Abstract
Purpose
Perennial forage systems (e.g., pastures and hayfields) cover a significant land area worldwide and are important for soil carbon storage; however, the degree to which these plant communities can be managed to accumulate and store soil carbon is not well understood. Additionally, less is known about how forage defoliation mediates C dynamics or if the effects of defoliation depend on plant community composition.
Methods
To address these questions, we quantified soil C pools and C-degrading enzyme activity in a three-year experiment where bicultures of alfalfa-orchardgrass and red clover-orchardgrass were managed under treatments of contrasting defoliation frequency (3 vs. 5 cuts per year) and severity (i.e., cutting height; 10 cm vs. 5 cm residual forage height).
Results
We found that more frequent defoliation resulted in greater permanganate oxidizable C (POX-C), particulate organic carbon (POC), mineral-associated organic C (MAOC), and the activity of β-glucosidase (BG) and cellobiohydrolase (CBH). The effects of defoliation frequency on total organic C (TOC) varied depending on biculture composition. Alfalfa-orchardgrass bicultures, characterized by a lower legume-grass proportion, had greater POX-C and lower hot-water extractable organic carbon (HWEOC) compared to red clover-orchardgrass which had a higher legume-grass proportion. We also found that BG activity and POX-C were positively correlated with MAOC and TOC. In contrast, we observed no effects of defoliation severity on any measured soil parameters.
Conclusion
Our study highlights that defoliation frequency and relative abundance of legumes to grass are both potential management levers for increasing SOC storage in legume-grass agroecosystems.
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References
Abdalla M, Hastings A, Chadwick DR et al (2018) Critical review of the impacts of grazing intensity on soil organic carbon storage and other soil quality indicators in extensively managed grasslands. Agric Ecosyst Environ 253:62–81. https://doi.org/10.1016/j.agee.2017.10.023
Acosta-Martínez V, Bell CW, Morris BEL et al (2010) Long-term soil microbial community and enzyme activity responses to an integrated cropping-livestock system in a semi-arid region. Agric Ecosyst Environ 137:231–240. https://doi.org/10.1016/j.agee.2010.02.008
Addo-danso SD, Prescott CE, Smith AR (2016) Methods for estimating root biomass and production in forest and woodland ecosystem carbon studies : a review. For Ecol Manag 359:332–351. https://doi.org/10.1016/j.foreco.2015.08.015
Averill C, Waring B (2018) Nitrogen limitation of decomposition and decay: how can it occur? Glob Chang Biol 24:1417–1427. https://doi.org/10.1111/gcb.13980
Awale R, Emeson MA, Machado S (2017) Soil organic carbon pools as early indicators for soil organic matter stock changes under different tillage practices in inland Pacific northwest. Front Ecol Evol 5:1–13. https://doi.org/10.3389/fevo.2017.00096
Ball KR, Baldock JA, Penfold C et al (2020) Soil organic carbon and nitrogen pools are increased by mixed grass and legume cover crops in vineyard agroecosystems: detecting short-term management effects using infrared spectroscopy. Geoderma 379:1–12. https://doi.org/10.1016/j.geoderma.2020.114619
Banger K, Toor GS, Biswas A et al (2010) Soil organic carbon fractions after 16-years of applications of fertilizers and organic manure in a Typic Rhodalfs in semi-arid tropics. Nutr Cycl Agroecosyst 86:391–399. https://doi.org/10.1007/s10705-009-9301-8
Bankó L, Gergely T, Marton CL, Hoffmann S (2021) Hot-water extractable C and N as indicators for 4p1000 goals in a temperate-climate long-term field experiment : a case study from Hungary. Ecol Indic 126. https://doi.org/10.1016/j.ecolind.2021.107364
