P.C. Brookes

Rothamsted Research, Harpenden, England, United Kingdom

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Publications (127)373.72 Total impact

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    ABSTRACT: Aims Replenishment of soils with carbon (C) produced during photosynthesis plays an important role in global C cycling. Nitrogen (N) fertilization is critical for rice production, but its effects on the deposition of photosynthesis-derived C into soil C pools is poorly understood. To address this, we used continuous 14C-labeling to quantify the deposition of photosynthesis-derived C into various soil organic pools in a rice-soil system. Methods Rice (Oryza sativa L.) was continuously supplied with 14C-labeled CO2 (14C-CO2) for 36 days, with increasing N fertilizer rates (0 [N0], 10 [N10], 20 [N20], or 40 mg N kg–1 soil [N40], respectively). Results Rice shoot and root biomass significantly increased following N fertilization. The amount of photosynthesis-derived C converted into soil organic carbon (14C-SOC) was proportional to the soil N concentration, and accounted for 8.0–19.3% of rice biomass C. The 14C-SOC content was positively correlated with the rice root biomass. Rice growth with N fertilization increased the inputs of photosynthesis-derived C into soil., indicating the release of root exudates. The amounts of 14C-labelled C in the dissolved organic carbon (14C-DOC) and in the microbial biomass carbon (14C-MBC), as proportions of 14C-SOC, were 3.9–7.8% and 6.6–24.0%, respectively. The 14C-DOC, 14C-MBC, and 14C-SOC as proportions of total DOC, MBC, and SOC were 9.7–11.6%, 6.9–10.6%, and 0.37–1.71%, respectively. Conclusions N promotes deposition of photosynthesis-derived C into SOC pools in a rate-dependent manner. However, the amounts of 14C-MBC increase during rice growth at low N concentrations.
    Full-text · Article · Sep 2014 · Plant and Soil
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    Full-text · Dataset · Aug 2014
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    ABSTRACT: Assimilating atmospheric carbon (C) into terrestrial ecosystems is recognized as a primary measure to mitigate global warming. Ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO) is the dominant enzyme by which terrestrial autotrophic bacteria and plants fix CO2. To investigate the possibility of using RubisCO activity as an indicator of microbial CO2 fixation potential, a valid and efficient method for extracting soil proteins is needed. We examined three methods commonly used for total soil protein extraction. A simple sonication method for extracting soil protein was more efficient than bead beating or freeze–thaw methods. Total soil protein, RubisCO activity, and microbial fixation of CO2 in different agricultural soils were quantified in an incubation experiment using 14C-CO2 as a tracer. The soil samples showed significant differences in protein content and RubisCO activity, defined as nmol CO2 fixed g−1 soil min−1. RubisCO activities ranged from 10.68 to 68.07 nmol CO2 kg−1 soil min−1, which were closely related to the abundance of cbbL genes (r = 0.900, P = 0.0140) and the rates of microbial CO2 assimilation (r = 0.949, P = 0.0038). This suggests that RubisCO activity can be used as an indicator of soil microbial assimilation of atmospheric CO2.
    Full-text · Article · Jul 2014 · Pedobiologia
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    ABSTRACT: Many soil microbes exist in biofilms. These biofilms are typified by variable quantities of extracellular polymeric substances (EPS: predominantly polysaccharides, glycoconjugates, and proteins) and the embedded microbial cells. A method to measure soil-EPS (the biofilm exclusive of microbial cells) has not yet been described. The present work investigates the potential of five extraction methods to estimate changes in soil-EPS content. A rationale for selection of appropriate EPS extraction and methodology is discussed, including the crucial consideration of both intracellular and extracellular contamination.
