response of plant and soil microbes to biochar amendment of an arsenic-contaminated soil
TRANSCRIPT
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ARTICLE IN PRESSG ModelGEE-4681; No. of Pages 9
Agriculture, Ecosystems and Environment xxx (2014) xxx–xxx
Contents lists available at ScienceDirect
Agriculture, Ecosystems and Environment
j ourna l h om epage: www.elsev ier .com/ locate /agee
esponse of plant and soil microbes to biochar amendment of anrsenic-contaminated soil
.J. Gregorya,∗, C.W.N. Andersonb, M. Camps Arbestaina, M.T. McManusc
New Zealand Biochar Research Centre, Private Bag 11222, Massey University, Palmerston North 4442, New ZealandSoil and Earth Sciences, Institute of Agriculture and Environment, Private Bag 11 222, Massey University, Palmerston North 4442, New ZealandPlant Biology, Institute of Fundamental Sciences, Private Bag 11 222, Massey University, New Zealand
r t i c l e i n f o
rticle history:eceived 31 July 2013eceived in revised form 17 March 2014ccepted 18 March 2014vailable online xxx
eywords:iocharrsenicoil Microbial Activityhytoextractionoil Remediationnvironmental Risk
a b s t r a c t
The historical treatment of livestock with arsenical-based pesticides has resulted in large areas of pas-toral land being highly contaminated with arsenic. This study investigated the effect of biochar on soilmicrobial activity and arsenic phytoextraction in an arsenic-contaminated soil during a 180 d glasshouseexperiment. Biochar made from willow feedstock (Salix sp) was pyrolysed at 350 and 550 ◦C (representinga low- and high-temperature biochar) and amended to soil at rates of 30 t ha−1 and 60 t ha−1 to 30 cmdepth (10 and 20 g biochar kg−1 soil, respectively). Ryegrass (Lolium perenne L.) was seeded and plantgrowth was monitored. Soil microbial activity, quantified using the dehydrogenase activity (DHA) assay,was significantly increased (P < 0.01) under all biochar treatments. This increase was in excess of 100%after 30 d of treatment and was significantly higher (P < 0.05) than the control throughout the trial for350 ◦C amended soils. The increase for the 550 ◦C amended soils relative to the control was greater than70%. No negative effect of biochar amendments on ryegrass germination was observed. Biochar promoteda 2-fold increase in shoot dry weight (DW) and a 3-fold increase in root DW after 180 d under all biocharamendments and this was attributed, at least in part, to the fertility value of biochar. By increasing doserates of biochar amendment from 30 t ha−1 to 60 t ha−1 shoot tissue of ryegrass extracted significantlyhigher (P < 0.05) concentrations of arsenic. Through extrapolation, 350 ◦C biochar-amended soils wereestimated to have the potential to increase ryegrass sward DW growth by 0.68 t ha−1 compared to rye-grass grown on unamended soils. This would correspond to an increase in the extraction of total arsenic
−1
by 14,000 mg ha compared to unamended soils and in doing so decreasing soil remediation times byover 50%. This investigation provides insight into the beneficial attributes of biochar in contaminatedsoil, and specifically that produced from willow wood, and its potential to reduce the time needed toremediate arsenic-contaminated soil. However, more studies are needed to understand the mechanismsthrough which these benefits are provided.© 2014 Elsevier B.V. All rights reserved.
. Introduction
Soil contamination is a global problem and occurs when the con-entration of an element or compound in soil exceeds a naturalackground threshold value (Chapman, 2007). Contamination canccur through geogenic or anthropogenic processes (Beesley et al.,011a). The agricultural development of New Zealand through the
Please cite this article in press as: Gregory, S.J., et al., Response of
contaminated soil. Agric. Ecosyst. Environ. (2014), http://dx.doi.org/10
0th century saw the use of a range of inorganic and organicompounds as pesticides to control production-limiting insects.hese pesticides included arsenicals and a range of organochlorines
∗ Corresponding author. Tel.: +64 6 356 9099x84850; fax: +64 6 350 5632.E-mail address: [email protected] (S.J. Gregory).
ttp://dx.doi.org/10.1016/j.agee.2014.03.035167-8809/© 2014 Elsevier B.V. All rights reserved.
used specifically to control parasites on sheep. Animals would besubmerged in baths containing these chemicals with the leftoversolution pumped onto surrounding soil. Today an estimated 50,000contaminated sheep dip sites exist in New Zealand with soil con-centrations of arsenic reaching as high as 11,000 mg kg−1 to a depthof 30 cm (NZ Ministry for the Environment, 2006).
Dipping with arsenic is no longer practiced. Today organophos-phate compounds are topically applied to animals to controlparasites. However, historically-contaminated soil (as a presentday risk) can negatively affect water quality where arsenic leachesthrough the soil profile and becomes a diffuse source of pollu-
plant and soil microbes to biochar amendment of an arsenic-.1016/j.agee.2014.03.035
tion to streams and rivers. Arsenic in soil can also detrimentallyaffect soil microbial activity and thus affect nutrient cyclingand soil biodiversity (Klose & Ajwa, 2004; Pampulha & Oliveira,2006; Zhou et al., 2006; Anderson et al., 2009). Therefore, the
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emediation of historically contaminated sheep-dip sites has beenefined as an important goal for future environmental sustain-bility in New Zealand (NZ Ministry for the Environment, 2006).wo technology-based concepts that have the potential to managend/or remediate arsenic in soil are biochar and phytoextraction.
Plants have a natural ability to take up metals and metalloidsrom soil by either passive or active means, but the technologi-al application of this trait to remediate contaminated areas canake hundreds of years depending on the severity of contamina-ion (Tsao, 2003; Saleh et al., 2004; Meers et al., 2008; Zhao et al.,009). The plant species that have been most commonly used toxtract arsenic from soil (phytoextraction) are arsenic hyperaccu-ulating ferns such as Pteris vittata and Pteris cretica. These plants
ave been used for arsenic remediation under both greenhouse andeld conditions (Zhao et al., 2002; Xiao et al., 2008). Niazi et al.2010) reported that hyperaccumulator ferns grown in the field at
historic cattle dip site had an arsenic concentration of more than500 mg kg−1 after 6 months of growth (Niazi et al., 2010). Ferns,owever, have slow growth rates and require low light-intensityonditions to flourish. Their use in field applications may thereforee limited.
