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Research Article | Open Access

Subtropical forest macro-decomposers rapidly transfer litter carbon and nitrogen into soil mineral-associated organic matter

Guoxiang Niub,c,dTao Liua,c,e( )Zhen ZhaocXuebing ZhangcHuiling GuancXiaoxiang HecXiankai Luc
National Engineering Laboratory for Applied Technology of Forestry and Ecology in South China, Central South University of Forestry and Technology, Changsha, 410004, China
Lushan Botanical Garden, Chinese Academy of Sciences, Jiujiang, 332900, China
Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, 510650, China
Section of Microbial Ecology, Department of Biology, Lund University, Lund, 22362, Sweden
Lutou National Station for Scientific Observation and Research of Forest Ecosystem in Hunan Province, Yueyang, 414000, China
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Abstract

Background

Forest soils in tropical and subtropical areas store a significant amount of carbon. Recent frameworks to assess soil organic matter (SOM) dynamics under evolving global conditions suggest that dividing bulk SOM into particulate and mineral-associated organic matter (POM vs. MAOM) is a promising method for identifying how SOM contributes to reducing global warming. Soil macrofauna, earthworms, and millipedes have been found to play an important role in facilitating SOM processes. However, how these two co-existing macrofaunae impact the litter decomposition process and directly impact the formation of POM and MAOM remains unclear.

Methods

Here, we set up a microcosm experiment, which consisted of 20 microcosms with four treatments: earthworm and litter addition (E), millipedes and litter addition (M), earthworm, millipedes, and litter addition (E+M), and control (only litter addition) in five replicates. The soil and litter were sterilized prior to beginning the incubation experiment to remove any existing microbes. After incubating the samples for 42 days, the litter properties (mass, C, and N contents), soil physicochemical properties, as well as the C and N contents, and POM and MAOM 13C abundance in the 0–5 and 5–10 ​cm soil layers were measured. Finally, the relative influences of soil physicochemical and microbial properties on the distribution of C and N in the soil fractions were analyzed.

Results

The litter mass, C, and N associated with all four treatments significantly decreased after incubation, especially under treatment E+M (litter mass: −58.8%, litter C: −57.0%, litter N: −75.1%, respectively), while earthworm biomass significantly decreased under treatment E. Earthworm or millipede addition alone showed no significant effects on the organic carbon (OC) and total nitrogen (TN) content in the POM fraction, but joint addition of both significantly increased OC and TN regardless of soil depth. Importantly, all three macrofauna treatments increased the OC and TN content and decreased the 13C abundance in the MAOM fraction. More than 65% of the total variations in the distribution of OC and TN throughout the two fractions can be explained by a combination of soil physicochemical and microbial properties. Changes in the OC distribution in the 0–5 ​cm soil layer are likely due to a decrease in soil pH and an increase in arbuscular mycorrhizal fungi (AMF), while those in the 5–10 ​cm layer are probably caused by increases in soil exchangeable Ca and Mg, in addition to fungi and gram-negative (GN) bacteria. The observed TN distribution changes in the 0–5 ​cm soil likely resulted from a decrease in soil pH and increases in AMF, GN, and gram-negative (GP) bacteria, while TN distribution changes in the 5–10 ​cm soil could be explained by increases in exchangeable Mg and GN bacteria.

Conclusions

The results indicate that the coexistence of earthworms and millipedes can accelerate the litter decomposition process and store more C in the MAOM fractions. This novel finding helps to unlock the processes by which complex SOM systems serve as C sinks in tropical forests and addresses the importance of soil macrofauna in maintaining C-neutral atmospheric conditions under global climate change.

References

 

Andreas, N., 2020. Tropical forests lost to land grabbing. Nat. Geosci. 13, 460–462.

 

Angst, G., Mueller, C., Prater, I., Angst, Š., Frouz, J., Jílková, V., Peterse, F., Nierop, K., 2019. Earthworms act as biochemical reactors to convert labile plant compounds into stabilized soil microbial necromass. Commun. Biol. 2, 441.