    Full-text · Article · May 2014 · Soil Biology and Biochemistry
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    ABSTRACT: This study compares a traditional agricultural approach to minimise N pollution of groundwater (incorporation of crop residues) with applications of small amounts of biodiesel co-product (BCP) to arable soils. Loss of N from soil to the aqueous phase was shown to be greatly reduced in the laboratory, mainly by decreasing concentrations of dissolved nitrate-N. Increases in soil microbial biomass occurred within 4 days of BCP application-indicating rapid adaptation of the soil microbial community. Increases in biomass-N suggest that microbes were partly mechanistic in the immobilisation of N in soil. Straw, meadow-grass and BCP were subsequently incorporated into experimental soil mesocosms of depth equal to plough layer (23 cm), and placed in an exposed netted tunnel to simulate field conditions. Leachate was collected after rainfall between the autumn of 2009 and spring of 2010. Treatment with BCP resulted in less total-N transferred from soil to water over the entire period, with 32.1, 18.9, 13.2 and 4.2 mg N kg(-1) soil leached cumulatively from the control, grass, straw and BCP treatments, respectively. More than 99 % of nitrate leaching was prevented using BCP. Accordingly, soils provided with crop residues or BCP showed statistically significant increases in soil N and C compared to the control (no incorporation). Microbial biomass, indicated by soil ATP concentration, was also highest for soils given BCP (p < 0.05). These results indicate that field-scale incorporation of BCP may be an effective method to reduce nitrogen loss from agricultural soils, prevent nitrate pollution of groundwater and augment the soil microbial biomass.
    Full-text · Article · Jan 2014 · Water Air and Soil Pollution
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    ABSTRACT: Many soil microbes exist in biofilms. These biofilms are typified by variable quantities of extracellular polymeric substances (EPS: predominantly polysaccharides, glycoconjugates, and proteins) and the embedded microbial cells. A method to measure soil-EPS (the biofilm exclusive of microbial cells) has not yet been described. The present work investigates the potential of five extraction methods to estimate changes in soil-EPS content. A rationale for selection of appropriate EPS extraction and methodology is discussed, including the crucial consideration of both intracellular and extracellular contamination. EPS was developed in situ by provision of labile C (glycerol) to the microbial biomass of a moist soil and then applying desiccation stress. Only two out of the five extraction methods showed statistically significant increases in polysaccharide production responding to substrate addition. Humified organic matter, estimated by its humic acid equivalent (HAE) was used to indicate the degree of extracellular contamination, and/or creation of humic artefacts – both of which affect detection of changes in EPS. The HAE concentration was very high when applying original and modified methods designed to extract glomalin related soil protein (GRSP). Extraction methods involving heating with dilute sulphuric acid appeared to overestimate EPS-polysaccharide. Using microbial ATP as an indicator of cell-lysis, confidence could only be ascribed to EPS extraction with cation exchange resin. Using this method, the expected increases in EPS-polysaccharide were clearly apparent. The HAE/protein ratios of EPS extracts were also lowest with cation exchange – indicating this method did not cause excessive contamination from humified soil organic matter or create related artefacts. FULL ARTICLE AVAILABLE OPEN ACCESS: http://www.sciencedirect.com/science/article/pii/S0038071714000261
    Full-text · Article · Jan 2014 · Soil Biology and Biochemistry
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    ABSTRACT: Elevated CO2 respiration rates have been observed in soils treated with complex mixtures versus single low molecular weight (LMW) organic substrates, and it has been postulated that a more diverse range of soil microorganisms responds to increasingly complex mixtures of LMW organic substrates. To test this hypothesis, 13C-labelled substrates (glycine, an amino acid mixture and an extract of water soluble compounds from plant roots) were applied at 15 μg C g−1 soil to an arable top soil. The soils were incubated and destructively sampled after 8, 24, 48, 120 and 240 h, and the 13C content of biomarker PLFA for Gram negative bacteria, Gram positive bacteria, Actinobacteria and fungi was determined. There was no significant increase in the concentration of the biomarker PLFA, apart from Actinobacteria at the end of the incubation (120 and 240 h). However there were significant changes in total PLFA concentration due to increases in the 16:0 and 18:0 PLFA, which cannot be assigned to specific functional groups of microorganisms. 13C incorporation into the biomarker PLFA of all microbial groups was significant at every time point, but more 13C was determined in the biomarker PLFA of all microbial groups after the application of the amino acid mixture compared to glycine. Calculations of the proportion of the incorporated of 13C in the different biomarker PLFA suggested the routing of substrate 13C between the microbial groups over time. This was related to the broad functional ecology (‘r’ or ‘K’ strategy) of the different microbial groups. In conclusion, we observed that the response of all microbial groups (detected as 13C incorporation) was increased by the addition of more complex mixtures of LMW organic substrates, but that different microbial groups responded differently over time.
