toxics

Article

Differential Effects of Low-Molecular-WeightOrganic Acids on the Mobilization of Soil-BorneArsenic and Trace Metals

Obinna Elijah Nworie 1, Junhao Qin 1,2 and Chuxia Lin 1,*1 School of Environment and Life Science, University of Salford, Greater Manchester M5 4WT, UK;

O.Nworie@edu.salford.ac.uk (O.E.N.); qinjunhao2015@gmail.com (J.Q.)2 Key Laboratory of Agro-Environment in the Tropics, Ministry of Agriculture,

South China Agricultural University, Guangzhou, 510642, China* Correspondence: C.Lin@salford.ac.uk; Tel.: +44-161-295-5356

Academic Editors: Carmen Corada-Fernández, Javier Valdes-Abellan and Lucila CandelaReceived: 2 August 2017; Accepted: 17 August 2017; Published: 21 August 2017

Abstract: A batch experiment was conducted to examine the effects of six low-molecular-weightorganic acids on the mobilization of arsenic and trace metals from a range of contaminated soils. Theresults showed that the organic acids behaved differently when reacting with soil-borne As and tracemetals. Oxalic acid and acetic acid had the strongest and weakest capacity to mobilize the investigatedelements, respectively. The solubilisation of iron oxides by the organic acids appears to play a criticalrole in mobilizing other trace metals and As. Apart from acidification and complexation, reductivedissolution played a dominant role in the dissolution of iron oxides in the presence of oxalic acid, whileacidification tended to be more important for dissolving iron oxides in the presence of other organicacids. The unique capacity of oxalic acid to solubilize iron oxides tended to affect the mobilization ofother elements in different ways. For Cu, Mn, and Zn, acidification-driven mobilization was likelyto be dominant while complexation might play a major role in Pb mobilization. The formation ofsoluble Fe and Pb oxalate complexes could effectively prevent arsenate or arsenite from combiningwith these metals to form solid phases of Fe or Pb arsenate or arsenite.

Keywords: organic acid; arsenic; trace metal; mobilization; complexation; reductive dissolution

1. Introduction

Environmental risk assessment and remediation of contaminated lands require knowledgeof contaminant mobility. Currently, mobility evaluation for soil-borne contaminants relies on theextraction of their “mobile” or “mobilizable” fractions using selected chemical reagents that arehardly encountered in soils [1–3]. Consequently, the usefulness and reliability of such information forpredicting contaminant mobility and bioavailability is less certain.

Low-molecular-weight organic acids (LMWOAs) are commonly present in soils as a result ofroot exudation and the microbially mediated decomposition of soil organic matter [4,5]. LMWOAsare capable of solubilizing trace metals and metalloids in the rhizosphere through soil acidification,complexation, and reduction reactions [6–8]. Except for highly acidic soils such as sulfidic soils wheretrace metals are largely mobilized by sulfuric acid [9,10], trace metals and metalloids tend to be tightlybound to the soil matrix in less and non-acidic soils [11–13]. Therefore, LMWOAs have a significantrole to play in mobilizing soil-borne trace metals/metalloids, particularly in rhizospheric soils, whichhas important implications for the uptake of trace metals and metalloids by plants. In theory, LMWOAsshould be superior to non-naturally occurring chemical reagents when being used as extracting agentsfor the evaluation of trace metal/metalloid mobility and bioavailability in contaminated soils.

Toxics 2017, 5, 18; doi:10.3390/toxics5030018 www.mdpi.com/journal/toxics

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Although there have been reports on the mobilization of trace metals/metalloids in soils byorganic acids [14–16], there is still a large gap in knowledge about the chemical behavior of differenttrace metals and metalloids in the presence of different LMWOAs. Mixed results are often observedfrom different experiments regarding the effects of LMWOAs on liberation of soil-borne trace metalsand metalloids. This is largely attributable to the complex nature of the reaction systems involvingso many affecting factors. In addition, many of the investigations only focused on a limited numberof either organic acids or trace metals/metalloids [17–21]. There is insufficient understanding of thedifferential effects of LMWOAs on the release of various trace metals and metalloids on a comparablebasis. In this study, a range of soils with different levels of contamination by multiple trace metals andarsenic were used to compare the effects of six common LMWOAs, as well as an inorganic acid, onextracting trace metals and arsenic from the investigated soils. The objectives were to (a) assess thecapacity of different organic acids to mobilize each of the investigated metals; (b) explain the observeddifferential effects; and (c) identify the major drawbacks of the metal extraction procedure using theinorganic acid as an extractant.

2. Materials and Methods

2.1. The Soil Samples Used in the Experiment

Twenty three soil samples were collected from a closed landfill site in the Greater Manchesterregion, United Kingdom. In the laboratory, the soil samples were oven-dried at 40 ◦C until they werecompletely dry. The samples were then ground to pass a 2 mm stainless steel sieve. Soil particles with adiameter >2 mm were discarded. The <2 mm soil fraction of each sample was homogenized and storedin an air-tight re-sealable polyethylene bag prior to use for analysis and the incubation experiment.

The total metal concentration of these samples ranged from 256 to 2469 mg/kg for As, from 44 to180 mg/kg for Cu, from 27,957 to 59,013 mg/kg for Fe, from 14 to 777 mg/kg for Mn, from 260 to1457 mg/kg for Pb, and from 25 to 150 mg/kg for Zn. Soil pH, electrical conductivity, and organicmatter content had a range of 3.32–5.31, 0.027–0.250 dS/m, and 1.2–12%, respectively.