 

Angst, G., Frouz, J., van-Groenigen, J., Scheu, S., Kögel-Knabner, I., Eisenhauer, N., 2022. Earthworms as catalysts in the formation and stabilization of soil microbial necromass. Global Change Biol. 28, 4775–4782.

 

Angst, G., Mueller, K., Castellano, M., Vogel, C., Wiesmeier, M., Mueller, C., 2023. Unlocking complex soil systems as carbon sinks: multi-pool management as the key. Nat. Commun. 14, 2967.

 

Arrazola-Vasquez, E., Larsbo, M., Capowiez, Y., Taylor, A., Sandin, M., Iseskog, D., Keller, T., 2022. Earthworm burrowing modes and rates depend on earthworm species and soil mechanical resistance. Appl. Soil Ecol. 178, 104568.

 

Bahram, M., Hildebrand, F., Forslund, S.K., Anderson, J.L., Soudzilovskaia, N.A., Bodegom, P.M., Bengtsson-Palme, J., Anslan, S., Coelho, L.P., Harend, H., Huerta-Cepas, J., Medema, M.H., Maltz, M.R., Mundra, S., Olsson, P.A., Pent, M., Põlme, S., Sunagawa, S., Ryberg, M., Tedersoo, L., Bork, P., 2018. Structure and function of the global topsoil microbiome. Nature 560, 233–237.

 

Bajwa, R., Read, D.J., 1985. The biology of mycorrhiza in the Ericaceae: Ⅸ. Peptides as nitrogen sources for the ericoid endophyte and for mycorrhizal and non-mycorrhizal plants. New Phytol. 101, 459–467.

 

Bar-On, Y.M., Phillips, R., Milo, R., 2018. The biomass distribution on Earth. Proc. Natl. Acad. Sci. USA 115, 6506–6511.

 

Blouin, M., Hodson, M., Delgado, E., Baker, G., Brussaard, L., Butt, K., Dai, J., Dendooven, L., Peres, G., Tondoh, J., Cluzeau, D., Brun, J., 2013. A review of earthworm impact on soil function and ecosystem services. Eur. J. Soil Sci. 64, 161–182.

 

Bradford, M.A., Tordoff, G.M., Eggers, T., Jones, T.H., Newington, J.E., 2002. Microbiota, fauna, and mesh size interactions in litter decomposition. Oikos 99, 317–323.

 

Bradford, M.A., Wieder, W.R., Bonan, G.B., Fierer, N., Raymond, P.A., Crowther, T.W., 2016. Managing uncertainty in soil carbon feedbacks to climate change. Nat. Clim. Change 6, 751–758.

 

Chandel, A.K., Jiang, L., Luo, Y., 2023. Microbial models for simulating soil carbon dynamics: a review. JGR Biogeosciences 128, e2023JG007436.

 

Chen, L., Fang, K., Wei, B., Qin, S., Feng, X., Hu, T., Ji, C., Yang, Y., 2021. Soil carbon persistence governed by plant input and mineral protection at regional and global scales. Ecol. Lett. 24, 1018–1028.

 

Cotrufo, M.F., Soong, J.L., Horton, A.J., Campbell, E.E., Haddix, M.L., Wall, D.H., Parton, W.J., 2015. Formation of soil organic matter via biochemical and physical pathways of litter mass loss. Nat. Geosci. 8, 776–779.

 

Cotrufo, M.F., Ranalli, M.C., Haddix, M.L., Six, J., Lugato, E., 2019. Soil carbon storage informed by particulate and mineral-associated organic matter. Nat. Geosci. 12, 989–994.

 

Craig, M., Gryer, K., Beidler, K., Brzostek, E., Frey, S., Grandy, A., Liang, C., Phillips, R., 2022. Fast-decaying plant litter enhances soil carbon in temperate forests but not through microbial physiological traits. Nat. Commun. 13, 1229.

