Advertisement

Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Influence of earthworms on apolar lipid features in soils after 1 year of incubation

Abstract

Molecular and compound specific isotope compositions of apolar lipids were characterized in soil mesocosms incubated for 1 year with or without 13C-labelled plant residues and earthworms, in order to investigate, at the molecular scale, the effect of earthworms on the fate of organic matter (OM) in soils. Molecular and isotope composition of long chain alkanes in casts confirmed that earthworms preferentially ingest soil fractions rich in plant debris. Apolar lipid specific isotope composition allowed calculation of the proportion of carbon derived from the labelled residues (Clab). Casts displayed higher Clab values than surrounding soil while soil without earthworm exhibited intermediate Clab. The odd-over-even predominance (OEP) of alkanes suggested they are probably less degraded in casts than in the surrounding soil. Taken together, OEP and Clab values suggested that besides high incorporation of plant residues, earthworms may also favor the preservation of plant apolar lipids in their casts. Additionally, chain length and isotope pattern of alkanes further suggested root lipids were probably less degraded than shoot lipids. High 13C-incorporation level for the bacterial biomarker hopene provided evidence for intense recycling of plant OM and suggested further contribution of bacterial necromass to soil OM.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Albro PW, Schroeder JL, Corbett JT (1992) Lipids of the earthworm Lumbricus terrestris. Lipids 27:136–143

  2. Alexander M (1981) Biodegradation of chemicals of environmental concern. Science 211:132–138

  3. Amblès A, Jambu P, Parlanti E, Joffre J, Riffe C (1994) Incorporation of natural monoacids from plant residues into an hydromorphic forest podzol. Eur J Soil Sci 45:175–182

  4. Angst G, Mueller CW, Prater I, Angst Š, Frouz J, Jílková V, Peterse F, Nierop KG (2019) Earthworms act as biochemical reactors to convert labile plant compounds into stabilized soil microbial necromass. Commun Biol 2:1–7

  5. Angst Š, Mueller CW, Cajthaml T, Angst G, Lhotáková Z, Bartuška M, Špaldoňová A, Frouz J (2017) Stabilization of soil organic matter by earthworms is connected with physical protection rather than with chemical changes of organic matter. Geoderma 289:29–35

  6. Bahri H, Dignac MF, Rumpel C, Rasse D, Chenu C, Mariotti A (2006) Lignin turnover kinetics in an agricultural soil is monomer specific. Soil Biol Biochem 38:1977–1988

  7. Balesdent J, Mariotti A (1996) Measurement of soil organic matter turnover using 13C natural abundance. In: Boutton TW, Yamasaki SI (eds) Mass spectrometry of soils. Marcel Dekker Inc, New York, pp 83–111

  8. Beyschlag W, Eckstein J (1997) Stomatal patchiness. Prog Bot 59:283–298

  9. Bossuyt H, Six J, Hendrix PF (2005) Protection of soil carbon by microaggregates within earthworm casts. Soil Biol Biochem 37:251–258

  10. Bouché M, Kretzschmar A (1974) Fonction des lombriciens; II: Recherches méthodologiques pour l’analyse du sol ingéré (étude du peuplement de la station RCP-165/PBI). Rev Écol Biol Sol 11:127–139

  11. Boutton TW (1996) Stable carbon isotope ratios of organic matter and their use as indicators of vegetation and climate changes. In: Boutton TW, Yamasaki SI (eds) Mass spectrometry of soils. Marcel Dekker Inc, New York, pp 47–82

  12. Brown GG, Barois I, Lavelle P (2000) Regulation of soil organic matter dynamics and microbial activity in the drilosphere and the role of interactions with other edaphic functional domains. Eur J Soil Biol 36:177–198

  13. Buggle B, Wiensenberg GL, Glaser B (2010) Is there a possibility to correct fossil n-alkane data for postsedimentary alteration effects? Appl Geochem 25:947–957

  14. Bull ID, van Bergen PF, Nott CJ, Poulton PR, Evershed RP (2000) Organic geochemical studies of soils from Rothamsted classical experiments-V. The fate of lipids in different long-term experiments. Org Geochem 31:389–408

  15. Canti MG (2009) Experiments on the origin of 13C in the calcium carbonate granules produced by the earthworm Lumbricus terrestris. Soil Biol Biochem 41:2588–2592