2.2. The Organic Acid Incubation Experiment

A batch experiment was conducted to observe the release of various trace metals and arsenicfrom the soil to the solution in the presence of organic acids. Six common LMW organic acids wereused in this study, including acetic acid, citric acid, formic acid, malic acid, oxalic acid, and tartaricacid. The concentration of all the six organic acids was set at 200 mmol/L. 125 mL plastic bottles wereused as batch reactors. For each soil sample, 50 mL of a relevant organic acid solution was addedinto the plastic bottle containing 10 g of the soil sample. Immediately after the solution addition, thebottle was hand-shaken for 1 min and then allowed to stand for 7 days. All the bottles were randomlyplaced in a covered paper box to avoid exposure to light during the entire period of the incubationexperiment. At the end of the experiment, each bottle was hand-shaken for 1 min and then 15 mLof supernatant was taken, put into a 15 mL polystyrene centrifuge tube, and centrifuged by a MSEMistral 1000 Centrifuge at a speed of 3600 rotations per minute (rpm) for 15 min. Centrifugation wasrequired in order to remove suspended materials in the solution samples prior to the analysis of metalsand arsenic. After centrifugation, each solution sample was transferred into a clean polystyrene tubeand stored in a fridge at 4 ◦C before being analysed.

2.3. The Extraction of Metals by 1 M HNO3

The acid-mobilizable pool of metals was also evaluated using the conventional inorganic acidextraction method. For each soil sample, 50 mL of 1 M HNO3 was added into a 125 mL plastic bottlecontaining 10 g of soil sample. The bottles were shaken in a rotary shaker for 1 h at room temperature.After shaking, 15 mL of supernatant was taken, put into a 15 mL polystyrene centrifuge tube, andcentrifuged by a MSE Mistral 1000 Centrifuge at a speed of 3600 rpm for 15 min. Centrifugation was

Toxics 2017, 5, 18 3 of 16

required in order to remove suspended materials in the solution samples prior to the analysis of themetals. After centrifugation, each solution sample was transferred into a clean polystyrene tube bypassing through a 0.45 µm membrane filter and was stored in a fridge at 4 ◦C before being analysed.

2.4. Analytical Methods

For the initial soil characterization, pH and the electrical conductivity of the soil samples weremeasured in a 1:5 (soil:water) extract using a calibrated Mettler Toledo 320 pH meter and a MettlerToledo electrical conductivity meter, respectively. Total metal concentration was determined usinga Niton XL2 Gold Hand-held XRF Analyzer. The instrument was calibrated by firstly analysing the73,308 standard reference materials prior to sample analysis. To ensure the accuracy and reliability ofthe results obtained, all analyses were performed in duplicates and the analysis time was set at 240 s.Soil organic matter content was determined using a Walkley-Black method.

For the soil extraction and incubation experiment, trace metals and arsenic in the solutionsamples were measured using a Varian 720-ES inductively coupled plasma optical emissionspectrometer (ICP-OES).

2.5. The Statistical Analysis Method

Statistical analysis of the experimental data was performed using IBM SPSS software Version 13.0.

3. Results

3.1. Arsenic and Trace Metals Released from the Soils by LMWOA

The mean concentration of each trace element released by the six LMWOAs is shown in Figure 1.A similar pattern is observed for the six investigated trace elements, and the oxalic acid incubationsolutions and the acetic acid incubation solutions had the highest and the lowest concentration of eachelement, respectively. However, the difference in the concentration of each element between the oxalicacid-extractable form and other organic acid-extractable forms varied from element to element.

The ratio of the oxalic acid-extractable form to the second highest organic acid-extractable formwas in the following decreasing order: As (6.38) > Cu (2.70) > Fe (2.63) = Pb (2.63) > Zn > (1.88) > Mn(1.39). Malic, citric, and tartaric acid incubation solutions had comparable concentration for all thesix investigated elements. For Mn and Zn, their concentrations in the formic acid solution were alsocomparable to those in the above three solutions.

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centrifuged by a MSE Mistral 1000 Centrifuge at a speed of 3600 rpm for 15 min. Centrifugation was 

required in order to remove suspended materials in the solution samples prior to the analysis of the 

metals. After centrifugation, each solution sample was transferred into a clean polystyrene tube by 

passing through a 0.45 μm membrane filter and was stored in a fridge at 4 °C before being analysed. 

2.4. Analytical Methods 

For the initial soil characterization, pH and the electrical conductivity of the soil samples were 

measured in a 1:5 (soil:water) extract using a calibrated Mettler Toledo 320 pH meter and a Mettler 

Toledo electrical conductivity meter, respectively. Total metal concentration was determined using a 

Niton XL2 Gold Hand‐held XRF Analyzer. The  instrument was calibrated by firstly analysing the 

73,308 standard reference materials prior to sample analysis. To ensure the accuracy and reliability 

of the results obtained, all analyses were performed in duplicates and the analysis time was set at 240 

s. Soil organic matter content was determined using a Walkley‐Black method. 

For  the  soil  extraction  and  incubation  experiment,  trace metals  and  arsenic  in  the  solution 

samples  were  measured  using  a  Varian  720‐ES  inductively  coupled  plasma  optical  emission 

spectrometer (ICP‐OES). 

2.5. The Statistical Analysis Method 

Statistical analysis of the experimental data was performed using IBM SPSS software Version 

13.0. 

3. Results 

3.1. Arsenic and Trace Metals Released from the Soils by LMWOA 

The mean concentration of each trace element released by the six LMWOAs is shown in Figure 

1. A similar pattern is observed for the six investigated trace elements, and the oxalic acid incubation 

solutions and the acetic acid  incubation solutions had the highest and the  lowest concentration of 

each element, respectively. However, the difference in the concentration of each element between the 

oxalic acid‐extractable form and other organic acid‐extractable forms varied from element to element. 

The ratio of the oxalic acid‐extractable form to the second highest organic acid‐extractable form 

was in the following decreasing order: As (6.38) > Cu (2.70) > Fe (2.63) = Pb (2.63) > Zn > (1.88) > Mn 

(1.39). Malic, citric, and tartaric acid incubation solutions had comparable concentration for all the six 

investigated elements. For Mn and Zn,  their concentrations  in  the  formic acid solution were also 

comparable to those in the above three solutions. 

 

0

50

100

150

200

250

300

Acetic Formic Malic Citric Oxalic Tartaric

As (m

g/kg)

(a)

0

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35

40

45

Acetic Formic Malic Citric Oxalic Tartaric

Cu (mg/kg)

(b)

Figure 1. Cont.

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Figure 1. Mean concentration of (a) arsenic, (b) copper, (c) iron, (d) manganese, (e) lead, and (f) zinc 

being released from the soils by the six organic acids. 

