Plant phosphorus availability index in rehabilitated bauxite-processing residue sand

REGULAR ARTICLE

Plant phosphorus availability index in rehabilitatedbauxite-processing residue sand

J. B. Goloran & C. R. Chen & I. R. Phillips &

Z. H. Xu & L. M. Condron

Received: 25 June 2013 /Accepted: 2 September 2013 /Published online: 22 September 2013# Springer Science+Business Media Dordrecht 2013

AbstractBackground and aims Soil phosphorus (P) indices thathave been originally developed and applied to agricul-tural soils for predicting P uptake by plants were exam-ined in a pot experiment to determine the most suitableindex for P availability in bauxite-processing residuesand (BRS).Methods Pot trials with ryegrass were established usingBRS that had been amended with various organic(greenwaste compost, biochar and biosolids) and inor-ganic (zeolite) materials and different levels of di-ammonium phosphate fertiliser. Soil P availability indi-ces tested included anion-exchange membrane (AEM-

P), 0.01 M calcium chloride (CaCl2-P), Colwell-P, andMehlich 3-P.Results AEM-P was found to most closely reflect theavailable P status in BRS across all treatments, and hadthe strongest associations with plant P uptake com-pared to Colwell-P, Mehlich 3-P and CaCl2-P. AEM-P was more closely correlated with P uptake by rye-grass than other P indices, while Colwell-P was closelyrelated to leaf dry matter. Interestingly, a strong inverserelationship between plant indices and pH in BRSgrowth media was observed, and an adequate level ofplant P uptake was found only in 15 year-old rehabil-itated BRS with pH <8.0.Conclusions AEM-P was found to be the most suitableindex for evaluating P availability in highly alkaline BRSand pH was an important parameter affecting uptake of Pby ryegrass. Importantly, time is required (> 5 years)before improved uptake of P by plants can be observedin rehabilitated residue sand embankments.

Keywords Bauxite-processing residuesand . Phosphorus availability index .Anion-exchangemembrane P. Colwell-P. Rehabilitation

Introduction

Establishing a sustainable vegetation cover across the outerembankments is part of Alcoa of Australia’s (Alcoa) com-mitment to progressive closure of its residue storage areas(RSAs). In Alcoa’s Western Australia operations, the outerperimeter embankments of the RSA are constructed using

Plant Soil (2014) 374:565–578DOI 10.1007/s11104-013-1900-0

Responsible Editor: Tim Simon George.

J. B. Goloran : C. R. Chen (*)Environmental Futures Centre, Griffith School ofEnvironment, Griffith University,Nathan, Qld 4111, Australiae-mail: c.chen@griffith.edu.au

I. R. PhillipsEnvironmental Research Department, Alcoa World AluminaAustralia,Huntly Mine, P.O. Box 172, Pinjarra, WA 6208, Australia

Z. H. XuEnvironmental Futures Centre, School of Bio-molecular andPhysical Sciences, Griffith University,Nathan, Qld 4111, Australia

L. M. CondronAgriculture and Life Sciences, Lincoln University,PO Box 84Lincoln 7647 Christchurch, New Zealand

bauxite processing residue sand (BRS, > 150 μm sizefraction of the bulk residue), which are subsequently veg-etated using a range of plant species native to south-westWestern Australia. The successful establishment and longterm sustainability of this vegetation will partly depend onthe BRS-water-nutrient dynamics. To date, water move-ment in rehabilitated BRS has been studied in detail (e.g.Gwenzi et al. 2011); however, the behaviour of nutrientsand their availability for plant growth has received muchless attention (Gherardi and Rengel 2003; Thiyagarajanet al. 2009; Phillips and Chen 2010; Jones et al. 2010;Jones and Haynes 2011).

Low levels of extractable P (<3 mg kg−1) have beenreported as one of the key limiting factors in establishinga sustainable plant cover system in BRS. Thus, thetiming and rate of application of appropriate fertilizersare critical for maintaining long-term vegetation coversfor RSAs. Currently, Alcoa applies about 2.7 t ha−1 ofdiammonium phosphate-based fertilizer (DAP), whichsupplies about 300 kg P ha−1. This high rate of P wasselected due to the high P retention properties of BRS(Bendfeldt et al. 2001; Courtney and Harrington 2010;Phillips and Chen 2010). Despite this high P rate, defi-ciencies of available P in vegetated bauxite residue(Courtney et al. 2009) and in above-ground biomass ofthe plant cover (Courtney and Timpson 2005; Easthamet al. 2006) have been reported.

A number of soil extraction methods have beenwidely used for evaluating soil P. These include theextractions of P by 0.01 M calcium chloride (CaCl2-P), Mehlich 3-P, Colwell-P and anion exchange mem-brane (AEM-P) methods. The use of 0.01 M CaCl2 hasbeen proposed as a multi-nutrient soil extractant, andwas developed to mimic the ionic strength of naturally-occurring soil solutions as a means to extract mostavailable P (Houba et al. 1990; Jones 1998). Mehlich3-P was developed for routine testing of P and is appli-cable to soils of varying pH (Mehlich 1984). This is anacidic extractant that can solubilize various P forms (e.g.Ca-P, Al-P and Fe-P) in soils and employs F− ion as acomplexer for Al and to inhibit readsorption of P by Feoxides (Jones 1998). Colwell-P test was also proposedfor a wide range of soils (Colwell 1963; Bolland et al.2003). This is a HCO3

− -based extraction reagent thatcan solubilize Ca-P due to precipitation of Ca2+ ascalcium carbonate (CaCO3), and thus, it tends to bemore applicable to alkaline soils where Ca-P is the mostabundant P form (Jones 1998). The AEM-P was pro-posed to be suitable in assessing P status of soils in

various conditions (Saunders 1964; Schoenau andHuang 1991). This test was developed to simulate theaction of plant roots in the uptake of phosphate ions as itmainly adsorbs P from soils that move into the soilsolution (Schoenau and Huang 1991; Nuernberg et al.1998; Raij et al. 2009). Despite the use of these methodsfor understanding P availability in natural soils, littleinformation is currently available on their performancein highly-alkaline bauxite residue.

