remediation of soils contaminated with molybdenum using soil amendments and phytoremediation

REMEDIATION OF SOILS CONTAMINATED WITH MOLYBDENUMUSING SOIL AMENDMENTS AND PHYTOREMEDIATION

C. NEUNHÄUSERER, M. BERRECK and H. INSAM∗University of Innsbruck, Institute of Microbiology, Microbial Ecology Working Group, Innsbruck,

Austria(∗ author for correspondence, e-mail: [email protected]; fax: +43 512 5072928)

(Received 9 February 1999; accepted 29 May 2000)

Abstract. For ruminants, there is a narrow span between nutritional deficiency of Molybdenum andits potential toxicity. Molybdenosis occurs among cattle feeding on forage with Mo concentrationsabove 10µg g−1 or a Cu:Mo ratio<2. In the area under investigation forage Mo contents in thevalley are as high as 180µg g−1 due to industrial pollution, while the alpine pastures, where cattlegraze during summer, are nutrient (e.g. Cu) deficient. When driven to the valley pastures in fall,animals often fell ill with molybdenosis, and several died. The aim of the study was to remediatethis 300 ha area. Two approaches were attempted: (1) to reduce the Mo contents of the forage byimmobilizing soil Mo, and (2) to increase plant Mo contents by mobilizing soil Mo to increaseplant Mo which may then be removed from the system (phytoremediation). In a soil extraction ex-periment we demonstrated that phosphate fertilization, ammonium sulfate amendment, vermiculite,humic acid and sewage sludge increased Mo leaching by 30 to 110%. Fe-humate and Mn-humateapplication decreased Mo in the leachate from 96µg L−1 to 55 and 7µg L−1, respectively. PlantMo contents were increased up to 170% by P-fertilizer and up to 150% by vermiculite. Conversely,sewage sludge, Fe- and Mn-humate decreased plant Mo contents by 60, 40 and 75% in the green-house. In the field study, the effects were smaller, but Mo export through plant harvest increasedby 88% after P-fertilization and 84% after vermiculite amendment. Mn-humate and sewage sludgedecreased plant Mo content by 25 and 40%, respectively, rendering the forage suitable for feeding ofruminants. P-fertilization and vermiculite may thus be recommended for the severely contaminatedsites to enhance phytoremediation through Mo export, and Mn-humate and sewage sludge applicationappear suited to remediate the less severely contaminated sites.

Keywords: fertilization, forage, heavy metal, Mo, molybdenosis, phytoremediation, ruminants, soilremediation, toxicity, waste management

1. Introduction

Molybdenum is an essential element in plant and animal nutrition. Low levels ofMo are required in the diets of animals for normal growth and development, butthere is a narrow span between nutritional deficiency for the crop (0.5µg g−1)and potential toxicity to ruminants (10µg g−1) (Albasel and Pratt, 1989). Cattleare the most sensitive, followed in order by sheep, horses and hogs (Jarrellet al.,1980). The toxicity is actually a Cu deficiency, since Mo decreases Cu uptake inruminants. Molybdenosis occurs among cattle feeding on forage with Mo concen-trations above 10µg g−1 (Fergusonet al., 1943) or an imbalance of the Cu:Mo

Water, Air, and Soil Pollution128: 85–96, 2001.© 2001Kluwer Academic Publishers. Printed in the Netherlands.

86 C. NEUNHÄUSERER, M. BERRECK AND H. INSAM

ratio in the diet (Wardet al., 1997). The excess Mo interferes with sulfide oxidase,causing sulfide levels in the animal to increase, thus decreasing Cu availability tothe animal (Gengelbachet al., 1994; Smith and White, 1997). Miltmore and Mason(1971) suggested a safe minimum Cu:Mo ratio of 2, lower ratios being potentiallytoxic.

In the case of this study the high soil Mo contents are due to the Mo outputof an industrial plant over the past decades (Horaket al., 1993). High availabilityfor plants led to high Mo contents of the herbage. The local farming practice ofcattle summer grazing on micronutrient (especially Cu) deficient alpine pasturesenhances the problem. Cu-deficient cattle, driven from the alpine pastures in thefall, are then fed Mo-enriched hay or graze on the valley-bottom contaminatedsites. Animals fell ill with molybdenosis, and numerous died. However, this wasno longer compatible with the organic farming practiced in the area.

Due to state-of-the art exhaust air cleansing technology, since 1979 the Mooutput of the industrial plant has decreased from 2400 to 130 kg annually (Horaket al., 1993). The current emissions are not problematic (except in close vicinity ofthe plant), but the burden of the past (contaminated soil) results in high plant Mocontents.

