Earthworms promote the accumulation of rhizodeposit carbon to soil macroaggregate in a Mollisol of northeast China, primarily in long-term no-till soil

Xinyu Zhu , Yunchuan Hu , Zhiguo Li , Donghui Wu

Soil Ecology Letters ›› 2021, Vol. 3 ›› Issue (2) : 84 -93.

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Soil Ecology Letters ›› 2021, Vol. 3 ›› Issue (2) : 84 -93. DOI: 10.1007/s42832-020-0062-2
RESEARCH ARTICLE
RESEARCH ARTICLE

Earthworms promote the accumulation of rhizodeposit carbon to soil macroaggregate in a Mollisol of northeast China, primarily in long-term no-till soil

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Abstract

•Ÿ Earthworms increased soil macroaggregate (>2 mm and 0.25–2 mm) formation

•Ÿ Maize roots and earthworms interact to produce soil macroaggregate

•Ÿ Earthworms were effective in transferring rhizodeposit carbon into macroaggregate, especially in soil derived from a long-term no-till system

•Ÿ Rhizodeposits were protected during soil aggregation

As soil ecosystem engineers, earthworms are the main promoters of soil aggregation, a process that drives the production of ecosystem services by soils. A crucial factor in the ecosystem service of carbon sequestration is rhizodeposit carbon, which is the main energy source of soil food webs. The effects of earthworms on the distribution of rhizodeposit-carbon in soil aggregates remain unclear. Here, we conducted a 13CO2 labeling experiment to determine the effects of earthworms on maize rhizodeposit carbon in soil aggregates after 14 years (2002–2016), in both conventional tillage (CT) and conservation tillage (no tillage, NT) soils. Four treatments were established in total: NTE (no tillage soil with earthworms), CTE (conventional tillage soil with earthworms), NTC (control, no tillage soil without earthworms), and CTC (control, conventional tillage soil without earthworms). Earthworms significantly enhanced the abundance of soil macroaggregates (>2000 μm and 250–2000 μm) on day 30 compared with day 2 (after labeling), especially in the NT soils. On day 30, in the presence of earthworms, the amounts of rhizodeposit carbon in the>2000 μm and 250–2000 μm soil aggregates in the NT soils were significantly higher than in those in the CT soils (P<0.05), and higher d13C signatures in the same size aggregates were observed in the NT soils than in the CT soils (P<0.05). These findings indicated that compared with the CT soils, with the involvement of earthworm activity, the NT soils promoted more rhizodeposit carbon transformation to the soil macroaggregates. Our results clearly indicate that soil macroaggregates formed in different tillage soils in the presence of 2 different engineers (earthworms and roots) significantly differ from those formed in the presence of only one organism (roots) in the long term.

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Keywords

Earthworms / Root-derived carbon / Soil aggregation / Isotope labeling / Rhizodeposotion / Tillage

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Xinyu Zhu, Yunchuan Hu, Zhiguo Li, Donghui Wu. Earthworms promote the accumulation of rhizodeposit carbon to soil macroaggregate in a Mollisol of northeast China, primarily in long-term no-till soil. Soil Ecology Letters, 2021, 3(2): 84-93 DOI:10.1007/s42832-020-0062-2

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References

[1]

Angers, D.A., Caron, J., 1998. Plant-induced changes in soil structure: processes and feedbacks. Biogeochemistry 42, 55–72

[2]

Arai, M., Tayasu, I., Komatsuzaki, M., Uchida, M., Shibata, Y., Kaneko, N., 2013. Changes in soil aggregate carbon dynamics under no-tillage with respect to earthworm biomass revealed by radiocarbon analysis. Soil & Tillage Research 126, 42–49

[3]

Ayuke, F.O., Pulleman, M.M., Vanlauwe, B., de Goede, R.G.M., Six, J., Csuzdi, C., Brussaard, L., 2011. Agricultural management affects earthworm and termite diversity across humid to semi-arid tropical zones. Agriculture, Ecosystems & Environment 140, 148–154

[4]

Bai, Z., Caspari, T., Ruiperez Gonzalez, M., Batjes, N.H., Mäder, P., Bünemann, E.K., de Goede, R., Brussaard, L., Xu, M., Santos Ferreira, C.S., Reintam, E., Fang, H., Mihelič R., Glavan, M., Tóth, Z., 2018. Effects of agricultural management practices on soil quality: a review of long-term experiments for Europe and China. Agriculture, Ecosystems & Environment 265, 1–7

[5]

Blanchart, E., Albrecht, A., Alegre, J., Duboisset, A., Pashanasi, B., Lavelle, P., Brussaard, L., 1999. Effects of earthworms on soil structure and physical properties. In: Lavelle, P., Brussaard, L., Hendrix, P., eds. Earthworm Management in Tropical Agroecosystems. CAB International, Wallingford, pp. 139–162.