3.2. The Relationship between Different Organic Acid‐Extractable Metal Forms 

There was no relationship in As between the oxalic acid‐extractable form and any of the other 

organic acid‐extractable forms. However, for the other five organic acids (acetic, formic, malic, citric, 

and tartaric acids), there was a close relationship in the extractable As for any pairs of these organic 

acids. For Cu, Mn, and Zn, there was a close relationship in each of these three metals between any 

pair of the six organic acid‐extractable forms. Similar to As, there was no relationship  in Fe or Pb 

between the oxalic acid‐extractable form and any other organic acid‐extractable forms. Acetic Fe was 

only related to tartaric Fe but closely related to formic Fe. Formic Fe, citric Fe, and tartaric Fe were all 

interrelated to each other. Acetic Pb was not related to any Pb forms extracted by other organic acids 

(Table 1). 

Table 1. Correlation matrices of six datasets involving various organic acid‐extractable metals (1) As, 

(2) Cu, (3) Fe, (4) Mn, (5) Pb, and (6) Zn.  

Acetic As Formic As Malic As Citric As Oxalic As Tartaric As Acetic As 1 Formic As 0.851** 1 Malic As 0.639** 0.743** 1 Citric As 0.612** 0.696** 0.991* 1 Oxalic As 0.052 0.071 -0.016 -0.059 1 Tartaric As 0.666** 0.740** 0.936** 0.925** 0.229 1

0

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Acetic Formic Malic Citric Oxalic Tartaric

Fe (mg/kg)

(c)

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Acetic Formic Malic Citric Oxalic Tartaric

Mn (mg/kg)

(d)

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Acetic Formic Malic Citric Oxalic Tartaric

Pb (mg/kg)

(e)

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Acetic Formic Malic Citric Oxalic Tartaric

Zn (mg/kg)

(f)

Figure 1. Mean concentration of (a) arsenic; (b) copper; (c) iron; (d) manganese; (e) lead; and (f) zincbeing released from the soils by the six organic acids.

3.2. The Relationship between Different Organic Acid-Extractable Metal Forms

There was no relationship in As between the oxalic acid-extractable form and any of the otherorganic acid-extractable forms. However, for the other five organic acids (acetic, formic, malic, citric,and tartaric acids), there was a close relationship in the extractable As for any pairs of these organicacids. For Cu, Mn, and Zn, there was a close relationship in each of these three metals between anypair of the six organic acid-extractable forms. Similar to As, there was no relationship in Fe or Pbbetween the oxalic acid-extractable form and any other organic acid-extractable forms. Acetic Fe wasonly related to tartaric Fe but closely related to formic Fe. Formic Fe, citric Fe, and tartaric Fe were allinterrelated to each other. Acetic Pb was not related to any Pb forms extracted by other organic acids(Table 1).

Table 1. Correlation matrices of six datasets involving various organic acid-extractable metals (1) As,(2) Cu, (3) Fe, (4) Mn, (5) Pb, and (6) Zn.

Acetic As Formic As Malic As Citric As Oxalic As Tartaric As

Acetic As 1Formic As 0.851** 1Malic As 0.639** 0.743** 1Citric As 0.612** 0.696** 0.991* 1Oxalic As 0.052 0.071 -0.016 -0.059 1

Tartaric As 0.666** 0.740** 0.936** 0.925** 0.229 1

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Table 1. Cont.

Acetic Cu Formic Cu Malic Cu Citric Cu Oxalic Cu Tartaric Cu

Acetic Cu 1Formic Cu 0.928** 1Malic Cu 0.852** 0.975** 1Citric Cu 0.813** 0.950** 0.972** 1Oxalic Cu 0.876** 0.932** 0.909** 0.890** 1

Tartaric Cu 0.821** 0.956** 0.989** 0.981** 0.903** 1

Acetic Fe Formic Fe Malic Fe Citric Fe Oxalic Fe Tartaric Fe

Acetic Fe 1Formic Fe 0.912** 1Malic Fe 0.385 0.495* 1Citric Fe 0.362 0.536** 0.848** 1Oxalic Fe 0.189 0.204 0.107 0.267 1

Tartaric Fe 0.421* 0.579** 0.816** 0.980** 0.285 1

Acetic Mn Formic Mn Malic Mn Citric Mn Oxalic Mn Tartaric Mn

Acetic Mn 1Formic Mn 0.964** 1Malic Mn 0.958** 0.989** 1Citric Mn 0.962** 0.994** 0.996** 1Oxalic Mn 0.935** 0.985** 0.983** 0.989** 1

Tartaric Mn 0.949** 0.987** 0.984** 0.991** 0.996** 1

Acetic Pb Formic Pb Malic Pb Citric Pb Oxalic Pb Tartaric Pb

Acetic Pb 1Formic Pb 0.213 1Malic Pb 0.213 0.905** 1Citric Pb 0.247 0.894** 0.923** 1Oxalic Pb 0.114 0.153 0.092 0.114 1

Tartaric Pb 0.263 0.841** 0.883** 0.946** 0.181 1

Acetic Zn Formic Zn Malic Zn Citric Zn Oxalic Zn Tartaric Zn

Acetic Zn 1Formic Zn 0.837** 1Malic Zn 0.767** 0.933** 1Citric Zn 0.836** 0.965** 0.966** 1Oxalic Zn 0.643** 0.839** 0.801** 0.868** 1

Tartaric Zn 0.854** 0.948** 0.914** 0.979** 0.898** 1

** Correlation is significant at the 0.01 level (2-tailed); * Correlation is significant at the 0.05 level (2-tailed).

3.3. The Mobility of As and Its Relationship with Mobilizable Fe

The percentage of organic acid-extractable As in the total As contained in the soils (i.e., the fractionof As mobilization) for each organic acid is plotted against the corresponding organic acid-extractableFe fraction (Figure 2). Less than 1% of the total soil As was mobilized by either acetic acid or formicacid (Figure 2a,c). In the citric, malic, and tartaric acid treatments, the rate of As mobilization wasless than 10% of the total soil As (Figure 2b,d,f). Oxalic acid treatment led to the release of about10–30% of the total As from the soils (Figure 2e). There was a close relationship between the rate of Asmobilization and the amount of Fe released from the soils for citric, malic, and tartaric acid treatments.A good relationship between the rate of As mobilization and the amount of Fe released from the soilswas also observed for formic acid treatment. However, there was no clear relationship between therate of As mobilization and the amount of released Fe for the acetic acid and oxalic acid treatments.

