Abstract
The objective of this study was to quantify the combined effects of long-term plant biomass retention/removal and environmental conditions on soil microbial biomass phosphorus (P), bioavailable P, and acid phosphomonoesterase activity. Topsoil samples (0–2.5 and 2.5–5 cm) were collected from replicate field-based plots that had been maintained under contrasting plant biomass retention and removal regime for 21 years. Samples were collected on 14 occasions over a 17-month period and assessed for microbial P, bioavailable P, and phosphomonoesterase activity. All P measurements were consistently and significantly higher under plant biomass retention compared with biomass removal. Temporal variations in microbial P and phosphomonoesterase activity were evident in top soil (0–2.5 cm) and were driven by environmental conditions, mainly soil moisture, rainfall, and potential evapotranspiration, while bioavailable P had no temporal variation. Detailed analysis of microbial P data for the top 2.5-cm soil depth revealed that annual P flux through this pool was two times greater under biomass retention (10.3 kg P ha−1 year−1) compared with plant biomass removal (5.0 kg P ha−1 year−1). Similar and consistent trends were observed in soil from 2.5- to 5-cm sampling depth; however, differences were not significant. The findings of this study confirm the importance of the microbial biomass in determining the bioavailability of P in temperate grassland systems.
Similar content being viewed by others
References
Adair KL, Wratten S, Lear G (2013) Soil phosphorus depletion and shifts in plant communities change bacterial community structure in a long-term grassland management trial. Environ Microbiol Rep 5:404–413. https://doi.org/10.1111/1758-2229.12049
Boitt G, Black A, Wakelin SA, McDowell RW, Condron LM (2017) Impacts of long-term plant biomass management on soil phosphorus under temperate grassland. Plant Soil. https://doi.org/10.1007/s11104-017-3429-0
Bonkowski M (2004) Protozoa and plant growth: the microbial loop in soil revisited. New Phytol 162:617–631. https://doi.org/10.1111/j.1469-8137.2004.01066.x
Breiman L, Friedman J, Stone CJ, Olshen RA (1984) Classification and regression trees. Chapman & Hall/CRC, Boca Raton
Brookes PC, Powlson DS, Jenkinson DS (1982) Measurement of microbial biomass phosphorus in soil. Soil Biol Biochem 14:319–329. https://doi.org/10.1016/0038-0717(82)90001-3
Brookes PC, Powlson DS, Jenkinson DS (1984) Phosphorus in the soil microbial biomass. Soil Biol Biochem 16:169–175. https://doi.org/10.1016/0038-0717(84)90108-1
Bünemann E, Oberson A, Liebisch F, Keller F, Annaheim K, Huguenin-Elie O, Frossard E (2012) Rapid microbial phosphorus immobilization dominates gross phosphorus fluxes in a grassland soil with low inorganic phosphorus availability. Soil Biol Biochem 51:84–95. https://doi.org/10.1016/j.soilbio.2012.04.012
Bünemann EK, Bossio DA, Smithson PC, Frossard E, Oberson A (2004) Microbial community composition and substrate use in a highly weathered soil as affected by crop rotation and P fertilization. Soil Biol Biochem 36:889–901. https://doi.org/10.1016/j.soilbio.2004.02.002
Chen C, Condron L, Davis M, Sherlock R (2002) Phosphorus dynamics in the rhizosphere of perennial ryegrass (Lolium perenne L.) and radiata pine (Pinus radiata D. Don.) Soil Biol Biochem 34:487–499. https://doi.org/10.1016/S0038-0717(01)00207-3
Chen CR, Condron LM, Davis MR, Sherlock RR (2003) Seasonal changes in soil phosphorus and associated microbial properties under adjacent grassland and forest in New Zealand. Forest Ecol Manag 177:539–557. https://doi.org/10.1016/S0378-1127(02)00450-4
Cichota R, Snow VO, Tait AB (2008) A functional evaluation of virtual climate station rainfall data. New Zeal J Agric Res 51:317–329. https://doi.org/10.1080/00288230809510463