  16. Chikaraishi Y, Naraoka H (2006) Carbon and hydrogen isotope variation of plant biomarkers in a plant-soil system. Chem Geol 231:190–202

  17. Cortez J (1998) Field decomposition of leaf litters: relationships between decomposition rates and soil moisture, soil temperature and earthworm activity. Soil Biol Biochem 30:783–793

  18. Crow SE, Filley TR, McCormick M, Szlávecz K, Stott DE, Gamblin D, Conyers G (2009) Earthworms, stand age, and species composition interact to influence particulate organic matter chemistry during forest succession. Biogeochemistry 92:61–82

  19. Curry JP, Schmidt O (2007) The feeding ecology of earthworms—a review. Pedobiologia 50:463–477

  20. Derrien D, Marol C, Balabane M, Balesdent J (2006) The turnover of carbohydrate carbon in a cultivated soil estimated by 13C natural abundances. Eur J Soil Sci 57:547–557

  21. Dinel H, Schnitzer M (1990) Soil lipids: origin, nature, content, decomposition, and effect on soil physical properties. In: Bollag JM, Stotzky G (eds) Soil biochemistry. Marcel Dekker, New York, pp 397–429

  22. Dotterweich H (1933) Die Funktion tierischer Kalkablagerungen als Pufferreserve im Dienste der Reaktionsregulation. Die Kalkdrusen des Regenwurms. Pflugers Arch Geschicte Physiol 232:263–286

  23. Eglinton G, Hamilton RJ (1967) Leaf epicuticular waxes. Science 156:1322–1335

  24. El-Otmani M, Coggins CW (1985) Fruit development and growth regulator effects on normal alkanes of “Washington” navel orange fruit epicuticular wax. J Agric Food Chem 33:656–663

  25. Fahey TJ, Yavitt JB, Sherman RE, Maerz JC, Groffman PM, Fisk MC, Bohlen PJ (2013) Earthworm effects on the incorporation of litter C and N into soil organic matter in a sugar maple forest. Ecol Appl 23:1185–1201

  26. Feakins SJ, Wu MS, Ponton C, Galy V, West AJ (2018) Dual isotope evidence for sedimentary integration of plant wax biomarkers across an Andes-Amazon elevation transect. Geochim Cosmochim Acta 242:64–81

  27. Filley TR, McCormick MK, Crow SE, Szlavecz K, Whigham DF, Johnston CT, van den Heuvel RN (2008) Comparison of the chemical alteration trajectory of Liriodendron tulipifera L. leaf litter among forests with different earthworm abundance. J Geophys Res 113:1–14

  28. Fontaine S, Bardoux G, Benest D, Verdier B, Mariotti A, Abbadie L (2004) Carbon input to soil may decrease soil carbon content. Ecol Lett 7:314–320

  29. Fonte SJ, Quintero DC, Velásquez E, Lavelle P (2012) Interactive effects of plants and earthworms on the physical stabilization of soil organic matter in aggregates. Plant Soil 359:205–214

  30. Frouz J, Špaldoňová A, Lhotáková Z, Cajthaml T (2015) Major mechanisms contributing to the macrofauna-mediated slow down of litter decomposition. Soil Biol Biochem 91:23–31

  31. Gocke M, Kuzyakov Y, Wiesenberg GLB (2013) Differentiation of plant derived organic matter in soil, loess and rhizoliths based on n-alkane molecular proxies. Biogeochemistry 112:23–40

  32. Gonzalez-Vila FJ (1995) Alkane biomarkers. Geochemichal significance and application in oil shale geochemistry. In: Snape C (ed) Composition, geochemistry and conversion of oil shales. NATO ASI Series C455:51–68

  33. Guggenberger G, Thomas RJ, Zech W (1996) Soil organic matter within earthworm casts of an anecic-endogeic tropical pasture community, Colombia. Appl Soil Ecol 3:263–274

  34. Gülz PG, Müller E, Prasad RBN (1991) Developmental and seasonal variations in the epicuticular waves of Tilia tomentosa leaves. Phytochemistry 30:769–773

  35. Harwood JL, Russel NJ (1984) Lipids in plants and microbes. George Allen & Unwin, London

  36. Hoefs JL, Rijpstra WI, Sinninghe Damsté JS (2002) The influence of oxic degradation on the sedimentary biomarker record I: evidence from Madeira Abyssal Plain turbidites. Geochim Cosmochim Acta 66:2719–2735