Improved physical, chemical and microbial propertiesof BRS as a plant growth medium can result from theaddition of organic and inorganic amendments (Joneset al. 2011; Courtney and Harrington 2010; Courtneyand Kirwan 2012). Previous growth studies using Acaciasaligna suggested that inorganic (e.g. unaltered or car-bonated residue mud) and organic amendments (e.g.poultry manure, greenwaste compost) had no significanteffect on foliar P concentrations (Jones et al. 2012; An-derson et al. 2011). Courtney and Harrington (2010)found that Colwell-P was a better method than Olsen-P,Morgan-P and CaCl2-P for extracting P from residue.However, this study was undertaken using the fine frac-tion of residue (e.g. residue mud) and currently the per-formance of these methods has not been evaluated forresidue sand. Furthermore, while extensive literature hasbeen published on the use of these methods for obtaininga P availability index for natural soils, little is knownwhether these methods are suitable for amended minewastes such as BRS. For example, nutrient extractiontechniques that use a buffered solution may over- orunder- estimate availability particularly for those nutrientsthat are pH-sensitive (e.g. N, P and trace elements). Theobjective of this study was to evaluate which of theseextraction methods is the best index of P availability inBRS by linking the concentrations of extractable P toplant P uptake using a pot experiment.

Materials and methods

Pot trial

Bauxite-processing residue sand was sourced fromAlcoa’s Kwinana Refinery in south-west Western Aus-tralia (latitude 32o11′ 54.22″ South and longitude 115o49′31.93″ East). Samples were collected from freshly depos-ited (unweathered and untreated) stockpiles, and fromrehabilitated embankments ranging in age from 5, 7 and15 years old. Samples were air-dried, and the <2 mm size

566 Plant Soil (2014) 374:565–578

fraction retained for pot experiments. To simulate Alcoa’scurrent protocol for remediating BRS, phosphogypsum(< 1 mm) was added to freshly deposited BRS at a rate of1 % w/w, rewetted to 60 % water holding capacity andincubated for 2 weeks. After incubation, fresh BRSamended with phosphogypsum was leached with theequivalent of the average annual rainfall at KwinanaRSAs (758 mm). Phosphogypsum was not added tothose samples from rehabilitated embankments as thesehad already received gypsum as part of the rehabilitationprescription.

Fresh BRS amended with phosphogypsum wasmixed with a range of organic and inorganic amend-ments at a rate of 10 %v/v; these included greenwastecomposts (GC), biochar (BC) (i.e. produced from ag-ricultural feedstock with a heat range of 550 0C),zeolite (ZL), and biosolids (BS). All amendment ma-terials were obtained from commercial suppliers ex-cept for biosolids which were collected from the OxleyCreek Wastewater Treatment Plant in Brisbane. Theseamendments were air-dried and sieved (2 mm) beforebeing added to BRS. The combination of amendmentsand BRS produced a total of 5 different BRS growthmedia such as BRS without amendment (BRSNA),BRS with Greenwaste compost (BRSGC), BRS withBiochar (BRSBC), BRS with Zeolite (BRSZL) andBRS with Biosolids (BRSBS). BRS from the olderrehabilitated areas were also included as growth mediain this study; specifically being 5 Year Rehab BRS(5YRRH BRS), 7 Year Rehab BRS (7YRRH BRS)and 15 Year Rehab BRS (15YRRH BRS). All BRStreatments were air-dried prior to the addition of fertil-izer solution (NH4NO3 plus Ca (H2PO4)2). This was toallow adjustment of BRS water-holding capacity to60 % even after the addition of fertilizer solution. Thefertilizer solution was added at a rate of 0, 83.38,125.07, 166.76 and 208.46 mg pot−1, which was equiv-alent on a surface area basis to 0, 1.0, 1.5, 2.0 and2.5 t ha−1 DAP, respectively. This experimental designresulted in eight (8) types of BRS growth media, one(1) grass species, five (5) N fertilizer levels with three(3) replicates (n=120) was set up in a completelyrandomized design.

BRS growing media was placed in plastic pots madefrom 250 mL containers (SARSTEDT Australia PtyLtd), and covered with aluminium foil to exclude lightreaching the plant roots throughout the growing period.The total mass of BRS growing media ranged from 248to 285 g pot−1, as it varied due to added organic/inorganic

amendments. Wimmera ryegrass (Lolium rigidum) wasplanted due to its ability to grow in highly alkaline soil,and because this is the primary grass species planted atAlcoa’s RSAs. Each pot was planted with 25 pre-germinated ryegrass seeds, grown in a controlled-environment room with a daily temperature of 22 to25 °C. Plants were grown at a light intensity of ca.115 W m−2 provided by Sylvania Grolux T8 36 Wfluorescent tubes. Plants were harvested after a 3 monthgrowing period. The above-ground material was cut atthe BRS surface and were dried at 60 °C and weighed formeasurement of leaf dry matter. A subsample of plantmaterials was taken for chemical analysis. BRS sampleswere mixed well, air dried, ground and sieved (2 mm).Both plants and BRS samples were finely ground with amill prior to chemical analysis for plant available P andtotal P.

Soil analyses

Soil pH and electrical conductivity (EC) were measuredin 1:5 water extract. Total N and P were extracted byKjeldahl digestion method and the digests were thenanalyzed for total N using SmartChem®200 DiscreteAnalyzer (WESTCO Scientific Instruments Inc.) andtotal P according to the Murphy–Riley method (1962).Total C was determined by isotope ratio mass spectrom-eter with a Eurovector Elemental Analyser (Isoprime-EuroEA 3000). Exchangeable bases such as Ca2+,Mg2+, Na+ and K+ were extracted by 0.01 M SrCl2and the extracts were analyzed by ICP-OES: VarianVista Pro Spectrophotometer (Woods 2006). The Effec-tive Cation Exchange Capacity (ECEC) and Exchange-able Sodium Percentage (ESP) were calculated directlybased on the concentrations of exchangeable cations(Abbott 1985; Hazelton and Murphy 2007).