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Figure 2. Relationship between the amount of Fe released from the soil and the rate of As mobilization 

in  (a) acetic acid,  (b) citric acid,  (c)  formic acid,  (d) malic acid,  (e) oxalic acid, and  (f)  tartaric acid 

treatments. 

3.4. The Mobility of Cu and Its Relationship with Mobilizable Fe 

In comparison with As, the rate of Cu mobilization was much higher between 1 and 2%, between 

3 and 20%, between 1 and 7%, between 2 and 16%, between 20 and 55%, and between 3 and 25% of 

the total Cu being released from the soils in the acetic, citric, formic, malic, oxalic, and tartaric acid 

treatments, respectively (Figure 3). 

y = 0.0008x + 0.1322

R² = 0.0349

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1

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Acetic As/Total As (%

)

Acetic Fe (mg/kg)

(a)

y = 0.0018x − 0.8725

R² = 0.8665

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Citric As/To

tal A

s (%

)

Citric Fe (mg/kg)

(b)

y = 0.0008x + 0.0933

R² = 0.4504

00.10.20.30.40.50.60.70.80.91

0 500 1000

Form

ic As/Total As (%

)

Formic Fe (mg/kg)

(c)

y = 0.0013x + 0.5665

R² = 0.62930

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Malic As/Total As (%

)

Malic Fe (mg/kg)

(d)

y = ‐0.0002x + 22.703

R² = 0.00590

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Oxalic As/Total As (%

)

Oxalic Fe (mg/kg)

(e)

y = 0.001x + 0.4203

R² = 0.7752

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Tartaric As/Total As (%

)

Tartaric Fe (mg/kg)

(f)

Figure 2. Relationship between the amount of Fe released from the soil and the rate of As mobilizationin (a) acetic acid; (b) citric acid; (c) formic acid; (d) malic acid; (e) oxalic acid; and (f) tartaricacid treatments.

3.4. The Mobility of Cu and Its Relationship with Mobilizable Fe

In comparison with As, the rate of Cu mobilization was much higher between 1 and 2%, between3 and 20%, between 1 and 7%, between 2 and 16%, between 20 and 55%, and between 3 and 25% ofthe total Cu being released from the soils in the acetic, citric, formic, malic, oxalic, and tartaric acidtreatments, respectively (Figure 3).

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Figure 3. Relationship between the amount of Fe released from the soil and the rate of Cu mobilization 

in  (a) acetic acid,  (b) citric acid,  (c)  formic acid,  (d) malic acid,  (e) oxalic acid, and  (f)  tartaric acid 

treatments. 

Similar to As, there was a good relationship between the rate of Cu mobilization and the amount 

of Fe released  from  the soils  in  the citric, malic, and  tartaric acid  treatments; a slight relationship 

between the rate of Cu mobilization and the amount of Fe released from the soils was also observed 

for formic acid treatment; and there was no clear relationship between the rate of Cu mobilization 

and the amount of released Fe for acetic and oxalic acid treatments. 

3.5. The Mobility of Pb and Its Relationship with Mobilizable Fe 

y = −0.001x + 1.3782

R² = 0.0009

0.0

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Acetic Cu/Total Cu (%)

Acetic Fe (mg/kg)

(a) y = 0.0028x + 0.7785

R² = 0.5254

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Citric Cu/Total Cu (%)

Citric Fe (mg/kg)

(b)

y = 0.0051x + 2.7397

R² = 0.1007

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Form

ic Cu/Total Cu (%)

Formic Fe (mg/kg)

(c)

y = 0.0024x + 2.9622

R² = 0.45280

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Malic Cu/Total Cu (%)

Malic Fe (mg/kg)

(d)

y = −7E − 05x + 37.119R² = 0.0001

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Oxalic Cu/Total Cu (%)

Oxalic Fe (mg/kg)

(e)y = 0.0044x + 2.7407

R² = 0.6118

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Tartaric Cu/Total Cu (%)

Tartaric Fe (mg/kg)

(f)

Figure 3. Relationship between the amount of Fe released from the soil and the rate of Cu mobilizationin (a) acetic acid; (b) citric acid; (c) formic acid; (d) malic acid; (e) oxalic acid; and (f) tartaricacid treatments.

Similar to As, there was a good relationship between the rate of Cu mobilization and the amountof Fe released from the soils in the citric, malic, and tartaric acid treatments; a slight relationshipbetween the rate of Cu mobilization and the amount of Fe released from the soils was also observedfor formic acid treatment; and there was no clear relationship between the rate of Cu mobilization andthe amount of released Fe for acetic and oxalic acid treatments.

Toxics 2017, 5, 18 8 of 16

3.5. The Mobility of Pb and Its Relationship with Mobilizable Fe

Very similar to Cu, the rate of Pb mobilization was closely related to the amount of Fe releasedfrom the soils for the citric acid, malic acid, and tartaric acid treatments (Figure 4b,d,f), and wasslightly related to the amount of released Fe for formic acid treatment (Figure 4c). There was no clearrelationship between the rate of Pb mobilization and the amount of released Fe for acetic and oxalicacid treatments (Figure 4a,e). The rate of Pb mobilization was less than 1%, 2.5%, and 6% for most ofthe samples in the acetic, formic, and malic acid treatments, respectively (Figure 4a,c,d).

Toxics 2017, 5, 18   8 of 16 

Very similar to Cu, the rate of Pb mobilization was closely related to the amount of Fe released 

from  the  soils  for  the citric acid, malic acid, and  tartaric acid  treatments  (Figure 4b,d,f), and was 

slightly related to the amount of released Fe for formic acid treatment (Figure 4c). There was no clear 

relationship between the rate of Pb mobilization and the amount of released Fe for acetic and oxalic 

acid treatments (Figure 4a,e). The rate of Pb mobilization was less than 1%, 2.5%, and 6% for most of 

the samples in the acetic, formic, and malic acid treatments, respectively (Figure 4a,c,d). 