The target characteristics for a plant species being used inhytoextraction include adequate rates of growth and biomass pro-uction (including the development of root biomass) along witholerance to the metal (metalloid) being targeted for remediationVamerali et al., 2010). Any strategy that can increase the rate oflant growth and that can manipulate soil chemistry and biologyo increase arsenic bioavailability for plant uptake may improve theotential and timeframe for phytoremediation. It is in the contextf optimised phytoextraction using a non-hyperaccumulator butigh biomass and growth rate species that biochar may be a soilmendment that can reduce the timeframe of remediation.
Biochar is charcoal added to soil to improve soil functions ando reduce emissions from organic material that would otherwiseaturally degrade to greenhouse gases (Sohi et al., 2010). The poten-ially useful surface properties of biochar can lead to contaminantontrol and nutrient retention and release. Fresh biochars usuallyave a low cation exchange capacity (CEC). However, with time itsurface will tend to oxidise as a result of weathering and increaseEC (Cheng et al., 2006; Cheng et al., 2008; Calvelo Pereira et al.,011). High CEC will lead to the retention of many heavy metals
n soil but not that of metalloids such as arsenic which mainlyxists as an oxyanion. Biochar can also have high liming equiva-ence which may raise the soil pH and thus has the potential toncrease the mobility of arsenic making it more available for uptakey plants (Hartley et al., 2009; Joseph et al., 2010). This scenarioan increase the extraction efficiency for arsenic uptake into plantsnd reduce remediation times for contaminated soil. Therefore,
coupled biochar and phytoextraction remediation system couldotentially reduce the remediation time due to the alkaline proper-ies of biochar increasing the elemental solubility of arsenic withinhe soil (Beesley et al., 2011a).
Previous studies investigating the interactions between biocharnd soil contaminants in a contaminated soil have focussed onetal availability and retention (Namgay et al., 2010; Beesley et al.,
011b). Less attention has been paid to the dual effect of biochar onlant growth and soil microbial activity, and the effect that theseay have in the stimulation of arsenic phytoextraction. Here, we
nvestigate the influence of biochar on soil chemistry and biologyhen applied to a highly arsenic-contaminated soil in the presence
f plants. We have used Lolium perenne L. (perennial ryegrass) as aodel non-arsenic accumulator plants species. Ryegrass is a com-
Please cite this article in press as: Gregory, S.J., et al., Response of
contaminated soil. Agric. Ecosyst. Environ. (2014), http://dx.doi.org/1
on species grown in New Zealand pastoral systems that thrivesn soil with a pH between 5.5 and 7.5 (Sartie, 2006). Ryegrass isoutinely used to investigate plant growth responses (germina-ion, root and shoot growth) to changing environmental conditions,
PRESSnd Environment xxx (2014) xxx–xxx
and has been used in this study to better understand plant–soildynamics in a biochar amended soil.
The specific objectives of our study were (i) to determinewhether biochar produced at 350 ◦C and 550 ◦C added to an arsenic-contaminated soil would promote arsenic uptake in L. perenne L., (ii)to investigate whether biochar additions would affect soil micro-bial activity in such a system, and (iii) to ascertain the potentialthat biochar amendment of sheep-dip contaminated soil has toimprove the efficacy of phytoextraction for soil remediation andmanagement.
2. Materials and methods
2.1. Sample collection and pre-treatment
A sheep dip site that was operational from 1860 to 1980 wasidentified on the east coast of the North Island of New Zealand.Previous analysis of soil from this location defined the pres-ence of heterogeneous arsenic contamination ranging from 200 to2000 mg kg−1 in the proximity of the dip (Gregory, 2013) along withmoderate concentrations of organochlorines (dieldrin, aldrin, DDT,lindane) which were not investigated as part of the current study. Abulk sample of soil (300 kg) was taken from the top soil (0–20 cm)across a 2 m × 2 m area identified as where the remaining arseni-cal solution was disposed of at the end of dipping. The soil wasmixed to obtain homogeneity using a nursery grade mixer withtwo sets of revolving sleeves that slowly fold the soil, and finallysieved through a 5 mm-mesh.
2.2. Biochar production
Wood from one-year-old willow (pyrolysed at 350 ◦C) and five-year-old willow (pyrolysed at 550 ◦C) (Salix sp.) was collected froma commercial willow farm and chipped into approximately 0.5 cmsize fragments and dried at 30 ◦C until constant weight. The woodwas pyrolysed using a 25 L gas-fired rotating drum kiln with anaverage heating rate of 23.3 and 36.6 ◦C min−1 for the 350 ◦C (lowtemperature) and 550 ◦C (high temperature) biochars respectively.The peak temperatures were achieved by controlled release ofpyrolysis gases in the kiln, and were maintained for 1–2 min fol-lowed by a 1 h cooling period prior to discharge into a sealed plasticbag.
2.3. Glasshouse experiment
Pot experiments were conducted under glasshouse conditionsusing square plastic pots measuring 20 × 20 cm and 30 cm deep,with drainage holes drilled at the base of the containers. Analysisof the soil showed that soil fertility was within agronomic guide-line parameters, and therefore fertiliser (N:P:K) was not applied.Two doses of biochar were selected: 10 and 20 g biochar kg−1 soil,which when incorporated to 30 cm depth corresponds to a loadingof 30 t ha−1 and 60 t ha−1, respectively. These doses are higher thanthose used in agronomic studies, and probably not feasible for largeareas of land. However, sheep dip sites are commonly small (30 m2)but highly contaminated, and may be amenable to high rates ofbiochar application. Biochar was manually mixed with soil prior tofilling of the pots. All pots were kept at 70% water holding capac-ity (WHC) with the addition of distilled water and left for 1 weekto incubate prior to planting with ryegrass. Fifty (Lolium perenneL. cv Nui) seeds obtained from AgResearch Grasslands NZ (Acces-sion No: A13509 Nil Endophyte), that were imbibed overnight in
plant and soil microbes to biochar amendment of an arsenic-0.1016/j.agee.2014.03.035
distilled water, were then placed on top of the soil using forceps(representing T = 0) and lightly sprayed with distilled water daily.The growth experiment was conducted over 6 months with threereplicate pots per treatment. Germination rate was recorded over
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he first 20 days. Contaminated soil that was not amended withiochar was the control treatment in this study.