Cole CV, Elliott ET, Hunt HW, Coleman DC (1977) Trophic interactions in soils as they affect energy and nutrient dynamics. V. Phosphorus transformations. Microb Ecol 4:381–387. https://doi.org/10.1007/bf02013281
De’ath G, Fabricius KE (2000) Classification and regression trees: a powerful yet simple technique for ecological data analysis. Ecology 81:3178–3192. https://doi.org/10.1890/0012-9658(2000)081[3178:CARTAP]2.0.CO;2
Delgado-Baquerizo M, Powell JR, Hamonts K, Reith F, Mele P, Brown MV, Dennis PG, Ferrari BC, Fitzgerald A, Young A, Singh BK, Bissett A (2017) Circular linkages between soil biodiversity, fertility and plant productivity are limited to topsoil at the continental scale. New Phytol 215:1–11. https://doi.org/10.1111/nph.14634
Ehlers K, Bakken LR, Frostegård Å, Frossard E, Bünemann EK (2010) Phosphorus limitation in a Ferralsol: impact on microbial activity and cell internal P pools. Soil Biol Biochem 42:558–566. https://doi.org/10.1016/j.soilbio.2009.11.025
Farrell M, Prendergast-Miller M, Jones DL, Hill PW, Condron LM (2014) Soil microbial organic nitrogen uptake is regulated by carbon availability. Soil Biol Biochem 77:261–267. https://doi.org/10.1016/j.soilbio.2014.07.003
Fraser TD, Lynch DH, Bent E, Entz MH, Dunfield KE (2015) Soil bacterial phoD gene abundance and expression in response to applied phosphorus and long-term management. Soil Biol Biochem 88:137–147. https://doi.org/10.1016/j.soilbio.2015.04.014
Frossard E, Condron LM, Oberson A, Sinaj S, Fardeau JC (2000) Processes governing phosphorus availability in temperate soils. J Environ Qual 29:15–23. https://doi.org/10.2134/jeq2000.00472425002900010003x
Gaiero JR, Bent E, Fraser TD, Condron LM, Dunfield KE (2017) Validating novel oligonucleotide primers targeting three classes of bacterial non-specific acid phosphatase genes in grassland soils. Plant Soil. https://doi.org/10.1007/s11104-017-3338-2
GenStat (2013) GenStat for Windows v.16. VSN International Ltd., Hemel Hempstead, UK
He ZL, Wu J, AG O‘D, Syers JK (1997) Seasonal responses in microbial biomass carbon, phosphorus and sulphur in soils under pasture. Biol Fertil Soils 24:421–428. https://doi.org/10.1007/s003740050267
Hedley MJ, Stewart JWB (1982) Method to measure microbial phosphate in soils. Soil Biol Biochem 14:377–385. https://doi.org/10.1016/0038-0717(82)90009-8
Jakobsen I, Leggett ME, Richardson AE (2005) Rhizosphere organisms and plant phosphorus uptake. In: Sims JT, Sharpley AN (eds) Phosphorus: agriculture and the environment. Agronomy monograph 46. ASA, CSSA, SSSA, Madison, pp 437–494. https://doi.org/10.2134/agronmonogr46.c14
Kohavi R (1995) A study of cross-validation and bootstrap for accuracy estimation and model selection. International Joint Conference Artificial Intelligence (IJCAI), Stanford, pp 1137–1145
Kuhn M (2008) Building predictive models in R using the caret package. J Stat Softw 28:1–26. https://doi.org/10.18637/jss.v028.i05
Lagos LM, Acuna JJ, Maruyama F, Ogram A, Mora M, Jorquera MA (2016) Effect of phosphorus addition on total and alkaline phosphomonoesterase-harboring bacterial populations in ryegrass rhizosphere microsites. Biol Fertil Soils 52:1007–1019. https://doi.org/10.1007/s00374-016-1137-1
Luo G, Ling N, Nannipieri P, Chen H, Raza W, Wang M, Guo S, Shen Q (2017) Long-term fertilization regimes affect the composition of the alkaline phosphomonoesterase encoding microbial community of a vertisol and its derivative soil fractions. Biol Fertil Soils 53:375–388. https://doi.org/10.1007/s00374-017-1183-3
Magid J, Tiessen H, Condron LM (1996) Dynamics of organic phosphorus in soils under natural and agricultural ecosystems. In: Piccolo A (ed) Humic substances in terrestrial ecosystems. Elsevier Science BV, Amsterdam, pp 429–466. https://doi.org/10.1016/B978-044481516-3/50012-8