The aim of this study was to find methods allowing restoration of this area(about 300 ha) for agricultural use. Anderson (1956) recommended a Mo content of<1.5 mg kg−1 for safe feed production on alkaline soils. The soils investigated hadMo contents of 2.5–11 mg kg−1. The primary objective was to enlarge the Cu:Moratio in the diet either by increasing Cu contents by addition of Cu rich amendments(for example, sewage sludge) or, preferably, by reducing the Mo content of theplants. To achieve this, two approaches were attempted:

(i) Soil Mo immobilization for the moderately contaminated sites. In previousstudies Mo immobilisation was attributed to high soil Fe-oxide contents (Kari-mian and Cox, 1978; Pierzynski and Jacobs, 1986; Sheppard and Thibault,1992; Goldberget al., 1996), humic acids (Morrison and Spangler, 1992),organic matter (Bloomfield and Kelso, 1973), clay minerals (Goldberget al.,1996) and amendment of (NH4)2SO4 (Williams and Thornton, 1972).Antagonistic effects between Mn and Mo (Karimian and Cox, 1978), and be-tween Cu and Mo (Cheng and Ouellette, 1973) have also been demonstrated.

(ii) Phytoremediation through initially enhancing plant Mo export, followed byMo immobilization in the soil for the severely contaminated sites. In previousstudies phosphate has been shown to mobilize soil Mo and to increase plantMo uptake (Gorlachet al., 1969; Barrow, 1986; Xie and MacKenzie, 1991).

REMEDIATION OF Mo CONTAMINATED SITES 87

2. Materials and Methods

Firstly, the natural leaching of Mo through the soil was determined to estimatepossible annual losses by vertical transport. Secondly, the effect of various soilamendments on mobility and plant availability of Mo was studied in the laboratory.In a greenhouse study employing intact soil cores, and in a final field experiment,the effects of various amendments on plant uptake of Mo was tested.

2.1. LEACHING OF MOLYBDENUM UNDER UNSATURATED CONDITIONS

Eighteen intact soil cores or mini-lysimeters (six replicates per location, 40 cmlong, 11 cm diameter) from three different locations and under different manage-ment (meadows and forest) were sampled with a steel corer in the summer of 1995and placed in the greenhouse for 4 months. The Mo content of the investigatedsoils was 10.7 mg kg−1 for the forest soil (rendzina), 2.5 mg kg−1 for the fluvisoland 7.2 mg kg−1 for the and rendzina meadow soil. The higher Mo content ofthe rendzinas is due to their location in the main wind direction of the industrialplant (Provincial Government of Tyrol, Dept. of Hydrography, pers. comm.). Thelysimeter cores were watered weekly with 250 mL of deionized water at a rate of5 mL min−1 (30 mm hr−1) in a total amount equivalent to the average rainfall onthe sites, i.e. 1500 mm yr−1. The percolate was collected weekly and analysed forMo content. The lysimeter system, designed to avoid edge flow, is described indetail by Insam and Palojärvi (1995).

2.2. EFFECT OF SOIL AMENDMENTS ON EXTRACTABLEMO

Soil of the surface layer (0–10 cm, 7.2 mg Mo kg−1) of the meadow rendzina wassampled, sieved (2 mm mesh) and homogenized. After addition of soil amendmentsin 4 replicates (Table I), 100 g samples were placed in 500 mL Erlenmeyer flasksand incubated for 42 d. Control soil remained untreated. After 14, 28 and 42 daysthe plant available Mo was extracted with 40 mL 1 M NH4Acetate-solution per 20 gof soil (Horaket al., 1993). The suspension was shaken for 1 hr at 220 rpm. Theextract (3.5 mL) was digested with 3.5 mL HNO3 (suprapur) and 0.5 mL H2O2

in a microwave oven (MLS GmbH) and Mo contents were measured by atomicabsorption spectrophotometry (Z-8200, Hitachi).

