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

PDF(1826 KB)
PDF(1826 KB)
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

Author information +
History +

Highlights

•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

Abstract

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.

Graphical abstract

Keywords

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

Cite this article

Download citation ▾
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 https://doi.org/10.1007/s42832-020-0062-2

References

[1]
Angers, D.A., Caron, J., 1998. Plant-induced changes in soil structure: processes and feedbacks. Biogeochemistry 42, 55–72
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[8]
Bossuyt, H., Six, J., Hendrix, P.F., 2005. Protection of soil carbon by microaggregates within earthworm casts. Soil Biology & Biochemistry 37, 251–258
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[25]
Judas, M., 1992. Gut content analysis of earthworms (Lumbricidae) in a beechwood. Soil Biology & Biochemistry 24, 1413–1417
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[31]
Miller, R.M., Jastrow, J.D., 1990. Hierarchy of root and mycorrhizal fungal interactions with soil aggregation. Soil Biology & Biochemistry 22, 579–584
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[36]
Rillig, M.C., 2004. Arbuscular mycorrhizae, glomalin, and soil aggregation. Canadian Journal of Soil Science 84, 355–363
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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., Lü, 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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar

Acknowledgments

This study was supported by the National Natural Science Foundation of China (41430857; 41501263), the Foundation for University Young Key Teacher of Henan Province (2017GGJS141), Science and Technology Project of Henan Province (172102410054), the Program of Introducing Talents of Discipline to Universities (No.B16011), National Science & Technology Fundamental Resources Investigation Program of China (2018FY100300) and sponsored by Program for Science & Technology Innovation Talents in Universities of Henan Province (21HASTIT015). The authors also wish to thank the editors and anonymous reviewers for their useful comments and suggestions on this manuscript.

RIGHTS & PERMISSIONS

2020 Higher Education Press
AI Summary AI Mindmap
PDF(1826 KB)

Accesses

Citations

Detail

Sections
Recommended

/