Skip to main content
SpringerLink
Log in

Stable Isotope Trophic Fractionation (13C/12C and 15N/14N) in Mycophagous Diptera Larvae

  • Published:
Biology Bulletin Aims and scope Submit manuscript

Abstract

The use of isotopic analysis for reconstructing the structure of food webs requires determination of the trophic fractionation of carbon and nitrogen stable isotopes (Δ13C and Δ15N). Fungi and mycophagous animals play a key role in soil communities, but there are very limited field data on the degree of isotope fractionation in animals that feed on fungi. We studied the bulk isotopic composition of mycetophagous Diptera larvae inhabiting fruit bodies of saprotrophic and mycorrhizal macromycetes, as well as larva feeding on parasitic rust fungi. Trophic enrichment in 13С and 15N was at the minimum (0.0 and 0.9‰, respectively) in the larvae of gall midges Mycodiplosis sp. feeding on rust fungi (Pucciniales). In the larvae of dipterans inhabiting fruiting bodies of saprotrophic and mycorrhizal macromycetes, the Δ13C and Δ15N values averaged 0.9 and 3.4‰, respectively. This corresponds to the values usually observed in grazing food chains. The accumulation of 15N was more pronounced in the larvae that fed on saprotrophic fungi, but no clear relationship was found between the degree of trophic fractionation and the taxonomic affiliation of animals or fungi. As suggested by our data and the analysis of published studies, the variations in the trophic fractionation in mycophages are strong, but they are not likely to impede the identification of the “mycorrhizal” and “saprotrophic” energy channels in the soil food webs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

Similar content being viewed by others

REFERENCES

  1. Gebauer, G. and Taylor, A.F., 15N natural abundance in fruit bodies of different functional groups of fungi in relation to substrate utilization, New Phytol., 1999, vol. 142, pp. 93–101.

    Article  Google Scholar 

  2. Goncharov, A.A. and Tiunov, A.V., Food webs in soil, Zh. Obshch. Biol., 2013, no. 6, pp. 450–462.

  3. Goncharov, A.A., Tsurikov, S.M., Potapov, A.M., and Tiunov, A.V., Short-term incorporation of freshly fixed plant carbon into the soil animal food web: field study in a spruce forest, Ecol. Res., 2016, vol. 31, pp. 923–933.

    Article  CAS  Google Scholar 

  4. Haubert, D., Langel, R., Scheu, S., and Ruess, L., Effects of food quality, starvation and life stage on stable isotope fractionation in Collembola, Pedobiologia, 2005, vol. 49, pp. 229–237.

    Article  CAS  Google Scholar 

  5. Henn, M.R. and Chapela, I.H., Ecophysiology of 13C and 15N isotopic fractionation in forest fungi and the roots of the saprotrophic–mycorrhizal divide, Oecologia, 2001, vol. 128, pp. 480–487.

    Article  Google Scholar 

  6. Hobbie, E.A., Sanchez, F.S., and Rygiewicz, P.T., Controls of isotopic patterns in saprotrophic and ectomycorrhizal fungi, Soil Biol. Biochem., 2012, vol. 48, pp. 60–68.

    Article  CAS  Google Scholar 

  7. Jackson, A.L., Inger, R., Parnell, A.C., and Bearhop, S., Comparing isotopic niche widths among and within communities: SIBER - Stable Isotope Bayesian Ellipses in R, J. Anim. Ecol., 2011, vol. 80, pp. 595–602.

    Article  Google Scholar 

  8. Korobushkin, D.I., Gongalsky, K.B., and Tiunov, A.V., Isotopic niche (δ13C and δ15N values) of soil macrofauna in temperate forests, Rapid Commun. Mass Spectrom., 2014, vol. 28, pp. 1303–1311.

    Article  CAS  Google Scholar 

  9. Kudrin, A.A., Tsurikov, S.M., and Tiunov, A.V., Trophic position of microbivorous and predatory soil nematodes in a boreal forest as indicated by stable isotope analysis, Soil Biol. Biochem., 2015, vol. 86, pp. 193–200.