  37. Hong HN, Rumpel C, Henry des Tureaux T, Bardoux G, Billou D, Tran Duc T, Jouquet P (2011) How do earthworms influence organic matter quantity and quality in tropical soils? Soil Biol Biochem 43:223–230

  38. Huang Y, Bol R, Harkness DD, Ineson P, Eglinton G (1996) Post-glacial variations in distributions, 13C, 14C contents of aliphatic hydrocarbons and bulk organic matter in three types of British acid upland soils. Org Geochem 24:273–287

  39. Huang X, Wang C, Zhang J, Wiesenberg GLB, Zhang Z, Xie S (2011) Comparison of free lipid compositions between roots and leaves of plants in the Dajiuhu Peatland, central China. Geochem J 45:365–373

  40. Innes HE, Bishop AN, Head IM, Farrimond P (1997) Preservation and diagenesis of hopanoids in Recent lacustrine sediments of Priest Pot, England. Org Geochem 26:565–576

  41. Jambu P, Fustec E, Jacquesy R (1978) Les lipides des sols: nature, origine, évolution, propriétés. Sci Sol Bull AFES 4:229–2040

  42. Jandl G, Leinweber P, Schulten HR, Ekschmitt K (2005) Contribution of primary organic matter to the fatty acid pool in agricultural soils. Soil Biol Biochem 37:1033–1041

  43. Jansen B, Nierop KGJ, Hageman JA, Cleef AM, Verstraten JM (2006) The straight-chain lipid biomarker composition of plant species responsible for the dominant biomass production along two altitudinal transects in the Ecuadorian Andes. Org Geochem 37:1514–1536

  44. Jansen B, Haussmann NS, Tonneijck FH, Verstraten JM, de Voogt P (2008) Characteristic straight-chain lipid ratios as a quick method to assess past forest–páramo transitions in the Ecuadorian Andes. Palaeogeogr Palaeoclimatol Palaeoecol 262:129–139

  45. Jégou D, Cluzeau D, Hallaire V, Balesdent J, Tréhen P (2000) Burrowing activity of the earthworms Lumbricus terrestris and Aporrectodea giardi and consequences on C transfers in soil. Eur J Soil Biol 36:27–34

  46. Jégou D, Schrader S, Diestel H, Cluzeau D (2001) Morphological, physical and biochemical characteristics of burrow walls formed by earthworms. Appl Soil Ecol 17:165–174

  47. Jobbágy EG, Jackson RB (2000) The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl 10:423–436

  48. Kelleher BP, Simpson AJ (2006) Humic substances in soils: are they really chemically distinct? Environ Sci Technol 40:4605–4611

  49. Kögel-Knabner I (2002) The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol Biochem 34:139–162

  50. Kögel-Knabner I (2017) The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter: fourteen years on. Soil Biol Biochem 105:A3–A8

  51. Kolattukudy PE, Croteau R, Buckner JS (1976) Biochemistry of plant waxes. In: Kolattukudy PE (ed) Chemistry and biochemistry of natural waxes. Elsevier, Amsterdam, pp 290–347

  52. Kuzyakov Y (2010) Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42:1363–1371

  53. Lavelle P, Martin A (1992) Small-scale and large-scale effects of endogeic earthworms on soil organic matter dynamics in soils of the humid tropics. Soil Biol Biochem 24:1491–1498

  54. Lavelle P, Pashanasi B, Charpentier F, Rossi JP, Derouard L, André J, Ponge JF, Bernier N (1998) Large-scale effects of earthworms on soil organic matter and nutrient dynamics. In: Edwards CA (ed) Earthworm ecology. CRC Press, Boca Raton, pp 103–122

  55. Lee KE (1985) Earthworms their ecology and relationships with soils and land use. Academic Press, Sydney

  56. Li R, Meyers PA, Fan J, Xue J (2016) Monthly changes in chain length distributions and stable carbon isotope composition of leaf n-alkanes during growth of the bamboo Dendrocalamus ronganensis and the grass Setaria viridis. Org Geochem 101:72–81

  57. Li R, Fan J, Xue J, Meyers PA (2017) Effects of early diagenesis on molecular distributions and carbon isotopic compositions of leaf wax long chain biomarker n-alkanes: comparison of two one-year-long burial experiments. Org Geochem 104:8–18

