Ecological Research

, Volume 28, Issue 5, pp 759–769 | Cite as

Use of carbon-13 and carbon-14 natural abundances for stream food web studies

Special Feature Trends in isotope ecology

Abstract

We review the use of stable carbon isotope ratios (δ13C) and radiocarbon natural abundances (Δ14C) for stream food web studies. The δ13C value of primary producers (e.g., periphytic algae, hereafter periphyton) in streams is controlled by isotopic fractionation during photosynthesis and variable δ13C of dissolved CO2. When periphyton δ13C differs from that of terrestrial primary producers, the relative contribution of autochthony and allochthony to stream food webs can be calculated. Moreover, the variation in periphyton δ13C can reveal how much stream consumers rely on local resources because each stream habitat (e.g., riffle vs. pool, open vs. shaded) usually has a distinctive δ13C. However, periphyton δ13C often overlaps with that of terrestrial organic matter. On the other hand, periphyton Δ14C is less variable than δ13C among habitats, and reflects the Δ14C of dissolved CO2, which could be a mixture of “aged” (Δ14C < 0 ‰) and “modern” (Δ14C > 0 ‰) carbon. This is because the Δ14C is corrected by its δ13C value for the isotopic fractionation during photosynthesis. Recent studies and our data indicate that many stream food webs are supported by “aged” carbon derived from the watershed via autochthonous production. The combined use of δ13C and Δ14C allows robust estimation of the carbon transfer pathway in a stream food web at multiple spatial scales ranging from the stream habitat level (e.g., riffle and pool) to watershed level (autochthony and allochthony). Furthermore, the Δ14C of stream food webs will expand our understanding about the time frame of carbon cycles in the watersheds.

Keywords

Periphyton Terrestrial litter Aquatic consumer Carbon stable isotope Radiocarbon 

Notes

Acknowledgments

The authors thank Dr. A. Kohzu for sampling the goby. We are grateful to two anonymous reviewers whose comments greatly improved the manuscript. This research was supported by a Grant-in-Aid for Scientific Research (B) (No. 22370011) from the Ministry of Education, Culture, Sports, Science and Technology, Japan. This research was partially funded by the River Fund in charge of the Foundation of River and Watershed Environment Management (FOREM), Japan. Partial support was also provided by Special Coordination Funds for Promoting Science and Technology and the Environment Research and Technology Development Fund (D-1102) of the Ministry of the Environment, Japan, and the Research Project 3-1 of the Research Institute for Humanity and Nature.