Soil samples (5 g) were collected from every pot each monthor chemical and biological analysis starting 30 d after seedingT = 30). At each sampling time two vertical cores were takensing a stainless steel corer to 10 cm depth (each core 6 g). Theseores were homogenised in a plastic bag and then split. One halfas analysed for microbial activity (fresh soil) and the other forater-extractable arsenic concentration (air-dried soil). To min-
mise disturbance of the developing root zone at each sampling,ored holes were filled with initial (control) soil and marked with
toothpick during monthly sampling. A new sampling locationoughly 3 cm adjacent to the previous was used at each samplingime.
.4. Plant growth analysis
Germination of ryegrass seeds was scored on the first sign ofadicle emergence by observing each seed under magnificationaily (T = 20d). At the termination of the experiment (T = 180d), rye-rass seedlings were separated into shoot and root respectively byutting at the remaining seed husk junction (emergence of plumulend radicle) and collectively pooled per pot. Roots were sepa-ated from the soil media by passing through a 5 mm sieve andhoroughly washed in distilled water to remove any attached soilarticles. Both root and shoot were placed in paper bags and oven-ried at 75 ◦C for 3 d to obtain dry weights. Tillering was quantifiedy the number of tillers per pot.
.5. Arsenic analysis
A composite sample of harvested ryegrass shoots was gener-ted for each pot and finely ground using a mechanical grinder. Inreparation for total arsenic analysis, a sub-sample (1 g) was pre-igested in aqua regia (3:1 mixture of concentrated HCl and HNO3)vernight. The shoot material was thereafter digested at 120 ◦C on aeat block for 2 h and left to cool before filtering through filter paperWhatman 42 C). The digest solution was made to a final volumef 50 mL with deionised water. Arsenic analysis was carried outsing Flow Injection Analysis System 400 (FIAS, Perkin Elmer) cou-led with Graphite Furnace Atomic Absorption SpectrophotometerAnalyst 600 (GFAAS, Perkin Elmer). Prior to analysis, aliquots ofach digest were pre-reduced by taking 1 mL of sample and adding
mL of HCl, and 1 mL of 5% (w/v) KI + 5% (w/v) ascorbic acid solu-ion. The treated samples were allowed to stand for 45 min at roomemperature and finally diluted to 10 mL with 10% (w/v) HCl. Theseamples were analysed for arsenic concentration using FIAS. Work-ng standards were prepared from the As (V) salt Na2HAsO4·7H2Ond a minimum correlation coefficient for the standard curve of.995 was required before analysis could proceed. The certified ref-rence plant sample 1573a (tomato) from the National Institute oftandards and Technology and soil reference CRM - GBW 07403rom the National Research Centre for CRMs of China were usedo determine the accuracy of the analytical method to quantify theoncentration of arsenic in plant and soil. Analysed values of thelant and soil reference material differed by less than 10% from theeported mean concentrations.
A modified version of the extraction method reported by Ko et al.2008) was used for the extraction of water soluble arsenic. 2 g ofir-dried sieved soil was placed in a 25 mL polycarbonate centrifugeube, mixed with 20 mL of deionised water, and shaken overnight
Please cite this article in press as: Gregory, S.J., et al., Response of
contaminated soil. Agric. Ecosyst. Environ. (2014), http://dx.doi.org/10
16 h) on a rotating over-end platform. Tubes were then removednd centrifuged at 8000 r.p.m for 3 min. The extractant solution wasltered through filter paper (Whatman 42 C) and then pre-reducednd analysed according to the method described for total arsenic.
PRESSnd Environment xxx (2014) xxx–xxx 3
2.6. Dehydrogenase activity (DHA) assay
Microbial oxidation of organic compounds is directly linked tothe electron transport chain (ETC) that utilises oxygen as a finalelectron acceptor. Dehydrogenases form a main branch of the ETCand are a fundamental enzyme system found in microorganisms(Camina et al., 1998). Such an attribute makes dehydrogenaseactivity a good indicator of total microbial activity and can bedetermined in laboratories by using artificial electron acceptorslike tetrazolium salt. In this work, microbial activity was quantifiedby measuring the dehydrogenase activity in the soil according tothe method of Chandler & Brooks (1991) with modification. Briefly,DHA measurement was performed using 5 g of fresh soil with theaddition of 0.1 g CaCO3 for activation. 3 mL of tetrazolium chloride(TTC) was added in the absence of light and the resulting mixturevortexed to remove any trapped air spaces. The mixture was thenincubated at 28 ◦C overnight and the resulting tri-phenyl formazan(TPF) extracted with 20 mL methanol. Colorimetric intensity wasmeasured at 490 nm using a Jenway Spectrophotometer (Jenway7315) to determine formazan concentration. Standard curves wereconstructed for each treatment to limit the effect of TPF colourabsorption caused by biochar.
2.7. Soil and biochar analysis
2.7.1. BiocharCarbon, hydrogen and nitrogen concentrations in biochars
were determined using Elementar vario MACRO CUBE (Elemen-tar; Germany). The pH of biochar was measured in deionized waterat a 1:100 (w/w) ratio according to the method of Ahmedna et al.(1997) after pre-heating for 20 min at 90 ◦C and cooling to roomtemperature. The ash content was determined by thermal analy-sis using a thermogravimetric analyser (SDT Q600, TA Instruments,Melbourne, Australia). For TGA analysis biochars (10–15 mg) wereplaced in an Al2O3 crucible and heated from room temperature to900 ◦C (at a rate of 5 ◦C min−1) under a N2 atmosphere before an aircurrent was provided (Calvelo Pereira et al., 2011). The ash contentof each sample was determined when there was no further weightchange.