  58. Liang C, Balser TC (2011) Microbial production of recalcitrant organic matter in global soils: implications for productivity and climate policy. Nat Rev Microbiol 9:75

  59. Lichtfouse E, Chenu C, Baudin F, Leblond C, Da Silva M, Behar F, Derenne S, Largeau C, Wehrung P, Albrecht P (1998) A novel pathway of soil organic matter formation by selective preservation of resistant straight-chain biopolymers: chemical and isotope evidence. Org Geochem 28:411–415

  60. Lockheart MJ, van Bergen PF, Evershed RP (1997) Variations in the stable carbon isotope composition of individual lipids from the leaves of modern angiosperms: implications for the study of higher plant-derived sedimentary organic matter. Org Geochem 26:137–153

  61. Lubbers IM, van Groenigen KJ, Fonte SJ, Six J, Brussaard L, van Groenigen JW (2013) Greenhouse-gas emissions from soils increased by earthworms. Nat Clim Change 3:187–194

  62. Lutzow MV, Kogel-Knabner I, Ekschmitt K, Matzner E, Guggenberger G, Marschner B, Flessa H (2006) Stabilization of organic matter in temperate soils: mechanisms and their relevance under different soil conditions—a review. Eur J Soil Sci 57:426–445

  63. Malossini F, Piasentier E, Bovolenta S (1990) n-alkane content of some forages. J Sci Food Agric 53:405–409

  64. Mariotti A, Balesdent J (1990) 13C natural abundance as a tracer of soil organic matter turnover and paleoenvironment dynamics. Chem Geol 84:217–219

  65. Martin A (1991) Short- and long-term effects of the endogeic earthworm Millsonia anomala (Omodeo) (Megascolecidæ, Oligochæta) of tropical savannas, on soil organic matter. Biol Fertil Soils 11:234–238

  66. Mendez-Millan M, Dignac MF, Rumpel C, Rasse DP, Derenne S (2010) Molecular dynamics of shoot vs. root biomarkers in an agricultural soil estimated by natural abundance 13C labelling. Soil Biol Biochem 42:169–177

  67. Mendez-Millan M, Nguyen Tu TT, Balesdent J, Derenne S, Derrien D, Egasse C, Thongo M’Bou A, Zeller B, Hatté C (2014) Compound-specific 13C and 14C measurements improve the understanding of soil organic matter dynamics. Biogeochemistry 118:205–223

  68. Miltner A, Bombach P, Schmidt-Brücken B, Kästner M (2012) SOM genesis: microbial biomass as a significant source. Biogeochemistry 111:41–55

  69. Mueller KE, Polissar PJ, Oleksyn J, Freeman KH (2012) Differentiating temperate tree species and their organs using lipid biomarkers in leaves, roots and soil. Org Geochem 52:130–141

  70. Mueller CW, Weber PK, Kilburn MR, Hoeschen C, Kleber M, Pett-Ridge J (2013) Advances in the analysis of biogeochemical interfaces: nanoSIMS to investigate soil microenvironments. In: Sparks DL (ed) Advances in agronomy, vol 121. Academic Press, Delaware, PA, pp 1–46

  71. Nguyen Tu TT, Derenne S, Largeau C, Mariotti A, Bocherens H (2003) Comparison of leaf lipids from a fossil ginkgoalean plant and its extant counterpart at two degradation stages: diagenetic and chemotaxonomic implications. Rev Palaeobot Palynol 124:63–78

  72. Nguyen Tu TT, Egasse C, Zeller B, Bardoux G, Biron P, Ponge JF, David B, Derenne S (2011) Early degradation of plant alkanes in soils: a litterbag experiment using 13C-labelled leaves. Soil Biol Biochem 43:2222–2228

  73. Nguyen Tu TT, Biron P, Maseyk K, Richard P, Zeller B, Quénéa K, Alexis M, Bardoux G, Vaury V, Girardin C, Pouteau V, Billiou D, Bariac T (2013) Variability of 13 C-labeling in plant leaves. Rapid Commun Mass Spectrom 27:1961–1968

  74. Nierop KGJ, Jansen B, Hageman JA, Verstraten JM (2006) The complementarity of extractable and ester-bound lipids in a soil profile under pine. Plant Soil 286:269–285