[6]

Boag, B., Legg, R.K., Neilson, R., Palmer, L.E., Hackett, C.A., 1994. The use of Taylor’s power law to describe the aggregated distribution of earthworms in permanent pasture and arable soil in Scotland. Pedobiologia 38, 303–306.

[7]

Boone, R.D., Nadelhoffer, K.J., Canary, J.D., Kaye, J.P., 1998. Roots exert a strong influence on the temperature sensitivity of soil respiration. Nature 396, 570–572

[8]

Bossuyt, H., Six, J., Hendrix, P.F., 2005. Protection of soil carbon by microaggregates within earthworm casts. Soil Biology & Biochemistry 37, 251–258

[9]

Briones, M.J., Schmidt, O., 2017. Conventional tillage decreases the abundance and biomass of earthworms and alters their community structure in a global meta-analysis. Global Change Biology 23, 4396–4419

[10]

Brown, G.G., Edwards, C.A., Brussaard, L., 2004. How earthworms affect plant growth: burrowing into the mechanisms. In: Edwards, C.A., ed. Earthworm Ecology. CRC, Boca Raton, pp. 13–49.

[11]

Capowiez, Y., Cadoux, S., Bouchant, P., Ruy, S., Roger-Estrade, J., Richard, G., Boizard, H., 2009. The effect of tillage type and cropping system on earthworm communities, macroporosity and water infiltration. Soil & Tillage Research 105, 209–216

[12]

Cheng, L., Booker, F.L., Tu, C., Burkey, K.O., Zhou, L.S., Rufty, T.W., Fiscus, E.L., Shew, D.H., Hu, S., 2012. Arbuscular mycorrhizal fungi increase organic C decomposition under elevated CO2. Science 337, 1084–1088

[13]

Decaëns, T., Jiménez, J.J., Lavelle, P., 1999. Effect of exclusion of the anecic earthworm Martiodrilus carimaguensis and Morena on soil properties and plant growth in grasslands of the eastern plains of Colombia. Pedobiologia 43, 835–841.

[14]

Denef, K., Six, J., 2006. Contributions of incorporated residue and living roots to aggregate-associated and microbial carbon in two soils with different clay mineralogy. European Journal of Soil Science 57, 774–786

[15]

Elliott, E.T., 1986. Aggregate structure and carbon, nitrogen, and phosphorus in native and cultivated soils. Soil Science Society of America Journal 50, 627–633

[16]

Fahey, T.J., Yavitt, J.B., Sherman, R.E., Groffman, P.M., Fish, M.C., Maerz, J.C., 2011. Transport of carbon and nitrogen between litter and soil organic matter in a Northern Hardwood forest. Ecosystems (New York, N.Y.) 14, 326–340

[17]

Fonte, S.J., Quintero, D.C., Velásquez, E., Lavelle, P., 2012. Interactive effects of plants and earthworms on the physical stabilization of soil organic matter in aggregates. Plant and Soil 359, 205–214

[18]

Gilbert, K.J., Fahey, T.J., Maerz, J.C., Sherman, R.E., Bohlen, P., Dombroskie, J.J., Groffman, P.M., Yavitt, J.B., 2014. Exploring carbon flow through the root channel in a temperate forest soil food web. Soil Biology & Biochemistry 76, 45–52

[19]

Gong, X., Wang, S., Wang, Z.W., Jiang, Y.J., Hu, Z.K., Zheng, Y., Chen, X.Y., Li, H.X., Hu, F., Liu, M.Q., Scheu, S., 2019. Earthworms modify soil bacterial and fungal communities through enhancing aggregation and buffering pH. Geoderma 347, 59–69

[20]