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using {lme4}. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Boddy E, Hill PW, Farrar J, Jones DL (2007) Fast turnover of low molecular weight components of the dissolved organic carbon pool of temperate grassland field soils. Soil Biol Biochem 39:827–835. https://doi.org/10.1016/j.soilbio.2006.09.030
Bongiorno G, Bünemann EK, Oguejiofor CU et al (2019) Sensitivity of labile carbon fractions to tillage and organic matter management and their potential as comprehensive soil quality indicators across pedoclimatic conditions in Europe. Ecol Indic 99:38–50. https://doi.org/10.1016/j.ecolind.2018.12.008
Burns RG, DeForest JL, Marxsen J et al (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234. https://doi.org/10.1016/j.soilbio.2012.11.009
Cambardella CA, Elliott ET (1992) Particulate soil organic-matter changes across a grassland cultivation sequence. Soil Sci Soc Am J 56:777–783. https://doi.org/10.2136/sssaj1992.03615995005600030017x
Conant RT, Cerri CEP, Osborne BB, Paustian K (2017) Grassland management impacts on soil carbon stocks : a new synthesis. Ecol Appl 27:662–668. https://doi.org/10.1002/eap.1473
Contosta AR, Arndt KA, Campbell EE et al (2021) Management intensive grazing on New England dairy farms enhances soil nitrogen stocks and elevates soil nitrous oxide emissions without increasing soil carbon. Agric Ecosyst Environ 317:107471. https://doi.org/10.1016/j.agee.2021.107471
Cotrufo MF, Wallenstein MD, Boot CM et al (2013) The microbial efficiency-matrix stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Glob Chang Biol 19:988–995. https://doi.org/10.1111/gcb.12113
Cotrufo MF, Soong JL, Horton AJ et al (2015) Formation of soil organic matter via biochemical and physical pathways of litter mass loss. Nat Geosci 8:776–779. https://doi.org/10.1038/ngeo2520
Culman SW, Snapp SS, Freeman MA et al (2012) Permanganate Oxidizable carbon reflects a processed soil fraction that is sensitive to management. Soil Sci Soc Am J 76:494–504. https://doi.org/10.2136/sssaj2011.0286
de Moraes Sá JC, Potma Gonçalves DR, Ferreira LA et al (2018) Soil carbon fractions and biological activity based indices can be used to study the impact of land management and ecological successions. Ecol Indic 84:96–105. https://doi.org/10.1016/j.ecolind.2017.08.029
Delonge M, Basche A (2018) Managing grazing lands to improve soils and promote climate change adaptation and mitigation: a global synthesis. Renew Agric Food Syst 33:267–278. https://doi.org/10.1017/S1742170517000588
Dignac MF, Derrien D, Barré P et al (2017) Increasing soil carbon storage: mechanisms, effects of agricultural practices and proxies. A review. Agron Sustain Dev 37. https://doi.org/10.1007/s13593-017-0421-2
Dungait JAJ, Hopkins DW, Gregory AS, Whitmore AP (2012) Soil organic matter turnover is governed by accessibility not recalcitrance. Glob Chang Biol 18:1781–1796. https://doi.org/10.1111/j.1365-2486.2012.02665.x
Fornara DA, Tilman D, Hobbie SE (2009) Linkages between plant functional composition , fine root processes and potential soil N mineralization rates. J Ecol 97:48–56. https://doi.org/10.1111/j.1365-2745.2008.01453.x
Gavrichkova O, Moscatelli MC, Kuzyakov Y et al (2010) Influence of defoliation on CO2 efflux from soil and microbial activity in a Mediterranean grassland. Agric Ecosyst Environ 136:87–96. https://doi.org/10.1016/j.agee.2009.11.015
German DP, Weintraub MN, Grandy AS et al (2011) Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43:1387–1397. https://doi.org/10.1016/j.soilbio.2011.03.017
Ghani A, Dexter M, Perrott KW (2003) Hot-water extractable carbon in soils: a sensitive measurement for determining impacts of fertilisation, grazing and cultivation. Soil Biol Biochem 35:1231–1243. https://doi.org/10.1016/S0038-0717(03)00186-X