  75. Nooner DW, Oro J, Cerbulis J (1973) Paraffinic hydrocarbon composition of earthworms (Lumbricus terrestris). Lipids 8:489–492

  76. Otto A, Shunthirasingham C, Simpson MJ (2005) A comparison of plant and microbial biomarkers in grassland soils from the Prairie Ecozone of Canada. Org Geochem 36:425–448

  77. Ourisson G, Albrecht P, Rohmer M (1979) Palaeobiochemistry and biochemistry of a group of natural products. Pure Appl Chem 51:709–729

  78. Peters KE, Walters JM, Moldowan JM (2005) The biomarker guide, 2nd edn. Cambridge University Press, Cambridge

  79. Pospíšilová J, Šantrůček J (1994) Stomatal patchiness. Biol Plantarum 36:481–510

  80. Quénéa K, Derenne S, Largeau C, Rumpel C, Mariotti A (2004) Variation in lipid relative abundance and composition among different particle size fractions of a forest soil. Org Geochem 35:1355–1370

  81. Quénéa K, Largeau G, Derenne S, Spaccini R, Bardoux G, Mariotti A (2006) Molecular and isotopic study of lipids in particle size fractions of a sandy cultivated soil (Cestas cultivation sequence, southwest of France): sources, degradation and comparison with Cestas forest soil. Org Geochem 3:20–44

  82. Quénéa K, Mathieu J, Derenne S (2012) Soil lipids from accelerated solvent extraction: influence of temperature and solvent on extract composition. Org Geochem 44:45–52

  83. Rasse DP, Rumpel C, Dignac MF (2005) Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation. Plant Soil 269:341–356

  84. Rawlins AJ, Bull ID, Poirier N, Ineson P, Evershed RP (2006) The biochemical transformation of oak (Quercus robur) leaf litter consumed by the pill millipede (Glomersi marginata). Soil Biol Biochem 38:1063–1076

  85. Sampedro L, Whalen JK (2007) Changes in the fatty acid profiles through the digestive tract of the earthworm Lumbricus terrestris L. Appl Soil Ecol 35:226–236

  86. Schaefer M, Petersen SO, Filser J (2005) Effects of Lumbricus terrestris, Allolobophora chlorotica and Eisenia fetida on microbial community dynamics in oil-contaminated soil. Soil Biol Biochem 37:2065–2076

  87. Schaefer IK, Lanny V, Franke J, Eglinton TI, Zech M, Vysloužilová B, Zech R (2016) Leaf waxes in litter and topsoils along a European transect. Soil 2:551–564

  88. Schaeffer A, Nannipieri P, Kästner M, Schmidt B, Botterweck J (2015) From humic substances to soil organic matter–microbial contributions. In honour of Konrad Haider and James P. Martin for their outstanding research contribution to soil science. J Soils Sediments 15:1865–1881

  89. Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kogel-Knabner I, Lehmann J, Manning DAC, Nannipieri P, Rasse DP, Weiner S, Trumbore SE (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56

  90. Shi A, Penfold C, Marschner P (2013) Decomposition of roots and shoots of perennial grasses and annual barley—separately or in two residue mixes. Biol Fertil Soils 49:673–680

  91. Six J, Bossuyt H, Degryze S, Denef K (2004) A history of research on the link between (micro)aggregates, soil biota, and soil organic matter dynamics. Soil Tillage Res 79:7–31

  92. Soong JL, Reuss D, Pinney C, Boyack T, Haddix ML, Stewart CE, Cotrufo MF (2014) Design and operation of a continuous 13C and 15N labeling chamber for uniform or differential, metabolic and structural, plant isotope labeling. J Vis Exp 83:e51117

  93. Srivastava K, Wiesenberg GLB (2018) Severe drought-influenced composition and δ13C of plant and soil n-alkanes in model temperate grassland and heathland ecosystems. Org Geochem 116:77–89

  94. Stefanovic D, Djurdjic V (1976) An investigation of lipids from Lumbricus terrestris. I. Study of the hydrocarbon fraction. Glas - Srp Akad Nauka Umet Odeljenje Prir-Mat Nauka 39:53–66

  95. Stromberger ME, Keith AM, Schmidt O (2012) Distinct microbial and faunal communities and translocated carbon in Lumbricus terrestris drilospheres. Soil Biol Biochem 46:155–162