    Article  CAS  Google Scholar 

  10. Lafferty, K.D., Allesina, S., Arim, M., Briggs, C.J., De Leo, G., Dobson, A.P., Dunne, J.A., Johnson, P.T.J., Kuris, A.M., Marcogliese, D.J., Martinez, N.D., Memmott, J., Marquet, P.A., McLaughlin, J.P., Mordecai, E.A., Pascual, M., Poulin, R., and Thieltges, D.W., Parasites in food webs: the ultimate missing links, Ecol. Lett., 2008, vol. 11, pp. 533–546.

    Article  Google Scholar 

  11. Larsen, T., Ventura, M., Damgaard, C., Hobbie, E.A., and Krogh, P.H., Nutrient allocations and metabolism in two collembolans with contrasting reproduction and growth strategies, Funct. Ecol., 2009, vol. 23, pp. 745–755.

    Article  Google Scholar 

  12. Martínez del Rio, C., Wolf, N., Carleton, S.A., and Gannes, L.Z., Isotopic ecology ten years after a call for more laboratory experiments, Biol. Rev., 2009, vol. 84, pp. 91–111.

    Article  Google Scholar 

  13. Mayor, J.D., Schuur, E.A., and Henkel, T.W., Elucidating the nutritional dynamics of fungi using stable isotopes, Ecol. Lett., 2009, vol. 12, pp. 171–183.

    Article  Google Scholar 

  14. Navarro, J., Albo-Puigserver, M., Coll, M., Saez, R., Forero, M.G., and Kutcha, R., Isotopic discrimination of stable isotopes of nitrogen (δ15N) and carbon (δ13C) in a host-specific holocephalan tapeworm, J. Helminthol., 2014, vol. 88, pp. 371–375.

    Article  CAS  Google Scholar 

  15. Pinnegar, J.K., Campbell, N., and Polunin, N.V., Unusual stable isotope fractionation patterns observed for fish host–parasite trophic relationships, J. Fish. Biol., 2001, vol. 59, pp. 494–503.

    Google Scholar 

  16. Pollierer, M.M., Langel, R., Körner, C., Maraun, M., and Scheu, S., The underestimated importance of belowground carbon input for forest soil animal food webs, Ecol. Lett., 2007, vol. 10, pp. 729–736.

    Article  Google Scholar 

  17. Pollierer, M.M., Langel, R., Scheu, S., and Maraun, M., Compartmentalization of the soil animal food web as indicated by dual analysis of stable isotope ratios (15N/14N and 13C/12C), Soil Biol. Biochem., 2009, vol. 41, pp. 1221–1226.

    Article  CAS  Google Scholar 

  18. Post, D.M., Using stable isotopes to estimate trophic position: models, methods, and assumptions, Ecology, 2002, vol. 83, pp. 703–718.

    Article  Google Scholar 

  19. Potapov, A.M. and Tiunov, A.V., Stable isotope composition of mycophagous collembolans versus mycotrophic plants: do soil invertebrates feed on mycorrhizal fungi?, Soil Biol. Biochem., 2016, vol. 93, pp. 115–118.

    Article  CAS  Google Scholar 

  20. Potapov, A.M., Semenina, E.E., Kurakov, A.V., and Tiunov, A.V., Large 13C/12C and small 15N/14N isotope fractionation in an experimental detrital foodweb (litter–fungi–collembolans), Ecol. Res., 2013, vol. 28, pp. 1069–1079.

    Article  CAS  Google Scholar 

  21. Potapov, A.M., Tiunov, A.V., and Scheu, S., Uncovering trophic positions and food resources of soil animals using bulk natural stable isotope composition, Biol. Rev., 2019, vol. 94, pp. 37–59.

    Article  Google Scholar 

  22. R Core Team, R: A Language and Environment for Statistical Computing, Vienna, Austria: R Foundation for Statistical Computing, 2014.

  23. Remen, C., Unravelling the feeding habits of fungivores, Doctoral Thesis, Uppsala: Swed. Univ. Agricult. Sci., 2010.

  24. Ruess, L., Tiunov, A., Haubert, D., Richnow, H.H., Haggblom, M.M., and Scheu, S., Carbon stable isotope fractionation and trophic transfer of fatty acids in fungal based soil food chains, Soil Biol. Biochem., 2005, vol. 37, pp. 945–953.

    Article  CAS  Google Scholar 

  25. Scheu, S. and Falca, M., The soil food web of two beech forests (Fagus sylvatica) of contrasting humus type: stable isotope analysis of a macro- and a mesofauna-dominated community, Oecologia, 2000, vol. 123, pp. 285–286.