Surface analysis of fresh biochars was conducted by x-ray pho-toelectron spectroscopy (XPS) with Mg K � (1253 eV) radiationemitted from a double anode at 50 W. Binding energies for the highresolution spectra were calibrated by setting C to 1 s at 284.6 eV. Theliming equivalence of biochar (CaCO3 equivalence) was determinedaccording to the AOAC standard method (AOAC, 1999) using anauto-titrator (TIM 865 Titration Manager, Radiometer Analytical).
Specific surface area of each biochar was calculated fromN2 physisorption data according to the Brunauer–Emmett–Teller(BET) method using P/Po values in the range 0.05–0.2. N2 physisorp-tion measurements were performed at liquid nitrogen temperature(−195
◦C) using a Micromeritics Tristar 3000 instrument. Samples
were degassed at 300 ◦C in N2 for 4 h prior to the N2 adsorptionmeasurements.
Extractable P in biochar was estimated using 2% formic acid fol-lowing the method of Rajan et al. (1992) as modified by Wanget al. (2012b). Extractable K, Mg, Ca and SO4–S were analysedaccording to the methods of Blakemore et al. (1987) but with mod-ification. Briefly 0.35 g of finely ground biochar was added to 35 mL1 M HCl acid solution and placed in 35 mL centrifuge tubes on anover-end shaker overnight. Samples were then filtered and the con-centration determined by atomic absorption spectroscopy (AAS)(auto-analyser for SO4–S).
plant and soil microbes to biochar amendment of an arsenic-.1016/j.agee.2014.03.035
2.7.2. SoilSoil pH was measured in deionised water at a ratio of 1:2.5.
Available phosphate (Olsen P), available sulphate and soil cations
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Table 1Elemental analysis of biochar, production and characteristics.
Parameter 350 ◦C Biochar 550 ◦C Biochar
Feedstock Salix sp. (1y.o) Salix sp. (5.y.o)Pyrolysis Temp (◦C) 350 ◦C 550 ◦CpH 8.6 8.6Yield (%) 27.5 25.0Organic C Content (g kg−1)a 739 774N (g kg−1) 8.0 7.0S (g kg−1) 3.0 2.0O (g kg−1)b 159 143H (g kg−1) 35 33Volatile C (%)c 30.8 27.5Atomic H/Corg 0.52 0.48Ash Content (%)c 5.6 4.1CaCO3-eq Equiv (%)c 8.9 9.2Surface Area (m2 g−1) 6.1 59.81 M HCl-extractable K (g kg−1) 11.9 10.71 M HCl-extractable Ca (g kg−1) 23.6 24.01 M HCl-extractable Mg (g kg−1) 1.5 1.41 M HCl-extractable SO4-S (g kg−1) 1.9 1.82% Formic acid-extractable P (g kg−1) 0.7 0.8
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.8
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13.2
±
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0.7
±
0.1a
3.5
±
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1.2
±
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0.4
±
0.1a
12
±
0.0a
202
±
3.3a
il
5.6
48.6
±
0.3a
12.5
±
0.7a
0.7
±
0.0a
3.5
±
0.0a
1.0
±
0.0a
0.3
±
0.0a
12.0
±
0.0a
200
±
2.3a
C
BC
(30
t ha−1
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5.6
47.9
±
2.1a
16.0
±
0.3b
1.0
±
0.0b
4.6
±
0.2b
1.1
±
0.0a
0.3
±
0.0a
16.0
±
0.6b
198
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C
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47.6
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25.7
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8
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1.3
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0.4
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19.0
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197
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C
BC
(30
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5.6
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18.5
±
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9
±
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1.1
±
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±
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15.0
±
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197
±
3.2a
C
BC
(60
t ha−1
)
5.8
49.3
±
1.3a
19.0
±
4.3b
1.2
± 0.
1b5.
9
±
0.1c
1.2
±
0.0a
0.3
±
0.1a
17.0
±
1.0b
196
±
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been
dep
icte
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as
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ble
cati
ons
(meq
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a Biochars contained <0.8% Cinorg thus Corg basically represents total C.b Estimated by difference O = 100 − (C + N + S + H + Ash).c Volatile C, ash content and CaCO3 – equivalence are provided in mass basis
ere measured according to the methods of Blakemore et al.1987). Available phosphate (Olsen P) was extracted in 0.5 Modium bicarbonate at a soil:solution ratio of 1:20 and deter-ined calorimetrically. Available sulphate was extracted with
.1 M potassium phosphate at a soil:solution ratio of 1:5 andetermined by automated colorimetric technique. Cations werextracted by leaching with 1 M ammonium acetate (pH 7) at aoil:solution ratio of 1:50 and determined by atomic absorptionpectroscopy (AAS). Cation exchange capacity was determined byhe summation of extractable cations and the extractable acidityHesse, 1971).
.8. Statistical analysis
To ascertain significant differences amongst the means, theukey’s test was applied. Statistical differences between the treat-ents under study were determined by analysis of variance
ANOVA) using SPSS version 16.0 (SPSS Inc., Chicago, USA).