Concentrations of inorganic P in the extracted solu-tion were analyzed according to the Murphy–Rileymethod (1962). Soil P indices used to evaluate P avail-ability in BRS are outlined as follow:

CaCl2-P: soil/solution ratio of 1:10; 0.01 MCaCl2; 2 h in an end-to-end shaker (Houba et al.1990).Colwell-P: soil/solution ratio of 1:100; 0.5 MNaHCO3 at pH 8.5; and an extraction time of16 h in an end-to-end shaker (Colwell 1963).Mehlich 3-P: soil/solution ratio of 1:10; 0.2 NCH3COOH+0.25 N NH4NO3+0.013 N HNO3+

Plant Soil (2014) 374:565–578 567

0.015 N NH4F+0.001 M EDTA at pH 2; and anextraction time of 5 min in an end-to-end shaker(Mehlich 1984).AEM-P: AEM (BDH no. 551642) sheet was cutinto strips (2.08 × 4.15 cm). These were convertedfrom Cl-form to HCO3-form by placing them in a500 ml glass bottle containing 250 ml 0.5 MNaHCO3 at pH 8.5; and shaking them using anend-to-end shaker for 30 min at room temperature(Kouno et al. 1995; Myers et al. 1999). P extrac-tion was done by placing 2 AEM strips (HCO3-form) into 50 ml Falcon tubes (Sarstedt) per 1.0 gsoil. These were then added with 30 ml of distilledwater and (tubes) placed in the shaker for 16 h.After shaking, the AEM strips were removed fromthe tube and rinsed with a stream of distilled waterfor a few seconds. The AEM strips (which haveabsorbed the P) were then placed into a wide-mouthed container (30 ml Sarstedt), with 30 mlof 0.5 M HCl added and placed in the shaker for1 h. After shaking, the AEM strips were removed,and the 30 ml container served as the final storagecontainer for the extract. Inorganic P in the eluentswas analysed immediately.

Plant analyses

The oven-dried plant samples were finely ground (<150 μm). Ground leaf samples were digested as per theTotal Kjeldahl Phosphorus method. Total P was deter-mined according to the Murphy–Riley method (1962).

Statistical analyses

A Pearson correlation analysis was carried out usingSTATISTIX 8.0. Only 7 types of BRS growth mediawere considered because no plants had survived inBRSBS growth media due to the inhibitory effect ofbiosolids (i.e. rich NH4

+ substrate). A total of 105 sam-ples (7 BRS types × 5 DAP fertilizer rates × 3 replicates)were analyzed.

Results

Selected chemical properties of the various amend-ments are presented in Table 1. Biochar, zeolite, andbiosolids materials were alkaline with pH values of

9.49, 8.05 and 7.32, respectively, while the greenwastecompost was acidic (pH 4.04). Biochar had the highestEC values (11.09 dS m−1) followed by biosolids(7.51 dS m−1), while the EC for both greenwaste com-post and zeolite was <2.0 dS m−1. All organic amend-ments generally contained P that could potentiallyimprove the fertility of BRS.

The pH, EC, exchangeable cations, ECEC and ESPwere significantly higher for organic–inorganicamended BRS than in the older rehabilitated BRS(Table 2). Concentrations of extractable P varied sig-nificantly (p<0.01) between growth media treatmentsand P extractant methods. For example, P extractedfrom BRSBS and BRSBC (organically amendedBRS) were generally higher compared to other growthmedia treatments (e.g. BRSNA, BRSZL, 5YRRH,7YRRH and 15YRRH), and P concentrations extractedby Mehlich 3-P and Colwell-P were consistentlyhigher than AEM-P and CaCl2-P. The P determinedby CaCl2-P was not presented in Tables 3 and 4 due tovery low concentrations (< 1 mg kg−1).

Both Mehlich 3-P and Colwell-P extracted thehighest concentrations of plant available P from allBRS treatments (Tables 3 and 4), with Mehlich 3-Pconcentrations being 2–3 times higher than those forColwell-P. With the exception of CaCl2-P, all P avail-ability indices used in this study displayed a signifi-cantly positive correlation with rate of applied P (DAPfertilizer) (Fig. 1). Colwell-P revealed the most signif-icant correlation with applied P compared to Mehlich3-P and AEM-P in BRSNA (r=0.98, p<0.01), BRSGC(r=0.89, p<0.01), BRSBC (r=0.95, p<0.01), BRSZL(r=0.97, p<0.01), 5YRRH (r=0.98, p<0.01), 7YRRH(r=0.94, p<0.01) and 15YRRH (r=0.97, p<0.01). In-terestingly, AEM-P closely followed Colwell-P andhad shown the same correlation coefficients in twogrowth media such as 7YRRH (r=0.94, p<0.01) and15YRRH (r=0.97, p<0.01). In addition, Colwell-P re-vealed significant correlations with total P in all BRSgrowth media compared to Mehlich 3-P and AEM-P inBRSNA (r=95, p<0.01), BRSGC (r=0.94, p<0.01),BRSZL (r=96, p<0.01), 5YRRH (r=96, p<0.01),7YRRH (r=0.83, p<0.01) and 15YRRH (r=0.92,p<0.01) (Fig. 2). However, AEM-P only revealedhigher association with total P in BRSBC (r=0.95,p<0.01).