References

  1. Allan JD, Castillo MM (2007) Stream ecology: structure and function of running waters, 2nd edn. Springer, Berlin Heidelberg New YorkCrossRefGoogle Scholar
  2. Briones MJI, Ineson P (2002) Use of 14C carbon dating to determine feeding behaviour of enchytraeids. Soil Biol Biochem 34:881–884. doi: 10.1016/S0038-0717(02)00010-X CrossRefGoogle Scholar
  3. Broecker WS, Peng TH (1994) Stratospheric contribution to the global bomb radiocarbon inventory: model versus observation. Glob Biogeochem Cycle 8:377–384. doi: 10.1029/94GB00680 CrossRefGoogle Scholar
  4. Bunn SE, Davies PM, Winning M (2003) Sources of organic carbon supporting the food web of an arid zone floodplain river. Freshw Biol 48:619–635. doi: 10.1046/j.1365-2427.2003.01031.x CrossRefGoogle Scholar
  5. Caraco N, Bauer JE, Cole JJ, Petsch S, Raymond P (2010) Millennial-aged organic carbon subsidies to a modern river food web. Ecology 91:2385–2393. doi: 10.1890/09-0330.1 CrossRefPubMedGoogle Scholar
  6. Cummins KW (1973) Trophic relations of aquatic insects. Annu Rev Entomol 18:183–206. doi: 10.1146/annurev.en.18.010173.001151 CrossRefGoogle Scholar
  7. Cummins KW, Klug MJ (1979) Feeding ecology of stream invertebrates. Ann Rev Ecol Syst 10:147–172. doi: 10.1146/annurev.es.10.110179.001051 CrossRefGoogle Scholar
  8. Deines P (1980) The isotopic composition of reduced organic carbon. In: Fritz P, Fontes JC (eds) Handbook of environmental isotope geochemistry. The terrestrial environment, A, vol. 1. Elsevier, Amsterdam, pp 329–406Google Scholar
  9. Dekar MP, Magoulick DD, Huxel GR (2009) Shifts in the trophic base of intermittent stream food webs. Hydrobiologia 635:263–277. doi: 10.1007/s10750-009-9919-1 CrossRefGoogle Scholar
  10. Doi H, Takemon Y, Ohta T, Ishida Y, Kikuchi E (2007) Effects of reach-scale canopy cover on trophic pathways of caddisfly larvae in a Japanese mountain stream. Mar Freshw Res 58:811–817. doi: 10.1071/MF07067 CrossRefGoogle Scholar
  11. England LE, Rosemond AD (2004) Small reductions in forest cover weaken terrestrial-aquatic linkages in headwater streams. Freshw Biol 49:721–734. doi: 10.1111/j.1365-2427.2004.01219.x CrossRefGoogle Scholar
  12. Evans CD, Freeman C, Cork LG, Thomas DN, Reynolds B, Billett MF, Garnett MH, Norris D (2007) Evidence against recent climate-induced destabilisation of soil carbon from 14C analysis of riverine dissolved organic matter. Geophys Res Lett 34:L07407. doi: 10.1029/2007GL029431 CrossRefGoogle Scholar
  13. Finlay JC (2001) Stable-carbon-isotope ratios of river biota: implications for energy flow in lotic food webs. Ecology 82:1052–1064. doi:10.1890/0012-9658(2001)082[1052:SCIROR]2.0.CO;2Google Scholar
  14. Finlay JC (2003) Controls of streamwater dissolved inorganic carbon dynamics in a forested watershed. Biogeochemistry 62:231–252. doi: 10.1023/A:1021183023963 CrossRefGoogle Scholar
  15. Finlay JC (2011) Stream size and human influences on ecosystem production in river networks. Ecosphere 2:art87. doi: 10.1890/ES11-00071.1
  16. Finlay JC, Power ME, Cabana G (1999) Effects of water velocity on algal carbon isotope ratios: implications for river food web studies. Limnol Oceanogr 44:1198–1203. doi: 10.4319/LO.1999.44.5.1198 CrossRefGoogle Scholar
  17. Finlay JC, Khandwala S, Power ME (2002) Spatial scale of carbon flow in a river food web. Ecology 83:1845–1859. doi:10.1890/0012-9658(2002)083[1845:SSOCFI]2.0.CO;2Google Scholar