 

 

 

Figure 4. Relationship between the amount of Fe released from the soil and the rate of Pb mobilization 

in  (a) acetic acid,  (b) citric acid,  (c)  formic acid,  (d) malic acid,  (e) oxalic acid, and  (f)  tartaric acid 

treatments. 

y = 0.0003x + 0.5161

R² = 0.001

0

0.5

1

1.5

2

2.5

0 50 100 150 200

Acetic Pb/Total Pb(%

)

Acetic Fe (ma/kg)

(a)

y = 0.0019x − 0.4945

R² = 0.779

0

2

4

6

8

10

12

14

0 2000 4000 6000Citric Pb/Total Pb (%)

Citric Fe (mg/kg)

(b)

y = 0.0013x + 0.6758

R² = 0.1031

0

0.5

1

1.5

2

2.5

3

0 200 400 600 800 1000

Form

ic Pb/Total Pb (%)

Formic Fe (mg/kg)

(c)

y = 0.0009x + 0.9811

R² = 0.4123

0

1

2

3

4

5

6

7

0 2000 4000 6000

Malic Pb/Total Pb (%)

Malic Fe (mg/kg)

(d)

y = 0.0002x + 10.594

R² = 0.0072

0

5

10

15

20

25

30

0 5000 10000 15000

Oxalic Pb/Total Pb (%)

Oxalic Fe (mg/kg)

(e)

y = 0.0019x + 1.0705

R² = 0.6923

0

2

4

6

8

10

12

0 1000 2000 3000 4000 5000

Tartaric Pb/Total Pb (%)

Tartaric Fe (mg/kg)

(f)

Figure 4. Relationship between the amount of Fe released from the soil and the rate of Pb mobilizationin (a) acetic acid; (b) citric acid; (c) formic acid; (d) malic acid; (e) oxalic acid; and (f) tartaricacid treatments.

Toxics 2017, 5, 18 9 of 16

Citric and tartaric acid treatments had a mobilization rate of between 1 and 10% of the total Pb formost of the samples (Figure 4b,f). About 5 to 25% of the total soil Pb was mobilized in the oxalic acidtreatment (Figure 4e).

3.6. The Mobility of Zn and Its Relationship with Mobilizable Fe

Largely unlike As, Cu, and Pb, there was no clear relationship between the rate of Zn mobilizationand the amount of Fe released from the soils for the citric and malic acid treatments (Figure 5b,d). Thetartaric acid-extractable Zn percentage was only slightly related to the amount of Fe released from thesoils (Figure 5f).

Toxics 2017, 5, 18   9 of 16 

Citric and tartaric acid treatments had a mobilization rate of between 1 and 10% of the total Pb 

for most of the samples (Figure 4b,f). About 5 to 25% of the total soil Pb was mobilized in the oxalic 

acid treatment (Figure 4e). 

3.6. The Mobility of Zn and Its Relationship with Mobilizable Fe 

Largely  unlike  As,  Cu,  and  Pb,  there  was  no  clear  relationship  between  the  rate  of  Zn 

mobilization and the amount of Fe released from the soils for the citric and malic acid treatments 

(Figure 5b,d). The tartaric acid‐extractable Zn percentage was only slightly related to the amount of 

Fe released from the soils (Figure 5f). 

 

 

 

y = 0.0587x + 7.9101

R² = 0.34870

5

10

15

20

25

0 50 100 150 200

Acetic Zn/Total Zn (%)

Acetic Fe (mg/kg)

(a)

y = 0.0015x + 16.373

R² = 0.0489

0

10

20

30

40

50

60

70

0 2000 4000 6000

Citric Zn/Total Zn (%)

Citric Fe (mg/kg)

(b)

y = 0.0151x + 13.969

R² = 0.0817

0

10

20

30

40

50

60

0 200 400 600 800 1000

Form

ic Zn/Total Zn (%)

Formic Fe (mg/kg)

(c)

y = −0.0007x + 24.066

R² = 0.0049

0

10

20

30

40

50

60

70

80

90

0 2000 4000 6000

Malic Zn/Total Zn (%)

Malic Fe (mg/kg)

(d)

y = −0.0048x + 80.157

R² = 0.24980

10

20

30

40

50

60

70

80

90

100

0 5000 10000 15000

Oxalic Zn/Total Zn (%)

Oxalic Fe (mg/kg)

(e)

y = 0.0024x + 16.4

R² = 0.1893

0

5

10

15

20

25

30

35

40

0 1000 2000 3000 4000 5000

Tartaric Zn/Total Zn (%)

Tartaric Fe (mg/kg)

(f)

Figure 5. Relationship between the amount of Fe released from the soil and the rate of Zn mobilizationin (a) acetic acid; (b) citric acid; (c) formic acid; (d) malic acid; (e) oxalic acid; and (f) tartaricacid treatments.

Toxics 2017, 5, 18 10 of 16

On the other hand, the acetic acid-extractable Zn percentage showed a relationship with theamount of released Fe (Figure 5a), and the oxalic acid-extractable Zn percentage was even negativelyrelated to oxalic acid-extractable Fe (Figure 5e). The poor relationship between the Zn extractablepercentage and extractable Fe for the formic acid treatment was consistent with those for As, Cu, andPb. In general, there was a markedly higher rate of Zn mobilization, as compared to other investigatedelements, especially for the acetic and formic acid treatments.

3.7. The Relationship between HNO3-Extractable Fraction and Oxalic Acid-Extractable Fraction

There was no clear relationship between the HNO3-extractable form and the oxalic form for As,Fe, and Pb (Figure 6a,c,e). In contrast, HNO3-extractable Cu, Mn, and Zn were closely related to oxalicCu, Mn, and Zn, respectively (Figure 6b,d,f). The slope for HNO3-extractable Cu vs. oxalic Cu andHNO3-extractable Mn vs. oxalic Mn is close to 1 (Figure 6b,d), while the slope of the HNO3-extractableZn vs. oxalic Zn is more than 1.5 (Figure 6f).