Phosphorus concentrations in leaves, P uptake andleaf dry matter of ryegrass grown in the various BRSmedia are shown in Tables 3 and 4. The correlation

568 Plant Soil (2014) 374:565–578

coefficients of P uptake by ryegrass and leaf dry matterwith P availability indices are shown in Table 5. Stron-ger correlations for Colwell-P and AEM-P with Puptake and leaf dry matter were observed in all BRSgrowth media. For example, the correlation coeffi-cients between AEM-P and P uptake were found tobe higher than between Colwell-P and P uptake in fivegrowth media such as BRSNA (r=0.82, p<0.01),BRSBC (r=0.74, p<0.01), BRSZL (r=0.91, p<0.01),7YRRH (r=0.93, p<0.01) and 15YRRH (r=0.88,p<0.01). Colwell-P showed better associations with P

uptake in other growth media such as BRSGC (r=0.92,p<0.01) and 5YRRH(r=0.87, p<0.01). Moreover,Colwell-P revealed higher correlations than AEM-Pwith ryegrass leaf dry matter in BRSNA (r=0.93,p<0.01), BRSZL (r=0.87, p<0.01), 5YRRH (r=0.93,p<0.01) and 15YRRH (r=0.89, p<0.01). Conversely,AEM-P had shown better relationships than Colwell-Pwith leaf dry matter in BRSGC (r=0.73, p<0.01),BRSBC (r=0.86, p<0.01) and 7YRRH (r=0.86,p<0.01). Although, Mehlich 3-P had shown significantand positive relationships with P uptake by ryegrass

Table 1 Means of chemical properties of organic and inorganic amendments used in the pot experiment (n=3)

Parameters pH(1:5)

EC(dSm−1)

NH4+-N

(mg kg−1)NO3

−-N(mg kg−1)

TC(%)

TN(g kg−1)

TP(g kg−1)

ExtractableColwell-P (g kg−1)

Exchangeable cations(cmol kg−1)

Ca Mg K Na

GreenwasteCompost

4.04 1.21 52.2 1.45 37.0 1.73 4.25 0.36 4.6 2.0 0.9 0.76

Biochar 9.49 11.09 18.37 10.5 36.0 36.0 21.2 9.4 0.77 7.42 44.5 17.1

Zeolite 8.05 0.04 2.74 ND 0.05 0.028 0.43 0.09 1.89 1.31 0.02 0.92

Biosolids 7.32 7.51 46875 1.66 30.0 64.0 45.0 10.0 2.21 8.47 4.4 2.23

TC total carbon, TN total nitrogen, TP total phosphorus

Table 2 Means of chemical properties of bauxite residue sand growth media measured before the pot experiment (n=3)

Chemical properties BRSNA BRSGC BRSBC BRSZL BRSBS 5YRRH 7YRRH 15YRRH

Total P (mg kg−1) 83c 90c 518b 112c 7223a 108c 104c 550b

AEM-P (mg kg−1) 1.27d 1.11d 23.8c 0.56d 198a 3.71d 0.90d 42.4b

CaCl2-P (mg kg−1) 0.07b 0.32b 0.37b 0.23b 6.21a 0.23b 0.24b 0.54b

Colwell-P (mg kg−1) 2.05c 21.8b 140b 28.7b 1581a 20.0b 25.3b 136b

Mehlich 3-P (mg kg−1) 3.26e 38.85d 290b 34.03d 3270a 50.78d 49.8d 210c

Total C (%) 0.16g 0.72c 1.63b 0.13h 2.53a 0.22f 0.31e 0.61d

Total N (mg kg−1) 4.22d 40d 1165b 4.93d 4141a 24d 71d 596c

NH4+ -N (mg kg−1) ND 7.42c 1.85f 3.90d 470a 3.27e 3.92d 8.86b

NO3- -N (mg kg−1) ND 1.34d 1.01d 0.12e 52.8b 2.86d 18.6c 194a

Ca (cmol kg−1) 2.54e 4.0a 2.62d 3.40b 3.10c 0.74h 1.20g 1.39f

Mg (cmol kg−1) 0.03g 0.16e 0.58b 0.24d 1.06a 0.02h 0.06f 0.30c

K (cmol kg−1) 0.04e 0.04e 2.02a 0.26c 0.37b 0.02f 0.05d 0.05d

Na (cmol kg−1) 6.00a 0.40f 1.82c 4.58b 1.46d 0.11h 0.17g 1.04e

ECEC (cmol kg−1) 8.61a 4.50e 7.05c 8.23b 5.97d 1.00h 1.48g 1.84f

ESP (%) 69.6a 8.52de 25.90c 55.57b 24.41c 13.18d 11.47d 5.65e

pHw (1:5) 9.55b 9.05d 9.85a 9.37c 8.95e 8.19g 8.78f 7.98h

EC (dS m−1) 0.46d 0.47c 0.87b 0.44e 1.15a 0.22g 0.33f 0.18h

Means in a row followed by the same letter are not significantly different from one another at 5 % level of significance

GC greenwaste compost, BC biochar, ZL zeolite, BS biosolid. 5, 7, 15YRRH, age of rehabilitated BRS, ND not detectable, ESPexchangeable sodium percentage, ECEC effective exchange cation capacity, BRS bauxite residue sand, AEM anion-exchange membrane

Plant Soil (2014) 374:565–578 569

Table 3 Ryegrass leaf dry matter, phosphorus (P) uptake, and P indexes in organic–inorganic amended BRS (n=15)