  18. Fry B (1984) 13C/12C ratios and the trophic importance of algae in Florida Syringodium filiforme seagrass meadows. Mar Biol 79:11–19. doi: 10.1007/BF00404980 CrossRefGoogle Scholar
  19. Fry B (1991) Stable isotope diagrams of freshwater food webs. Ecology 72:2293–2297. doi: 10.2307/1941580 CrossRefGoogle Scholar
  20. Godwin H (1962) Half-life of radiocarbon. Nature 195:984. doi: 10.1126/science.149.3690.1326 CrossRefGoogle Scholar
  21. Griffith DR, Raymond PA (2011) Multiple-source heterotrophy fueled by aged organic carbon in an urbanized estuary. Mar Chem 124:14–22. doi: 10.1016/j.marchem.2010.11.003 CrossRefGoogle Scholar
  22. Hadwen WL, Spears M, Kennard MJ (2010) Temporal variability of benthic algal δ13C signatures influences assessments of carbon flows in stream food webs. Hydrobiologia 651:239–251. doi: 10.1007/s10750-010-0303-y CrossRefGoogle Scholar
  23. Hedges JI, Ertel JR, Quay PD, Grootes PM, Richey JE, Devol AH, Farwell GW, Schmidt FW, Salati E (1986) Organic carbon-14 in the Amazon River system. Science 231:1129–1131. doi: 10.1126/science.231.4742.1129 Google Scholar
  24. Hill WR, Fanta SE, Roberts BJ (2008) 13C dynamics in benthic algae: effects of light, phosphorus, and biomass development. Limnol Oceanogr 53:1217–1226. doi: 10.4319/LO.2008.53.4.1217 CrossRefGoogle Scholar
  25. Hitchon B, Krouse HR (1972) Hydrogeochemistry of the surface waters of the Mackenzie River drainage basin, Canada—III. Stable isotopes of oxygen, carbon and sulphur. Geochim Cosmochim Acta 36:1337–1357. doi: 10.1016/0016-7037(72)90066-X CrossRefGoogle Scholar
  26. Hobbie EA, Weber NS, Trappe JM, van Klinken GJ (2002) Using radiocarbon to determine the mycorrhizal status of fungi. New Phytol 156:129–136. doi: 10.1046/j.1469-8137.2002.00496.x CrossRefGoogle Scholar
  27. Hood E, Fellman J, Spencer RGM, Hernes PJ, Edwards R, D’Amore D, Scott D (2009) Glaciers as a source of ancient and labile organic matter to the marine environment. Nature 462:1044–1047. doi: 10.1038/nature08580 CrossRefPubMedGoogle Scholar
  28. Huryn AD, Rilley RH, Young RG, Arbuckle CJ, Peacock K, Lyon G (2001) Temporal shift in contribution of terrestrial organic matter to consumer production in a grassland river. Freshw Biol 46:213–226. doi: 10.1046/j.1365-2427.2001.00648.x CrossRefGoogle Scholar
  29. Hyodo F, Tayasu I, Wada E (2006) Estimation of the longevity of C in terrestrial detrital food webs using radiocarbon (14C): how old are diets in termites? Funct Ecol 20:385–393. doi: 10.1111/j.1365-2435.2006.01081.x CrossRefGoogle Scholar
  30. Hyodo F, Tayasu I, Konaté S, Tondoh JE, Lavelle P, Wada E (2008) Gradual enrichment of 15N with humification of diets in a below-ground food web: relationship between 15N and diet age determined using 14C. Funct Ecol 22:516–522. doi: 10.1111/j.1365-2435.2008.01386.x CrossRefGoogle Scholar
  31. Ishikawa NF, Uchida M, Shibata Y, Tayasu I (2010) A new application of radiocarbon concentrations (14C) to stream food web analysis. Nucl Instrum Methods Phys Res Sect B-Beam Interact Mater Atoms 268:1175–1178. doi: 10.1016/j.nimb.2009.10.127 CrossRefGoogle Scholar
  32. Ishikawa NF, Doi H, Finlay JC (2012a) Global meta-analysis for controlling factors on carbon stable isotope ratios of lotic periphyton. Oecologia 170:541–549. doi: 10.1007/s00442-012-2308-x CrossRefPubMedGoogle Scholar
