Skip to main content

Advertisement

Log in

Carbon fluxes within tree-crop-grass agroforestry system: 13C field labeling and tracing

  • Original Paper
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

Agroforestry systems are characterized by a high complexity between vegetation components and niche partitioning. In a crop-grass-tree agroforestry system, rape, willow, and grasses were in situ pulse labeled separately with 13CO2 for 6 h, and 13C was traced in shoots, roots, topsoil (0–15 cm) and subsoil (15–30 cm), microbial biomass carbon (C), and dissolved organic C, as well as respiration losses (CO2) up to 28 days after labeling to investigate the effects of vegetation components on C allocation belowground. 13C recovery in roots after 28 days was 7.0% of total assimilated C for grassland, which was 3.5- and 5.2-fold higher than that for rape and willow, respectively. The larger C allocation belowground in grassland was ascribed to its higher root/shoot ratio compared to willow and rape. Grassland facilitated higher accumulation of root-derived C in soil compared to rape (9.2% of recovered 13C) and compared to willow (1.6% of 13C). Willow retained more photosynthetic C aboveground and less was allocated to roots compared to rape. Although the C allocated to the top 15-cm soil was similar between willow and rape, willow facilitated C allocation in deeper soil compared to rape (0.6% vs. 0.2%). This could be explained by the lower microbial activity and subsequent weaker decomposition of rhizodeposits in 15–30-cm depth under willow. The net belowground C inputs in grassland, willow, and rape were 0.53, 0.06, and 0.10 g C m−2 month−1 of vegetation period, including rhizodeposition of 0.24, 0.05, and 0.04 g C m−2 month−1, respectively. Overall, integrating trees and grassland within cropland facilitates higher root-derived C input into soil, thus contributing to the soil C sequestration in agroforestry systems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  • Anderson-Teixeira KJ, Masters MD, Black CK, Zeri M, Zaman H, Bernacchi CJ, Delucia EH (2013) Altered belowground carbon cycling following land-use change to perennial bioenergy crops. Ecosystems 16:508–520

    Article  CAS  Google Scholar 

  • Bahn M, Lattanzi FA, Hasibeder R, Wild B, Koranda M, Danese V, Brüggemann N, Schmitt M, Siegwolf R, Richter A (2013) Responses of belowground carbon allocation dynamics to extended shading in mountain grassland. New Phytol 198:116–126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blagodatskaya EV, Blagodatsky SA, Anderson T, Kuzyakov Y (2007) Priming effects in Chernozem induced by glucose and N in relation to microbial growth strategies. Appl Soil Ecol 37:95–105

    Article  Google Scholar 

  • Blagodatskaya E, Yuyukina T, Blagodatsky S, Kuzyakov Y (2011) Turnover of soil organic matter and of microbial biomass under C3–C4 vegetation change: consideration of 13C fractionation and preferential substrate utilization. Soil Biol Biochem 43:159–166

    Article  CAS  Google Scholar 

  • Buckeridge KM, Mason KE, Ostle N, McNamara NP, Grant HK, Whitaker J (2022) Microbial necromass carbon and nitrogen persistence are decoupled in agricultural grassland soils. Commun Earth Environ 3:1–10

    Article  Google Scholar 

  • Cheng W, Parton WJ, Gonzalez-Meler MA, Phillips R, Asao S, McNickle GG, Brzostek E, Julie D, Jastrow Jastrow JD (2014) Synthesis and modeling perspectives of rhizosphere priming. New Phytol 201:31–44

    Article  CAS  PubMed  Google Scholar 

  • Clemmensen KE, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A, Wallander H, Stenlid J, Finlay RD, Wardle DA, Lindahl BD (2013) Roots and associated fungi drive long-term carbon sequestration in boreal forests. Science 339:1615–1618

    Article  CAS  PubMed  Google Scholar 

  • De Deyn GB, Cornelissen JHC, Bardgett RD (2008) Plant functional traits and soil carbon sequestration in contrasting biomes. Ecol Lett 11:516–531

    Article  PubMed  Google Scholar 

  • De Deyn GB, Quirk H, Oakley S, Ostle N, Bardgett RD (2011) Rapid transfer of photosynthetic carbon through the plant-soil system in differently managed species-rich grasslands. Biogeosciences 8:1131–1139

    Article  CAS  Google Scholar 

  • Domanski G, Kuzyakov Y, Siniakina S, Stahr K (2001) Carbon flows in the rhizosphere of ryegrass (Lolium perenne). J Plant Nutr Soil Sci 164:381–387

    Article  CAS  Google Scholar 

  • Ehret M, Bühle L, Graß R, Lamersdorf N, Wachendorf M (2015) Bioenergy provision by an alley cropping system of grassland and shrub willow hybrids: biomass, fuel characteristics and net energy yields. Agrofor Syst 89:365–381