Parameters Min Max Mean SE

BRS without amendmentb

Leaf dry matter (g pot−1) 4.48 5.56 5.17 0.09

Leaf P content (g pot−1) 0.37 0.94 0.57 0.48

P uptake (g pot−1) 0.18 0.52 0.29 0.03

P availability indexesa

Total P 80.6 241 167 14.0

AEM 0.79 14.0 7.0 1.2

Colwell 1.71 40.42 21.5 3.40

Mehlich 3 0.61 98.6 42.8 7.45

BRS with Greenwaste compost

Leaf dry matter (g pot−1) 5.97 7.22 6.82 0.11

Leaf P content (g pot−1) 0.39 2.21 0.97 0.49

P uptake (g pot−1) 0.23 1.57 0.67 0.93

P availability indexes

Total P 78.2 340 200 19.9

AEM 0.01 17.6 8.05 1.41

Colwell 0.50 44.2 22.5 3.29

Mehlich 3 8.05 59.5 31.4 4.50

BRS with Biochar

Leaf dry matter (g pot−1) 5.51 6.69 6.32 0.10

Leaf P content (g pot−1) 0.22 1.81 0.97 0.97

P uptake (g pot−1) 0.12 1.19 0.62 0.67

P availability indexes

Total P 466 778 655 24.5

AEM 22.3 72.9 46.8 4.22

Colwell 72.9 157 117 7.21

Mehlich 3 92.8 290 158 15.6

BRS with Zeolite

Leaf dry matter (g pot−1) 5.58 8.95 7.85 0.32

Leaf P content (g pot−1) 0.50 1.45 0.93 0.84

P uptake (g pot−1) 0.28 1.26 0.75 0.08

P availability indexes

Total P 109 300 200 16.7

AEM 0.09 17.2 8.08 1.56

Colwell 0.65 44.6 21.8 3.60

Mehlich 3 1.43 89.1 32.0 6.16

BRS with Biosolids

Leaf dry matter (g pot−1) nps nps nps nps

P availability indexes 820 1121 991 13.6

Total P 190 364 242 8.80

AEM 215 326 257 5.12

Colwell 696 1026 894 16.57

BRS bauxite residue sand, AEM anion exchange membrane, SE standard error of the mean, nps no plants surviveda Results for CaCl2 P extractant were not presented due to very low concentrations (< 1 mg kg−1 )b All units of concentration are expressed in milligram per kilogram (mg kg−1 ) unless otherwise indicated

570 Plant Soil (2014) 374:565–578

and leaf dry matter, it did not outperform the correla-tion coefficients obtained by AEM-P, and Colwell-P.

Discussion

Significant improvements in chemical properties oforganic amended BRS and older rehabilitated BRSwere observed compared to BRS without amendments(control). Extractable P was greatly increased with theaddition of organic amendments, and extractable P inolder rehabilitated BRS was within the range previous-ly reported by Jones et al. (2012) and Banning et al.

(2011). The growth media with different amendmentsand different application rates of DAP provided a gra-dient of P in BRS for testing P availability indexes inrelation to Plant growth and uptake.

Comparisons of different soil P availability indexes

The amounts of P measured by P indices used in thisstudy varied significantly due to differences in pH ofthe extractant and influence of other mechanisms (i.e.ionic competitions and dissolutions of P compounds)that are involved during extractions of available P fromBRS. The amounts of P extracted by CaCl2-P were

Table 4 Ryegrass leaf dry matter, phosphorus (P) uptake, and P indexes in older rehabilitated BRS (n=15)

Parameters Min Max Mean SE

5 Year Old Rehab BRSb

Leaf dry matter (g pot−1) 5.27 7.80 6.87 0.24

Leaf P content (g pot−1) 0.61 2.33 1.20 0.13

P uptake (g pot−1) 0.32 1.77 0.83 0.10

P availability indexesa

Total P 104 308 219 17.2

AEM 3.18 30.9 15.9 2.96

Colwell 3.72 40.4 21.0 3.09

Mehlich 3 9.67 82.7 54.8 7.06

7 Year Old Rehab BRS

Leaf dry matter (g pot−1) 6.69 8.37 7.80 0.15

Leaf P content (g pot−1) 0.69 3.13 1.65 0.19

P uptake (g pot−1) 0.46 2.61 1.32 0.17

P availability indexes

Total P 73.1 300 188 17.5

AEM 0.50 45.6 21.4 3.85

Colwell 2.99 50.0 26.1 4.02

Mehlich 3 9.29 78.5 41.7 6.64

15 Year Old Rehab BRS

Leaf dry matter (g pot−1) 7.44 8.96 8.42 0.14

Leaf P content (g pot−1) 1.43 3.45 2.50 0.15

P uptake (g pot−1) 1.07 4.55 2.41 0.26

P availability indexes

Total P 529 679 611 12.4

AEM 38.0 82.0 62.0 3.61

Colwell 49.3 160 104 9.41

Mehlich 3 203 315 251 9.56

BRS bauxite residue sand, AEM anion exchange membrane, SE standard error of the mean, nps no plants surviveda Results for CaCl2 P extractant were not presented due to very low concentrations (< 1 mg kg−1 )b All units of concentration are expressed in milligram per kilogram (mg kg−1 ) unless otherwise indicated

Plant Soil (2014) 374:565–578 571

(a)

-0.5 0.0 0.5 1.0 1.5 2.0 2.5 3.0

Ext

ract

able

P in

BR

S (

mg

kg-1

)0

20

40

60

80

100

120

140

160

AEM, r = 0.94**CaCl2, r =0.43ns

Colwell, r = 0.98**Mehlich 3, r = 0.79**

(b)

0.0 0.5 1.0 1.5 2.0 2.5 3.0

Ext

ract

able

P in

BR

S (

mg

kg-1

)

0

20

40

60

80

100

120

AEM, r = 0.77**CaCl2, r = 0.25ns

Colwell, r =0.89**Mehlich 3, r = 0.69**

(c)

0.0 0.5 1.0 1.5 2.0 2.5 3.0

Ext

ract

able

P in

BR

S (

mg

kg-1

)

0

100

200

300

400

AEM, r = 0.93**CaCl2, r = 0.74**

Colwell, r = 0.95*Mehlich 3, r = 0.84**

(d)

Applied P fertilizer (t ha-1)

0.0 0.5 1.0 1.5 2.0 2.5 3.0

Ext

ract

able

P in

BR

S (

mg

kg-1

)

0

20

40

60

80

100

120

140

AEM, r = 0.96**CaCl2, r = 0.32ns

Colwell, r = 0.97**Mehlich 3, r = 0.82**

(e)