    Article  CAS  Google Scholar 

  26. Scheu, S. and Folger, M., Single and mixed diets in Collembola: effects on reproduction and stable isotope fractionation, Funct. Ecol., 2004, vol. 18, pp. 94–102.

    Article  Google Scholar 

  27. Semenina, E.E. and Tiunov, A.V., Trophic fractionation (Δ15N) in Collembola depends on nutritional status: a laboratory experiment and mini-review, Pedobiologia, 2011, vol. 54, pp. 101–109.

    Article  CAS  Google Scholar 

  28. Staaden, S., Milcu, A., Rohlfs, M., and Scheu, S., Fungal toxins affect the fitness and stable isotope fractionation of Collembola, Soil Biol. Biochem., 2010, vol. 42, pp. 1766–1773.

    Article  CAS  Google Scholar 

  29. Striganova, B.R., Pitanie pochvennykh saprofagov (Feeding of Soil Saprophages), Moscow: Nauka, 1980.

  30. Tiunov, A.V., Stable isotopes of carbon and nitrogen in soil ecological studies, Biol. Bull. (Moscow), 2007, vol. 34, no. 4, pp. 395–407.

    Article  CAS  Google Scholar 

  31. Tiunov, A.V., Semenina, E.E., Aleksandrova, A.V., Tsurikov, S.M., Anichkin, A.E., and Novozhilov, Y.K., Stable isotope composition (δ13C and δ15N values) of slime molds: placing bacterivorous soil protozoans in the food web context, Rapid Commun. Mass Spectrom., 2015, vol. 29, pp. 1465–1472.

    Article  CAS  Google Scholar 

  32. Tsurikov, S.M., Goncharov, A.A., and Tiunov, A.V., Isotopic composition (13C/12C and 15N/14N) of different tissues of coleopteran insects (Insecta, Coleoptera) and its changes in ontogenesis, Zool. Zh., 2015, no. 94, pp. 336–344.

  33. Vanderklift, M.A. and Ponsard, S., Sources of variation in consumer-diet δ15N enrichment: a meta-analysis, Oecologia, 2003, vol. 136, pp. 169–182.

    Article  Google Scholar 

  34. Wallander, H., Goransson, H., and Rosengren, U., Production, standing biomass and natural abundance of 15N and 13C in ectomycorrhizal mycelia collected at different soil depths in two forest types, Oecologia, 2004, vol. 139, pp. 89–97.

  35. Wardle, D.A., Communities and Ecosystems: Linking the Aboveground and Belowground Components, Princeton: Princeton Univ. Press, 2002.

    Google Scholar 

Download references

ACKNOWLEDGMENTS

The authors are grateful to E.А. Astakhova, V.O. Bakumenko, M.I. Varsanofyeva, A.A. Gorshkova, T.V. Loginova, M.A. Perfil’eva, A.D. Semenov, and D.A. Fedorov for assistance in collecting the material.

Funding

This work was supported by the Russian Foundation for Basic Research, project no. 17-04-01856.

Author information

Authors and Affiliations

  1. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, 119071, Moscow, Russia

    A. G. Zuev, O. L. Rozanova, S. M. Tsurikov, M. G. Krivosheina & A. V. Tiunov

  2. Faculty of Biology, Moscow State University, 119234, Moscow, Russia

    S. M. Tsurikov, P. L. Panchenko, M. A. Ershova, D. D. Smolyarova, A. V. Aleksandrova, S. B. Ivnitsky & Yu. V. Maleeva

Authors
  1. A. G. Zuev
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. O. L. Rozanova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. M. Tsurikov
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. P. L. Panchenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. A. Ershova
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. D. D. Smolyarova
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M. G. Krivosheina
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. A. V. Aleksandrova
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. S. B. Ivnitsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Yu. V. Maleeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. A. V. Tiunov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. G. Zuev.

Ethics declarations

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by P. Kuchina

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zuev, A.G., Rozanova, O.L., Tsurikov, S.M. et al. Stable Isotope Trophic Fractionation (13C/12C and 15N/14N) in Mycophagous Diptera Larvae. Biol Bull Russ Acad Sci 46, 457–465 (2019). https://doi.org/10.1134/S1062359019050157

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062359019050157

Search

Navigation