. 1996;53:528–533. doi: 10.1139/f95-209
  • Newsome S, Bentall G, Tinker M, LOftedal O, Ralls K, Estes J, Fogel M. Variation in d13C and d15N diet–vibrissae trophic discrimination factors in a wild population of California sea otters. Ecol Appl. 2010;20:1744–1752. doi: 10.1890/09-1502.1
  • Marshall R, Orwin D, Gillespie J. Structure and biochemistry of mammalian hard keratin. Electron Microsc Rev. 1991;4:47–83. doi: 10.1016/0892-0354(91)90016-6
  • Howland M, Corr L, Young S, Jones V, Jim S, Van Der Merwe N, Mitchell A, Evershed R. Expression of the dietary isotope signal in the compound-specific δ13C values of pig bone lipids and amino acids. Int J Osteoarchaeol. 2003;13:54–65. doi: 10.1002/oa.658
  • Jim S, Jones V, Ambrose SH, Evershed R. Quantifying dietary macronutrient sources of carbon for bone collagen biosynthesis using natural abundance stable carbon isotope analysis. Br J Nutr. 2006;95:1055–1062. doi: 10.1079/BJN20051685
  • Jacques H, Deshaies Y, Savoie L. Relationship between dietary proteins, their in vitro digestion products, and serum cholesterol in rats. Artherosclerosis. 1986;61:89–98. doi: 10.1016/0021-9150(86)90067-5
  • Waterlow J, Garlick P, Millward D. Protein turnover in mammalian tissues and in the whole body. Amsterdam: Elsevier/North-Holland Biomedical Press; 1978.
  • Ayliffe L, Cerling T, Robinson T, West A, Sponheimer M, Passey B, Hammer J, Roeder B, Dearing M, Ehleringer JR. Turnover of carbon isotopes in tail hair and breath CO2 of horses fed an isotopically varied diet. Oecologia. 2004;139:11–22. doi: 10.1007/s00442-003-1479-x
  • Smith J, Millar J, Longstaffe F, Boonstra R. The effect of metabolic rate on stable carbon and nitrogen isotope compositions in deer mice, Peromyscus maniculatus. Can J Zool. 2010;88:36–42. doi: 10.1139/Z09-116
  • Kojadinovic J, Richard P, Le Corre M, Cosson P, Bustamante P. Effects of lipid extraction on δ13C and δ15N values in seabird muscle, liver and feathers. Waterbirds. 2008;31:169–178. doi: 10.1675/1524-4695(2008)31[169:EOLEOC]2.0.CO;2
  • Post D, Layman C, Arrignton D, Takimoto G, Quattrochi J, Montana C. Getting to the fat of the matter: models, methods and assumptions for dealing with liipids in stable isotope analyses. Oecologia. 2007;152:179–189. doi: 10.1007/s00442-006-0630-x

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.