0.0 0.5 1.0 1.5 2.0 2.5 3.0

0

20

40

60

80

100

120

140 AEM, r = 0.94**CaCl2, r = 0.43nsColwell, r = 0.98**Mehlich 3, r = 0.72**

(f)

0.0 0.5 1.0 1.5 2.0 2.5 3.0

0

20

40

60

80

100

120

140

AEM, r = 0.94**CaCl2, r = 0.71**

Colwell, r = 0.94**Mehlich 3, r = 0.90**

(g)

Applied P fertilizer (t ha-1)

0.0 0.5 1.0 1.5 2.0 2.5 3.00

100

200

300

400

500 AEM, r = 0.97**CaCl2, r = 0.71**

Colwell, r = 0.97**Mehlich 3, r = 0.77**

Fig. 1 Relationships betweenapplied P fertilizer and P avail-ability indices in (a) BRSNA,(b) BRSGC, (c) BRSBC, (d)BRSZL, (e) 5YRRH, (f)7YRRH, and (g) 15YRRHgrowth media (n=15)

572 Plant Soil (2014) 374:565–578

(a)

80 100 120 140 160 180 200 220 240 260E

xtra

ctab

le P

in B

RS

(m

g kg

-1)

0

20

40

60

80

100 AEM, r = 0.87**CaCl2, r = 0.45ns

Colwell, r = 0.95**Mehlich 3, r = 0.79**

(b)

100 150 200 250 300 350

Ext

ract

able

P in

BR

S (

mg

kg-1

)

0

20

40

60

80

100

120

AEM, r = 0.86**CaCl2, r = 0.06ns

Colwell, r = 0.94**Mehlich, r = 0.59*

(c)

450 500 550 600 650 700 750 800

Ext

ract

able

P in

BR

S (

mg

kg-1

)

0

100

200

300

400

AEM, r = 0.95**CaCl2, r =0.70**

Colwell, r = 0.94**Mehlich 3, r = 0.81**

(d)

Total P in BRS (mg kg-1)100 150 200 250

Ext

ract

able

P in

BR

S (

mg

kg-1

)

0

20

40

60

80

AEM, r = 0.95**CaCl2, r = 0.51*

Colwell, r = 0.96**Mehlich 3, r = 0.87**

(e)

100 150 200 250 300

0

20

40

60

80

100

120

140AEM, r = 0.95**CaCl2, r = 0.51*

Colwell, r = 0.96**Mehlich 3, r = 0.75**

(f)

100 150 200 250

0

20

40

60

80

100

120

AEM, r = 0.82**CaCl2, r = 0.63**

Colwell, r = 0.83**Mehlich 3, r = 0.81**

(g)

Total P in BRS (mg kg-1)540 560 580 600 620 640 660 680

0

100

200

300

400

500

AEM, r = 0.79**CaCl2, r = 0.56*Colwell, r = 0.82**Mehlich 3, r = 0.54*

Fig. 2 Relationship betweentotal P and various P avail-ability indices in (a) BRSNA,(b) BRSGC, (c) BRSBC, (d)BRSZL, (e) 5YRRH, (f)7YRRH, and (g) 15YRRHgrowth media (n=15)

Plant Soil (2014) 374:565–578 573

very low (data not presented), which could be attribut-ed to the weaker effect of Cl− ions in displacing phos-phate ions and destabilizing P compounds such as Al-P, Ca-P and Fe-P (Hylander et al. 1995; Hartikainenand Yli-Halla 1982). Similar results (low CaCl2extractable-P) have been found in previous studies onvarious agricultural soils (Bibiso et al. 2012; Kulháneket al. 2009) and in alkaline bauxite residue fine frac-tions (Courtney and Harrington 2010). Mehlich 3-Pbeing an acidic extractant (pH 2) was consistentlyfound to extract more plant available P than Colwell-P, AEM-P and CaCl2-P across all BRS growth media(Fig. 1). The strong acidity of the Mehlich 3-P reagentcan facilitate rapid dissolution of mobile and non-mobile P during extractions (Bolland et al. 2003) evenat a very short shaking/extracting time (e.g. 5 min)

resulting in an overestimation of available P. This isconsistent with previous reports in the use of acidicextractants (e.g. 0.005 M H2SO4, and Morgan extract-able P) for extracting available P in bauxite residue(e.g. Al-P and Fe-P) (Courtney and Harrington 2010;Meecham and Bell 1977; Wong and Ho 1995), thus, itssuitability to alkaline BRS is problematic.

The amounts of P extracted by Colwell-P were 2 to3 times higher than that by AEM-P. There are twopossible reasons for higher amounts of P extracted byColwell-P method. First, the longer period of extrac-tion (16 h shaking time) weakens P buffering capacity,hence extracting more available P (Courtney and Har-rington 2010; Barrow and Shaw 1976). Second, it mayhave dissolved P-sesquioxide/allophone complexes inthe residue due to high soil-solution ratio of the

Table 5 Correlation coefficient (r) of ryegrass growth responses with soil P availability indices at different types of BRS growth media

Growth parameter P availability indicesa

AEM-P CaCl2-P Colwell-P Mehlich 3-P

BRSNA (n=15)

Leaf dry matter 0.85** 0.36ns 0.93** 0.76**

P uptake 0.82** 0.45 ns 0.80** 0.64*

BRSGC (n=15)

Leaf dry matter 0.73** 0.12ns 0.68** 0.61*

P uptake 0.71** 0.18 ns 0.92** 0.58*

BRSBC (n=15)

Leaf dry matter 0.86** 0.56* 0.85** 0.63**

P uptake 0.74** 0.57* 0.73** 0.66**

BRSZL (n=15)

Leaf dry matter 0.80** 0.37 ns 0.87** 0.70**

P uptake 0.91** 0.12 ns 0.90** 0.79**

5YRRH BRS (n=15)

Leaf dry matter 0.90** 0.47 ns 0.93** 0.79**

P uptake 0.85** 0.41 ns 0.87** 0.71**

7YRRH BRS (n=15)

Leaf dry matter 0.86** 0.62* 0.85** 0.80**

P uptake 0.93** 0.76** 0.90** 0.82**

15YRRH BRS (n=15)

Leaf dry matter 0.85** 0.56* 0.89** 0.71**

P uptake 0.88** 0.63* 0.88** 0.77**

a Correlation coefficients in bold text indicate the highest relationships with ryegrass leaf dry matter and leaf P uptake

*Significant at p≤0.05**Significant at p≤0.01ns non significant

574 Plant Soil (2014) 374:565–578

extractant (Courtney and Harrington 2010; Kirchhofet al. 2008). Barrow and Shaw (1976) also revealedthat bicarbonate extractant (Colwell-P) associated withlong period of shaking (16 h) can displace around 90 %of phosphate firmly held from soil by competitions ofhydroxide ions where it also restricts re-adsorption ofphosphate.