Toxics 2017, 5, 18   10 of 16 

Figure 5. Relationship between the amount of Fe released from the soil and the rate of Zn mobilization 

in  (a) acetic acid,  (b) citric acid,  (c)  formic acid,  (d) malic acid,  (e) oxalic acid, and  (f)  tartaric acid 

treatments. 

On  the other hand,  the acetic acid‐extractable Zn percentage showed a  relationship with  the 

amount of released Fe (Figure 5a), and the oxalic acid‐extractable Zn percentage was even negatively 

related  to oxalic acid‐extractable Fe  (Figure 5e). The poor relationship between  the Zn extractable 

percentage and extractable Fe for the formic acid treatment was consistent with those for As, Cu, and 

Pb.  In  general,  there  was  a  markedly  higher  rate  of  Zn  mobilization,  as  compared  to  other 

investigated elements, especially for the acetic and formic acid treatments. 

3.7. The Relationship between HNO3‐Extractable Fraction and Oxalic Acid‐Extractable Fraction 

There was no clear relationship between the HNO3‐extractable form and the oxalic form for As, 

Fe, and Pb (Figure 6a,c,e). In contrast, HNO3‐extractable Cu, Mn, and Zn were closely related to oxalic 

Cu, Mn, and Zn, respectively (Figure 6b,d,f). The slope for HNO3‐extractable Cu vs. oxalic Cu and 

HNO3‐extractable Mn vs. oxalic Mn is close to 1 (Figure 6b,d), while the slope of the HNO3‐extractable 

Zn vs. oxalic Zn is more than 1.5 (Figure 6f). 

 

 

y = −0.3514x + 200.3

R² = 0.0076

0

50

100

150

200

250

300

350

400

450

0 50 100 150

Oxalic As (m

g/kg)

HNO3‐extractable As (mg/kg)

(a)

y = 0.9274x + 7.746

R² = 0.7447

0

10

20

30

40

50

60

70

80

0 20 40 60

Oxalic Cu (mg/kg)

HNO3‐extractable Cu (mg/kg)

(b)

y = 0.3371x + 6256.4

R² = 0.07770

2000

4000

6000

8000

10000

12000

0 2000 4000 6000

Oxalic Fe (m

g/kg)

HNO3‐extractable Fe (mg/kg)

(c)

y = 1.0862x + 40.851

R² = 0.86860

50

100

150

200

250

300

350

400

450

500

0 100 200 300 400

Oxalic M

n (mg/kg)

HNO3‐extractable Mn (mg/kg)

(d)

Figure 6. Cont.

Toxics 2017, 5, 18 11 of 16Toxics 2017, 5, 18   11 of 16 

 

Figure 6. Relationship between the HNO3‐extractable fraction and the oxalic acid‐extractable fraction 

for (a) As, (b) Cu, (c) Fe, (d) Mn, (e) Pb, and (f) Zn. 

3.8. The Relationship between the HNO3‐Extractable Fraction and the Citric Acid‐Extractable Fraction 

In contrast with the oxalic acid treatment, there was a very close relationship between the HNO3‐

extractable  fraction and  the citric acid extractable fraction  for all  the six  investigated  trace metals. 

However, the slope of regression line differed among the different elements. Fe had a slope of nearly 

1, the slope dropped to below 0.9 for Zn, Mn and As. The slope for Cu was only about 0.5 and Pb 

only had a slope of less than 0.3. The regression equation showed a negative intercept for As, Cu and 

Pb (Figure 7). 

 

y = 0.2834x + 42.228

R² = 0.0668

0

50

100

150

200

250

0 100 200 300

Oxalic Pb (mg/kg)

HNO3‐extractable Pb (mg/kg)

(e)

y = 1.5636x + 5.4014

R² = 0.73790

10

20

30

40

50

60

70

0 10 20 30 40

Oxalic Zn (mg/kg)

HNO3‐extractable Zn (mg/kg)

(f)

y = 0.7808x − 4.0412

R² = 0.9416

0

10

20

30

40

50

60

70

80

90

0 50 100 150

Citric As (m

g/kg)

HNO3‐extractable As (mg/kg)

y = 0.533x − 4.5706

R² = 0.9052

0

5

10

15

20

25

30

0 20 40 60

Citric Cu (mg/kg)

HNO3‐extractable Cu (mg/kg)

(a) (b)

Figure 6. Relationship between the HNO3-extractable fraction and the oxalic acid-extractable fractionfor (a) As; (b) Cu; (c) Fe; (d) Mn; (e) Pb; and (f) Zn.

3.8. The Relationship between the HNO3-Extractable Fraction and the Citric Acid-Extractable Fraction

In contrast with the oxalic acid treatment, there was a very close relationship between theHNO3-extractable fraction and the citric acid extractable fraction for all the six investigated tracemetals. However, the slope of regression line differed among the different elements. Fe had a slope ofnearly 1, the slope dropped to below 0.9 for Zn, Mn and As. The slope for Cu was only about 0.5 andPb only had a slope of less than 0.3. The regression equation showed a negative intercept for As, Cuand Pb (Figure 7).

Toxics 2017, 5, 18   11 of 16 

 

Figure 6. Relationship between the HNO3‐extractable fraction and the oxalic acid‐extractable fraction 

for (a) As, (b) Cu, (c) Fe, (d) Mn, (e) Pb, and (f) Zn. 

3.8. The Relationship between the HNO3‐Extractable Fraction and the Citric Acid‐Extractable Fraction 

In contrast with the oxalic acid treatment, there was a very close relationship between the HNO3‐

extractable  fraction and  the citric acid extractable fraction  for all  the six  investigated  trace metals. 

However, the slope of regression line differed among the different elements. Fe had a slope of nearly 

1, the slope dropped to below 0.9 for Zn, Mn and As. The slope for Cu was only about 0.5 and Pb 

only had a slope of less than 0.3. The regression equation showed a negative intercept for As, Cu and 

Pb (Figure 7). 

