Abstract
Earthworms not only facilitate carbon (C) stabilization, but also accelerate organic matter mineralization by enhancing microbial respiration. However, the fate (mineralization vs stabilization) of newly added C by straw returning in arable lands with earthworm activity is still unclear. In the present 40 days incubation study, we incorporated artificially 13C–labeled straw into soil with and without presence of earthworms (Metaphire guillelmi). Flux measurements of CO2 from soil (mineralization) were taken regularly, while straw-derived C remaining in the soil (stabilization) was measured at the end of the incubation. There was no significant difference of the cumulative CO2 emission between earthworm presence and absence treatment. However, earthworm presence significantly decreased straw-derived cumulative CO2-C emission when compared with the treatment without earthworm. Besides, earthworm incubation led to a significantly low light fraction organic carbon (LFOC) content and straw-derived LFOC proportion. Relative to the non-earthworm treatment, straw-derived C content significantly decreased in micro-aggregates (< 0.25 mm), but increased in large macro-aggregates (> 2 mm) in the earthworm treatment. In total, only 3.8% of added straw C was assimilated by earthworm within 40 days, while most of the straw C remained in the soil. Earthworms decreased straw-derived CO2-C emission from 10.0 to 8.1% when compared with the non-earthworm treatment. In the present short period incubation experiment, compared with the soil without earthworms, the presence of Metaphire guillelmi (1) resulted a higher soil CO2 emissions, which may mainly evolved from the older SOC, and (2) stabilized more residue-derived C in the soil aggregates. We therefore propose that Metaphire guillelmi may increase soil organic carbon pool turnover rates in the short term after straw returning by replacement of older SOC with newly added straw C.
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References
Aira M, Monroy F, Dominguez J (2006a) Eisenia fetida (Oligochaeta, Lumbricidae) activates fungal growth, triggering cellulose decomposition during vermicomposting. Microb Ecol 52(4):738–747. https://doi.org/10.1007/s00248-006-9109-x
Aira M, Monroy F, Dominguez J (2006b) Changes in microbial biomass and microbial activity of pig slurry after the transit through the gut of the earthworm Eudrilus eugeniae (Kinberg, 1867). Biol Fert Soils 42(4):371–376. https://doi.org/10.1007/s00374-005-0047-4
Bohlen PJ, Pelletier DM, Groffman PM, Fahey TJ, Fisk MC (2004) Influence of earthworm invasion on redistribution and retention of soil carbon and nitrogen in northern temperate forests. Ecosystems 7(1):13–27. https://doi.org/10.1007/s10021-003-0127-y
Bossuyt H, Six J, Hendrix PF (2005) Protection of soil carbon by microaggregates within earthworm casts. Soil Biol Biochem 37(2):251–258. https://doi.org/10.1016/j.soilbio.2004.07.035
Bossuyt H, Six J, Hendrix PF (2006) Interactive effects of functionally different earthworm species on aggregation and incorporation and decomposition of newly added residue carbon. Geoderma 130(1-2):14–25. https://doi.org/10.1016/j.geoderma.2005.01.005
Briones MJI, Garnett MH, Piearce TG (2005) Earthworm ecological grou**s based on C-14 analysis. Soil Biol Biochem 37(11):2145–2149. https://doi.org/10.1016/j.soilbio.2005.03.001
Brown GG, Doube BM (2004) Functional interactions between earthworms, microorganisms, organic matter, and plants, earthworm ecology. CRC Press, Boca Raton, pp 213–239
Chan KY (2001a) An overview of some tillage impacts on earthworm population abundance and diversity—implications for functioning in soils. Soil Till Res 57(4):179–191. https://doi.org/10.1016/S0167-1987(00)00173-2
Chan KY (2001b) Soil particulate organic carbon under different land use and management. Soil Use Manag 17(4):217–221. https://doi.org/10.1079/SUM200180
Chen YX, Zhang YF, Zhang QG, Xu LX, Li R, Luo XP, Zhang X, Tong J (2015) Earthworms modify microbial community structure and accelerate maize stover decomposition during vermicomposting. Environ Sci Pollut R 22(21):17161–17170. https://doi.org/10.1007/s11356-015-4955-z
Coq S, Barthes BG, Oliver R, Rabary B, Blanchart E (2007) Earthworm activity affects soil aggregation and organic matter dynamics according to the quality and localization of crop residues—an experimental study (Madagascar). Soil Biol Biochem 39(8):2119–2128. https://doi.org/10.1016/j.soilbio.2007.03.019
