Oecologia

, Volume 146, Issue 1, pp 148–156 | Cite as

Controlling for anthropogenically induced atmospheric variation in stable carbon isotope studies

  • Eric S. Long
  • Richard A. Sweitzer
  • Duane R. Diefenbach
  • Merav Ben-David
Global Change Ecology

Abstract

Increased use of stable isotope analysis to examine food-web dynamics, migration, transfer of nutrients, and behavior will likely result in expansion of stable isotope studies investigating human-induced global changes. Recent elevation of atmospheric CO2 concentration, related primarily to fossil fuel combustion, has reduced atmospheric CO2 δ13C (13C/12C), and this change in isotopic baseline has, in turn, reduced plant and animal tissue δ13C of terrestrial and aquatic organisms. Such depletion in CO2 δ13C and its effects on tissue δ13C may introduce bias into δ13C investigations, and if this variation is not controlled, may confound interpretation of results obtained from tissue samples collected over a temporal span. To control for this source of variation, we used a high-precision record of atmospheric CO2 δ13C from ice cores and direct atmospheric measurements to model modern change in CO2 δ13C. From this model, we estimated a correction factor that controls for atmospheric change; this correction reduces bias associated with changes in atmospheric isotopic baseline and facilitates comparison of tissue δ13C collected over multiple years. To exemplify the importance of accounting for atmospheric CO2 δ13C depletion, we applied the correction to a dataset of collagen δ13C obtained from mountain lion (Puma concolor) bone samples collected in California between 1893 and 1995. Before correction, in three of four ecoregions collagen δ13C decreased significantly concurrent with depletion of atmospheric CO2 δ13C (n ≥ 32, P ≤ 0.01). Application of the correction to collagen δ13C data removed trends from regions demonstrating significant declines, and measurement error associated with the correction did not add substantial variation to adjusted estimates. Controlling for long-term atmospheric variation and correcting tissue samples for changes in isotopic baseline facilitate analysis of samples that span a large temporal range.