2.3. PLANT UPTAKE OF CU AND MO IN GLASSHOUSE EXPERIMENTS

For these experiments, 1 kg of sieved (5 mm mesh) rendzina meadow soil from thesurface layer (0–10 cm, 6.5 mg Mo kg−1) was placed in pots (15 cm diameter),seeded (0.6 g pasture seed mixture per pot, Table II) and amended in 5 replicateswith the supplements (Table I). Forty and 97 days after seeding crop dry matterwas determined, and Mo and Cu content were measured. Of each pot 250 mgfinely ground plant material was dissolved in 3.5 mL HNO3 and 0.5 mL H2O2

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TABLE I

Soil additives per 1 kg soil (experiment 2 and 3) and per 1 m2 (experiment 4)

Treatment Mo Cu Experiment 2 Experiment 3 Experiment 4

(mg kg−1)

1 Control n.d. n.d.

2 P-fertilizer 1 n.d. n.d. 3.18 mg phosphorus 3.18 mg phosphorus 950 mg phosphorus

P-fertilizer 2 6.35 mg phosphorus – –

P-fertilizer 3 12.70 mg phosphorus – –

3 AS 1 n.d. n.d. 131 mg ammonium sulfate – –

AS 2 262 mg ammonium sulfate – –

4 Vermiculite n.d. n.d. 1% of soil weight 1% of soil weight 750 g

5 Humic acid 1.72 13.8 1% of soil weight – –

6 Sewage sludge 0.91 282.2 1% of soil weight 1% of soil weight 750 g

7 Fe-humate 2.30 2.7 2.05 mL Fe-humate 2.05 mL Fe-humate –

8 Mn-humate 1 2.30 2.7 2.8 mL Mn-humate 2.8 mL Mn-humate 105 mL Mn-humate

Mn-humate 2 – – 210 mL Mn-humate

Materials 4, 5, 7 and 8 were provided by R. Pretterebner, (PlantCo, Zagersdorf, Austria), sewage sludge originated fromSölden, Austria, and was chosen because of its particularly high copper content.


TABLE II

Pasture seed mixture used in the greenhouse experiments

Species Mixture in % Mixture in %

of area of weight (dm)

Trifolium repensL. 10 8.1

Trifolium hybridum. L. 5 4.1

Lotus corniculatusL. 5 6.1

Lolium perenneL. 5 5.1

Dactylis glomerataL. 10 8.1

Phleum pratenseL. 15 12.1

Festuca pratensisHuds. 10 12.1

Trisetum flavescensL. 5 4.0

Festuca rubraL. 10 12.1

Agrostis tenuisL. 5 4.0

Poa pratensisL. 20 24.2

Amount 24.8 kg ha−1

and digested in a microwave oven. Cu and Mo were determined by AAS, as above.At the end of the experiment, soil pH (0.01 M CaCl2-solution), microbial biomassand basal respiration (Anderson and Domsch, 1978) were determined.

2.4. PLANT GROWTH AND MO UPTAKE IN THE FIELD

According to the results of experiments 2 and 3, six soil amendments (Table I,4 replicates each) were tested under field conditions on the meadow rendzina, anArrhenatherionKoch 1926, described in Section 2.3. The study area, comprisedof 24 5.5×5.5 m plots (distance between plots 1 m), was situated in the centralhighly polluted area (soil Mo contents>5 mg kg−1). The first cut was done 42days after soil treatment, the second cut again 42 days later. From each plot fourseparate plant samples were taken, dried, milled and analysed for Mo content. Theleached Mo was determined by anion-exchange-resin bags inserted into the soil ina depth of 10 cm at the beginning of the experiment (10 replicates each treatment).Resin bags were collected at the end of the experiment. At the end of the fieldexperiment, one intact 40 cm soil core (11 cm diameter) was sampled from eachplot, placed in a mini-lysimeter (as in Section 2.1.) and watered. The Mo contentof the leachate was then determined.


Figure 1.Molybdenum leaching from intact soil cores of three soil types during an incubation periodof 97 days (mini-lysimeters in the greenhouse). Mean± standard deviation.

2.4.1. Statistical analysisElemental contents are expressed on oven dry basis. Results presented are arith-metic means of replicates. For the comparison of means, the Mann-Whitney-U-Testwas used (SPSS, 1994).

3. Results and Discussion

3.1. LEACHING OF MOLYBDENUM

From the leachate data it may be estimated that the Mo content decreases by 1–2% yr−1 (Figure 1), which corresponds to the earlier observations that even strongirrigation does not decrease topsoil Mo contents under field conditions (Stark andRedente, 1986). To obtain safe soil Mo levels (<1.5 mg kg−1, according to An-derson, 1956) would thus require 50 to 100 yr. The necessity of soil treatmentscontrolling Mo mobility was thus confirmed.