. Results
.1. Biochar properties and characteristics
Elemental analysis and the yield of the two biochars are described in Table 1.oth biochars had high pH (8.6) with yields of 25% and 27.5% for the 550 ◦C and 350 ◦Ciochar, respectively. Organic C in both biochars was >70%, whereas inorganic C waslmost negligible (<0.8%). The 350 ◦C biochar had a higher volatile C content than the50 ◦C biochar (30.8% compared to 27.5%), higher atomic H/Corg ratio, and a lowerroportion of fixed C (63.6% compared to 68.4%), as expected. The liming equiva-
ence of biochar was 8.9% and 9.2% for the 350 ◦C and 550 ◦C biochars, respectively.ncreased pyrolysation temperature significantly increased the specific surface areaP < 0.01) from 6.1 m2 g−1 for the 350 ◦C biochar to 59.8 m2 g−1 for the 550 ◦C biochar.igh-energy XPS spectra of fresh biochars describe the surface functionality of car-on (C1s). The XPS spectra define energy signals corresponding to four functionalroups: aliphatic/aromatic (284.6 eV assigned to CHx, C–C, C C), hydroxyl and ether285.8 eV to C–OR), carbonyl (287.2 eV to C O) and carboxyl groups (288–289 eV to–OOR). Biochars had a very high proportion of aliphatic/aromatic carbon (83.56%nd 87.08% for 350 and 550 ◦C biochars) and low proportions of carboxylic andarbonyl groups (Table S1). Both biochars contained high concentrations of 1 M HCl-xtractable K+ (10–12 g kg−1) and Ca2+ (24 g kg−1) and moderate concentrations ofg2+ (1.5 g kg−1), and SO4–S (1.8 g kg−1) while formic-P yielded 0.7 g kg−1 (Table 1).
he chemical composition of the biochars in our study is in agreement with previoustudies (Cheng et al., 2006; Hina et al., 2010).
Please cite this article in press as: Gregory, S.J., et al., Response of plant and soil microbes to biochar amendment of an arsenic-contaminated soil. Agric. Ecosyst. Environ. (2014), http://dx.doi.org/10.1016/j.agee.2014.03.035
.2. Effect of biochar amendment on soil nutrient properties
The chemical properties of the control soil and the biochar-amended soilsere analysed at T = 180 d (Table 2). Soil amended with both types of biochar had Ta
ble
2El
emen
tal a
n
Con
trol
SoC
ontr
ol
SoSo
il
+
350
◦
Soil
+
350
◦
Soil
+
550
◦
Soil
+
550
◦
Cat
ion
s
hav
e
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Table 3Water extractable arsenic (mg L−1) in soil under biochar and control treatments. Time (T) is noted in days after amendment. Significant differences are denoted by differentletters at P < 0.05 (mean n = 3; ± s.e.). Soil pH values are listed in italics and in brackets for each treatment.
T = 0d T = 30d T = 60d T = 90d T = 120d
Control Soil 1.3 ± 0.16a (5.7 ± 0.0a) 1.4 ± 0.11a (5.8 ± 0.0a) 1.2 ± 0.13a (5.7 ± 0.0a) 1.3 ± 0.08a (5.8 ± 0.0a) 1.4 ± 0.00a (5.8 ± 0.0a)350 ◦C BC (30t ha−1) 1.4 ± 0.10a (6.0 ± 0.0b) 0.8 ± 0.03b (6.0 ± 0.0b) 1.1 ± 0.04a (5.8 ± 0.1a) 1.2 ± 0.04a (5.9 ± 0.1a) 1.4 ± 0.02a (5.9 ± 0.1a)
◦ −1 a b b b 1.1 a b a b a b
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350 C BC (60t ha ) 1.2 ± 0.22 (6.2 ± 0.0 ) 0.9 ± 0.08 (6.0 ± 0.0 )
550 ◦C BC (30t ha−1) 1.3 ± 0.05a (6.1 ± 0.0b) 0.9 ± 0.09b (5.9 ± 0.0b)
550 ◦C BC (60t ha−1) 1.4 ± 0.15a (6.1 ± 0.0b) 1.0 ± 0.16b (6.1 ± 0.0b)
ignificantly (P < 0.05) higher concentrations of extractable SO42-, K+, Ca2+ and Mg2+
han the control soil yet Olsen P values were slightly lower. Soil pH was significantlyncreased at high doses for both biochars, from pH 5.6 to pH 5.8 (P < 0.05). At T = 180
total arsenic was lower under all biochar treatments compared to the control soilet differences were not significant (P > 0.05).
.3. Effect of biochar on water-extractable arsenic
All treatments initially (T = 0 d) had similar water-extractable arsenic concen-rations (Table 3). In soils collected at T = 30 d, all biochar treatments showed aignificant reduction (P < 0.05) in the concentration of water available arsenic com-ared to the control soil. By T = 60 d, the concentration of water-soluble arsenic had
ncreased to be the same as that recorded for the control soil and differences amongreatments remained not significant (P > 0.05) thereafter.
.4. Soil dehydrogenase activity
Please cite this article in press as: Gregory, S.J., et al., Response of
contaminated soil. Agric. Ecosyst. Environ. (2014), http://dx.doi.org/10
Biochar-amended soils had significantly higher (P < 0.05) DHA compared to theontrol soil yet the relative rate of increase over time was similar among treatmentsFig. 1). The increase for the control soil was 155 �g g−1 soil DM (dry matter) after80 days. The 350 ◦C biochar increased DHA by 163 �g g−1 DM and 235 �g g−1 DM
ig. 1. Soil dehydrogenase activity (DHA) measured in �g per g of dry matter (DM)s a function of 350 ◦C and 550 ◦C biochar treatment (mean n = 3; ± s.e.). Biocharreatment (BC) doses are denoted as ‘low’ (30 t ha−1) or ‘high’ (60 t ha−1).
± 0.02 (6.0 ± 0.0 ) 1.2 ± 0.04 (5.9 ± 0.0 ) 1.4 ± 0.05 (6.1 ± 0.0 ) ± 0.03a (5.9 ± 0.0b) 1.1 ± 0.07a (5.8 ± 0.0a) 1.3 ± 0.01a (5.9 ± 0.0b) ± 0.06a (5.9 ± 0.0b) 1.3 ± 0.14a (5.8 ± 0.0a) 1.5 ± 0.05a (6.0 ± 0.0b)
(30 t ha−1 and 60 t ha−1 respectively) whereas the 550 ◦C biochar increased DHA by169 �g g−1 DM and 175 �g g−1 DM (30 t ha−1 and 60 t ha−1).