Phosphorus concentrations measured by theColwell-P method are all above the critical concentra-tions (< 20 mg kg−1) in moderate to high soil P sorptioncategories for dry land pasture (Baldock and Skjemstad1999). However, P concentrations in the leaves ofryegrass growing in the mentioned growth media wereP-deficient or below adequate levels for plant growth(Reuter and Robinson 1997), despite the significantamount of P added as DAP fertilizer. Similar observa-tions have been pointed out by Bertrand et al. (2003)for the alkaline soils (e.g. Calcarosols) from SouthAustralia, which have Colwell-P extractable values>18 mg kg−1. However, cereals growing in these alka-line soils were P-deficient, suggesting that Colwell-P

may have overestimated plant available P due to itsability to destabilise P-compounds (Courtney and Har-rington 2010; Kirchhof et al. 2008).

Colwell-P has previously been used to measureplant available P in rehabilitated RSAs (e.g. Anderson2009; Jones et al. 2010), and these studies have shownvarying levels of Colwell extractable P in BRS asinfluenced by amendments. For example, inunfertilized BRS extractable Colwell-P ranged from 5to 7 mg kg−1 (Anderson 2009), 8.5–10.5 mg kg−1 inBRS that received P fertilizer (Eastham et al. 2006),11.8 mg kg−1 in phosphogypsum amended BRS, and27–50 mg kg−1 in organic-compost amended BRS(Jones et al. 2010). In our study, extractable Colwell-P concentrations in all BRS growth media were highlyinfluenced by the addition of DAP fertilizer. For ex-ample, the minimum amounts (unfertilized or control)of extractable Colwell-P in unamended (BRSNA),organic/inorganic amended (BRSGC and BRSZL),and older rehabilitated BRS (5YRRH and 7YRRH),were <5 mg kg−1 (Tables 3 and 4). However, a

(a)

7 8 9 10 11

Leaf

P c

onte

nt (

g po

t-1)

0

1

2

3r = -0.86p < 0.001n = 105

(b)

pH

7 8 9 10 11

Leaf

dry

mat

ter

(g p

ot-1

)

4

5

6

7

8

9r = -0.77p < 0.001n = 105

(c)

0.0 0.2 0.4 0.6 0.8 1.0

Leaf

P c

onte

nt (

g po

t-1)

0.0

0.5

1.0

1.5

2.0

2.5

3.0

3.5

r = 0.06p = nsn = 105

(d)

EC0.0 0.2 0.4 0.6 0.8 1.0

Leaf

dry

mat

ter

(g p

ot-1)

4

5

6

7

8

9

r = -0.10p = nsn = 105

Fig. 3 Relationship of ryegrass leaf P content and leaf dry matter with pH and EC in all BRS growth media

Plant Soil (2014) 374:565–578 575

dramatic increase to 40–50 mg kg−1 (maximumamounts) was observed in these growth media afterDAP applications (Tables 3 and 4). This correspondsto significantly higher extractable Colwell-P in BRS(upper 0.1 m) applied with inorganic fertilizer(17.5 mg kg−1) compared with compost (4.5 mg kg−1),poultry manure (8.5 mg kg−1) and compost manure(10.5 mg kg−1) (Eastham et al. 2006). In addition,Colwell-P showed the highest correlation coefficientswith the total P in most growth media (Fig. 2). Thesesuggest that Colwell-P method may be efficient inextracting inorganic P added as fertilizer to BRS. How-ever, it may also extract non labile P due to its capacityto destabilise P-compounds (Courtney and Harrington2010), hence negatively influencing the correlation co-efficients with P uptake by ryegrass as discussed in thesucceeding sections of this report.

Unlike Colwell-P, AEM-P tended to only remove thesurface-adsorbed P (Bertrand et al. 2003), and act as asink for available P without causing dissolution of pre-cipitated P or residual P fertilizer (Nuernberg et al.1998). AEM-P also demonstrated a very strong positiverelationship between total applied P fertilizer and total Pin BRS across all growth media. Although the amountsof extracted P were 2–3 times lower than Colwell-P, itscorrelation coefficients across all BRS growth mediawere comparable with Colwell-P. In fact, in somegrowth media it revealed similarities of correlation co-efficients with Colwell-P. AEM-P has not been used forextracting available P in BRS prior to this study socomparing efficiency of AEM-P from the previous re-ports would not be possible. Previous studies usingAEM-P to extract plant available P from various highlyalkaline soils (e.g. Calcarosols, Vertosols, Alkaline du-plex soils, Sodosols and Red brown Calcarosols) fromSouthern Australia revealed better prediction perfor-mance of AEM-P compared with Colwell-P, Ca Lac-PandWater-P (Bolland et al. 2003). Although amounts ofP extracted by AEM-P were consistently lower thanColwell-P, it did correlate well with other P availabilityindices (Bolland et al. 2003). Guggenberger et al. (1996)reported significant relationship between anion ex-change resin (HCO3 - form) and NaHCO3 at pH 8.5extractant. Although it was extracting less inorganic Pthan the NaHCO3 (Chen et al. 2000), it had a betterresponse to fertilization (Rubaek and Sibbesen 1993).These previous findings correspond to the results of thisstudy, confirming the efficiency of AEM-P in assessingand predicting plant available P in BRS growth media.

