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

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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.

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References

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Book  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Google Scholar 

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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.

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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

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