Abstract
Background and aims
Biochar addition to soil is a carbon capture and storage option with potential to mitigate rising atmospheric CO2 concentrations, yet the consequences for soil organisms and linked ecosystem processes are inconsistent or unknown. We tested biochar impact on soil biodiversity, ecosystem functions, and their interactions, in temperate agricultural soils.
Methods
We performed a 27-month factorial experiment to determine effects of biochar, soil texture, and crop species treatments on microbial biomass (PFLA), soil invertebrate density, crop biomass and ecosystem CO2 flux in plant-soil mesocosms.
Results
Overall soil microbial biomass, microarthropod abundance and crop biomass were unaffected by biochar, although there was an increase in fungal-bacterial ratio and a positive relationship between the 16:1ω5 fatty acid marker of AMF mass and collembolan density in the biochar-treated mesocosms. Ecosystem CO2 fluxes were unaffected by biochar, but soil carbon content of biochar-treated mesocosms was significantly lower, signifying a possible movement/loss of biochar or priming effect.
Conclusions
Compared to soil texture and crop type, biochar had minimal impact on soil biota, crop production and carbon cycling. Future research should examine subtler effects of biochar on biotic regulation of ecosystem production and if the apparent robustness to biochar weakens over greater time spans or in combination with other ecological perturbations.
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References
Ayres E, Wall DH, Bardgett R (2010) Trophic interactions and their implications for soil carbon fluxes. In: Kutsch WL (ed) Soil carbon dynamics, an integrated methodology. Cambridge University Press, Cambridge, UK
Backer RGM, Schwinghamer TD, Whalen JK, Seguin P, Smith DL (2016) Crop yield and SOC responses to biochar application were dependent on soil texture and crop type in southern Quebec, Canada. J Plant Nutr Soil Sci 179:399–408. https://doi.org/10.1002/jpln.201500520
Bardgett RD, van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515:505–511. https://doi.org/10.1038/nature13855
Bargmann I, Rillig MC, Buss W, Kruse A, Kuecke M (2013) Hydrochar and biochar effects on germination of spring barley. J Agron Crop Sci 199:360–373. https://doi.org/10.1111/jac.12024
Beesley L, Moreno-Jiménez E, Gomez-Eyles JL (2010) Effects of biochar and greenwaste compost amendments on mobility, bioavailability and toxicity of inorganic and organic contaminants in a multi-element polluted soil. Environ Pollut 158:2282–2287
Bretherton S, Tordoff GM, Jones TH, Boddy L (2006) Compensatory growth of Phanerochaete velutina mycelial systems grazed by Folsomia candida (Collembola). FEMS Microbiol Ecol 58:33–40
Bruun S, Clauson-Kaas S, Bobulska L, Thomsen IK (2014) Carbon dioxide emissions from biochar in soil: role of clay, microorganisms and carbonates. Eur J Soil Sci 65:52–59
Case S, McNamara N, Reay D, Whitaker J (2012) The effect of biochar addition on N2O and CO2 emissions from a sandy loam soil - the role of soil aeration. Soil Biol Biochem 51:125–134
Chan KY, Xu Z (2009) Biochar: nutrient properties and their enhancement. In: Lehmann J, Joseph S (eds) Biochar for environmental management. Earthscan, London
Chen G, Qin J, Shi D, Zhang Y, Ji W (2009) Diversity of soil nematodes in areas polluted with heavy metals and polycyclic aromatic hydrocarbons (PAHs) in Lanzhou, China. Environ Manag 44:163–172. https://doi.org/10.1007/s00267-008-9268-2
Chen J, Liu X, Zheng J, Zhang B, Lu H, Chi Z, Pan G, Li L, Zheng J, Zhang X, Wang J, Yu X (2013) Biochar soil amendment increased bacterial but decreased fungal gene abundance with shifts in community structure in a slightly acid rice paddy from Southwest China. Appl Soil Ecol 71:33–44. https://doi.org/10.1016/j.apsoil.2013.05.003
Cross A, Sohi S (2011) The priming potential of biochar products in relation to labile carbon contents and soil organic matter status. Soil Biol Biochem 43:2127–2134
Domene X, Hanley K, Enders A, Lehmann J (2015) Short-term mesofauna responses to soil additions of corn Stover biochar and the role of microbial biomass. Appl Soil Ecol 89:10–17. https://doi.org/10.1016/j.apsoil.2014.12.005
Dungait JAJ, Ghee C, Rowan JS, McKenzie BM, Hawes C, Dixon ER, Paterson E, Hopkins DW (2013) Microbial responses to the erosional redistribution of soil organic carbon in arable fields. Soil Biol Biochem 60:195–201. https://doi.org/10.1016/j.soilbio.2013.01.027