 

Dong, Y., Agathokleous, E., Liu, S., Yu, Z., 2023. Demographic changes in China's forests from 1998 to 2018. For. Ecosyst. 10, 100094.

 
Edwards, C.A., Arancon, N., Bohlen, P.J., Hendrix, P., 2013. Biology and Ecology of Earthworms. Springer, New York.
 

El-Wakeil, K.F.A., 2015. Effects of terrestrial isopods (crustacea: oniscidea) on leaf litter decomposition processes. J. Basic Appl. Zool. 69, 10–16.

 

Frouz, J., Pižl, V., Tajovský, K., Balík, H., Starý, J., Lukesšová, A., Šourková, M., 2004. The role of saprophagous macro-fauna on soil formation in reclaimed and non-reclaimed post-mining sites in Central Europe. Int. J. Ecol. Environ. Sci. 30, 257–261.

 

Gergocs, V., Hufnagel, L., 2016. The effect of microarthropods on litter decomposition depends on litter quality. Eur. J. Soil Biol. 75, 24–30.

 

Gill, A., Schilling, J., Hobbie, S., 2021. Experimental nitrogen fertilization globally accelerates, then slows decomposition of leaf litter. Ecol. Lett. 24, 802–811.

 

Gongalsky, K.B., 2021. Soil macrofauna: study problems and perspectives. Soil Biol. Biochem. 159, 108281.

 

Gonzälez, G., Seastedt, T.R., 2001. Soil fauna and plant litter decomposition in tropical and subalpine forests. Ecology 82, 955–964.

 

Grayston, S.J., Campbell, C.D., Bardgett, R.D., Mawdsley, J.L., Clegg, C.D., Ritz, K., Griffiths, B.S., Rodwell, J.S., Edwards, S.J., Davies, W.J., Elston, D.J., Millard, P., 2004. Assessing shifts in microbial community structure across a range of grasslands of differing management intensity using CLPP, PLFA and community DNA techniques. Appl. Soil Ecol. 25, 63–84.

 

Hendriksen, N.B., 1990. Leaf litter selection by detritivore and geophagous earthworms. Biol. Fertil. Soils 10, 17–21.

 

Huang, W., González, G., Zou, X., 2020. Earthworm abundance and functional group diversity regulate plant litter decay and soil organic carbon level: a global meta-analysis. Appl. Soil Ecol. 150, 103473.

 

Jackson, R.B., Lajtha, K., Crow, S.E., Hugelius, G., Kramer, M.G., Pineiro, G., 2017. The ecology of soil carbon: pools, vulnerabilities, and biotic and abiotic controls. Annu. Rev. Ecol. Evol. 48, 419–445.

 

Joly, F., Coq, S., Coulis, M., Nahmani, J., Hättenschwiler, S., 2018. Litter conversion into detritivore faeces reshuffles the quality control over C and N dynamics during decomposition. Funct. Ecol. 32, 2605–2614.

 

Kleber, M., Bourg, I.C., Coward, E.K., Hansel, C.M., Myneni, S.C.B., Nunan, N., 2021. Dynamic interactions at the mineral–organic matter interface. Nat. Rev. Earth Environ. 2, 402–421.

 

Lai, J., Zou, Y., Zhang, J., Peres-Neto, P., 2022. Generalizing hierarchical and variation partitioning in multiple regression and canonical analyses using the rdacca. hp R package. Methods Ecol. Evol. 13, 782–788.

 

Lavallee, J., Soong, J., Cotrufo, M., 2020. Conceptualizing soil organic matter into particulate and mineral-associated forms to address global change in the 21st century. Global Change Biol. 26, 261–273.

 

Le-Mer, G., Jouquet, P., Capowiez, Y., Maeght, J., Tran, T.M., Doan, T.T., Bottinelli, N., 2021. Age matters: dynamics of earthworm casts and burrows produced by the anecic Amynthas khami and their effects on soil water infiltration. Geoderma 382, 114709.