Gilmullina A, Rumpel C, Blagodatskaya E, Chabbi A (2020) Management of grasslands by mowing versus grazing – impacts on soil organic matter quality and microbial functioning. Appl Soil Ecol 156:1–34. https://doi.org/10.1016/j.apsoil.2020.103701
Hamilton EW, Frank DA (2001) Can plants stimulate soil microbes and their own nutrient supply? Evidence from a grazing tolerant grass. Ecology 82:2397–2402. https://doi.org/10.2307/2679923
Hamilton EW, Frank DA, Hinchey PM, Murray TR (2008) Defoliation induces root exudation and triggers positive rhizospheric feedbacks in a temperate grassland. Soil Biol Biochem 40:2865–2873. https://doi.org/10.1016/j.soilbio.2008.08.007
Haynes RJ (2005) Labile organic matter fractions as central components of the quality of agricultural soils: an overview. Adv Agron 85:221–268. https://doi.org/10.1016/S0065-2113(04)85005-3
Hewins DB, Broadbent T, Carlyle CN, Bork EW (2016) Extracellular enzyme activity response to defoliation and water addition in two ecosites of the mixed grass prairie. Agric Ecosyst Environ 230:79–86. https://doi.org/10.1016/j.agee.2016.05.033
Hok L, de Moraes Sá JC, Reyes M et al (2018) Enzymes and C pools as indicators of C build up in short-term conservation agriculture in a savanna ecosystem in Cambodia. Soil Tillage Res 177:125–133. https://doi.org/10.1016/j.still.2017.11.015
Hurisso TT, Culman SW, Horwath WR et al (2016) Comparison of permanganate-Oxidizable carbon and Mineralizable carbon for assessment of organic matter stabilization and mineralization. Soil Sci Soc Am J 80:1352–1364. https://doi.org/10.2136/sssaj2016.04.0106
Kuzyakov Y, Domanski G (2000) Carbon input by plants into the soil. Review. J Plant Nutr Soil Sci 163:421–431. https://doi.org/10.1002/1522-2624(200008)163:4<421::AID-JPLN421>3.0.CO;2-R
Lavallee JM, Soong JL, Cotrufo MF (2020) Conceptualizing soil organic matter into particulate and mineral-associated forms to address global change in the 21st century. Glob Chang Biol 26:261–273. https://doi.org/10.1111/gcb.14859
Lenth RV (2022) Emmeans: estimated marginal means, aka least-squares means. R package version 1.7.2. https://CRAN.R-project.org/package=emmeans
Liang C, Schimel JP, Jastrow JD (2017) The importance of anabolism in microbial control over soil carbon storage. Nat Microbiol 2:1–6. https://doi.org/10.1038/nmicrobiol.2017.105
Mikola J, Yeates GW, Barker GM et al (2001) Effects of defoliation intensity on soil food-web properties in an experimental grassland community. Oikos 92:333–343. https://doi.org/10.1034/j.1600-0706.2001.920216.x
Oksanen J, Blanchet FG, Friendly M et al (2020) Vegan: community ecology package. R package version 2.5–7. https://CRAN.R-project.org/package=vegan
Piñeiro G, Paruelo JM, Oesterheld M, Jobbágy EG (2010) Pathways of grazing effects on soil organic carbon and nitrogen. Rangel Ecol Manag 63:109–119. https://doi.org/10.2111/08-255.1
Poeplau C, Marstorp H, Thored K, Kätterer T (2016) Effect of grassland cutting frequency on soil carbon storage - a case study on public lawns in three Swedish cities. Soil 2:175–184. https://doi.org/10.5194/soil-2-175-2016
Prommer J, Walker TWN, Wanek W et al (2020) Increased microbial growth, biomass, and turnover drive soil organic carbon accumulation at higher plant diversity. Glob Chang Biol 26:669–681. https://doi.org/10.1111/gcb.14777
RStudio Team (2022) RStudio: integrated development environment for R. RStudio, PBC, Boston. http://www.rstudio.com
Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315. https://doi.org/10.1016/S0038-0717(02)00074-3
Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404. https://doi.org/10.1016/j.soilbio.2009.10.014