3.5. Ryegrass germination
Amendment of the soil with biochar (both rates and temperatures) had no sig-nificant (P > 0.05) effect on overall germination of ryegrass seeds over the first 20days of the trial when compared to the unamended soil (Fig. 2). The control soil hada germination rate after 20 days of 93% while the biochar treatments had a germi-nation rate ranging from 93 to 97%. Germination started 3 d after imbibition andreached 60% after 6 d for all treatments. Both biochars at 60 t ha−1 caused a decreasein germination percentage over the period 6–13 d relative to the control. A similardecrease was apparent for the 350 ◦C biochar at 30 t ha−1. However, by day 15 thecumulative germination rate was the same for all treatments.
3.6. Ryegrass dry weight (biomass)
Lolium perenne L. root and shoot dry weight (biomass) was significantlyincreased (P < 0.01 and <0.05 respectively) for all biochar treatments relative to thecontrol (Fig. 3), although no significant differences (P > 0.05) were observed betweenthe four biochar treatments. Soil amendment with biochar (550 ◦C) resulted in anincrease in shoot DW to 6.1 g and 5.5 g per pot for 30 t ha−1 and 60 t ha−1, respec-tively. Shoot biomass for the control treatment was 3.67 g per pot. The effect ofbiochar was therefore an approximate doubling of total shoot DW after 180 days rel-ative to the control (P < 0.01). Root DW for the control treatment (4.5 g per pot) wasnearly three-fold lower than for the biochar treatments (<0.05). Root DW growthfor the biochar amended soil was 10.8 g and 11.2 g for the 350 ◦C biochar (30 t ha−1
and 60 t ha−1) and 11.1 and 11.0 g for the 550 ◦C biochar (30 t ha−1 and 60 t ha−1
respectively).
3.7. Ryegrass tillering
plant and soil microbes to biochar amendment of an arsenic-.1016/j.agee.2014.03.035
Ryegrass tillering was significantly increased by all biochar treatments (P < 0.05)(Fig. 4). The control pots yielded an average 89 tillers per pot. At 30 t ha−1 for the550 ◦C biochar treatment, each pot yielded 113 tillers and 107 tillers for 60 t ha−1
although no significant difference (P > 0.05) was noted between the rates of 550 ◦Cbiochar. For soil amended with 350 ◦C biochar, pots yielded 120 tillers and 140 tillers
Fig. 2. Ryegrass seed germination (%) between 0 and 20 d after seeding onto soilamended with both 350 ◦C and 550 ◦C biochar at two rates (30 t ha−1 and 60 t ha−1).The control soil is soil not amended with biochar.
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6 S.J. Gregory et al. / Agriculture, Ecosystems and Environment xxx (2014) xxx–xxx
F r treaP ha−1).
ffb
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FB
ig. 3. Averaged ryegrass DW (g) yield at harvest (T = 180 d) as a function of biocha < 0.05. Biochar treatment (BC) doses are denoted as ‘low’ (30 t ha−1) or ‘high’ (60 t
or 30 t ha−1 and 60 t ha−1, respectively. A significant greater tillering was observedor the 350 ◦C biochar treatment at a dose of 60 t ha−1 compared to the other threeiochar treatments (P < 0.05).
.8. Arsenic concentration in Ryegrass shoot biomass
The arsenic concentration in ryegrass shoot biomass was significantly increasedP < 0.05) as a function of both biochar treatments at 60 t ha−1 relative to the controlFig. 5). However no change was apparent for biochar applied at a rate of 30 t ha−1
ompared to the control (P > 0.05). The maximum concentration of shoot arsenic was5.3 mg kg−1 for the 60 t ha−1 application of 350 ◦C biochar. This was an increase of3% over the control concentration (11.5 mg kg−1).
. Discussion
Our research forms part of a three-year investigation designedo analyse the effects of biochar–plant interactions on arsenic andrganochlorine concentration and arsenic bioavailability in a his-oric sheep dip contaminated soil. In this study we describe thepecific effects of biochar on both soil properties and plant responseo arsenic in the soil. Biochar technology was initially developed as
Please cite this article in press as: Gregory, S.J., et al., Response of
contaminated soil. Agric. Ecosyst. Environ. (2014), http://dx.doi.org/1
means to sequester carbon in the soil for long periods of timen order to offset the effects of increasing carbon dioxide emis-ions and to improve soil fertility (Kookana, 2010; Lehmann andoseph, 2009). However, in recent years many researchers have
ig. 4. Average number of ryegrass tillers per pot as a function of biochar treatment (miochar treatment (BC) doses are denoted as ‘low’ (30 t ha−1) or ‘high’ (60 t ha−1).
tment (mean n = 3; ±s.e.). Significant differences are denoted by different letters at
observed that biochar addition to soil may effect environmentalimprovement within contaminated soil as a result of changes toplant–soil–microbial interactions (Beesley et al., 2011a; Beesleyet al., 2011b; Hartley et al., 2009).
4.1. Biochar stimulates soil dehydrogenase activity
We quantified total soil microbial activity using the DHA assayto assess whether the biochar amendment caused a change in therelative environmental toxicity of arsenic. This assay was first usedfor this purpose by Chander and Brookes (1991) when working withcopper-contaminated soils. The addition of both low and high tem-perature biochar caused a significant increase in DHA relative tothe control (Fig. 1), but there was no difference between the twodose treatments used (30 t ha−1 and 60 t ha−1). Low temperature(350 ◦C) biochar has a greater labile fraction of carbon (C) thanthe high temperature biochar, as inferred from its volatile fraction,and this C can be used as an energy source by soil microorgan-isms (Lehmann et al., 2011). Increased energy supply may stimulate
plant and soil microbes to biochar amendment of an arsenic-0.1016/j.agee.2014.03.035
microbial activity leading to a higher soil DHA. However, the lackof differences between the two types of biochar suggests that otherfactors may be also influencing microbial activity. Possible fac-tors include the nutrient status of the biochar and pH as bacteria
ean n = 3; ± s.e.). Significant differences are denoted by different letters at P < 0.05.