    Article  Google Scholar 

  • Eisenhauer N, Beßler H, Engels C, Gleixner G, Habekost M, Milcu A, Partsch ACW, Sabais C, Scherber S, Steinbeiss A, Weigeit WW, Scheu S (2010) Plant diversity effects on soil microorganisms support the singular hypothesis. Ecology 91:485–496

    Article  CAS  PubMed  Google Scholar 

  • Franke AC, Laberge G, Oyewole BD, Schulz S (2008) A comparison between legume technologies and fallow, and their effects on maize and soil traits, in two distinct environments of the West African savannah. Nutr Cycl Agroecosystems 82:117–135

    Article  Google Scholar 

  • Freschet GT, Cornwell WK, Wardle DA (2013) Linking litter decomposition of above- and below-ground organs to plant-soil feedbacks worldwide. J Ecol 101:943–952

    Article  CAS  Google Scholar 

  • Hafner S, Unteregelsbacher B, Seeber E, Lena B, Xu X, Li X, Guggenberger G, Miehe G, Kuzyakov Y (2012) Effect of grazing on carbon stocks and assimilate partitioning in a Tibetan montane pasture revealed by 13CO2 pulse labeling. Glob Change Biol 18:528–538

    Article  Google Scholar 

  • Hasibeder R, Fuchslueger L, Richter A, Bahn M (2015) Summer drought alters carbon allocation to roots and root respiration in mountain grassland. New Phytol 205:1117–1127

    Article  CAS  PubMed  Google Scholar 

  • Högberg MN, Bååth E, Nordgren A, Arnebrant K, Högberg P (2003) Contrasting effects of nitrogen availability on plant carbon supply to mycorrhizal fungi and saprotrophs - a hypothesis based on field observations in boreal forest. New Phytol 160:225–238

    Article  PubMed  CAS  Google Scholar 

  • Huang XM, Liu SR, Wang H, Hu ZD, Li ZG, You YM (2014) Changes of soil microbial biomass carbon and community composition through mixing nitrogen-fixing species with Eucalyptus urophylla in subtropical China. Soil Biol Biochem 73:42–48

    Article  CAS  Google Scholar 

  • Ingrisch J, Karlowsky S, Hasibeder R, Gleixner G, Bahn M (2020) Drought and recovery effects on belowground respiration dynamics and the partitioning of recent carbon in managed and abandoned grassland. Glob Change Biol 26:4366–4378

    Article  Google Scholar 

  • Kell DB (2012) Large-scale sequestration of atmospheric carbon via plant roots in natural and agricultural ecosystems: why and how. Philos Trans r Soc B Biol Sci 367:1589–1597

    Article  CAS  Google Scholar 

  • Kravchenko A, Guber A, Razavi BS, Koestel J, Quigley MY, Robertson GP, Kuzyakov Y (2019) Microbial spatial footprint as a driver of soil carbon stabilization. Nat Commun 10:3121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kravchenko AN, Zheng H, Kuzyakov Y, Robertson GP, Guber A (2021) Belowground interplant carbon transfer promotes soil carbon gains in diverse plant communities. Soil Biol Biochem 159:108297

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kuzyakov Y, Domanski G (2000) Carbon inputs into soil. Rev J Plant Nutr Soil Sci 163:421–423

    Article  CAS  Google Scholar 

  • Kuzyakov Y, Gavrichkova O (2010) Time lag between photosynthesis and carbon dioxide efflux from soil: a review. Glob Change Biol 16:3386–3406

    Article  Google Scholar 

  • Lal R (2004) Soil carbon sequestration impacts on global climate change and food security. Science 304:1623–1627

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Scheunemann N, Potapov AM, Shi L, Pausch J, Scheu S, Pollierer MM (2020) Incorporation of root-derived carbon into soil microarthropods varies between cropping systems. Biol Fertil Soils 56:839–851

    Article  CAS  Google Scholar 

  • Liu M, Quyang SN, Tian YQ, Wen SH, Zhao Y, Li XB, Baoyin T, Kuzyakov Y, Xu XL (2021) Effects of rotational and continuous overgrazing on newly assimilated C allocation. Biol Fertil Soils 57:193–202

    Article  CAS  Google Scholar 

  • Meier IC, Finzi AC, Phillips RP (2017) Root exudates increase N availability by stimulating microbial turnover of fast-cycling N pools. Soil Biol Biochem 106:119–128

    Article  CAS  Google Scholar 

  • Midwood AJ, Boutton TW (1998) Soil carbonate decomposition by acid has little effect on δ13C of organic matter. Soil Biol Biochem 30:1301–1307