 

y = 0.2834x + 42.228

R² = 0.0668

0

50

100

150

200

250

0 100 200 300

Oxalic Pb (mg/kg)

HNO3‐extractable Pb (mg/kg)

(e)

y = 1.5636x + 5.4014

R² = 0.73790

10

20

30

40

50

60

70

0 10 20 30 40

Oxalic Zn (mg/kg)

HNO3‐extractable Zn (mg/kg)

(f)

y = 0.7808x − 4.0412

R² = 0.9416

0

10

20

30

40

50

60

70

80

90

0 50 100 150

Citric As (m

g/kg)

HNO3‐extractable As (mg/kg)

y = 0.533x − 4.5706

R² = 0.9052

0

5

10

15

20

25

30

0 20 40 60

Citric Cu (mg/kg)

HNO3‐extractable Cu (mg/kg)

(a) (b)

Figure 7. Cont.

Toxics 2017, 5, 18 12 of 16Toxics 2017, 5, 18   12 of 16 

 

 

Figure 7. Relationship between the HNO3‐extractable fraction and the citric acid‐extractable fraction 

for (a) As, (b) Cu, (c) Fe, (d) Mn, (e) Pb, and (f) Zn. 

3.9. The Relationship between the HNO3‐Extractable Fraction and the Malic Acid‐Extractable Fraction 

Largely  similar  to  the  citric  acid  treatment,  there was  a very  close  relationship between  the 

HNO3‐extractable  fraction and  the malic acid extractable  fraction  for all  the six  investigated  trace 

elements (Figure 8). However, the slope of regression line differed among the different elements. Fe 

had the highest slope (0.9391), followed by Mn (0.8377), Zn (0.7970), As (0.6976), and Cu (0.5119). Pb 

only had a slope of less than 0.2. The regression equation showed a negative intercept for As, Cu, and 

Pb (Figure 8a,b,e). 

y = 1.0072x + 107.88

R² = 0.9738

0

1000

2000

3000

4000

5000

6000

0 2000 4000 6000

Citric Fe (m

g/kg)

HNO3‐extractable Fe (mg/kg)

y = 0.843x + 10.696

R² = 0.9799

0

50

100

150

200

250

300

350

0 100 200 300 400

Citric Mn (mg/kg)

HNO3‐extractable Mn (mg/kg)

y = 0.2995x − 13.452

R² = 0.8097

0

10

20

30

40

50

60

70

0 100 200 300

Citric Pb (mg/kg)

HNO3‐extractable Pb (mg/kg)

y = 0.8638x + 0.1516

R² = 0.8265

0

5

10

15

20

25

30

35

0 10 20 30 40

Citric Zn (mg/kg)

HNO3‐extractable Zn (mg/kg)

(c) (d)

(e) (f)

Figure 7. Relationship between the HNO3-extractable fraction and the citric acid-extractable fractionfor (a) As; (b) Cu; (c) Fe; (d) Mn; (e) Pb; and (f) Zn.

3.9. The Relationship between the HNO3-Extractable Fraction and the Malic Acid-Extractable Fraction

Largely similar to the citric acid treatment, there was a very close relationship between theHNO3-extractable fraction and the malic acid extractable fraction for all the six investigated traceelements (Figure 8). However, the slope of regression line differed among the different elements.Fe had the highest slope (0.9391), followed by Mn (0.8377), Zn (0.7970), As (0.6976), and Cu (0.5119).Pb only had a slope of less than 0.2. The regression equation showed a negative intercept for As, Cu,and Pb (Figure 8a,b,e).

Toxics 2017, 5, 18 13 of 16Toxics 2017, 5, 18   13 of 16 

 

 

 

Figure 8. Relationship between the HNO3‐extractable fraction and the malic acid‐extractable fraction 

for (a) As, (b) Cu, (c) Fe, (d) Mn, (e) Pb, and (f) Zn. 

4. Discussion 

The poor  relationship between  the oxalic acid‐extractable Fe and  the extractable Fe by other 

organic acids (Table 1) suggests that the dominant mechanism responsible for mobilization of Fe in 

the oxalic acid  treatment was  significantly different  from  those  in other organic  acid  treatments. 

Dissolution of iron oxides by organic acids involves the initial adsorption of organic ligands on the 

iron oxide surface and the subsequent release of iron ions from the solid surfaces through either non‐

y = 0.6976x − 6.2961

R² = 0.942

0

10

20

30

40

50

60

70

80

0 50 100 150

Malic As (m

g/kg)

HNO3‐extractable As (mg/kg)

(a)

y = 0.5119x − 4.4695

R² = 0.9206

0

5

10

15

20

25

30

0 20 40 60

Malic Cu (mg/kg)

HNO3‐extractable Cu (mg/kg)

(b)

y = 0.9391x − 275.26

R² = 0.9711

0

1000

2000

3000

4000

5000

6000

0 2000 4000 6000

Malic Fe (m

g/kg)

HNO3‐extractable Fe (mg/kg)

(c)

y = 0.8377x + 10.027

R² = 0.9727

0

50

100

150

200

250

300

350

0 100 200 300 400

Malic M

n (mg/kg)

HNO3‐extractable Mn (mg/kg)

(d)

y = 0.1841x − 8.7711

R² = 0.778

0

5

10

15

20

25

30

35

40

45

0 100 200 300

Malic Pb (mg/kg)

HNO3‐extractable Pb (mg/kg)

(e)

y = 0.797x + 1.7895

R² = 0.719

0

5

10

15

20

25

30

35

0 10 20 30 40

Malic Zn (mg/kg)

HNO3‐extractable Zn (mg/kg)

(f)

Figure 8. Relationship between the HNO3-extractable fraction and the malic acid-extractable fractionfor (a) As; (b) Cu; (c) Fe; (d) Mn; (e) Pb; and (f) Zn.