Curry JP, Schmidt O (2007) The feeding ecology of earthworms—a review. Pedobiologia 50(6):463–477. https://doi.org/10.1016/j.pedobi.2006.09.001
Don A, Kalbitz K (2005) Amounts and degradability of dissolved organic carbon from foliar litter at different decomposition stages. Soil Biol Biochem 37(12):2171–2179. https://doi.org/10.1016/j.soilbio.2005.03.019
Don A, Steinberg B, Schöning I, Pritsch K, Joschko M, Gleixner G, Schulze ED (2008) Organic carbon sequestration in earthworm burrows. Soil Biol Biochem 40(7):1803–1812. https://doi.org/10.1016/j.soilbio.2008.03.003
Drake HL, Horn MA (2007) As the worm turns: the earthworm gut as a transient habitat for soil microbial biomes. Annu Rev Microbiol 61(1):169–189. https://doi.org/10.1146/annurev.micro.61.080706.093139
Ernst G, Henseler I, Felten D, Emmerling C (2009) Decomposition and mineralization of energy crop residues governed by earthworms. Soil Biol Biochem 41(7):1548–1554. https://doi.org/10.1016/j.soilbio.2009.04.015
Feller C, Brown GG, Blanchart E, Deleporte P, Chernyanskii SS (2003) Charles Darwin, earthworms and the natural sciences: various lessons from past to future. Agric Ecosyst Environ 99(1-3):29–49. https://doi.org/10.1016/S0167-8809(03)00143-9
Ferlian O (2014) Carbon food resources of earthworms of different ecological groups as indicated by 13C compound-specific stable isotope analysis. Soil Biol Biochem 77:22–30. https://doi.org/10.1016/j.soilbio.2014.06.002
Fonte SJ, Kong A, Van KC, Hendrix PF, Six J (2007) Influence of earthworm activity on aggregate-associated carbon and nitrogen dynamics differs with agroecosystem management. Soil Biol Biochem 39(5):1014–1022. https://doi.org/10.1016/j.soilbio.2006.11.011
Gomez-Brandon M, Lazcano C, Lores M, Dominguez J (2010) Detritivorous earthworms modify microbial community structure and accelerate plant residue decomposition. Appl Soil Ecol 44(3):237–244. https://doi.org/10.1016/j.apsoil.2009.12.010
Gregorich EG, Monreal CM, Carter MR, Angers DA, Ellert BH (1994) Towards a minimum data set to assess soil organic matter quality in agricultural soils. Can J Soil Sci 74(4):367–385. https://doi.org/10.4141/cjss94-051
Haynes RJ, Fraser PM, Piercy JE, Tregurtha RJ (2003) Casts of Aporrectodea caliginosa (Savigny) and Lumbricus rubellus (Hoffmeister) differ in microbial activity, nutrient availability and aggregate stability. Pedobiologia 47:882–887
Hedde M, Bureau F, Delporte P, Cécillon L, Decaëns T (2013) The effects of earthworm species on soil behaviour depend on land use. Soil Biol Biochem 65:264–273. https://doi.org/10.1016/j.soilbio.2013.06.005
Jones DL, Willett VB (2006) Experimental evaluation of methods to quantify dissolved organic nitrogen (DON) and dissolved organic carbon (DOC) in soil. Soil Biol Biochem 38(5):991–999. https://doi.org/10.1016/j.soilbio.2005.08.012
Kernecker M, Whalen JK, Bradley RL (2014) Litter controls earthworm-mediated carbon and nitrogen transformations in soil from temperate riparian buffers. Appl Environ Soil Sci 2014:329031. https://doi.org/10.1155/2014/329031
Knapp BA, Podmirseg SM, Seeber J, Meyer E, Insam H (2009) Diet-related composition of the gut microbiota of Lumbricus rubellus as revealed by a molecular fingerprinting technique and cloning. Soil Biol Biochem 41(11):2299–2307. https://doi.org/10.1016/j.soilbio.2009.08.011
Leifeld J, Kogel-Knabner I (2005) Soil organic matter fractions as early indicators for carbon stock changes under different land-use? Geoderma 124(1-2):143–155. https://doi.org/10.1016/j.geoderma.2004.04.009
Liu C, Lu M, Cui J, Li B, Fang CM (2014) Effects of straw carbon input on carbon dynamics in agricultural soils: a meta-analysis. Glob Chang Biol 20(5):1366–1381. https://doi.org/10.1111/gcb.12517
Lou Y, Li Z, Zhang T, Liang Y (2004) CO2 emission from subtropical arable soils of China. Soil Biol Biochem Soil Biol Biochem 36(11):1835–1842. https://doi.org/10.1016/j.soilbio.2004.05.006
Lubbers IM, Groenigen KJV, Fonte SJ, Six J, Brussaard L, Groenigen JWV (2013) Greenhouse-gas emissions from soils increased by earthworms. Nat Clim Chang 3(3):187–194. https://doi.org/10.1038/nclimate1692
Lubbers IM, Pulleman MM, Van Groenigen JW (2017) Can earthworms simultaneously enhance decomposition and stabilization of plant residue carbon? Soil Biol Biochem 105:12–24. https://doi.org/10.1016/j.soilbio.2016.11.008