    Full-text · Article · Sep 2013 · Soil Biology and Biochemistry
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    ABSTRACT: Autotrophic microorganisms, which can fix atmospheric CO2 to synthesize organic carbon, are numerous and widespread in soils. However, the extent and the mechanism of CO2 fixation in soils remain poorly understood. We incubated five upland and five paddy soils from subtropical China in an enclosed, continuously 14CO2-labeled, atmosphere and measured 14CO2 incorporated into soil organic matter (SOC14) and microbial biomass (MBC14) after 110 days. The five upland soils supported dominant crops soils (maize, wheat, sweet potato, and rapeseed) in the region, while all paddy soils were cultivated in a regime consisting of permanently-flooded double-cropping rice cultivation. The upland and paddy soils represented typical soil types (fluvisols and ultisols) and three landforms (upland, hill, and low mountain), ranging in total carbon from low (<10 g kg−1 soil organic carbon) to medium (10–20 g kg−1) to high (>20 g kg−1). Substantial amounts of 14CO2 were fixed into SOC14 (mean 20.1 ± 7.1 mg C kg−1 in upland soil, 121.1 ± 6.4 mg C kg−1 in paddy soil) in illuminated soils (12 h light/12 h dark), whereas no 14C was fixed in soils incubated in continuous darkness. We concluded that the microbial CO2 fixation was almost entirely phototrophic rather than chemotrophic. The rate of SOC14 synthesis was significantly higher in paddy soils than in upland soils. The SOC14 comprised means of 0.15 ± 0.01% (upland) and 0.65 ± 0.03% (paddy) of SOC. The extent of 14C immobilized as MBC14 and that present as dissolved organic C (DOC14) differed between soil types, accounting for 15.69–38.76% and 5.54–18.37% in upland soils and 15.57–40.03% and 3.67–7.17% of SOC14 in paddy soils, respectively. The MBC14/MBC and DOC14/DOC were 1.76–5.70% and 1.69–5.17% in the upland soils and 4.23–28.73% and 5.65–14.30% in the paddy soils, respectively. Thus, the newly-incorporated C stimulated the dynamics of DOC and MBC more than the dynamics of SOC. The SOC14 and MBC14 concentrations were highly significantly correlated (r = 0.946; P < 0.0001). We conclude that CO2 uptake by phototrophic soil microorganisms can contribute significantly to carbon assimilation in soil, and so warrants further future study.
    Full-text · Article · Jul 2013 · Geochimica et Cosmochimica Acta
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    ABSTRACT: Autotrophic microorganisms, which can fix atmospheric CO2 to synthesize organic carbon, are numerous and widespread in soils. However, the extent and the mechanism of CO2 fixation in soils remain poorly understood. We incubated five upland and five paddy soils from subtropical China in an enclosed, continuously 14CO2-labeled, atmosphere and measured 14CO2 incorporated into soil organic matter (SOC14) and microbial biomass (MBC14) after 110 days. The five upland soils supported dominant crops soils (maize, wheat, sweet potato, and rapeseed) in the region, while all paddy soils were cultivated in a regime consisting of permanently-flooded double-cropping rice cultivation. The upland and paddy soils represented typical soil types (fluvisols and ultisols) and three landforms (upland, hill, and low mountain), ranging in total carbon from low (< 10 g kg–1 soil organic carbon) to medium (10–20 g kg–1) to high (> 20 g kg–1). Substantial amounts of 14CO2 were fixed into SOC14 (mean 20.1±7.1 mg C kg–1 in upland soil, 121.1±6.4 mg C kg–1 in paddy soil) in illuminated soils (12 h light/12 h dark), whereas no 14C was fixed in soils incubated in continuous darkness. We concluded that the microbial CO2 fixation was almost entirely phototrophic rather than chemotrophic. The rate of SOC14 synthesis was significantly higher in paddy soils than in upland soils. The SOC14 comprised means of 0.15±0.01% (upland) and 0.65±0.03% (paddy) of SOC. The extent of 14C immobilized as MBC14 and that present as dissolved organic C (DOC14) differed between soil types, accounting for 15.69–38.76% and 5.54–18.37% in upland soils and 15.57–40.03% and 3.67–7.17% of SOC14 in paddy soils, respectively. The MBC14/MBC and DOC14/DOC were 1.76–5.70% and 1.69–5.17% in the upland soils and 4.23–28.73% and 5.65–14.30% in the paddy soils, respectively. Thus, the newly-incorporated C stimulated the dynamics of DOC and MBC more than the dynamics of SOC. The SOC14 and MBC14 concentrations were highly significantly correlated (r = 0.946; P < 0.0001). We conclude that autotrophic CO2 assimilation by phototrophic soil microbes may make a significant contribution to C cycle, and so warrants further future study.
