Oecologia

, Volume 138, Issue 2, pp 161–167 | Cite as

Sulfur stable isotopes separate producers in marine food-web analysis

  • Rod M. Connolly
  • Michaela A. Guest
  • Andrew J. Melville
  • Joanne M. Oakes
Methods

Abstract

Ecological applications of stable isotope analysis rely on different producers having distinct isotopic ratios to trace energy and nutrient transfer to consumers. Carbon (C) and nitrogen (N) are the usual elements analysed. We tested the hypothesis that producers unable to be separated using C and N would be separated by sulphur (S), by reviewing estuarine and marine food web studies using all three elements (total of 836 pairwise comparisons between producers). S had a wider range of values across all producers than C and N (S: 34.4, C: 23.3, N: 18.7‰), and a higher mean difference among producers (S: 9.3, C: 6.5, N: 3.3‰). We varied from 1 to 10‰ the distance producers must be apart to be considered separate. For each of these gap distances, S-separated producers tied on C and N in 40% or more of cases. Comparing the three elements individually, S had fewer tied pairs of producers for any gap distance than C or N. However, S also has higher within-producer variability. Statistical tests on simulated data showed that this higher variability caused S to be less effective than C for analysing differences among mean producer values, yet mixing models showed that S had the smallest confidence intervals around mean estimates of source contributions to consumers. We also examined the spatial and temporal scales over which S isotope signatures of the saltmarsh plant Spartina alterniflora varied. Differences between samples taken within tens of metres were smallest, but between samples hundreds of metres apart were as different as samples thousands of kilometres apart. The time between samples being taken did not influence S signatures. Overall, the use of S is recommended because it has a high probability of distinguishing the contribution of different producers to aquatic food webs. When two elements are employed, the combination of S and C separates more producers than any other combination.