Dupuy L, Vignes M, McKenzie BM, White PJ (2010) The dynamics of root meristem distribution in the soil. Plant Cell Environ 33:358–369
Frostegård Å, Tunlid A, Bååth E (2011) Use and misuse of PLFA measurements in soils. Soil Biol Biochem 43:1621–1625. https://doi.org/10.1016/j.soilbio.2010.11.021
Gebremikael MT, Steel H, Buchan D, Bert W, De Neve S (2016) Nematodes enhance plant growth and nutrient uptake under C and N-rich conditions. Sci Rep 6:32862. https://doi.org/10.1038/srep32862
George C, Kohler J, Rillig MC (2016) Biochars reduce infection rates of the root-lesion nematode Pratylenchus penetrans and associated biomass loss in carrot. Soil Biol Biochem 95:11–18. https://doi.org/10.1016/j.soilbio.2015.12.003
Hagner M, Kemppainen R, Jauhiainen L, Tiilikkala K, Setala H (2016) The effects of birch (Betula spp.) biochar and pyrolysis temperature on soil properties and plant growth. Soil Tillage Res 163:224–234. https://doi.org/10.1016/j.still.2016.06.006
Hale SE, Jensen J, Jakob L, Oleszczuk P, Hartnik T, Henriksen T, Okkenhaug G, Martinsen V, Cornelissen G (2013) Short-term effect of the soil amendments activated carbon, biochar, and ferric oxyhydroxide on bacteria and invertebrates. Environ Sci Technol 47:8674–8683. https://doi.org/10.1021/es400917g
Heemsbergen DA, Berg MP, Loreau M, van Haj JR, Faber JH, Verhoef HA (2004) Biodiversity effects on soil processes explained by interspecific functional dissimilarity. Science 306:1019–1020
Hol WHG, Vestergard M, ten Hooven F, Duyts H, van de Voorde TFJ, Bezemer TM (2017) Transient negative biochar effects on plant growth are strongest after microbial species loss. Soil Biol Biochem 115:442–451. https://doi.org/10.1016/j.soilbio.2017.09.016
Jeffery S, Verheijen F, van der Velde M, Bastos AC (2011) A quantitative review of the effects of biochar application to soils on crop productivity using meta-analysis. Agric Ecosyst Environ 144:175–187
Jenkins JR, Viger M, Arnold EC, Harris ZM, Ventura M, Miglietta F, Girardin C, Edwards RJ, Rumpel C, Fornasier F, Zavalloni C, Tonon G, Alberti G, Taylor G (2017) Biochar alters the soil microbiome and soil function: results of next-generation amplicon sequencing across Europe. GCB Bioenergy 9:591–612. https://doi.org/10.1111/gcbb.12371
Jones DL, Rousk J, Edwards-Jones G, DeLuca TH, Murphy DV (2012) Biochar-mediated changes in soil quality and plant growth in a three year field trial. Soil Biol Biochem 45:113–124
Lal R (2004) Soil carbon sequestration to mitigate climate change. Geoderma 123:1–22
Lehmann J (2007) A handful of carbon. Nature 447:143–144
Lehmann J, Rondon M (2006) Bio-char soil management on highly-weathered soils in the tropics. In: Uphoff NT (ed) Biological approaches to sustainable soil systems. CRC Press, Boca Raton
Lehmann J, Rillig MC, Thies JE, Masiello CA, Hockaday WC, Crowley DC (2011) Biochar effects on soil biota - a review. Soil Biol Biochem 43:1812–1836
Liang B, Lehmann J, Sohi SP, Thies JE, O'Neill B, Trujillo L, Gaunt J, Solomon D, Grossman J, Neves EG, Luizao FJ (2010) Black carbon affects the cycling of non-black carbon in soil. Org Geochem 41:206–213
Liu S, Zhang Y, Zong Y, Hu Z, Wu S, Zhou J, Jin Y, Zou J (2016) Response of soil carbon dioxide fluxes, soil organic carbon and microbial biomass carbon to biochar amendment: a meta-analysis. GCB Bioenergy 8:392–406. https://doi.org/10.1111/gcbb.12265
Maestrini B, Nannipieri P, Abiven S (2015) A meta-analysis on pyrogenic organic matter induced priming effect. GCB Bioenergy 7:577–590. https://doi.org/10.1111/gcbb.12194
Major J, Lehmann J, Rondon MA, Goodale C (2010) Fate of soil-applied black carbon: downward migration, leaching and soil respiration. Glob Chang Biol 16:1366–1379
Marks EAN, Mattana S, Alcaniz JM, Domene X (2014) Biochars provoke diverse soil mesofauna reproductive responses in laboratory bioassays. Eur J Soil Biol 60:104–111
McCormack S, Ostle NJ, Bardgett R, Hopkins DW, Vanbergen AJ (2013) Biochar in bioenergy cropping systems: impacts on soil faunal communities and linked ecosystem processes. Glob Chang Biol 5:81–95
McKenzie SW, Johnson SN, Jones H, Ostle NJ, Hails RS, Vanbergen AJ (2016) Root herbivores drive changes to plant primary chemistry, but root loss is mitigated under elevated atmospheric CO2. Front Plant Sci 7. https://doi.org/10.3389/fpls.2016.00837
Ngosong C, Gabriel E, Ruess L (2012) Use of the signature fatty acid 16:1ω5 as a tool to determine the distribution of arbuscular mycorrhizal fungi in soil. J Lipid 2012:236807–236807. https://doi.org/10.1155/2012/236807