    Full-text · Article · Apr 2013 · Geochimica et Cosmochimica Acta
  • Y. Luo · M. Durenkamp · M. De Nobili · Q. Lin · B. J. Devonshire · P. C. Brookes
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    ABSTRACT: Biochar has been widely proposed as a soil amendment, with reports of benefits to soil physical, chemical and biological properties. To quantify the changes in soil microbial biomass and to understand the mechanisms involved, two biochars were prepared at 350 °C (BC350) and 700 °C (BC700) from Miscanthus giganteus, a C4 plant, naturally enriched with 13C. The biochars were added to soils of about pH 4 and 8, which were both sampled from a soil pH gradient of the same soil type. Isotopic (13C) techniques were used to investigate biochar C availability to the biomass. Scanning Electron Microscopy (SEM) was used to observe the microbial colonization, and Attenuated Total Reflectance (ATR) to highlight structural changes at the surface of the biochars. After 90 days incubation, BC350 significantly increased the biomass C concentration relative to the controls in both the low (p < 0.05) and high pH soil (p < 0.01). It declined between day 90 and 180. The same trend occurred with soil microbial ATP. Overall, biomass C and ATP concentrations were closely correlated over all treatments (R2 = 0.87). This indicates that neither the biomass C, nor ATP analyses were affected by the biochars, unless, of course, they were both affected in the same way, which is highly unlikely. About 20% of microbial biomass 13C was derived from BC350 after 90 days of incubation in both low and high pH soils. However, less than 2% of biomass 13C was derived from BC700 in the high pH soil, showing very low biological availability of BC700. After 90 days of incubation, microbial colonization in the charsphere (defined here as the interface between soil and biochar) was more pronounced with the BC350 in the low pH soil. This was consistent with the biomass C and ATP results. The microbial colonization following biochar addition in our study was mainly attributed to biochar C availability and its large surface area. There was a close linear relationship between 13CO2 evolved and biomass 13C, suggesting that biochar mineralization is essentially a biological process. The interactions between non-living and living organic C forms, which are vital in terms of soil fertility and the global C cycle, may be favoured in the charsphere, which has unique properties, distinct from both the internal biochar and the bulk soil.
    No preview · Article · Feb 2013 · Soil Biology and Biochemistry
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    Dataset: 90 knownsC
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    ABSTRACT: Soil contains approximately 2344 Gt (1 gigaton = 1 billion tonnes) of organic carbon globally and is the largest terrestrial pool of organic carbon. Small changes in the soil organic carbon stock could result in significant impacts on the atmospheric carbon concentration. The fluxes of soil organic carbon vary in response to a host of potential environmental and anthropogenic driving factors. Scientists world- wide are contemplating questions such as: ‘What is the average net change in soil organic carbon due to environmental conditions or management practices?’, ‘How can soil organic carbon sequestration be enhanced to achieve some mitigation of atmospheric carbon dioxide?’ and ‘Will this secure soil quality?’. These questions are far reaching, because maintaining and improving the world’s soil resource is imper- ative to providing sufficient food and fibre to a growing population. Additional challenges are expected through climate change and its potential to increase food shortages. This review highlights knowledge of the amount of carbon stored in soils globally, and the potential for carbon sequestration in soil. It also discusses successful methods and models used to determine and estimate carbon pools and fluxes. This knowledge and technology underpins decisions to protect the soil resource.
    Full-text · Dataset · Jan 2013
  • Phil Brookes · Sarah Kemmitt
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    ABSTRACT: Nearly all soil organic matter is extensively humified, with some fractions existing for more than 1,000 years. Soil microorganisms are surrounded by about 50 times their mass of soil organic matter but can only metabolise it very slowly (‘basal mineralisation’ rate). Here, we show that the rate-limiting step in soil organic matter mineralisation is independent of microbial biomass size, community structure or activity. We suggest that the rate-limiting step is governed by abiological processes (the ‘regulatory gate’ hypothesis). This has significant implications for our understanding of carbon mineralisation in soils and the role of soil microorganisms in the global carbon cycle.