  33. Ishikawa NF, Uchida M, Shibata Y, Tayasu I (2012b) Natural C-14 provides new data for stream food-web studies: a comparison with C-13 in multiple stream habitats. Mar Freshw Res 63:210–217. doi: 10.1071/MF11141 CrossRefGoogle Scholar
  34. Junk WJ, Bayley PB, Sparks RE (1989) The flood pulse concept in river-floodplain ecosystems. In: Dodge DP (ed) Proceedings of the international large rivers symposium, vol 106. Canadian Special Publication in Fisheries and Aquatic Sciences, Ottawa, pp 110–127Google Scholar
  35. Kitagawa H, van der Plicht J (1998) Atmospheric radiocarbon calibration to 45,000 yr B.P.: late glacial fluctuations and cosmogenic isotope production. Science 279:1187–1190. doi: 10.1126/science.279.5354.1187 CrossRefPubMedGoogle Scholar
  36. Koarashi J, Atarashi-Andoh M, Ishizuka S, Miura S, Saito T, Hirai K (2009) Quantitative aspects of heterogeneity in soil organic matter dynamics in a cool temperate Japanese beech forest: a radiocarbon-based approach. Glob Change Biol 15:631–642. doi: 10.1111/j.1365-2486.2008.01745.x CrossRefGoogle Scholar
  37. Kohzu A, Kato C, Iwata T, Kishi D, Murakami M, Nakano N, Wada E (2004) Stream food web fueled by methane-derived carbon. Aquat Microb Ecol 36:189–194. doi: 10.3354/ame036189 CrossRefGoogle Scholar
  38. Kohzu A, Tayasu I, Yoshimizu C, Maruyama A, Kohmatsu Y, Hyodo F, Onoda Y, Igeta A, Matsui K, Nakano T, Wada E, Nagata T, Takemon Y (2009) Nitrogen-stable isotopic signatures of basal food items, primary consumers and omnivores in rivers with different levels of human impact. Ecol Res 24:127–136. doi: 10.1007/s11284-008-0489-x CrossRefGoogle Scholar
  39. Lau DCP, Leung KMY, Dudgeon D (2009) Are autochthonous foods more important than allochthonous resources to benthic consumers in tropical headwater streams? J N Am Benthol Soc 28:426–439. doi: 10.1899/07-079.1 CrossRefGoogle Scholar
  40. Levin I, Hesshaimer V (2000) Radiocarbon: a unique tracer of global carbon cycle dynamics. Radiocarbon 42:69–80Google Scholar
  41. Levin I, Naegler T, Kromer B, Dieh M, Francey RJ, Gomez-Pelaez AJ, Steele LP, Wagenbach D, Weller R, Worthy DE (2010) Observations and modelling of the global distribution and long-term trend of atmospheric 14CO2. Tellus Ser B Chem Phys Meteorol 62:26–46. doi: 10.1111/J.1600-0889.2009.00446.X CrossRefGoogle Scholar
  42. MacDonald GM, Beukens RP, Kieser WE (1991) Radiocarbon dating of limnic sediments: a comparative analysis and discussion. Ecology 72:1150–1155. doi: 10.2307/1940612 CrossRefGoogle Scholar
  43. Mayorga E (2008) Carbon cycle: harvest of the century. Nature 451:405–406. doi: 10.1038/451405a CrossRefPubMedGoogle Scholar
  44. Mayorga E, Aufdenkampe AK, Masiello CA, Krusche AV, Hedges JI, Quay PD, Richey JE, Brown TA (2005) Young organic matter as a source of carbon dioxide outgassing from Amazonian rivers. Nature 436:538–541. doi: 10.1038/NATURE03880 CrossRefPubMedGoogle Scholar
  45. McCallister SL, Bauer JE, Cherrier JE, Ducklow HW (2004) Assessing sources and ages of organic matter supporting river and estuarine bacterial production: a multiple-isotope (Δ14C, δ13C, and δ15N) approach. Limnol Oceanogr 49:1687–1702. doi: 10.4319/LO.2008.53.4.1204 CrossRefGoogle Scholar