Groffman, P.M., Fahey, T.J., Fisk, M.C., Yavitt, J.B., Sherman, R.E., Bohlen, P.J., Maerz, J.C., 2015. Earthworms increase soil microbial biomass carrying capacity and nitrogen retention in northern hardwood forests. Soil Biology & Biochemistry 87, 51–58

[21]

Guggenberger, G., Thomas, R.J., Zech, W., 1996. Soil organic matter within earthworm casts of an anecic-endogeic tropical pasture community, Colombia. Applied Soil Ecology 3, 263–274

[22]

Huang, J.H., Zhang, W.X., Liu, M.Y., Briones, M.J.I., Eisenhauer, N., Shao, Y.H., Cai, X.A., Fu, S.L., Xia, H.P., 2015. Different impacts of native and exotic earthworms on rhizodeposit-carbon sequestration in a subtropical soil. Soil Biology & Biochemistry 90, 152–160

[23]

Jones, D.L., Nguyen, C., Finlay, R.D., 2009. Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant and Soil 321, 5–33

[24]

Jouquet, P., Bottinelli, N., Podwojewski, P., Hallaire, V., Duc, T.T., 2008. Chemical and physical properties of earthworm casts as compared to bulk soil under a range of different land-use systems in Vietnam. Geoderma 146, 231–238

[25]

Judas, M., 1992. Gut content analysis of earthworms (Lumbricidae) in a beechwood. Soil Biology & Biochemistry 24, 1413–1417

[26]

Kaštovská E., Šsantrůčková H., 2007. Fate and dynamics of recently fixed C in pasture plant-soil system under field conditions. Plant and Soil 300, 61–69

[27]

Kong, A.Y.Y., Six, J., 2010. Tracing root vs. residue carbon into soils from conventional and alternative cropping systems. Soil Science Society of America Journal 74, 1201–1210

[28]

Lavelle, P., Blanchart, E., Martin, A., Spain, A.V., Martin, S., 1992. Impact of soil fauna on the properties of soils in the humid tropics. Myths and Science of Soils of the Tropics. Soil Science Society of America and American Society of Agronomy, Special Publication no. 29, Madison, 157–185.

[29]

Liang, A.Z., Zhang, X.P., Fang, H.J., Yang, X.M., Drury, C.F., 2007. Short-term effects of tillage practices on organic carbon in clay loam soil of northeast China. Pedosphere 17, 619–623

[30]

Lubbers, I.M., Pulleman, M.M., Groenigen, J.W.V., 2017. Can earthworms simultaneously enhance decomposition and stabilization of plant residue carbon? Soil Biology & Biochemistry 105, 12–24

[31]

Miller, R.M., Jastrow, J.D., 1990. Hierarchy of root and mycorrhizal fungal interactions with soil aggregation. Soil Biology & Biochemistry 22, 579–584

[32]

Mo, F., Zhang, Y.Y., Li, T., Wang, Z.T., Yu, K.L., Wen, X.X., Xiong, Y.C., Jia, Z.K., Liao, Y.C., 2019. Fate of photosynthesized carbon as regulated by long-term tillage management in a dryland wheat cropping system. Soil Biology & Biochemistry 138, 107581

[33]

Nieminen, M., Hurme, T., Mikola, J., Regina, K., Nuutinen, V., 2015. Impact of earthworm Lumbricus terrestris living sites on the greenhouse gas balance of no-till arable soil. Biogeosciences 12, 5481–5493

[34]

Pinheiro, E.F.M., Pereira, M.G., Anjos, L.H.C., 2004. Aggregate distribution and soil organic matter under different tillage systems for vegetable crops in a Red Latosol from Brazil. Soil & Tillage Research 77, 79–84

[35]

Pulleman, M.M., Six, J., Van Breemen, N., Jongmans, A.G., 2005. Soil organic matter distribution and microaggregate characteristics as affected by agricultural management and earthworm activity. European Journal of Soil Science 56, 453–467

[36]

Rillig, M.C., 2004. Arbuscular mycorrhizae, glomalin, and soil aggregation. Canadian Journal of Soil Science 84, 355–363

[37]

Rogers, H.H., Runion, G.B., Krupa, S.V., 1994. Plant responses to atmospheric CO2 enrichment with emphasis on roots and the rhizosphere. Environmental Pollution 83, 155–189

[38]