 

Lehmann, J., Hansel, C.M., Kaiser, C., Kleber, M., Maher, K., Manzoni, S., Nunan, N., Reichstein, M., Schimel, J., Torn, M., Wieder, W., Kögel-Knabner, I., 2020. Persistence of soil organic carbon caused by functional complexity. Nat. Geosci. 13, 529–534.

 

Li, X., Zhang, Q., Feng, J., Jiang, D., Zhu, B., 2023. Forest management causes soil carbon loss by reducing particulate organic carbon in Guangxi, Southern China. For. Ecosyst. 10, 100092.

 

Liang, C., Schimel, J.P., Jastrow, J.D., 2017. The importance of anabolism in microbial control over soil carbon storage. Nat. Microbiol. 2, 17105.

 

Liu, T., Wang, Z., Guan, H., Zhong, B., He, X., Wang, Y., Qi, Y., Yan, W., Lu, X., 2023. Soil macrofauna disperse and reconstruct soil nematode communities: takeaways from a microcosm study. Forests 14, 748.

 

Lugato, E., Lavallee, J.M., Haddix, M.L., Panagos, P., Cotrufo, M.F., 2021. Different climate sensitivity of particulate and mineral-associated soil organic matter. Nat. Geosci. 14, 295–300.

 

Lyu, M., Homyak, P.M., Xie, J., Peñuelas, J., Ryan, M.G., Xiong, X., Sardans, J., Lin, W., Wang, M., Chen, G., Yang, Y., 2023. Litter quality controls tradeoffs in soil carbon decomposition and replenishment in a subtropical forest. J. Ecol. 111, 2181–2193.

 

Macias, A., Marek, P., Morrissey, E., Brewer, M., Short, D., Stauder, C., Wickert, K., Berger, M., Metheny, A., Stajich, J., Boyce, G., Rio, R., Panaccione, D., Wong, V., Jones, T., Kasson, M., 2019. Diversity and function of fungi associated with the fungivorous millipede, Brachycybe lecontii. Fungal Ecol. 41, 187–197.

 

Mendez-Millen, M., Nguyen Tu, T., 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.

 

Niu, G., Hasi, M., Wang, R., Wang, Y., Geng, Q., Hu, S., Xu, X., Yang, J., Wang, C., Han, X., Huang, J., 2021. Soil microbial community responses to long-term nitrogen addition at different soil depths in a typical steppe. Appl. Soil Ecol. 167, 104054.

 

Niu, G., Liu, L., Wang, Y., Guan, H., Ning, Q., Liu, T., Rousk, K., Zhong, B., Yang, J., Lu, X., Han, X., Huang, J., 2022. Effects of decadal nitrogen addition on carbon and nitrogen stocks in different organic matter fractions of typical steppe soils. Ecol. Indic. 144, 109471.

 

Pant, M., Negi, G., Kumar, P., 2017. Macrofauna contributes to organic matter decomposition and soil quality in Himalayan agroecosystems, India. Appl. Soil Ecol. 120, 20–29.

 

Pelosi, C., Barot, S., Capowiez, Y., Hedde, M., Vandenbulcke, F., 2014. Pesticides and earthworms. A review. Agron. Sustain. Dev. 34, 199–228.

 

Potapov, A.M., Rozanova, O.L., Semenina, E.E., Leonov, V.D., Belyakova, O.I., Bogatyreva, V.Y., Degtyarev, M.I., Esaulov, A.S., Korotkevich, A.Y., Kudrin, A.A., Malysheva, E.A., Mazei, Y.A., Tsurikov, S.M., Zuev, A.G., Tiunov, A.V., 2021. Size compartmentalization of energy channeling in terrestrial belowground food webs. Ecology 102, e03421.