    No preview · Chapter · Jan 2013
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    ABSTRACT: Elucidating the biodiversity of CO2-assimilating bacterial communities under different land uses is critical for establishing an integrated view of the carbon sequestration in agricultural systems. We therefore determined the abundance and diversity of CO2 assimilating bacteria using terminal restriction fragment length polymorphism and quantitative PCR of the cbbL gene (which encodes ribulose-1,5-biphosphate carboxylase/oxygenase). These analyses used agricultural soils collected from a long-term experiment (Pantang Agroecosystem) in subtropical China. Soils under three typical land uses, i.e., rice–rice (RR), upland crop (UC), and paddy rice–upland crop rotation (PU), were selected. The abundance of bacterial cbbL (0.04 to 1.25 × 108 copies g−1 soil) and 16S rDNA genes (0.05–3.00 × 1010 copies g−1 soil) were determined in these soils. They generally followed the trend RR > PU > UC. The cbbL-containing bacterial communities were dominated by facultative autotrophic bacteria such as Mycobacterium sp., Rhodopseudomonas palustris, Bradyrhizobium japonicum, Ralstonia eutropha, and Alcaligenes eutrophus. Additionally, the cbbL-containing bacterial community composition in RR soil differed from that in upland crop and paddy rice–upland crop rotations soils. Soil organic matter was the most highly statistically significant factor which positively influenced the size of the cbbL-containing population. The RR management produced the greatest abundance and diversity of cbbL-containing bacteria. These results offer new insights into the importance of microbial autotrophic CO2 fixation in soil C cycling.
    Full-text · Article · Dec 2012 · Biology and Fertility of Soils
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    ABSTRACT: Information on the input, distribution and fate of photosynthesized carbon (C) in plant–soil systems is essential for understanding their nutrient and C dynamics. Our objectives were to: 1) quantify the input to, and distribution of, photosynthesized C by rice into selected soil C pools by using a C14 continuous labelling technique and 2) determine the influence of the photosynthesized C input on the decomposition of native soil organic carbon (SOC) under laboratory conditions. The amounts of C14 in soil organic C (SOC14) were soil dependent, and ranged from 114.3 to 348.2 mg C kg−1, accounting for 0.73%–1.99% of total SOC after continuous labelling for 80 days. However, the mean SOC14 concentrations in unplanted soils (31.9–64.6 mg kg−1) were accounted for 21.5% of the rice-planted soils. The amounts of C14 in the dissolved organic C (DOC14) and in the microbial biomass C (MBC14), as percentages of SOC14, were 2.21%–3.54% and 9.72%–17.97%, respectively. The DOC14 and MBC14 were 6.72%–14.64% and 1.70%–7.67% of total DOC and MBC respectively after 80-d of rice growth. At 80-d of labelling, the SOC14 concentration was positively correlated with the MBC14 concentration and rice root biomass. Rice growth promotes more photosynthesized (newly-derived) C into soil C pools compared to unplanted soils, reflecting the release of root exudates from rice roots. Laboratory incubation of photosynthesized (plant-derived) C in soil decreased the decomposition of native SOC (i.e. a negative priming effect), in some, but not all cases. If this negative priming effect of the new C on native SOC also occurs in the field in the longer term, paddy soils will probably sequester more C from the atmosphere if more photosynthesized C enters them.