Sinsabaugh RL, Lauber CL, Weintraub MN et al (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264. https://doi.org/10.1111/j.1461-0248.2008.01245.x
Tirol-Padre A, Ladha JK (2004) Assessing the reliability of permanganate-Oxidizable carbon as an index of soil labile carbon. Soil Sci Soc Am J 68:969–978. https://doi.org/10.2136/sssaj2004.9690
Van Hees PAW, Jones DL, Finlay R et al (2005) The carbon we do not see - the impact of low molecular weight compounds on carbon dynamics and respiration in forest soils: a review. Soil Biol Biochem 37:1–13. https://doi.org/10.1016/j.soilbio.2004.06.010
Villarino SH, Pinto P, Jackson RB, Piñeiro G (2021) Plant rhizodeposition : a key factor for soil organic matter formation in stable fractions. Sci Adv 7:1–14. https://doi.org/10.1126/sciadv.abd3176
Von Lützow M, Kögel-Knabner I, Ludwig B et al (2008) Stabilization mechanisms of organic matter in four temperate soils: development and application of a conceptual model. J Plant Nutr Soil Sci 171:111–124. https://doi.org/10.1002/jpln.200700047
Wei Z, Maxwell TMR, Robinson B, Dickinson N (2022) Legume nutrition is improved by neighbouring grasses. Plant Soil 1–13. https://doi.org/10.1007/s11104-022-05379-4
Weil RR, Islam KR, Stine MA et al (2003) Estimating active carbon for soil quality assessment: a simplified method for laboratory and field use. Am J Altern Agric 18:3–17. https://doi.org/10.1079/AJAA2003003
Whalen ED, Grandy AS, Sokol NW et al (2022) Clarifying the evidence for microbial- and plant-derived soil organic matter, and the path toward a more quantitative understanding. Glob Chang Biol 7167–7185. https://doi.org/10.1111/gcb.16413
Wilson CH, Strickland MS, Hutchings JA et al (2018) Grazing enhances belowground carbon allocation, microbial biomass, and soil carbon in a subtropical grassland. Glob Chang Biol 24:2997–3009. https://doi.org/10.1111/gcb.14070
Zhang D, Junjun W, Yang F et al (2020) Linkages between soil organic carbon fractions and carbon- hydrolyzing enzyme activities across riparian zones in the Three Gorges of China. Sci Rep 1–11. https://doi.org/10.1038/s41598-020-65200-z
Acknowledgements
We thank Melissa Knorr, Nathan Alexander, Maxim Desjardins, and the 2021 Soil Ecology class in the Department of Natural Resources & the Environment at the University of New Hampshire for field and laboratory support.
Funding
The experiment was funded by grants from the USDA NIFA ORG (Project No. 2016–51106-25713) and OREI (Project No. 2020–51300-32196) Programs. Partial funding was provided by the New Hampshire Agricultural Experiment Station and a fellowship to CdST from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. This work was supported by the USDA National Institute of Food and Agriculture Hatch Project NH00702 and NH00667. This is Scientific Contribution Number 2967.
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Richard G. Smith designed and initiated the field experiment. Cristhian dos Santos Teixeira, Lukas Bernhardt, Nicholas D. Warren and Buck T. Castillo performed the measurements for this study. Cristhian dos Santos Teixeira, Lukas Bernhardt and Nicholas D. Warren analyzed the data. The first draft of the manuscript was written by Cristhian dos Santos Teixeira and Serita D. Frey. Richard G. Smith, Jessica D. Ernakovich, Claudia Petry and Serita D. Frey revised the manuscript. All authors read and approved the final manuscript.
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Teixeira, C.d., Castillo, B.T., Bernhardt, L. et al. Frequent defoliation of perennial legume-grass bicultures alters soil carbon dynamics. Plant Soil 490, 423–434 (2023). https://doi.org/10.1007/s11104-023-06091-7
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DOI: https://doi.org/10.1007/s11104-023-06091-7