    Article  CAS  Google Scholar 

  • Miltner A, Bombach P, Brücken BS, Kästner M (2011) SOM genesis: microbial biomass as a significant source. Biogeochemistry 111:41–55

    Article  CAS  Google Scholar 

  • Orwin KH, Kirschbaum MUF, St John MG, Dickie IA (2011) Organic nutrient uptake by mycorrhizal fungi enhances ecosystem carbon storage: a model-based assessment. Ecol Lett 14:493–502

    Article  PubMed  Google Scholar 

  • Panchal P, Preece C, Peñuelas J, Giri J (2022) Soil carbon sequestration by root exudates. Trends Plant Sci 27:749–757

    Article  PubMed  CAS  Google Scholar 

  • Pang R, Xu X, Tian Y, Cui X, Ouyang X, Kuzyakov Y (2021) In-situ 13CO2 labeling to trace carbon fluxes in plant-soil-microorganism systems: review and methodological guideline. Rhizosphere 20:100441

    Article  Google Scholar 

  • Paterson E, Gebbing T, Abel C, Sim A, Telfer G (2007) Rhizodeposition shapes rhizosphere microbial community structure in organic soil. New Phytol 173:600–610

    Article  CAS  PubMed  Google Scholar 

  • Pausch J, Kuzyakov Y (2018) Carbon input by roots into the soil: quantification of rhizodeposition from root to ecosystem scale. Glob Change Biol 24:1–12

    Article  Google Scholar 

  • Pausch J, Kramer S, Scharroba A, Scheunemann N, Butenschoen O, Kandele E, Marhan S, Riederer M, Scheu S, Kuzyakov Y, Ruess L (2016) Small but active-pool size does not matter for carbon incorporation in below-ground food webs. Funct Ecol 30:479–489

    Article  Google Scholar 

  • Rabbi SM, Tighe MK, Flavel RJ, Kaiser BN, Guppy CN, Zhang X, Young IM (2018) Plant roots redesign the rhizosphere to alter the three-dimensional physical architecture and water dynamics. New Phytol 219:542–550

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kögel-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  CAS  PubMed  Google Scholar 

  • Schmitt A, Pausch J, Kuzyakov Y (2013) C and N allocation in soil under ryegrass and alfalfa estimated by 13C and 15N labelling. Plant Soil 368:581–590

    Article  CAS  Google Scholar 

  • Shahzad T, Chenu C, Genet P, Barot S, Perveen N, Mougin C, Fontaine S (2015) Contribution of exudates, arbuscular mycorrhizal fungi and litter depositions to the rhizosphere priming effect induced by grassland species. Soil Biol Biochem 80:146–155

    Article  CAS  Google Scholar 

  • Shi L, Feng W, Xu J, Kuzyakov Y (2018) Agroforestry systems: meta-analysis of soil carbon stocks, sequestration processes, and future potentials. Land Degrad Dev 29:3886–3897

    Article  Google Scholar 

  • Sommer J, Dippold MA, Flessa H, Kuzyakov Y (2016) Allocation and dynamics of C and N within plant-soil system of ash and beech. J Plant Nutr Soil Sc 179:376–387

    Article  CAS  Google Scholar 

  • Sousa FP, Ferreira TO, Mendonça ES, Romero RE, Oliveira JGB (2012) Carbon and nitrogen in degraded Brazilian semi-arid soils undergoing desertification. Agric Ecosyst Environ 148:11–21

    Article  CAS  Google Scholar 

  • Studer MS, Siegwolf RTW, Abiven S (2014) Carbon transfer, partitioning and residence time in the plant-soil system: a comparison of two 13CO2 labelling techniques. Biogeosciences 11:1637–1648

    Article  CAS  Google Scholar 

  • Sun T, Zhou J, Shi L, Feng W, Dippold MA, Zang H, Kurganova I, Lopesde Gerenyu V, Kalinina O, Gian L, Kuzyakov Y (2022) Microbial growth rates, carbon use efficiency and enzyme activities during post-agricultural soil restoration. CATENA 214:106226

    Article  CAS  Google Scholar 

  • Tariq A, Gunina A, Lamersdorf N (2018) Initial changes in soil properties and carbon sequestration potential under monocultures and short-rotation alley coppices with poplar and willow after three years of plantation. Sci Total Environ 634:963–973

    Article  CAS  PubMed  Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707

    Article  CAS  Google Scholar 

  • Wang SP, Wilkes A, Zhang ZC, Chang XF, Lang R, Wang YF, Niu HS (2011) Management and land use change effects on soil carbon in northern China’s grasslands: a synthesis. Agric Ecosyst Environ 142:329–340