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S.J. Gregory et al. / Agriculture, Ecosystems and Environment xxx (2014) xxx–xxx 7
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ig. 5. Total average arsenic concentration (mg kg−1) in ryegrass shoot biomass as aifferent letters at P < 0.05. Biochar treatment (BC) doses are denoted as ‘low’ (30 t h
re thought to respond positively to increases in soil pH (Josepht al., 2010; Lehmann et al., 2011), although Avalos & Fouz (2012)bserved a decrease in DHA activity with slight increases in pH.
greater root development, as quantified by root biomass, inhe presence of biochar may have also affected microbial activ-ty through a greater input of root exudates and detritus into thehizosphere.
Microbial activity in a contaminated environment can be neg-tively affected by the chemicals that constitute contamination.espite being non-target organisms of pesticide applications, soilicrobes are affected by dip chemicals once added to the soil
Chopra et al., 2007). Pesticides such as arsenicals reduce soilnzyme activity (Antonious, 2003; Monkiedje et al., 2002) and canave a detrimental impact on the makeup of soil microbial com-unities that exist in and around a dip site (Pampulha & Oliveira,
006; Zhou et al., 2006; Klose & Ajwa, 2004). A short-term reduc-ion to the water-extractable concentration of arsenic in soil mayave decreased toxicity pressure on some soil microorganisms. Thenset of the increase in DHA (Fig. 1) was simultaneous to this reduc-ion in water soluble arsenic (Table 3).
A temporary reduction in the water-extractable arsenic con-entration could be due to the precipitation of arsenic with metalations, such as Ca2+, from soluble salts found in the initial ashraction (e.g., chlorine and sulphate salts). These arsenic salts will,owever, readily redissolve, releasing the arsenic again to theater-extractable phase (Beesley et al., 2011a,b) or may leach
although in this study leaching was minimised by holding the soilt 70% WHC). Alternatively, as the incubation proceeded, the limingffect of the amendment may have become more evident increasingrsenic solubilisation due to the associated increase in soil pH. Spe-ific adsorption of arsenic onto the non-weathered biochar surfaceannot be discarded, although the magnitude of positive charge onhe carbonaceous surface is generally low (Liang et al., 2006).
.2. Manipulation of ryegrass growth with biochar additions
In our study, biochar made from willow feedstock did not affecthe extent of final germination but did slow the germination rateelative to the control for three treatments between 6 and 13 daysFig. 2). Germination was scored at the first sign of radicle emer-
Please cite this article in press as: Gregory, S.J., et al., Response of
contaminated soil. Agric. Ecosyst. Environ. (2014), http://dx.doi.org/10
ence and we observed that some seeds were placed directly onop of biochar chips. However, after 18 d the extent of germinationor the biochar treatments was the same as that for the control.ur research therefore shows that the effect of biochar on plant
ion of biochar treatment (mean n = 3; ± s.e.). Significant differences are denoted byr ‘high’ (60 t ha−1).
germination varies in the short term (<15 d) but is not significantly(P > 0.05) beneficial or detrimental in the long term (>20 d). Thiseffect is in agreement with Free et al. (2010) who studied maizegermination in soil amended with different types of biochar. How-ever, variation in germination is likely to be a function of plantspecies and soil type. Biochars have been suggested to contain phy-totoxic compounds that may decrease overall seed germination(Kookana, 2010) or contain organic compounds such as buteno-lide that can trigger germination (Dixon, 1998). Biochars derivedfrom paper mill waste (applied at 10 t ha−1) have been shown toimprove germination in wheat (van Zwieten et al., 2010) and let-tuce (Lactuca sativa) when using a sorghum feedstock (Keller et al.,2010) while biochar made from wheat chaff did not affect wheatseed germination (Solaiman et al., 2012).
The nutrient value of biochar is strongly associated to the typeof feedstock and the pyrolysing temperature used (Wang et al.,2012a,b). Soil amended with both types of biochar in our work hadsignificantly (P < 0.05) higher concentrations of SO4
2-, K+, Ca2+ andMg2+ when compared with the control soil (Table 2). We believethat this is due to the high soil application rates of biochars thatcontained a relatively high concentration of available K+, Ca2+, andSO4
2− (Camps-Arbestain et al., 2014) but also moderate concentra-tion of available Mg2+ (Table 1). In our study, addition of biocharto soil caused an increase in both root and shoot DW after 180 dof growth (Fig. 3). This increase can be partly associated with thenutrient composition of biochar (Table 1). However, increased soilfertility may also promote increased activity of soil microorgan-isms that are responsible for element cycling and transformation.Gregory (2013) detected the presence of plant growth-promotingrhizobacteria (PGPR) in the biochar-amended soils of the currentstudy. These bacteria are able to fix nitrogen and solubilise unavail-able forms of nutrient such as phosphate, making these elementsmore available for plant uptake (Ambrosini et al., 2012; Harelet al., 2012). The extent to which such soil bacteria may constituteincreased DHA is unknown, but genetic fingerprinting of the abun-dance of soil microorganisms in the biochar-treated soils relative tothe control soils is currently underway to determine whether thestructure of the soil community has become more dominated bymicroorganisms such as PGPR as a function of biochar amendment.
plant and soil microbes to biochar amendment of an arsenic-.1016/j.agee.2014.03.035
4.3. Biochar increased arsenic uptake in ryegrass shoot tissue
Biochar addition to soil led to an increase in the arsenic con-centration of ryegrass shoots relative to the control (Fig. 5). We
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ttribute this to an increase in soil alkalinity caused by biocharmendment (Table 3), despite the initial reduction in the water-xtractable arsenic concentration in soil. The liming effect ofiochar and resulting pH increase plays a major part in arsenicobility within the soil (Frost & Griffin, 1977; Masscheleyn et al.,
991; Mahimairaja et al., 2005; Carrillo-Gonzalez et al., 2006;artley et al., 2009; Beesley et al., 2011a; Namgay et al., 2010).
n our trial, biochars slightly raised soil pH over the six-monthxperimental period and this was attributed to the liming effect ofiochar as both biochars contained a CaCO3-equivalence of greaterhan 8.8%. The liming effect was more evident in the 60 t ha−1 treat-
ents.Conflicting results are reported in literature regarding the effect
f biochar on arsenic mobility, but there is consensus that biocharill change the chemistry of arsenic in soil. This change may beediated through change in redox status of the soil or by an effect
n soil pH (e.g. liming effect) (Joseph et al., 2010). Microbial activ-ty within the soil can also affect both the redox status of the soilnd arsenic speciation. Recent studies have provided insights into
change in arsenic speciation from arsenate to arsenite causedy increased microbial activity leading to greater bioavailability tolants (Ruiz-Chancho et al., 2008; Bolan et al., 2012).