  96. van Bergen PF, Flannery MB, Poulton PR, Evershed RP (1998) Organic geochemical studies of soils from Rothamsted experimental station: III. Nitrogen-containing oragnic matter in soil from Geescroft Wilderness. In: Stankiewicz BA, van Bergen PF (eds) Nitrogen-containing macromolecules in the bio- and geosphere. American Chemical Society Symposium Series 707:321–338

  97. Versteegh EAA, Black S, Hodson ME (2014) Environmental controls on the production of calcium carbonate by earthworms. Soil Biol Biochem 70:159–161

  98. Vidal A, Quénéa K, Alexis M, Derenne S (2016a) Molecular fate of root and shoot litter on incorporation and decomposition in earthworm casts. Org Geochem 101:1–10

  99. Vidal A, Remusat L, Watteau F, Derenne S, Quénéa K (2016b) Incorporation of 13C labelled shoot residues in Lumbricus terrestris casts: a combination of transmission electron microscopy and nanoscale secondary ion mass spectrometry. Soil Biol Biochem 93:8–16

  100. Vidal A, Quénéa K, Alexis M, Nguyen Tu TT, Mathieu J, Vaury V, Derenne S (2017) Fate of 13C labelled root and shoot residues in soil and anecic earthworm casts: a mesocosm experiment. Geoderma 285:9–18

  101. Vidal A, Watteau F, Rémusat L, Mueller CW, Nguyen Tu TT, Buegger F, Derenne S, Quénéa K (2019) Earthworm cast formation and development: a shift from plant litter to mineral associated organic matter. Front Environ Sci 7:55

  102. Walthall CL, Hatfield J, Backlund P et al (2012) Climate change and agriculture in the United States: effects and adaptation. USDA Technical Bulletin, Washington

  103. Wannigama GP, Volkman JK, Gillan FT, Nichols GJ, Johns RB (1981) A comparison of lipid components of the fresh and dead leaves and pneumatophores of the mangrove Avicennia marina. Phytochemistry 20:659–666

  104. Waring RH, Silvester WB (1994) Variation in foliar δ13C values within the crowns of Pinus radiata trees. Tree Physiol 14:1203–1213

  105. Wiesenberg GLB, Schwarzbauer J, Schmidt MWI, Schwark L (2004) Source and turnover of organic matter in agricultural soils derived from n-alkane/n-carboxylic acid compositions and C-isotope signatures. Org Geochem 35:1371–1393

  106. Wiesenberg GLB, Dorodnikov M, Kuzyakov Y (2010) Source determination of lipids in bulk soil and soil density fractions after four years of wheat cropping. Geoderma 156:267–277

  107. Zangerlé A, Pando A, Lavelle P (2011) Do earthworms and roots cooperate to build soil macroaggregates? A microcosm experiment. Geoderma 167–168:303–309

  108. Zech M, Buggle B, Leiber K, Marković Glaser B, Hambach U, Huwe B, Stevens T, Sümegi P, Wiesenberg G, Zöller L (2009) Reconstructing quaternary vegetation history in the Carpathian Basin, SE Europe, using n-alkane biomarkers as molecular fossils. Quat Sci J 58:148–155

Download references

Acknowledgements

The study was funded by an EC2CO (CNRS-INSU) grant that was greatly appreciated. We are grateful to Patrick Dumont of Sorbonne Université greenhouse facilities for access to the experimental chamber and technical support. Elise Canolle and Anne-Sophie Permal are thanked for their help in preparing the lipids during their internship at METIS. We are indebted to Christelle Anquetil and Véronique Vaury for GC–MS and EA-IRMS analyses, respectively. CSIA were obtained from the ALYSES facility (IRD-SU) that was supported by grants from Région Ile-de-France. Thanks are also due to the two anonymous referees who provided constructive reviews of the manuscript.

Author information

Correspondence to Thanh Thuy Nguyen Tu.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Responsible Editor: Karsten Kalbitz.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Nguyen Tu, T., Vidal, A., Quénéa, K. et al. Influence of earthworms on apolar lipid features in soils after 1 year of incubation. Biogeochemistry 147, 243–258 (2020). https://doi.org/10.1007/s10533-020-00639-w

Download citation

Keywords

  • Earthworms
  • Organic matter
  • Lipids
  • 13C-labelling
  • Soil
  • Cast