Keywords

Estuary Spartina Trophic ecology Variability 

References

  1. Chanton JP, Lewis FG (1999) Plankton and dissolved inorganic carbon isotopic composition in a river dominated estuary: Apalachicola Bay, Florida. Estuaries 22:575–583Google Scholar
  2. Chukhrov FV, Ermilova LP, Churikov VS, Nosik LP (1980) The isotopic condition of plant sulfur. Org Geochem 2:69–75Google Scholar
  3. Coffin RB, Fry B, Wright RT (1989) Carbon isotopic compositions of estuarine bacteria. Limnol Oceanogr 34:1305–1310Google Scholar
  4. Cornwell JC, Stevenson JC, Stribling JM (1990) Biogeochemical studies in the Monie Bay National Estuarine Research Reserve. Report No. NA89AA/D C2 130. Chesapeake Bay National Estuarine Research Reserve, Washington, D.C.Google Scholar
  5. Couch CA (1989) Carbon and nitrogen stable isotopes of meiobenthos and their food resources. Estuar Coast Shelf Sci 28:433–441Google Scholar
  6. Currin CA, Newell SY, Paerl HW (1995) The role of standing dead Spartina alterniflora and benthic microalgae in salt marsh food webs—considerations based on multiple stable isotope analysis. Mar Ecol Prog Ser 121:99–116Google Scholar
  7. Deegan LA, Garritt RH (1997) Evidence for spatial variability in estuarine food webs. Mar Ecol Prog Ser 147:31–47Google Scholar
  8. Deegan LA, Peterson BJ, Portier R (1990) Stable isotopes and cellulase activity as evidence for detritus as a food source for juvenile gulf menhaden. Estuaries 13:14–19Google Scholar
  9. Farquhar GD, Ehleringer JR, Hubrick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537Google Scholar
  10. Fry B (1983) Fish and shrimp migrations in the northern Gulf of Mexico analysed using stable C, N and S isotope ratios. Fish Bull 81:789–801Google Scholar
  11. Fry B (1988) Food web structure on Georges Bank from stable C, N, and S isotopic compositions. Limnol Oceanogr 33:1182–1190Google Scholar
  12. Fry B, Scalan RS, Winters JK, Parker PL (1982) Sulphur uptake by salt grasses, mangroves, and seagrasses in anaerobic sediments. Geochim Cosmochim Acta 46:1121–1124Google Scholar
  13. Fry B, Mumford PL, Tam F, Fox DD, Warren GL, Havens KE, Steinman AD (1999) Trophic position and individual feeding histories of fish from Lake Okeechobee, Florida. Can J Fish Aquat Sci 56:590–600CrossRefGoogle Scholar
  14. Fry B, Silva SR, Kendall C, Anderson RK (2002) Oxygen isotope corrections for online δ34S analysis. Rapid Commun Mass Spectrom 16:854–858PubMedGoogle Scholar
  15. Harrigan P, Zieman JC, Macko SA (1989) The base of nutritional support for the Gray Snapper (Lutjanus griseus): an evaluation based on a combined stomach content and stable isotope analysis. Bull Mar Sci 44:65–77Google Scholar
  16. Hsieh YP, Shieh YN (1997) Analysis of reduced inorganic sulfur by diffusion methods: improved apparatus and evaluation for sulfur isotopic studies. Chem Geol 137:255–261CrossRefGoogle Scholar
  17. Kharlamenko VI, Kiyashko SI, Imbs AB, Vyshkvartzev DI (2001) Identification of food sources of invertebrates from the seagrass Zostera marina community using carbon and sulfur stable isotope ratio and fatty acid analyses. Mar Ecol Prog Ser 220:103–117Google Scholar
  18. Kwak TJ, Zedler JB (1997) Food web analysis of southern California coastal wetlands using multiple stable isotopes. Oecologia 110:262–277CrossRefGoogle Scholar
  19. Lajtha K, Michener RH (eds) (1994) Stable isotopes in ecology and environmental science. Blackwell, LondonGoogle Scholar
  20. Loneragan NR, Bunn SE, Kellaway DM (1997) Are mangroves and seagrasses sources of organic carbon for penaeid prawns in a tropical Australian estuary? A multiple stable isotope study. Mar Biol 130:289–300CrossRefGoogle Scholar
  21. Machás R, Santos R (1999) Sources of organic matter in Ria Formosa revealed by stable isotope analysis. Acta Oecol 20:463–469CrossRefGoogle Scholar
  22. Macko SA, Estep MLF (1984) Microbial alteration of stable nitrogen and carbon isotopic compositions of organic matter. Org Geochem 6:787–790Google Scholar
  23. McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen and sulfur. Oikos 102:378–390Google Scholar
  24. Mekhtiyeva VL, Pankina RG, Gavrilov YY (1976) Distributions and isotopic compositions of forms of sulfur in water animals and plants. Geochem Int 13:82–87Google Scholar
  25. Melville AJ, Connolly RM (2003) Spatial analysis of stable isotope data to determine primary sources of nutrition for fish. Oecologia 136:499–507PubMedGoogle Scholar
  26. Michener RH, Schell DM (1994) Stable isotope ratios as tracers in marine aquatic food webs. In: Lajtha K, Michener RH (eds) Stable isotopes in ecology and environmental science. Blackwell, London, pp 121–157Google Scholar
  27. Monaghan JM, Scrimgeour CM, Stein WM, Zhao FJ, Evans EJ (1999) Sulphur accumulation and redistribution in wheat (Triticum aestivum): a study using stable sulphur isotope ratios as a tracer. Plant Cell Environ 22:831–839Google Scholar
  28. Moncreiff CA, Sullivan MJ (2001) Trophic importance of epiphytic algae in subtropical seagrass beds: evidence from multiple stable isotope analyses. Mar Ecol Prog Ser 215:93–106Google Scholar
  29. Newell RIE, Marshall N, Sasekumar A, Chong VC (1995) Relative importance of benthic microalgae, phytoplankton, and mangroves as sources of nutrition for penaeid prawns and other coastal invertebrates from Malaysia. Mar Biol 123:595–606Google Scholar
  30. O’Leary MH (1988) Carbon isotopes in photosynthesis. Bioscience 38:328–336Google Scholar
  31. Peterson BJ (1999) Stable isotopes as tracers of organic matter input and transfer in benthic food webs: a review. Acta Oecol 20:479–487CrossRefGoogle Scholar
  32. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320CrossRefGoogle Scholar
  33. Peterson BJ, Howarth RW (1987) Sulfur, carbon, and nitrogen isotopes used to trace organic matter flow in the salt-marsh estuaries of Sapelo Island, Georgia. Limnol Oceanogr 32:1195–1213Google Scholar
  34. Peterson BJ, Howarth RW, Garritt RH (1985) Multiple stable isotopes used to trace the flow of organic matter in estuarine food webs. Science 227:1361–1363Google Scholar
  35. Peterson BJ, Howarth RW, Garritt RH (1986) Sulfur and carbon isotopes as tracers of salt-marsh organic matter flow. Ecology 67:865–874Google Scholar
  36. Phillips DL, Gregg JW (2001) Uncertainty in source partitioning using stable isotopes. Oecologia 127:171–179CrossRefGoogle Scholar
  37. Pinnegar J, Polunin N (2000) Contributions of stable-isotope data to elucidating food webs of Mediterranean rocky littoral fishes. Oecologia 122:399–409CrossRefGoogle Scholar
  38. Stribling JM, Cornwell JC, Currin C (1998) Variability of stable sulfur isotopic ratios in Spartina alterniflora. Mar Ecol Prog Ser 166:73–81Google Scholar
  39. Sullivan MJ, Moncreiff CA (1990) Edaphic algae are an important component of salt marsh food-webs: evidence from multiple stable isotope analyses. Mar Ecol Prog Ser 62:149–159Google Scholar
  40. Thode HG (1991) Sulfur isotopes in nature and the environment: an overview. In: Krouse HR, Grinenko VA (eds) Stable isotopes: natural and anthropogenic sulphur in the environment. Wiley, Chichester, pp 1–26Google Scholar
  41. Trust BA, Fry B (1992) Stable sulphur isotopes in plants: a review. Plant Cell Environ 15:1105–1110Google Scholar
  42. Wainright SC, Weinstein MP, Able KW, Currin CA (2000) Relative importance of benthic microalgae, phytoplankton and the detritus of smooth cordgrass Spartina alterniflora and the common reed Phragmites australis to brackish-marsh food webs. Mar Ecol Prog Ser 200:77–91Google Scholar
  43. Weinstein MP, Litvin S, Bosley KL, Fuller CM, Wainright SC (2000) The role of tidal salt marsh as an energy source for marine transient and resident finfishes: a stable isotope approach. Trans Am Fish Soc 129:797–810Google Scholar
  44. Zieman JC, Macko SA, Mills AL (1984) Role of seagrasses and mangroves in estuarine food webs: temporal and spatial changes in stable isotope composition and amino acid content during decomposition. Bull Mar Sci 35:380–392Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Rod M. Connolly
    • 1
    • 2
    • 3
  • Michaela A. Guest
    • 1
    • 2
    • 3
  • Andrew J. Melville
    • 1
  • Joanne M. Oakes
    • 1
    • 3
  1. 1.School of Environmental and Applied SciencesGriffith UniversityAustralia
  2. 2.The Cooperative Research Centre for Coastal Zone, Estuary and Waterway ManagementIndooroopillyAustralia
  3. 3.Centre for Aquatic Processes and PollutionGriffith University, Gold Coast CampusAustralia

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