McDowell RW, Condron LM, Stewart I (2016) Variation in environmentally- and agronomically-significant soil phosphorus concentrations with time since stopping the application of phosphorus fertilisers. Geoderma 280:67–72. https://doi.org/10.1016/j.geoderma.2016.06.022
McGill WB, Cannon KR, Robertson JA, Cook FD (1986) Dynamics of soil microbial biomass and water-soluble organic C in Breton L after 50 years of cropping to two rotations. Can J Soil Sci 66:1–19. https://doi.org/10.4141/cjss86-001
McGill WB, Cole CV (1981) Comparative aspects of cycling of organic C, N, S and P through soil organic matter. Geoderma 26:267–286. https://doi.org/10.1016/0016-7061(81)90024-0
Morel C, Tiessen H, Stewart JWB (1996) Correction for P-sorption in the measurement of soil microbial biomass P by CHCl3 fumigation. Soil Biol Biochem 28:1699–1706. https://doi.org/10.1016/S0038-0717(96)00245-3
Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soil. In: Bünemann E, Oberson A, Frossard E (eds) Phosphorus in action, vol 26. Soil biology. Springer, Berlin, pp 215–243. https://doi.org/10.1007/978-3-642-15271-9_9
National Institute of Water and Atmospheric Research (2017) National Institute of Water and Atmospheric Research - NIWA, 1981-2010 climate data. https://www.niwa.co.nz/education-and-training/schools/resources/climate. Accessed 09 June 2017
Oberson A, Besson JM, Maire N, Sticher H (1996) Microbiological processes in soil organic phosphorus transformations in conventional and biological cropping systems. Biol Fertil Soils 21:138–148. https://doi.org/10.1007/bf00335925
Oberson A, Friesen DK, Rao IM, Bühler S, Frossard E (2001) Phosphorus transformations in an Oxisol under contrasting land-use systems: the role of the soil microbial biomass. Plant Soil 237:197–210. https://doi.org/10.1023/A:1013301716913
Oberson A, Joner EJ (2005) Microbial turnover of phosphorus in soil. In: Turner BL, Frossard E, Baldwin D (eds) Organic phosphorus in the environment. CABI, Wallingford, pp 133–164. https://doi.org/10.1079/9780851998220.0133
Oehl F, Frossard E, Fliessbach A, Dubois D, Oberson A (2004) Basal organic phosphorus mineralization in soils under different farming systems. Soil Biol Biochem 36:667–675. https://doi.org/10.1016/j.soilbio.2003.12.010
Oehl F, Oberson A, Probst M, Fliessbach A, Roth H-R, Frossard E (2001) Kinetics of microbial phosphorus uptake in cultivated soils. Biol Fertil Soils 34:31–41. https://doi.org/10.1007/s003740100362
Olsen SR (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. United States Department of Agriculture. Circular 939:1–24
Olsen SR, Sommers LE (1982) Phosphorus. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis (second edition). Soil Science Society of America, Inc., Madison, pp 403–430
Perrott K, Sarathchandra S, Dow B (1992) Seasonal and fertilizer effects on the organic cycle and microbial biomass in a hill country soil under pasture. Soil Res 30:383–394. https://doi.org/10.1071/SR9920383
Perrott K, Sarathchandra S, Waller J (1990) Seasonal storage and release of phosphorus and potassium by organic matter and the microbial biomass in a high producing pastoral soil. Soil Res 28:593–608. https://doi.org/10.1071/SR9900593
Randhawa PS, Condron LM, Di HJ, Sinaj S, McLenaghen RD (2005) Effect of green manure addition on soil organic phosphorus mineralisation. Nutr Cycl Agroecosyst 73:181–189. https://doi.org/10.1007/s10705-005-0593-z
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Richardson AE, Barea JM, McNeill AM, Prigent Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339. https://doi.org/10.1007/s11104-009-9895-2
Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiol 156:989–996. https://doi.org/10.1104/pp.111.175448