Keywords

13Carbon dioxide Correction factor Isotopic baseline Puma concolor 

References

  1. Arens NC, Jahren AH, Amundson R (2000) Can C3 plants faithfully record the carbon isotopic composition of atmospheric carbon dioxide? Paleobiology 26:137–164CrossRefGoogle Scholar
  2. Barber VA, Juday GP, Finney BP (2000) Reduced growth of Alaskan white spruce in the twentieth century from temperature-induced drought stress. Nature 405:668–672PubMedCrossRefGoogle Scholar
  3. Beier P (1993) Determining minimum habitat areas and habitat corridors for cougars. Cons Biol 7:94–108CrossRefGoogle Scholar
  4. 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
  5. Ben-David M, Bowyer RT, Duffy LK, Roby DD, Schell DM (1998a) Social behavior and ecosystem processes: river otter latrines and nutrient dynamics of terrestrial vegetation. Ecology 79:2567–2571Google Scholar
  6. Ben-David M, Hanley TA, Schell DM (1998b) Fertilization of terrestrial vegetation by spawning Pacific salmon: the role of flooding and predator activity. Oikos 83:47–55CrossRefGoogle Scholar
  7. Ben-David M, Titus K, Beier LR (2004) Consumption of salmon by Alaskan brown bears: a trade-off between nutritional requirements and the risk of infanticide? Oecologia 138:465–474PubMedCrossRefGoogle Scholar
  8. Bergengren JC, Thompson SL, Pollard D, Deconto RM (2001) Modeling global climate-vegetation interactions in a doubled CO2 world. Clim Change 50:31–75CrossRefGoogle Scholar
  9. Böhm F, Joachimski MM, Lehnert H, Morgenroth G, Kretschmer W, Vacelet J, Dullo WC (1996) Carbon isotopes from extant Caribbean and South Pacific sponges: evolution of δ13C in surface water DIC. Earth Planet Sci Lett 139:291-303CrossRefGoogle Scholar
  10. Burton RK, Snodgrass JJ, Gifford-Gonzalez D, Guilderson T, Brown T, Koch PL (2001) Holocene changes in the ecology of northern fur seals: insights from stable isotopes and archaeofauna. Oecologia 128:107–115CrossRefGoogle Scholar
  11. Cabana G, Rasmussen JB (1994) Modeling food-chain structure and contaminant bioaccumulation using stable nitrogen isotopes. Nature 372:255–257CrossRefGoogle Scholar
  12. Cerling TE, Harris JM (1999) Carbon isotope fractionation between diet and bioapatite in ungulate mammals and implications for ecological and paleoecological studies. Oecologia 120: 347–363CrossRefGoogle Scholar
  13. Cerling TE, Harris JM, MacFadden BJ, Leakey MG, Quade J, Eisenmann V, Ehleringer JR (1997) Global vegetation change through the Miocene/Pliocene boundary. Nature 389:153–158CrossRefGoogle Scholar
  14. Cerling TE, Harris JM, MacFadden BJ, Leakey MG, Quade J, Eisenmann V, Ehleringer JR (1998) Miocene/Pliocene shift: one step or several? A reply. Nature 393:127CrossRefGoogle Scholar
  15. DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506CrossRefGoogle Scholar
  16. DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351CrossRefGoogle Scholar
  17. DeNiro MJ, Schoeninger MJ (1983) Stable carbon and nitrogen isotope ratios of bone collagen: variations within individuals, between sexes and within populations raised on monotonous diets. J Arch Sci 10:199–203CrossRefGoogle Scholar
  18. Druffel ERM, Benavides LM (1986) Input of excess CO2 to the surface ocean calculated from stable carbon isotope ratios in a banded Jamaican sclerosponge. Nature 321:58–61CrossRefGoogle Scholar
  19. France RL (1995) Differentiation between littoral and pelagic food webs in lakes using carbon isotopes. Limnol Oceanogr 40:1310–1313CrossRefGoogle Scholar
  20. Francey RJ, Allison CE, Etheridge DM, Trudinger CM, Enting IG, Leuenberger M, Langenfelds RL, Michel E, Steele LP (1999) A 1000-year high precision record of δ13C in atmospheric CO2. Tellus 51B:170–193Google Scholar
  21. Freyer HD (1979) On the 13C record in tree rings. Part I. 13C variations in northern hemispheric trees during the last 150 years. Tellus 31:124–137Google Scholar
  22. Friedli H, Lötscher H, Oeschger H, Siegenthaler U, Stauffer B (1986) Ice core record of the 13C/12C ratio of atmospheric CO2 of the past two centuries. Nature 324:237–238CrossRefGoogle Scholar
  23. Hafner MS, Gannon WL, Salazar-Bravo J, Alvarez-Casteñeda ST (1997) Mammal collections in the Western Hemisphere: a survey and directory of existing collections. American Society of Mammalogists, Lawrence, KSGoogle Scholar
  24. Hibbard KA, Archer S, Schimel DS, Valentine DW (2001) Biogeochemical changes accompanying woody plant encroachment in a subtropical savanna. Ecology 82:1999–2011Google Scholar
  25. Hickman JC (1993) The Jepson manual: higher plants of California. University of California Press, Berkeley, CAGoogle Scholar
  26. Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120:314–326CrossRefGoogle Scholar
  27. Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor 94:181–188CrossRefGoogle Scholar
  28. Iacumin P, Bocherens H, Delgado Huertes A, Mariotti A, Longinelli A (1997) A stable isotope study of fossil mammal remains from the Paglicci cave, Southern Italy. N and C as palaeoenvironmental indicators. Earth Planet Sci Lett 148:349–357CrossRefGoogle Scholar
  29. Iacumin P, Nikolaev V, Ramigni M (2000) C and N stable isotope measurements on Eurasian fossil mammals, 40,000 to 10,000 years BP: herbivore physiologies and palaeoenvironmental reconstruction. Palaeogeog Palaeoclim Palaeoecol 163:33–47CrossRefGoogle Scholar
  30. Keeling CD, Mook WG, Tans PP (1979) Recent trends in the 13C/12C ratio of atmospheric carbon dioxide. Nature 277:121–123CrossRefGoogle Scholar
  31. Keeling CD, Bacastow RB, Carter AF, Piper SC, Whorf TP, Heimann M, Mook WG, Roeloffzer H (1989) A three-dimensional model of atmospheric CO2 transport based on observed winds: 1. In: Peterson DH (ed) Analysis of observational data. American Geophysical Monograph No. 55. American Geophysical Union, Washington, DC, pp 165–236Google Scholar