 

Potapov, A.M., Beaulieu, F., Birkhofer, K., Bluhm, S., Degtyarev, M., Goncharov, A., Gongalsky, K., Klarner, B., Korobushkin, D., Liebke, D., Maraun, M., Mc Donnell, R., Pollierer, M., Schaefer, I., Shrubovych, J., Semenyuk, I., Sendra, A., Tuma, J., Tumova, M., Vassilieva, A., Chen, T., Geisen, S., Schmidt, O., Tiunov, A., Scheu, S., 2022. Feeding habits and multifunctional classification of soil-associated consumers from protists to vertebrates. Biol. Rev. 97, 1057–1117.

 

Rochette, P., Flanagan, L.B., Gregorich, E.G., 1999. Separating soil respiration into plant and soil components using analyses of the natural abundance of carbon-13. Soil Sci. Soc. Am. J. 63, 1207–1213.

 

Rossel, R., Lee, J., Behrens, T., Luo, Z., Baldock, J., Richards, A., 2019. Continental-scale soil carbon composition and vulnerability modulated by regional environmental controls. Nat. Geosci. 12, 547–552.

 

Sauvadet, M., Chauvat, M., Fanin, N., Coulibaly, S., Bertrand, I., 2016. Comparing the effects of litter quantity and quality on soil biota structure and functioning: application to a cultivated soil in Northern France. Appl. Soil Ecol. 107, 261–271.

 

Scheu, S., Schaefer, M., 1998. Bottom-up control of the soil macrofauna community in a beechwood on limestone: manipulation of food resources. Ecology 79, 1573–1585.

 

Seeber, J., Scheu, S., Meyer, E., 2006. Effects of macro-decomposers on litter decomposition and soil properties in alpine pastureland: a mesocosm experiment. Appl. Soil Ecol. 34, 168–175.

 

Snyder, B.A., Hendrix, P.F., 2008. Current and potential roles of soil macroinvertebrates (earthworms, millipedes, and isopods) in ecological restoration. Restor. Ecol. 16, 629–636.

 

Špaldoňová, A., Frouz, J., 2014. The role of Armadillidium vulgare (isopoda: oniscidea) in litter decomposition and soil organic matter stabilization. Appl. Soil Ecol. 83, 186–192.

 

Tian, G., Brussaard, L., Kang, B.T., 1995. Breakdown of plant residues with contrasting chemical compositions under humid tropical conditions: effects of earthworms and millipedes. Soil Biol. Biochem. 27, 277–280.

 

Toyota, K., Kimura, M., 2000. Microbial community indigenous to the earthworm Eisenia foetida. Biol. Fertil. Soils 31, 187–190.

 

Verbaendert, I., Boon, N., De Vos, P., Heylen, K., 2011. Denitrification is a common feature among members of the genus Bacillus. Syst. Appl. Microbiol. 34, 385–391.

 

Vidal, A., Blouin, M., Lubbers, I., Capowiez, Y., Sanchez-Hernandez, J., Calogiuri, T., van-Groenigen, J., 2023. The role of earthworms in agronomy: consensus, novel insights and remaining challenges. Adv. Agron. 181, 1–78. https://doi.org/10.1016/bs.agron.2023.05.001.

 

Wardle, D.A., Bardgett, R.D., Klironomos, J.N., Stetälä, H., Van der putten, W.H., Wall, D.H., 2004. Ecological linkages between aboveground and belowground biota. Science 304, 1629–1633.

 

Yang, X., Shao, M., Li, T., 2020. Effects of terrestrial isopods on soil nutrients during litter decomposition. Geoderma 376, 114546.

Forest Ecosystems
Article number: 100172
Cite this article:
Niu G, Liu T, Zhao Z, et al. Subtropical forest macro-decomposers rapidly transfer litter carbon and nitrogen into soil mineral-associated organic matter. Forest Ecosystems, 2024, 11(2): 100172. https://doi.org/10.1016/j.fecs.2024.100172

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Received: 03 August 2023
Revised: 25 January 2024
Accepted: 25 January 2024
Published: 10 February 2024
© 2024 The Authors.

This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

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