Relationship between soil P indices and plant P uptakeand leaf dry matter

Colwell-P and AEM-P showed the highest correlationswith plant P uptake and leaf dry matter compared toMehlich 3-P and CaCl2-P methods. While Cowell-Ptended to be highly correlated to the leaf dry matter,AEM-P was better correlated to uptake of P by ryegrassin five (e.g. BRSNA, BRSBC, BRSZL, 7YRRH and 15YRRH) out of seven BRS growth media (Table 5). Thesignificant relationship between Colwell-P and plantbiomass was also observed by Courtney and Harrington(2010) in a field trial using bauxite residue fine fractions,however the correlation coefficients were much lower(0.47, p<0.05) than the values (r=0.68–0.93, p<0.01)observed in the present study. Further, Courtney andHarrington (2010) did not observe any correlation be-tween P in plant (Holcus lanatus) leaves and P avail-ability indices (e.g. Olsen-P, Colwell-P and Morgan-P),which could be attributed to the varying texture ofbauxite residue that affects plant P availability and plantuptake. It is possible that the lower P sorption by BRSrelative to residue mud (fine fraction) rendered more Pin a plant available form, thereby a higher P uptake. Onthe other hand, the greater association of AEM-P with Pcontent in ryegrass leaves may be due to mechanismsthat favour dissolution of weakly retained or labile P andits subsequent diffusion to the AEM strips. This processis similar to that of P extraction by plant roots (Schoenauand Huang 1991; Raij et al. 2009). This mechanismmayonly be extracting surface-adsorbed plant available P,which may explain why AEM-P consistently extractedlower amounts of P than Colwell-P (Bolland et al. 2003).Previous studies showed similarities of coefficient deter-minations between AEM-P and conventional P (e.g. so-dium bicarbonate P and water extractable P) tests, andhave an advantage over alkaline (Colwell-P) and acidic(Mehlich 3-P) extractants as it is largely independent ofsoil chemical properties (e.g. pH), hence applicable to awide range of soils (Raij et al. 2009; Schoenau andHuang 1991). This study has shown (1) the suitabilityof AEM-P as an indicator of plant available P, and that (2)more research on the interaction of sorbed P and plantroot extraction in the rhizosphere is warranted.

The positive correlation coefficient between soil Pavailability indexes (e.g. AEM-P, Colwell-P andMehlich 3-P) and plant P uptake showed that therewas a substantial amount of plant available P acrossall BRS growth media. The P contents in ryegrass

576 Plant Soil (2014) 374:565–578

leaves however, were below adequate levels requiredfor plant growth (Reuter and Robinson 1997). Thissuggests that uptake of P by ryegrass is still restricted,possibly by the alkalinity of BRS and other associatedmechanisms such as low solubility of Al-P and Ca-Pprecipitates (Phillips and Chen 2010), and P adsorptionby CaCO3 (Eastham and Morald 2006). Limited Puptake by ryegrass due to alkalinity of BRS is clearlyrevealed by a strong inverse relationship between pHand plant indices (Fig. 3). The P content in ryegrassleaves tended to decrease as the pH of growth mediaincreases. Among the BRS growth media, only the15YRRH had a pH of <8.0 (Table 2) and the meanfor leaf P content (2.5 g kg-1) of ryegrass leaves grow-ing under this growth medium was above adequatelevels required for plant growth as indicated by Peverillet al. (1999). This better uptake of P by ryegrass in15YRRH also implies that time is required (> 5 years)for improved P cycling in highly alkaline BRS. This isevident in the higher correlation coefficient (r=0.87–0.92, p≤0.01) found between AEM-P and ryegrass leafP content in older rehabilitated BRS (e.g. 7YRRH and15YRRH). Thus, a field study on assessing suitable Pindices and P cycling in RSAs with differing age ofrehabilitation may be warranted. Moreover, in this stud-y, EC has been found to have no influence on P uptakeand growth of ryegrass, which is attributable to lowerEC (< 1 dSm−1) of all growth media, and ryegrass beingknown to be salt tolerant up to 8 dS m−1 (Nizam 2011).

Conclusions

This study has demonstrated that the amounts of Pextracted from BRS varied among different extractantsused. Mehlich 3-P extracted higher amounts of availableP than AEM-P and Colwell-P. CaCl2 extracted the low-est amounts of P in all BRS growth media. Results forMehlich 3-P and CaCl2-P tests overestimated andunderestimated the amounts of P, respectively. AlthoughAEM-P and Colwell-P displayed the strongest relation-ships with the rate of applied P fertilizer and total P inBRS, the AEM-P is likely to reflect the most accuratestatus of plant available P in BRS due to the strongestcorrelation between this index and uptake of P by rye-grass. It also showed comparable correlation coefficientwith Colwell-P in terms of their relationships with theleaf dry matter. AEM-P unlike Colwell-P, Mehlich 3-Pand CaCl2-P is independent of soil types (e.g. pH, coarse

or fine textured soil), which can be used over a widerange of soils and offers analytical simplicity and effi-ciency especially for routine laboratory work. Impor-tantly, this study has highlighted the need to undertakemore detailed P (and other nutrient) uptake studies in therhizosphere of rehabilitated residue sand embankments.

Acknowledgments MsMarijke Heenan for her assistance dur-ing field work, and in chemical analysis. Gregory Stephen ofZeolite Australia Pty Ltd. for supplying the zeolite and BarryBatchelor of Black Earth Products Pty Ltd. for supplying thebiochar. This research was supported under the Australian Re-search Council’s Linkage Projects funding scheme (project num-ber LP0989670) and by Alcoa World Alumina, Australia. Asso-ciate Professor CR Chen is the recipient of an Australian Re-search Council Future Fellowship (project number FT0990547).

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