  46. McCutchan JH Jr, Lewis WM Jr (2002) Relative importance of carbon sources for macroinvertebrates in a Rocky Mountain stream. Limnol Oceanogr 47:742–752. doi: 10.4319/LO.2002.47.3.0742 CrossRefGoogle Scholar
  47. Meritt RW, Cummins KW (1978) An introduction to aquatic insects of North America. Kendall-Hunt, DubuqueGoogle Scholar
  48. Nagao S, Usui T, Yamamoto M, Minagawa M, Iwatsuki T, Noda A (2005) Combined use of Δ14C and δ13C values to trace transportation and deposition processes of terrestrial particulate organic matter in coastal marine environments. Chem Geol 218:63–72. doi: 10.1016/j.physletb.2003.10.071 CrossRefGoogle Scholar
  49. Nara F, Imai A, Yoneda M, Matsushige K, Komatsu K, Nagai T, Shibata Y, Watanabe T (2007) Seasonal variation in sources of dissolved organic carbon in a lacustrine environment revealed by paired isotopic measurements (Δ14C and δ13C). Radiocarbon 49:767–773Google Scholar
  50. Ohte N, Tayasu I, Kohzu A, Yoshimizu C, Osaka K, Makabe A, Koba K, Yoshida N, Nagata T (2010) Spatial distribution of nitrate sources of rivers in the Lake Biwawatershed, Japan: controlling factors revealed by nitrogen and oxygen isotope values. Water Resour Res 46:W07505. doi: 10.1029/2009WR007871 CrossRefGoogle Scholar
  51. Petsch ST, Eglinton TI, Edwards KJ (2001) 14C-dead living biomass: evidence for microbial assimilation of ancient organic carbon during shale weathering. Science 292:1127–1131. doi: 10.1126/science.1058332 CrossRefPubMedGoogle Scholar
  52. Power ME, Dietrich WE (2002) Food webs in river networks. Ecol Res 17:451–471. doi: 10.1046/j.1440-1703.2002.00503.x CrossRefGoogle Scholar
  53. Raymond PA, Bauer JE (2001) Riverine export of aged terrestrial organic matter to the North Atlantic Ocean. Nature 409:497–500. doi: 10.1038/35054034 CrossRefPubMedGoogle Scholar
  54. Raymond PA, Cole JJ (2003) Increase in the export of alkalinity from North America’s largest river. Science 301:88–91. doi: 10.1126/science.1083788 CrossRefPubMedGoogle Scholar
  55. Raymond PA, Bauer JE, Caraco NF, Cole JJ, Longworth B, Petsch ST (2004) Controls on the variability of organic matter and dissolved inorganic carbon ages in northeast US rivers. Mar Chem 92:353–366. doi: 10.1016/j.marchem.2004.06.036 CrossRefGoogle Scholar
  56. Schell DM (1983) Carbon-13 and carbon-14 abundances in Alaskan organisms: delayed production from peat in arctic food webs. Science 219:1068–1071. doi: 10.1126/science.219.4588.1068 CrossRefPubMedGoogle Scholar
  57. Shin HS, Mitamura O (2011) Spatial variation in the trophic base of the trichopteran filter feeder Stenopsyche marmorata in an intermittent river in Japan. Aquat Biol 12:291–298. doi: 10.3354/AB00344 CrossRefGoogle Scholar
  58. Stern J, Wang Y, Gu B, Newman J (2007) Distribution and turnover of carbon in natural and constructed wetlands in the Florida Everglades. Appl Geochem 22:1936–1948. doi: 10.1016/j.apgeochem.2007.04.007 CrossRefGoogle Scholar
  59. Stuiver M, Polach HA (1977) Discussion: reporting of 14C data. Radiocarbon 19:355–363Google Scholar
  60. Stuiver M, Quay PD (1981) Atmospheric 14C changes resulting from fossil fuel CO2 release and cosmic ray flux variability. Earth Planet Sci Lett 53:349–362. doi: 10.1016/0012-821X(81)90040-6 CrossRefGoogle Scholar
  61. Suess HE (1955) Radiocarbon concentration in modern wood. Science 122:415–417. doi: 10.1126/science.122.3166.415-a CrossRefGoogle Scholar