Nielsen UN, Ayres E, Wall DH, Bardgett RD (2011) Soil biodiversity and carbon cycling: a review and synthesis of studies examining diversity-function relationships. Eur J Soil Sci 62:105–116
Olsson PA, Bååth E, Jakobsen I, Söderström B (1995) The use of phospholipid and neutral lipid fatty acids to estimate biomass of arbuscular mycorrhizal fungi in soil. Mycol Res 99:623–629. https://doi.org/10.1016/S0953-7562(09)80723-5
Orwin KH, Ostle N, Wilby A, Bardgett RD (2014) Effects of species evenness and dominant species identity on multiple ecosystem functions in model grassland communities. Oecologia 174:979–992. https://doi.org/10.1007/s00442-013-2814-5
Prayogo C, Jones JE, Baeyens J, Bending GD (2014) Impact of biochar on mineralisation of C and N from soil and willow litter and its relationship with microbial community biomass and structure. Biol Fertil Soils 50:695–702
Prendergast-Miller MT, Duvall M, Sohi SP (2014) Biochar-root interactions are mediated by biochar nutrient content and impacts on soil nutrient availability. Eur J Soil Sci 65:173–185
Pressler Y, Foster EJ, Moore JC, Cotrufo MF (2017) Coupled biochar amendment and limited irrigation strategies do not affect a degraded soil food web in a maize agroecosystem, compared to the native grassland. GCB Bioenergy 9:1344–1355. https://doi.org/10.1111/gcbb.12429
Rousk J, Brookes PC, Bååth E (2009) Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization. Appl Environ Microbiol 75:1589–1596. https://doi.org/10.1128/AEM.02775-08
Smith P (2016) Soil carbon sequestration and biochar as negative emission technologies. Glob Chang Biol 22:1315–1324. https://doi.org/10.1111/gcb.13178
Sohi S, Lopez-Capel E, Krull E, Bol R (2009) Biochar, climate change and soil: a review to guide future research. CSIRO land and water science report series ISSN: 1834-6618: 56 pp.
Staddon PL, Ramsey CB, Ostle N, Ineson P, Fitter AH (2003) Rapid turnover of hyphae of mycorrhizal Fungi determined by AMS microanalysis of 14C. Science 300:1138–1140. https://doi.org/10.1126/science.1084269
Steinbeiss S, Gleixner G, Antonietti M (2009) Effect of biochar amendment on soil carbon balance and soil microbial activity. Soil Biol Biochem 41:1301–1310
Wang J, Xiong Z, Kuzyakov Y (2016) Biochar stability in soil: meta-analysis of decomposition and priming effects. GCB Bioenergy 8:512–523. https://doi.org/10.1111/gcbb.12266
Wardle DA, Nilsson MC, Zackrisson O (2008) Fire-derived charcoal causes loss of forest humus. Science 320:629
Warnock DD, Lehmann J, Kuyper TW, Rillig MC (2007) Mycorrhizal responses to biochar in soil – concepts and mechanisms. Plant Soil 200:9–20
Yeates GW, Bongers T, Degoede RGM, Freckman DW, Georgieva SS (1993) Feeding habits in soil nematode families and genera – an outline for soil ecologists. J Nematol 25:315–331
Zheng H, Wang X, Luo X, Wang Z, Xing B (2018) Biochar-induced negative carbon mineralization priming effects in a coastal wetland soil: roles of soil aggregation and microbial modulation. Sci Total Environ 610-611:951–960. https://doi.org/10.1016/j.scitotenv.2017.08.166
Zhu YG, Miller RM (2003) Carbon cycling by arbuscular mycorrhizal fungi in soil-plant systems. Trends Plant Sci 8:407–409
Acknowledgements
This research was funded by a Natural Environment Research Council Open CASE PhD studentship grant (NE/HO18085/1). Thanks to Blair McKenzie and Euan Caldwell (James Hutton Institute) and Sean Case (Centre for Ecology and Hydrology) for providing advice and assistance with experimental set-up. Thanks to Adam Butler (Biomathematics and Statistics Scotland) for advice on LMMs. Thanks to Stuart Smith, Emily Taylor, Scott McKenzie, Will Hentley, Albert Johnston and Wilma Johnston for assistance with experiment set-up, maintenance and data collection.
Data statement
Raw data will be archived at the NERC Environmental Information Data Centre http://eidc.ceh.ac.uk/. Summary data (means + SE) for soil invertebrate densities, above-belowground crop biomass and PFLA are contained in online resources linked to this article (Tables 7S–9S).
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McCormack, S.A., Ostle, N., Bardgett, R.D. et al. Soil biota, carbon cycling and crop plant biomass responses to biochar in a temperate mesocosm experiment. Plant Soil 440, 341–356 (2019). https://doi.org/10.1007/s11104-019-04062-5
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DOI: https://doi.org/10.1007/s11104-019-04062-5