  32. Kelly JF (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can J Zool 78:1–27CrossRefGoogle Scholar
  33. Kling GW, Fry B, Obrien WJ (1992) Stable isotopes and planktonic trophic structure in arctic lakes. Ecology 73:561–566CrossRefGoogle Scholar
  34. Kritzberg ES, Cole JJ, Pace ML, Granéli W, Bade DL (2004) Autochthonous versus allochthonous carbon sources of bacteria: results from whole-lake 13C addition experiments. Limnol Oceanogr 49:588–596Google Scholar
  35. Libby WF, Berger R, Mead JF, Alexander GV, Ross JF (1964) Replacement rates for human tissue from atmospheric radiocarbon. Science 146:1170–1172PubMedCrossRefGoogle Scholar
  36. Lipp J, Trimborn P, Fritz P, Moser H, Becker B, Frenzel B (1991) Stable isotopes in tree ring cellulose and climate change. Tellus 43B:322–330CrossRefGoogle Scholar
  37. Long ES (2001) Response of mountain lions to a changing prey base in California. Masters thesis, University of North DakotaGoogle Scholar
  38. Long ES, Sweitzer RA (2001) Museum collection records of mountain lions in California. Calif Fish Game 87:153–167Google Scholar
  39. Marino BD, McElroy MB (1991) Isotopic composition of atmospheric CO2 inferred from carbon in C4 plant cellulose. Nature 349:127–131CrossRefGoogle Scholar
  40. Matheus PE (1997) Paleoecology and ecomorphology of the giant short-faced bear in eastern Beringia. Ph.D. dissertation, University of Alaska FairbanksGoogle Scholar
  41. Mazany T, Lerman JC, Long A (1980) Carbon-13 in tree-ring cellulose as an indicator of past climates. Nature 287:432–435CrossRefGoogle Scholar
  42. McConnaughey TA, Burdett J, Whelan JF, Paull CK (1997) Carbon isotopes in biological carbonates: respiration and photosynthesis. Geochim Cosmochim Acta 61:611–612CrossRefGoogle Scholar
  43. Moens T, Luyten C, Middelburg JJ, Herman PMJ, Vincx M (2002) Tracing organic matter sources of estuarine tidal flat nematodes with stable carbon isotopes. Mar Ecol Prog Ser 234:127–137CrossRefGoogle Scholar
  44. Nozaki Y, Rye DM, Turekian KK, Dodge RE (1978) A 200 year record of carbon-13 and carbon-14 variations in a Bermuda coral. Geophys Res Lett 5:825–828CrossRefGoogle Scholar
  45. O’Leary MH (1981) Carbon isotope fractionation in plants. Phytochemistry 20:553–567CrossRefGoogle Scholar
  46. Osmond CB, Valaane N, Haslam SM, Uotila P, Roksandic Z (1981) Comparison of δ13C values in leaves of aquatic macrophytes from different habitats in Britain and Finland: some implications for photosynthetic processes in aquatic plants. Oecologia 50:117–124CrossRefGoogle Scholar
  47. Pace ML, Cole JJ, Carepenter SR, Kitchell JF, Hodgson JR, Van de Bogert MC, Bade DL, Kritzberg ES, Bastviken D (2004) Whole-lake carbon-13 additions reveal terrestrial support of aquatic food webs. Nature 427:240–242PubMedCrossRefGoogle Scholar
  48. Petchy OL, McPhearson PT, Casey TM, Morin PJ (1999) Environmental warming alters food-web structure and ecosystem function. Nature 402:69–72CrossRefGoogle Scholar
  49. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320CrossRefGoogle Scholar
  50. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718CrossRefGoogle Scholar
  51. Post DM (2003) Individual variation in the timing of ontogenetic niche shifts in largemouth bass. Ecology 84:1298–1310CrossRefGoogle Scholar
  52. Post E, Peterson RO, Steneth NC, McLaren BE (1999) Ecosystem consequences of wolf behavioral response to climate. Nature 401:905–907CrossRefGoogle Scholar
  53. Richards MP, Hedges REM (2003) Variations in bone collagen δ13C and δ15N values of fauna from Northwest Europe over the last 40,000 years. Palaeogeog Palaeoclim Palaeoecol 193:261–267CrossRefGoogle Scholar
  54. Richards MP, Mays S, Fuller BT (2002) Stable carbon and nitrogen isotope values of bone and teeth reflect weaning age at the medieval Wharram Percy site, Yorkshire, UK. Am J Phys Anthropol 119:205–210PubMedCrossRefGoogle Scholar
  55. Seber GAF (1982) The estimation of animal abundance and related parameters, 2nd edn. Macmillan, New YorkGoogle Scholar
  56. Stuiver M, Braziunas TF (1987) Tree cellulose 13C/12C isotope ratios and climate change. Nature 328:58–60CrossRefGoogle Scholar
  57. Stuiver M, Burk RL, Quay PD (1984) 13C/12C ratios in tree rings and the transfer of biospheric carbon to the atmosphere. J Geophys Res 89:11731–1174CrossRefGoogle Scholar
  58. Sukumar R, Ramash R (1992) Stable carbon isotope ratios in Asian elephant collagen: implications for dietary studies. Oecologia 91:536–539CrossRefGoogle Scholar
  59. Tieszen LL, Boutton TW (1989) Stable carbon isotopes in terrestrial ecosystem research. In: Rundel PW, Ehleringer JR, Nagy KA (eds) Stable isotopes in ecological research. Springer, Berlin Heidelberg New York, pp167–195Google Scholar
  60. Vander Zanden MJ, Cabana G, Rasmussen JB (1997) Comparing trophic position of freshwater fish calculated using stable nitrogen isotope ratios (δ15N) and literature dietary data. Can J Fish Aquat Sci 54:1142–1158CrossRefGoogle Scholar
  61. Vander Zanden MJ, Casselman JM, Rasmussen JB (1999) Stable isotope evidence for the food web consequences of species invasions in lakes. Nature 401:464–467CrossRefGoogle Scholar
  62. White JW, Ciaias P, Figge RA, Kenny R, Markgraf V (1994) A high resolution record of atmospheric CO2 content from carbon isotopes in peat. Nature 367:153–156CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Eric S. Long
    • 1
  • Richard A. Sweitzer
    • 1
  • Duane R. Diefenbach
    • 2
  • Merav Ben-David
    • 3
  1. 1.Department of BiologyUniversity of North DakotaGrand ForksUSA
  2. 2.U.S. Geological Survey, Pennsylvania Cooperative Fish and Wildlife Research UnitThe Pennsylvania State UniversityUniversity ParkUSA
  3. 3.Department of Physiology and ZoologyUniversity of WyomingWYUSA

Personalised recommendations