    Full-text · Article · May 2012 · Soil Biology and Biochemistry
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    ABSTRACT: Export Date: 2 January 2013, Source: Scopus, Article in Press
    Full-text · Conference Paper · Jan 2012
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    Y. Luo · M. Durenkamp · M. De Nobili · Q. Lin · P.C. Brookes
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    ABSTRACT: The aim of this work was to determine the magnitude of the priming effect, i.e. short-term changes in the rate (negative or positive) of mineralisation of native soil organic carbon (C), following addition of biochars. The biochars were made from Miscanthus giganteus, a C4 plant, naturally enriched with 13C. The biochars were produced at 350 °C (biochar350) and 700 °C (biochar700) and applied with and without ryegrass as a substrate to a clay-loam soil at pH 3.7 and 7.6. A secondary aim was to determine the effect of ryegrass addition on the mineralisation of the two biochars.After 87 days, biochar350 addition caused priming effects equivalent to 250 and 319 μg CO2–C g−1 soil, in the low and high pH soil, respectively. The largest priming effects occurred at the start of the incubations. The size of the priming effect was decreased at higher biochar pyrolysis temperatures, which may be a way of controlling priming effects following biochar incorporation to soil, if desired. The priming effect was probably induced by the water soluble components of the biochar. At 87 days of incubation, 0.14% and 0.18% of biochar700 and 0.61% and 0.84% of biochar350 were mineralized in the low and high pH soil, respectively. Ryegrass addition gave an increased biochar350 mineralisation of 33% and 40%, and increased biochar700 at 137% and 70%, in the low and high pH soils, respectively. Certainly, on the basis of our results, if biochar is used to sequester carbon a priming effect may occur, increasing CO2–C evolved from soil and decreasing soil organic C. However, this will be more than compensated for by the increased soil C caused by biochar incorporation. A similar conclusion holds for accelerated mineralisation of biochar due to incorporation of fresh labile substrates. We consider that our results are the first to unequivocally demonstrate the initiation, progress and termination of a true positive priming effect by biochar on native soil organic C.
    Full-text · Article · Nov 2011 · Soil Biology and Biochemistry
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    M. Redmile-Gordon · R. P. White · P. C. Brookes
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    ABSTRACT: The trichloroacetic acid (TCA) based reagent proposed by Jenkinson and Oades (1979) fits all the criteria required to measure soil microbial biomass ATP (biomass ATP). Amongst other components it contains paraquat (0.1 M 1,1′ dimethyl-4,4′ bipyridylium dichloride), usually extracted from the herbicide Gramoxone. Paraquat is added as an analogue of ATP. It is tightly fixed to soil and so decreases ATP fixation. However, Gramoxone is now banned as an agricultural chemical in both Europe and North America. Our aim was to find an effective replacement for paraquat to measure biomass ATP. The best replacement was 0.6 M imidazole in 1.10 M TCA containing 0.25 M P (termed the TIP reagent). Biomass ATP concentrations were not significantly different in five soils extracted by either reagent 10.37 and 11.17 μmol ATP g−1 biomass C, respectively; standard error of differences of means = 0.36; p = 0.091.
    Full-text · Article · May 2011 · Soil Biology and Biochemistry

  • No preview · Article · Jan 2011 · European Journal of Soil Science
  • M. De Nobili · D. Powlson · P. Brookes

    No preview · Article · Jan 2011
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    L.C. Babujia · M. Hungria · J.C. Franchini · P.C. Brookes
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    ABSTRACT: The advantages of no-tillage (NT) over conventional tillage (CT) systems in improving soil quality are generally accepted, resulting from benefits in soil physical, chemical and biological properties. However, most evaluations have only considered surface soil layers (maximum 0–30 cm depth), and values have not been corrected to account for changes in soil bulk density. The objective of this study was to estimate a more realistic contribution of the NT to soil fertility, by evaluating C- and N-related soil parameters at the 0–60 cm depth in a 20-year experiment established on an oxisol in southern Brazil, with a soybean (summer)/wheat (winter) crop succession under NT and CT. At full flowering of the soybean crop, soil samples were collected at depths of 0–5, 5–10, 10–20, 20–30, 30–40, 40–50 and 50–60 cm. For the overall 0–60 cm layer, correcting the values for soil bulk density, NT significantly increased the stocks of C (18%) and N (16%) and microbial biomass C (35%) and N (23%) (MB-C and -N) in comparison to CT. Microbial basal respiration and microbial quotient (qMic) were also significantly increased under NT. When compared with CT, NT resulted in gains of 0.8 Mg C ha−1 yr−1 (67% of which was in the 0–30 cm layer) and 70 kg N ha−1 yr−1 (73% in the 0–30 cm layer). In the 0–5-cm layer, MB-C was 82% higher with NT than with CT; in addition, the 0–30 cm layer accumulated 70% of the MB-C with NT, and 58% with CT. In comparison to CT, the NT system resulted in total inputs of microbial C and N estimated at 38 kg C ha−1 yr−1 and 1.5 kg N ha−1 yr−1, respectively. Apparently, N was the key nutrient limiting C and N stocks, and since adoption of NT resulted in a significant increase of N in soils which were deficient in N, efforts should be focused on increasing N inputs on NT systems.
    Full-text · Article · Dec 2010 · Soil Biology and Biochemistry