Sánchez-de León, Y., Lugo-Pérez, J., Wise, D.H., Jastrow, J.D., González-Meler, M.A., 2014. Aggregate formation and carbon sequestration by earthworms in soil from a temperate forest exposed to elevated atmospheric CO2: A microcosm experiment. Soil Biology & Biochemistry 68, 223–230

[39]

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 Research 79, 7–31

[40]

Six, J., Elliott, E.T., Paustian, K., 2000. Soil macroaggregate turnover and microaggregate formation: a mechanism for C sequestration under no-tillage agriculture. Soil Biology & Biochemistry 32, 2099–2103

[41]

Six, J., Feller, C., Denef, K., Ogle, M., Moraes, J.C., Albrecht, A., 2002. Soil organic matter, biota and aggregation in temperate and tropical soils: effects of tillage. Agronomie 22, 755–775

[42]

Six, J., Paustian, K., 2014. Aggregate-associated soil organic matter as an ecosystem property and a measurement tool. Soil Biology & Biochemistry 68, A4–A9

[43]

SDA, 1993. Soil Survey Manual. United States Department of Agriculture Handbook No. 18. US Department of Agriculture, Washington, DC.

[44]

van Groenigen, J.W., Lubbers, I.M., Vos, H.M.J., Brown, G.G., De Deyn, G.B., van Groenigen, K.J., 2014. Earthworms increase plant production: a meta-analysis. Scientific Reports 4, 63–65.

[45]

Wander, M.M., Yang, X., 2000. Influence of tillage on the dynamics of loose and occluded-particulate and humified organic matter fractions. Soil Biology & Biochemistry 32, 1151–1160

[46]

Wieland, G., Neumann, R., Backhaus, H., 2001. Variation of microbial communities in soil, rhizosphere, and rhizoplane in response to crop species, soil type, and crop development. Applied and Environmental Microbiology 67, 5849–5854

[47]

Wilson, G.W.T., Rice, C.W., Rillig, M.C., Springer, A., Hartnett, D.C., 2009. Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: results from long-term field experiments. Ecology Letters 12, 452–461

[48]

Yavitt, J.B., Fahey, T.J., Sherman, R.E., Groffman, P.M., 2015. Lumbricid earthworm effects on incorporation of root and leaf litter into aggregates in a forest soil, New York State. Biogeochemistry 125, 261–273

[49]

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

[50]

Zhang, C., Liu, G.B., Xue, S., Song, Z.L., Zhang, C.S., 2011. Fractal features of rhizosphere soil microaggregate and particle – size distribution under different vegetation types in the Hilly-Gully region of Loess Plateau. Scientia Agricultura Sinica 44, 507–515.

[51]

Zhang, S., Li, Q., Y., Sun, X., Jia, S., Zhang, X., Liang, W., 2015. Conservation tillage positively influences the microflora and microfauna in the black soil of Northeast China. Soil & Tillage Research 149, 46–52

[52]

Zhang, W.X., Hendrix, P.F., Dame, L.E., Burke, R.A., Wu, J.P., Neher, D.A., Li, J.X., Shao, Y.H., Fu, S.L., 2013. Earthworms facilitate carbon sequestration through unequal amplification of carbon stabilization compared with mineralization. Nature Communications 4, 2576

[53]

Zhang, Y., Li, X.J., Gregorich, E.G., McLaughlin, N.B., Zhang, X.P., Guo, Y.F.,Liang, A.Z., Fan, R.Q.,Sun, B.J.,2018. No-tillage with continuous maize cropping enhances soil aggregation and organic carbon storage in Northeast China. Geoderma 330, 204–211.

[54]

Zhu, B., Gutknecht, J.L.M., Herman, D.J., Keck, D.C., Firestone, M.K., Cheng, W., 2014. Rhizosphere priming effects on soil carbon and nitrogen mineralization. Soil Biology & Biochemistry 76, 183–192

[55]

Zhu, X.Y., Chang, L., Liu, J., Zhou, M.H., Li, J.J., Gao, B., Wu, D.H., 2016. Exploring the relationships between soil fauna, different tillage regimes and CO2 and N2O emissions from black soil in China. Soil Biology & Biochemistry 103, 106–116

[56]

Zhu, X.Y., Hu, Y.C., Wang, W., Wu, D.H., 2019. Earthworms promote the accumulation of maize root-derived carbon in a black soil of Northeast China, especially in soil from long-term no-till. Geoderma 340, 124–132

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