    Article  Google Scholar 

  • Wang X, Yang Y, Pei K, Zhou J, Peixoto L, Gunina A, Zeng Z, Zang H, Rasmussen J, Kuzyakov Y (2021) Nitrogen rhizodeposition by legumes and its fate in agroecosystems: a field study and literature review. Land Degrad Dev 32:410–419

    Article  Google Scholar 

  • Warembourg FR, Estelrich HD (2001) Plant phenology and soil fertility effects on below-ground carbon allocation for an annual (Bromus madritensis) and a perennial (Bromus erectus) grass species. Soil Biol Biochem 33:1291–1303

    Article  CAS  Google Scholar 

  • Wu J, Jorgensen RG, Pommerening B, Chaussod R, Brookes PC (1990) Measurement of soil microbial biomass-C by fumigation-extraction e an automated procedure. Soil Biol Biochem 22:1167–1169

    Article  CAS  Google Scholar 

  • Xu X, Kuzyakov Y, Wanek W, Richter A (2008) Root-derived respiration and non-structural carbon of rice seedlings. Eur J Soil Biol 44:22–29

    Article  CAS  Google Scholar 

  • Yan Z, Zhou J, Yang L, Gunina A, Yang Y, Peixoto L, Zeng ZH, Zang HD, Kuzyakov Y (2022) Diversified cropping systems benefit soil carbon and nitrogen stocks by increasing aggregate stability: results of three fractionation methods. Sci Total Environ 824:153878

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Furey G, Lehman C, Tilman D (2019) Soil carbon sequestration accelerated by restoration of grassland biodiversity. Nat Commun 10:1–7

    CAS  Google Scholar 

  • Zang H, Xiao M, Wang Y, Ling N, Wu J, Ge T, Kuzyakov Y (2019) Allocation of assimilated carbon in paddies depending on rice age, chase period and N fertilization: experiment with 13CO2 labeling and literature synthesis. Plant Soil 445:113–123

    Article  CAS  Google Scholar 

  • Zang H, Zhou J, Marshall MR, Chadwick DR, Wen Y, Jones DL (2020) Microplastics in the agroecosystem: are they an emerging threat to the plant-soil system? Soil Biol Biochem 148:107926

    Article  CAS  Google Scholar 

  • Zhao L, Chen DD, Zhao N, Li Q, Cheng Q, Lua CY, Xu SX, Wang SP, Zhao XQ (2015) Responses of carbon transfer, partitioning, and residence time to land use in the plant-soil system of an alpine meadow on the Qinghai-Tibetan Plateau. Biol Fertil Soils 51:781–790

    Article  CAS  Google Scholar 

  • Zhou J, Zang H, Loeppmann S, Gube M, Kuzyakov Y, Pausch J (2020) Arbuscular mycorrhiza enhances rhizodeposition and reduces the rhizosphere priming effect on the decomposition of soil organic matter. Soil Biol Biochem 140:107641

    Article  CAS  Google Scholar 

  • Zhou J, Wen Y, Shi L, Marshall MR, Kuzyakov Y, Blagodatskaya E, Zang H (2021a) Strong priming of soil organic matter induced by frequent input of labile carbon. Soil Biol Biochem 152:108069

    Article  CAS  Google Scholar 

  • Zhou J, Gui H, Banfield CC, Wen Y, Zang HD, Dippold MA, Charlton A, Jones DL (2021b) The microplastisphere: biodegradable microplastics addition alters soil microbial community structure and function. Soil Biol Biochem 156:108211

    Article  CAS  Google Scholar 

  • Zhu X, Liu W, Chen J, Bruijnzeel LA, Mao Z, Yang X, Cardinael R, Meng FR, Sidle RC, Seitz S, Nair VD, Nanko K, Zhou X, Chen CF, Jiang XJ (2020) Reductions in water, soil and nutrient losses and pesticide pollution in agroforestry practices: a review of evidence and processes. Plant Soil 453:45–86

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The isotopic analyses were performed at the Centre for Stable Isotope Research and Analysis (KOSI), Göttingen. Yakov Kuzyakov thanks the RUDN University Strategic Academic Leadership Program. Jie Zhou (201606850093) and Guodong Shao (201703270029) also thank the China Scholarship Council (CSC) for supporting their study in Germany.

Funding

This study was financially supported by the German Research Foundation (DFG) within the project BMBF project SIGNAL, the National Natural Science Foundation of China (318611430002), and the Yunnan Fundamental Research Projects (202101AS070045).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lingling Shi.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOC 2270 KB)

Supplementary file2 (DOC 840 KB)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhou, J., Shao, G., Kumar, A. et al. Carbon fluxes within tree-crop-grass agroforestry system: 13C field labeling and tracing. Biol Fertil Soils 58, 733–743 (2022). https://doi.org/10.1007/s00374-022-01659-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-022-01659-4

Keywords

Navigation