Rose TJ, Wood RH, Gleeson DB, Rose MT, Van Zwieten L (2016) Removal of phosphorus in residues of legume or cereal plants determines growth of subsequently planted wheat in a high phosphorus fixing soil. Biol Fertil Soils 52:1085–1092. https://doi.org/10.1007/s00374-016-1143-3
Scott JT, Condron LM (2003) Dynamics and availability of phosphorus in the rhizosphere of a temperate silvopastoral system. Biol Fertil Soils 39:65–73. https://doi.org/10.1007/s00374-003-0678-2
Seeling B, Zasoski RJ (1993) Microbial effects in maintaining organic and inorganic solution phosphorus concentrations in a grassland topsoil. Plant Soil 148:277–284. https://doi.org/10.1007/bf00012865
Simpson M, McLenaghen RD, Chirino-Valle I, Condron LM (2012) Effects of long-term grassland management on the chemical nature and bioavailability of soil phosphorus. Biol Fertil Soils 48:607–611. https://doi.org/10.1007/s00374-011-0661-2
Sparling GP, Hart PBS, August JA, Leslie DM (1994) A comparison of soil and microbial carbon, nitrogen, and phosphorus contents, and macro-aggregate stability of a soil under native forest and after clearance for pastures and plantation forest. Biol Fertil Soils 17:91–100. https://doi.org/10.1007/bf00337739
Stewart JWB, Tiessen H (1987) Dynamics of soil organic phosphorus. Biogeochemistry 4:41–60. https://doi.org/10.1007/bf02187361
Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307. https://doi.org/10.1016/0038-0717(69)90012-1
Tait A, Turner R (2005) Generating multiyear gridded daily rainfall over New Zealand. J Appl Meteorol 44:1315–1323. https://doi.org/10.1175/jam2279.1
Tate KR, Speir TW, Ross DJ, Parfitt RL, Whale KN, Cowling JC (1991) Temporal variations in some plant and soil P pools in two pasture soils of widely different P fertility status. Plant Soil 132:219–232. https://doi.org/10.1007/bf00010403
Therneau T, Atkinson B, Ripley B (2017) rpart: recursive partitioning and regression trees. R package version 4.1–10. https://CRAN.R-project.org/package=rpart. Accessed 26 May 2017
Turner BL, Cade-Menun BJ, Condron LM, Newman S (2005) Extraction of soil organic phosphorus. Talanta 66:294–306. https://doi.org/10.1016/j.talanta.2004.11.012
Turner BL, Lambers H, Condron LM, Cramer MD, Leake JR, Richardson AE, Smith SE (2013) Soil microbial biomass and the fate of phosphorus during long-term ecosystem development. Plant Soil 367:225–234. https://doi.org/10.1007/s11104-012-1493-z
Vincent AG, Turner BL, Tanner EVJ (2010) Soil organic phosphorus dynamics following perturbation of litter cycling in a tropical moist forest. Eur J Soil Sci 61:48–57. https://doi.org/10.1111/j.1365-2389.2009.01200.x
Wardle DA, Yeates GW, Nicholson KS, Bonner KI, Watson RN (1999) Response of soil microbial biomass dynamics, activity and plant litter decomposition to agricultural intensification over a seven-year period. Soil Biol Biochem 31:1707–1720. https://doi.org/10.1016/S0038-0717(99)00090-5
Acknowledgements
Lincoln University was responsible for the establishment of the long-term ecology field trial and its ongoing maintenance. The authors are particularly indebted to the efforts of Mr. David Jack who has managed the trial since establishment. The first author of this study was financially supported by the Brazilian Ministry of Education (MEC) through the CAPES agency (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, process: 10359/13-3).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
ESM 1
(DOCX 12 kb).
Rights and permissions
About this article
Cite this article
Boitt, G., Simpson, Z.P., Tian, J. et al. Plant biomass management impacts on short-term soil phosphorus dynamics in a temperate grassland. Biol Fertil Soils 54, 397–409 (2018). https://doi.org/10.1007/s00374-018-1269-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-018-1269-6