4. Discussion

The poor relationship between the oxalic acid-extractable Fe and the extractable Fe by otherorganic acids (Table 1) suggests that the dominant mechanism responsible for mobilization of Fein the oxalic acid treatment was significantly different from those in other organic acid treatments.Dissolution of iron oxides by organic acids involves the initial adsorption of organic ligands on theiron oxide surface and the subsequent release of iron ions from the solid surfaces through eithernon-reductive or reductive dissolution pathways [22]. The stronger capacity of oxalic acid, relative

Toxics 2017, 5, 18 14 of 16

to some other organic acids, to solubilize iron oxides was previously observed and attributed to thehigh affinity of the oxalate species to the iron oxide surfaces [23] and oxalic acid’s high acid strength,good complexing capacity, and reducing power [24]. The results obtained from this study are generallyconsistent with these findings. While the similar pattern observed for manganese may be, to someextent, due to the same reasons [25], the markedly reduced gap in extractable Mn between oxalicacid and other organic acids suggests that oxalic acid did not work much better than non-oxalic acidsin terms of mobilizing soil-borne Mn. This may be due to the fact that manganese oxides are moreresistant to oxalic acid-driven reduction, as compared to iron oxides. It is interesting to note that oxalicacid-extractable Mn was closely related to some of the non-oxalic acid-extractable Mn, suggesting thatMn tended to behave similarly in the presence of either oxalic acid or other organic acids in this study.Probably under the set experimental conditions, Mn mobilization was primarily driven by acidificationand complexation rather than reductive dissolution (when the soil-borne Mn reacts with oxalic acid).

Oxides of iron and manganese play important roles in binding arsenic and trace metals insoils [26–29]. Consequently, the high degree of similarity in the pattern of organic acid-extractablefractions observed for As, Cu, Pb, and Zn (Figure 1) may indicate that the release of these elements are,to a certain extent, associated with the dissolution of iron and manganese oxides in the presenceof organic acids. Like Fe, oxalic acid-extractable As and Pb were not related to the non-oxalicacid-extractable As and Pb, respectively. This appears to suggest that As and Pb in the oxalic acidsolution also behaved differently from those in other organic acid solutions. Oxalic acid was likely tomobilize certain As and Pb species that could not be easily solubilized by other organic acids.

The close relationship between the rate of As mobilization and the amount of Fe released fromthe soils for the citric, malic, and tartaric acid treatments suggests that these acids effectively corrodedthe surfaces of the iron oxide particles, leading to the mobilization of As and the trace metals that werebound to the mineral surfaces. In the case of oxalic acid treatment, the much stronger corrosion ofiron oxides led to the liberation of substantial amounts of iron from the deeper layers of iron oxideparticles that contained fewer trace metals and As. This may explain the poor relationship between therate of As mobilization and the amount of Fe released from the soils in the oxalic acid treatment. Theclose relationship among citric, formic, malic, and tartaric acid-extractable fractions for each element(Table 1) suggests that these organic acids behaved similarly in terms of solubilizing the trace metalsand As in the soils.

The close relationship between the HNO3-extractable fraction and the oxalic acid-extractablefraction for Cu, Mn, and Zn further confirms that the mobilization of these three metals in the oxalicacid treatment was predominantly driven by acidification, while the poor relationship between theHNO3-extractable fraction and the oxalic acid-extractable fraction for As, Fe, and Pb points to othermechanisms. The formation of Fe and Pb oxalate complexes, which is not necessarily dependent onpH condition, was likely to be the dominant process that kept these metals in the solution. This couldalso prevent the combination of arsenate or arsenite with Fe and Pb to form precipitates [30,31].

In contrast with oxalic acid treatment, there was a close relationship between the HNO3-extractablefraction and either the citric acid-extractable fraction or the malic acid-extractable fraction for all thesix investigated elements. This suggests that for these two organic acids, the major driving force formobilizing As and trace metals was similar to that for HNO3, i.e., acidification.

The research findings in this study have implications for evaluating the mobility of As and tracemetals in contaminated soils. While the traditional inorganic acid extraction procedure may, to certaindegree of reliability, allow estimation of mobilizable metal pools in the presence of many LMW organicacids, it fails to give any sensible indication of the oxalic acid-mobilizable pools of As and trace metals.Since different types of organic acids have different effects on mobilizing As and trace metals in soils.The composition of organic acids in rihzospheric soils is therefore very important in terms of thecontrols on the dynamics of trace metals and metalloids in soil-plant systems.

Toxics 2017, 5, 18 15 of 16

The results also provide information that can be used for developing soil remediation techniquessuch as soil washing and phytoextraction. Clearly oxalic acid is much more effective and efficient forenhancing the mobility and phytoavailability of soil-borne As and trace metals.

5. Conclusions

Under the set experimental conditions, LMWOAs behaved differently when reacting withsoil-borne trace metals and As. Oxalic acid and acetic acid had the strongest and weakest capacity tomobilize the six investigated elements, respectively. Malic, citric, and tartaric acids showed a similarelement-mobilizing capacity and formic acid had the capacity somewhere between this group of acidsand acetic acid for most of the elements. The differential effects of various LMWOAs on elementmobilization also varied from element to element with Mn and Zn showing smaller differences inmobility among the six LMWOAs, as compared to As and other trace metals.

It was likely that solubilisation of iron oxides by the LMWOAs played a critical role in mobilizingother trace metals and As. The driving force for the dissolution of iron oxides in the presence of oxalicacid was markedly different from that in the presence of other LMWOAs. Apart from acidification andcomplexation, reductive dissolution played a dominant role in the dissolution of iron oxides in thepresence of oxalic acid, while acidification tended to be more important for dissolving iron oxides inthe presence of other LMWOAs.

The unique capacity of oxalic acid to solubilize iron oxides tended to affect the mobilization ofother elements in different ways. For Cu, Mn, and Zn, acidification-driven mobilization was likely tobe dominant, while complexation might play a major role in Pb mobilization. The formation of solubleFe and Pb oxalate complexes could effectively prevent arsenate or arsenite from combining with thesemetals to form solid phases of Fe or Pb arsenate or arsenite.

Acknowledgments: The authors would like to thank Andrew Clark for his assistance with soil sampling and XRFanalysis, Tonye Georgewill for her assistance with soil sample collection and preparation, and Laurie Cunliffe forher assistance with the ICP analysis.

Author Contributions: O.E.N. and C.L. conceived and designed the experiments; O.E.N. performed theexperiments; C.L. and J.Q. analyzed the data; C.L. wrote the paper

Conflicts of Interest: The authors declare no conflicts of interest.

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