3.2. EFFECT OF SOIL AMENDMENTS ON EXTRACTABLEMO

After amendment of sewage sludge, vermiculite (clay mineral) and P-fertilizer, soilextractable Mo increased significantly by 110, 90 and 60%, respectively, comparedto the control (Figure 2). Ammonium sulfate as well as humic acid increased NH4-acetate extractable Mo contents by 28%. It is known that increasing phosphateavailability reduces the sorption of Mo (Gorlachet al., 1969; Barrow, 1986; Xieand MacKenzie, 1991), even at pH at 7.1. We found that increasing amounts of


Figure 2.Plant available Mo in dependence on different soil amendments (mean of three extractionsafter 14, 28 and 42 days of incubation) compared with control soil. The extraction of plant availableMo was done with 1 M NH4Ac-solution. Mean± standard deviation.

P-fertilizer did not further enhance Mo mobility so that we chose the lowest con-centration (3.18 mg P-fertilizer kg−1) for the follow-up experiments. The effectof sewage sludge was attributed to its alkalinity (pH 12.1), rendering Mo moremobile, but sewage sludge was likely to have affected the Mo availability by othermechanisms as well. For example, Jarrellet al. (1980) emphasized the Mo com-plexing effect of low molecular organic matter (e.g. in sewage sludge), protectingMo against precipitation on Al and Fe oxides. Molybdenum adsorption on clayminerals exhibits a peak near pH 3 and then decreases rapidly with increasingpH until adsorption is virtually zero near pH 7 (Goldberget al., 1996). Xie andMacKenzie (1991) attributed the mobilizing effect of vermiculite at higher soilalkalinity to the negative charge of clay minerals, intensifying the desorption ofmolybdate by other native anions like phosphate and sulfate.

Fe-humate and Mn-humate decreased significantly (p < 0.01) the plant avail-ability for Mo by 44 and 93%, respectively. The effect of Mn-humate is due to theadsorption of Mo on the organic matter by Mn2+-bridges (Bloomfield and Kelso,1973; Karimian and Cox, 1978) and a similar functionality may be attributed to Fein the Fe-humate.

3.3. PLANT UPTAKE OF MO IN GLASSHOUSE EXPERIMENTS

Molybdenum concentrations in meadow plants were significantly (p < 0.01) af-fected by soil amendments (Figure 3). Vermiculite and phosphate treatments in-creased Mo contents by 50 and 72%, respectively, due to the increased mobilityof Mo in the soil solution. Plants showed lower Mo contents compared to the con-trol when they were grown on soils treated with Fe-Humate (–40%), Mn-Humate(–75%) and sewage sludge (–60%). In the latter case this was found despite an


Figure 3.Mo content of plants in a greenhouse experiment after soil treatment with various additives,first and second harvest. Mean± standard deviation.

increase in plant availability of Mo (measured by ammonium acetate extract), pos-sibly due to the Ca2+ content of the sewage sludge. Ca in the soil solution lowersMo uptake by grasses due to the competition between molybdate and orthophos-phate for plant absorption (Williams and Thornton, 1972). Mo was immobilizedmost effectively by Mn-humate, with a 71% decrease in plant Mo contents in thefirst and a 78% decrease in the second cut. This may be attributed to negativeinteractions between Mo and Mn on the plant uptake (Jones and Ruckman, 1973).The decreases in plant-Mo concentrations due to Fe-humate (24 and 40%) andsewage sludge (60 and 55%) were smaller, but also significant.

The Cu content of the plants was not affected by any treatment, despite the highCu contents in the sewage sludge (250 mg kg−1). Improved Cu:Mo ratios were thusonly due to decreased plant Mo contents. Amending the soils did not affect plantbiomass yields. An exception was P-fertilization, increasing the yield in the first(+30%) and second cut (+12%) because of the low P-status of the soil.

Soil pH was not affected by any treatment, indicating a high buffer capacity ofthe soil. Microbial biomass and basal respiration were not influenced significantlyby any treatment, suggesting only minor effects on the soil microbiota.

3.4. PLANT GROWTH AND MO UPTAKE IN THE FIELD

Plant growth in the field was significantly increased by vermiculite (+56%) andphosphate (+31%); no negative effects on plant growth were observed. The Mocontents of the plants were generally higher than in the greenhouse experiment.This may be attributed to differences in water regimes (Wanget al., 1994). Theeffects of the treatment on plant Mo contents were generally smaller than in thegreenhouse experiment. In the first cut the Mo content was significantly lowered by


Figure 4.Plant growth (a), Mo content (b) and Mo export (c) of plants in a field experiment after soiltreatment with various amendments, second cut. Mean± standard deviation.