Research into the effect of biochar–arsenic interactions on metalptake by plants has provided contrasting views. Both Hartley et al.2009) and Namgay et al. (2010) observed no significant increasen arsenic uptake in Miscanthus sp. and Zea mays respectively whenoils were amended with biochar. However, the fact that the soilsed by the former was naturally alkaline (pH 7–8) may haveasked the effect of biochar amendment.
.4. Application of an integrated biochar and phytoextractiontrategy to remediate sheep dip sites
Environment-friendly technologies that not only reduce thempact of a contaminant on the environment but that also haveeneficial additional effects such as increasing soil functionsre becoming popular with the general public and researchersAdriano et al., 2004; Pilon-Smits and Freeman, 2006). The tan-em use of biochar and phytoremediation has been shown hereo provide benefit for the remediation of soil contaminated withrsenic. Under controlled glasshouse conditions this study hashown that biochar amendment can have a number of interact-ng beneficial effects in a contaminated soil that ultimately hashe potential to decrease soil remediation time using techniqueshat can be applied in situ. Here, we have shown that a couplediochar–phytoextraction system can both stimulate plant growthnd also the uptake of arsenic across root and into shoot tissue.
The potential benefit of integrating biochar with phytoex-raction can be quantified through consideration of the biomassnd arsenic uptake data that we have recorded. Extrapolationf the recorded shoot biomass shows that amendment of soilith 350 ◦C biochar (at 60 t ha−1) can increase DW yield from
.95 t ha−1 (control) to 1.63 t ha−1. Total arsenic removal from soilan be determined by multiplying these biomass yields by thersenic concentration in the above-ground biomass. Using the dataecorded in our study, total arsenic removal from the control soil is0,900 mg ha−1, but this increases to 24,900 mg ha−1 for the 350 ◦Ciochar amended soil (60 t ha−1). Our calculations show that this
ncrease would lead to a 56% reduction in the timeframe needed toemediate soil to a defined target.
Despite the figures presented in the above paragraph, we do notropose that the phytoextraction of arsenic could be realistically
Please cite this article in press as: Gregory, S.J., et al., Response of
contaminated soil. Agric. Ecosyst. Environ. (2014), http://dx.doi.org/1
chieved using ryegrass; this is neither a hyperaccumulator nor aigh biomass species. We have used ryegrass in this work as a modellant species to better understand plant-soil dynamics in a biocharmended soil. Biochar would, however, lead to real increases in the
PRESSnd Environment xxx (2014) xxx–xxx
efficiency of phytoextraction where the same biochar-promotedbiomass and arsenic concentration effects were apparent in knownhyperaccumulator or high-biomass species. We propose that thecosts of biochar would not preclude the usefulness of the describedscenario. Arsenic (at high concentrations) at dip sites usually occu-pies an area of about 2500 m2. Assuming a cost for the preparationand incorporation of biochar to soil of $400/t (Jones, 2013) then theadditional cost of using biochar at a rate of 30 t ha−1 as part of aremediation option would be approximately $3000 per site.
Nonetheless, the extent to which the same effect as thatobserved here can be achieved by adding lime and fertilisers insteadof biochar needs to be investigated. To fully understand biocharamendment effects, the use of controls that mimic biochar (i.e. soilamended with a liming agent with the same liming equivalenceas biochar) should be investigated to determine biochars’ uniqueproperties (Jeffery et al., 2013). If the biomass and arsenic concen-tration can be similarly manipulated without the use of biochar,then this may be a more feasible route to enhance phytoextrac-tion efficiency. The extent to which the effects we have observedare attributable to biochar is an area that needs further validation.Moreover, it is yet to be seen what effect these type of biocharswill have on arsenic mobility and phytoextraction under field con-ditions when using high biomass crops like willow (Salix sp.).
The design and utilisation of a remedial plan for arsenic usinga biochar–phytoextraction system is aimed at being carbon nega-tive and creating zero waste. Under this scenario, plant biomass isharvested and chipped on site. The chipped contaminated biomassis then transported to an on-site pyrolyer that contains a filter sys-tem to capture volatilised arsenic, with the clean biochar returnedto the soil (Gregory, 2013). This would create a closed loop systemwhere carbon is being stored in the soil while providing a meansfor the sustainable remediation of the contaminated site and wouldprovide an end-use for the arsenic-contaminated plant material.
5. Conclusion
We have shown that in a highly arsenic-contaminated soil,microbial activity, soil–arsenic dynamics, and plant growth can beboth manipulated with the additions of biochar. Using an indicatorplant species, Lolium perenne L., significant changes in soil–arsenicdynamics in relation to the bioavailability of arsenic for phytoex-traction were observed. Extrapolation of our data infers that soilsamended with 350 ◦C biochar (60 t ha−1) have the potential to yieldincreased ryegrass sward DW growth by 0.68 t ha−1 compared toryegrass grown on unamended soils. This represents an increaseof 14,000 mg ha−1 of arsenic being extracted compared to una-mended soils. Biochar amended soils also evidenced noticeablyincreased soil microbial activity. Increases in both plant growth andsoil microbial activity may be due to the inherent fertility of biochar(K+, Ca2+, Mg2+) and to the labile C fraction of biochar that can beused as a microbial food source. More research is needed to developgreater mechanistic understanding of the soil–plant processes thatare associated with the amendment of soil with biochar, as well asto investigate whether the use of alternative soil amendments (e.g.,lime, fertilisers, organic wastes) would lead to similar results.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, inthe online version, at http://dx.doi.org/10.1016/j.agee.2014.03.035.
plant and soil microbes to biochar amendment of an arsenic-0.1016/j.agee.2014.03.035
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