  62. Takemon Y (2005) Life-type concept and functional feeding groups of benthos communities as indicators of lotic ecosystem conditions. Japan J Ecol 55:189–197 (In Japanese)Google Scholar
  63. Tayasu I, Nakamura T, Oda H, Hyodo F, Takematsu Y, Abe T (2002) Termite ecology in a dry evergreen forest in Thailand in terms of stable (δ13C and δ15N) and radio (14C, 137Cs and 210Pb) isotopes. Ecol Res 17:195–276. doi: 10.1046/j.1440-1703.2002.00479.x CrossRefGoogle Scholar
  64. Thorp JH, Delong MD (1994) The riverine productivity model: and heuristic view of carbon sources and organic processing in large river ecosystems. Oikos 70:305–308. doi: 10.2307/3545642 CrossRefGoogle Scholar
  65. Thorp JH, Delong MD (2002) Dominance of autochthonous autotrophic carbon in food webs of heterotrophic rivers. Oikos 96:543–550. doi: 10.1034/j.1600-0706.2002.960315.x CrossRefGoogle Scholar
  66. Toyota A, Tayasu I, Fujimaki R, Kaneko N, Uchida M, Shibata Y, Hiura T (2010) Effects of vegetation switch and subsequent change in soil invertebrate composition on soil carbon accumulation patterns, revealed by radiocarbon concentrations. Radiocarbon 52:1471–1486Google Scholar
  67. Trumbore S (2000) Age of soil organic matter and soil respiration: radiocarbon constraints on belowground C dynamics. Ecol Appl 10:399–411. doi: 10.2307/2641102 CrossRefGoogle Scholar
  68. Trumbore S (2009) Radiocarbon and soil carbon dynamics. Annu Rev Earth Planet Sci 37:47–66. doi: 10.1146/annurev.earth.36.031207.124300 CrossRefGoogle Scholar
  69. Trumbore SE, Chadwick OA, Amundson R (1996) Rapid exchange between soil carbon and atmospheric carbon dioxide driven by temperature change. Science 272:393–396. doi: 10.1126/science.272.5260.393 Google Scholar
  70. Uchida M, Shibata Y, Yoneda M, Kobayashi T, Morita T (2004) Technical progress in AMS microscale radiocarbon analysis. Nucl Instrum Methods Phys Res Sect B Beam Interact Mater Atoms 223–224:313–317. doi: 10.1016/j.nimb.2004.04.062 CrossRefGoogle Scholar
  71. Vander Zanden MJ, Rasmussen JB (2001) Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnol Oceanogr 46:2061–2066. doi: 10.4319/lo.2001.46.8.2061 CrossRefGoogle Scholar
  72. Vannote RL, Minshall GW, Cummins KW, Sedell JR, Cushing CE (1980) The river continuum concept. Can J Fish Aquat Sci 37:130–137. doi: 10.1139/f80-017 CrossRefGoogle Scholar
  73. Zah R, Burgherr P, Bernasconi SM, Uehlinger U (2001) Stable isotope analysis of macroinvertebrates and their food sources in a glacier stream. Freshw Biol 46:871–882. doi: 10.1046/j.1365-2427.2001.00720.x CrossRefGoogle Scholar
  74. Zeug SC, Winemiller KO (2008) Evidence supporting the importance of terrestrial carbon in a large-river food web. Ecology 89:1733–1743. doi: 10.1890/07-1064.1 CrossRefPubMedGoogle Scholar
  75. Zigah PK, Minor EC, Werne JP, McCallister SL (2011) Radiocarbon and stable carbon isotopic insights into provenance and cycling of carbon in Lake Superior. Limnol Oceanogr 56:867–886. doi: 10.4319/lo.2011.56.3.0867 CrossRefGoogle Scholar

Copyright information

© The Ecological Society of Japan 2013

Authors and Affiliations

  • Naoto F. Ishikawa
    • 1
  • Fujio Hyodo
    • 2
  • Ichiro Tayasu
    • 1
  1. 1.Center for Ecological ResearchKyoto UniversityOtsuJapan
  2. 2.Research Core for Interdisciplinary SciencesOkayama UniversityOkayamaJapan

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