all treatments compared with the control plants (Figure 4). The most pronouncedeffect was found for sewage sludge (–40% in the first cut, –49% in the secondcut). Also Mn-humate significantly lowered plant Mo contents (–22 and –29%,respectively, to 105 and 118 mg kg−1). The Mo content of the plants treated withphosphate and vermiculite was not different from control plants; however, the en-hanced plant biomass production increased total Mo exports (Figure 4). It is known


from other studies that fertilization may dilute Mo contents in the plant biomass(Gupta and Cutcliffe, 1968; Jones and Ruckman, 1973). The Mo exports fromthe soil were 21.8 mg m−2 for the control; vermiculite and phosphate increasedMo exports by 47 and 33%, respectively. Mn-humate (–25%) and sewage sludge(–40%) reduced plant Mo exports significantly (Figure 4).

The leaching of Mo through downward water movement, measured with ionexchange resins, was enhanced by phosphate, vermiculite and sewage sludge by64% (p = 0.18), 75% (p = 0.14) and 41% (p = 0.51), respectively. The lackof significant effects may be explained by (i) the high data variability, and (ii) at adepth of 10 cm, plant roots may still have been actively taking up Mo. The leach-ing of Mo below 40 cm (as determined with the mini-lysimeters) was enhancedsignificantly (p < 0.01) by phosphate (+368%), sewage sludge (+347%) andvermiculite (+274%) (Table III), confirming the results observed in the precedingextraction experiment. Mn-humate did not affect the Mo content in the soil solutionat 40 cm depth.

The molybdenum output of the soil by plant harvesting and leaching was summedup over one year. Treating the soil with P-fertilizer, vermiculite or sewage sludgeincreased the Mo loss of the soil by 88, 84 and 24%, respectively (Table III). WhenMn-humate was applied, Mo was immobilized and thus losses decreased comparedto the control.

4. Conclusions

The natural cycling of Mo in the study area is mainly defined by two input andtwo output factors. The output factors are the leaching into deeper soil layers andthe Mo export by harvesting and grazing of the plants. The input factors are theatmospheric emissions and farmyard manure (fm). The Mo content of the fm isclosely related to the Mo content of the feed, because dietary Mo is not stored inanimal tissue (Ankeet al., 1985).

At the highly contaminated sites the first aim was to decrease the total Mocontent of the system. This was made possible by increasing the soil Mo mobil-ity, thus enhancing the leaching of Mo from the topsoil, and enhancing plant Mouptake. These plants may be harvested and removed from the system, interruptingthe internal cycling. As a compensation, farmers receive uncontaminated feed, sothat the Mo content of the fm will decrease and thus the Mo will be lowered.

On the less severely contaminated areas, immobilization of soil Mo is recom-mended. These areas with soil Mo between 2.0 and 4.5 mg kg−1 are located atgreater distances to the industrial plant, off the main wind direction. The naturalleaching exceeds the atmospheric input, but the plant availability and content isstill too high for feeding ruminants. Treating these soils with Mn-humate leads tolow Mo contents of the plants by immobilizing the Mo, rendering the hay ediblefor ruminants.

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TABLE III

Annual plant Mo uptake and Mo in the leachate per m2. The Mo content of the investigated soil was 6.2 mg kg−1, corresponding to a totalMo content in the 0–15 cm soil layer of 550 mg m−2

Mo export Mo export Mo export Mo in the Mo in the % of Mo export

through in % of in % of leachate leachate soil Mo in % of

plant harvest control soil leached total soil (%) of

(mg m−2) content (µg L−1) (% of control) Mo control

Control 21.8±1.2 7.92 19.1±2.9 1.56 9.48

P-fertilizer 29.0±5.9 133.1 10.55 89.4±6.7 467.7 7.31 17.86 188

Vermiculite 32.0±2.2 146.8 11.64 71.5±5.8 374.3 5.85 17.49 184

Mn humate 1 17.5±4.5 80.3 6.36 13.0±4.0 68.2 1.07 7.43 78

Mn humate 2 15.9±3.5 73.1 5.79 21.4±3.8 111.7 1.75 7.54 80

Sewage sludge 13.2±2.5 60.6 4.80 85.4±8.1 447.0 6.98 11.78 124


The results obtained in the laboratory have been confirmed in the field exper-iments. Application of the acquired knowledge is under way, and usual farmingpractices will soon be implemented again in large parts around the metal plant.

Acknowledgements

We thank R. Pretterebner for providing humic acids and clay minerals, and G.Moosmann for organizing the co-operation with the government of Tyrol/Austriaand Metallwerk Plansee.

References

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remediation of soils contaminated with molybdenum using soil amendments and phytoremediation

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