Marhan S, Langel R, Kandeler E, Scheu S (2007) Use of stable isotopes (C-13) for studying the mobilisation of old soil organic carbon by endogeic earthworms (Lumbricidae). Eur J Soil Biol 43:S201–S208. https://doi.org/10.1016/j.ejsobi.2007.08.017
Pulleman MM, Six J, Uyl A, Marinissen JCY, Jongmans AG (2005) Earthworms and management affect organic matter incorporation and microaggregate formation in agricultural soils. Appl Soil Ecol 29(1):1–15. https://doi.org/10.1016/j.apsoil.2004.10.003
Qiu JX, Turner MG (2017) Effects of non-native Asian earthworm invasion on temperate forest and prairie soils in the Midwestern US. Biol Invasions 19(1):73–88. https://doi.org/10.1007/s10530-016-1264-5
Rizhiya E, Bertora C, Pcjvan V, Kuikman PJ, Faber JH, Jwvan G (2007) Earthworm activity as a determinant for N2O emission from crop residue. Soil Biol Biochem 39(8):2058–2069. https://doi.org/10.1016/j.soilbio.2007.03.008
Scheu S, Schlitt N, Tiunov AV, Newington JE, Jones HT (2002) Effects of the presence and community composition of earthworms on microbial community functioning. Oecologia 133(2):254–260. https://doi.org/10.1007/s00442-002-1023-4
Shaaban M, Wu YP, Peng QA, Lin S, Mo YL, Wu L, Hu RG, Zhou W (2016) Effects of dicyandiamide and dolomite application on N2O emission from an acidic soil. Environ Sci Pollut R 23(7):6334–6342. https://doi.org/10.1007/s11356-015-5863-y
Shahbaz M, Kuzyakov Y, Sanaullah M, Heitkamp F, Zelenev V, Kumar A, Blagodatskaya E (2017) Microbial decomposition of soil organic matter is mediated by quality and quantity of crop residues: mechanisms and thresholds. Biol Fertil Soils:1–15
Six J, Callewaert P, Lenders S, De Gryze S, Morris SJ, Gregorich EG, Paul EA, Paustian K (2002) Measuring and understanding carbon storage in afforested soils by physical fractionation. Soil Sci Soc Am J 66(6):1981–1987. https://doi.org/10.2136/sssaj2002.1981
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 Till Res 79(1):7–31. https://doi.org/10.1016/j.still.2004.03.008
Vidal A, Quenea K, Alexis M, Tu TTN, Mathieu J, Vaury V, Derenne S (2017) Fate of C-13 labelled root and shoot residues in soil and anecic earthworm casts: a mesocosm experiment. Geoderma 285:9–18. https://doi.org/10.1016/j.geoderma.2016.09.016
Wachendorf C, Potthoff M, Ludwig B, Joergensen RG (2014) Effects of addition of maize litter and earthworms on C mineralization and aggregate formation in single and mixed soils differing in soil organic carbon and clay content. Pedobiologia 57(3):161–169. https://doi.org/10.1016/j.pedobi.2014.03.001
Wu J, Li H, Zhang W, Li F, Huang J, Mo Q, **a H (2017) Contrasting impacts of two subtropical earthworm species on leaf litter carbon sequestration into soil aggregates. J Soils Sediments:1–10
Wu Y, Shaaban M, Zhao J, Hao R, Hu R (2015a) Effect of the earthworm gut-stimulated denitrifiers on soil nitrous oxide emissions. Eur J Soil Biol 70:104–110. https://doi.org/10.1016/j.ejsobi.2015.08.001
Wu YP, Liu T, Peng Q, Shaaban M, Hu RG (2015b) Effect of straw returning in winter fallow in Chinese rice fields on greenhouse gas emissions: evidence from an incubation study. Soil Res 53(3):298–305. https://doi.org/10.1071/SR14261
Zangerlé A, Pando A, Lavelle P (2011) Do earthworms and roots cooperate to build soil macroaggregates? A microcosm experiment. Geoderma s 167–168:303–309
Zhang JJ, Hu F, Li HX, Gao Q, Song XY, Ke XK, Wang LC (2011) Effects of earthworm activity on humus composition and humic acid characteristics of soil in a maize residue amended rice-wheat rotation agroecosystem. Appl Soil Ecol 51:1–8. https://doi.org/10.1016/j.apsoil.2011.08.004
Zhang WX, Hendrix PF, Dame LE, Burke RA, Wu JP, Neher DA, Li JX, Shao YH, Fu SL (2013) Earthworms facilitate carbon sequestration through unequal amplification of carbon stabilization compared with mineralization. Nat Commun 4:2576
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This work was supported by the National Key Research and Development Program of China (2017YFD0202001) and the National Natural Science Foundation of China (41401267, 41750110485).
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Wu, Y., Shaaban, M., Peng, Q.a. et al. Impacts of earthworm activity on the fate of straw carbon in soil: a microcosm experiment. Environ Sci Pollut Res 25, 11054–11062 (2018). https://doi.org/10.1007/s11356-018-1397-4
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DOI: https://doi.org/10.1007/s11356-018-1397-4