Effect of Fertilizer Application on Phytoremediating Potentials of Euphorbia heterophylla, Axonopus compressus, Emilia coccinea and Scoparia dulcis against Hg²⁺, Pb²⁺, Cd²⁺ and As³⁺

Introduction

Environmental pollution which has been present from the very beginning of life, but today, it is reaching worrying proportions worldwide that threatens the survival of mankind.^{1, 2} Soil is the fundamental foundation of our agricultural resources, food security, global economy and environmental quality. With the development of urbanization and industrialization, soils have become increasingly polluted by heavy metals and organic pollutants.³ Soil contamination is defined as the change in the soil properties due to accumulation and build- up in soils of harmful substances including toxic compounds.⁴ Soils may also be contaminated by the accumulation of heavy metals and metalloids through emissions from the rapidly expanding industrial areas, mine tailings, disposal of high metal wastes, leaded gasoline, paints, land application of fertilizers, animal manures, sewage sludge, pesticides, wastewater irrigation, coal combustion residues, spillage of petrochemicals, and atmospheric deposition.⁵ Heavy metals are those metals with specific density of more than 5 g/cm³ which are detrimental to the environment and anything that is beneficial to the environment.⁶ Heavy metals occur as natural constituents of the earth crust, and are persistent environmental contaminants since they cannot be degraded by chemical method but could be evacuated by physical method.^{7, 8} Some examples of the heavy metals include lead, cadmium, mercury, Arsenic, Copper, Nickel, Zinc and chromium.⁹ Pollution of the environment by heavy metals has been a global problem and the clean up using the common engineering methods being very expensive.¹⁰ Plants have shown to have the ability of absorbing both essential elements.^{11, 12, 13} and heavy metals from the soil. Phytoremediation which is cheap and environmentally friendly is a process that uses various types of plants to remove, transfer, stabilize, and/or destroy pollutants in the soil,  and water,^{14, 15} and includes   several processes namely, phytoextraction, phytodegradation, rhizofiltration, phytostabilization and phytovolatilization.¹⁶ Phytoextraction is contaminant uptake by the root with subsequent accumulation above ground portion of a plant. It is a contaminant removal process use for some heavy metals and metalloids like Pb, Cd, As, Se, Hg, Ni, Co, Zn, etc.¹⁷ Phytostabilization involves the establishment of a plant cover on the surface of the contaminated sites with the aim of reducing the translocation of pollutants and subsequent accumulation by roots.¹⁸ Phytovolatilization is extraction and release of elements to atmosphere in the form of gas compounds and it is important for mercury and arsenic.¹⁹ Phytotransformation/ phytodegradation process is the breakdown of pollutants taken up by plants through metabolic processes within the plant or the breakdown of contaminants externally to the plant through the effect of compounds produced by the plants .²⁰ In the previous works, various plants have been used in absorbing pollutants such as lead, cadmium, Zinc, Cobalt, chromium, arsenic, and various radionuclides from soils.^{21, 22, 23, 24, 25, 26, 27, 28, 29} It has been reported that Long-term use of excessive chemical fertilizers and organic manures in the bare vegetable field and the greenhouse vegetable field contributed to the accumulation heavy metals in the soils.³⁰ Various researchers have reported that fertilizer application increased the uptake of cadmium, arsenic, mercury and lead from the soil by some plants.^{31, 32, 33, 34, 35, 36, 37, 38, 39}

The aim of this work is to investigate the effect of organic manure and NPK fertilizers applications on uptake  of  Pb²⁺, Cd²⁺, Hg²⁺, and As³⁺ by some non-edible African plants since previous works have  reported that   application of fertilizer could increase the uptake of the metals.⁴⁰

Methods

Eighty-four seedlings of Euphorbia heterophylla, Axonopus compressus, Emilia coccinea and Scoparia dulcis were collected from Awka, State Capital of Anambra State Nigeria. Twenty one seedlings each, of Euphorbia heterophylla , Axonopus compressus, Emilia coccinea and Scoparia dulcis were grown on soils isolated in polyethene pots. Twenty seedling pots of each of the plant were inoculated with 20cm³ of 0.1M Cd(NO₃)₂·4H₂O and Pb(NO₃)₂, Hg(NO₃)₂, As₂O₃, buffer 7, Organic (organic manure) and Inorganic(NPK) fertilizers.  0.1M Cd²⁺ and Pb²⁺ were prepared by the method used by Anarado et al., 2019[21]. 0.1M solution of Hg(NO₃)₂ was prepared by dissolving 32.46g of mercuric nitrate in a mixture of 5 ml of nitric acid and 0.5dm³ of distilled water, and diluted with distilled water to 1dm³. 0.1M As₂O₃ was prepared by adding water to 19.78g of As₂O₃, heating mixture close to boiling point and NaOH crystals were added, while constantly stirring the solution. When dissolved, 2M solution of sulphuric acid was added and the solution made up to 1dm³ with distilled water. Controls were left. Plant parts were harvested after 14 weeks of inoculation. The harvested parts were washed, air-dried, ashed at 450⁰C, digested with aqua regia and amount of the metal ions concentrations taken up by parts of the plants was done using VARIAN AA240 Atomic Absorption Spectrophotometer. The pH of the soil sample was determined with pH meter.

Results and Discussions

Table 1: Concentration Of Pb²⁺  Taken up  By The Plants In mg/kg

Innoculant	Eh1	Eh2	Eh3	Ac1	Ac2	Ec1	Ec2	Ec3	Sd1	Sd2	Sd3
P	0.004	0.050	0.273	0.056	0.163	0.017	0.159	0.219	0.123	0.018	0.165
BP	0.039	0.123	0.043	0.035	0.043	0.015	0.020	0.284	0.001	0.113	0.175
BIP	0.002	0.074	0.236	0.271	0.853	0.140	0.234	0.024	0.230	0.190	0.000
BOP	0.057	0.071	0.407	0.167	0.138	0.004	0.020	0.276	0.056	0.035	0.000
IP	0.099	0.008	0.115	0.021	0.267	0.016	0.000	0.125	0.023	0.106	0.000
OP	0.024	0.020	0.167	0.263	0.203	0.056	0.159	0.219	0.010	0.067	0.000

Table 2: Concentration of Cd²⁺ Taken up  by The Plants in mg/kg

Innoculant	Eh1	Eh2	Eh3	Ac1	Ac2	Ec1	Ec2	Ec3	Sd1	Sd2	Sd3
C	0.057	0.268	0.026	0.200	0.390	0.098	0.269	0.650	1.521	1.331	0.843
BC	0.016	0.056	0.045	0.118	0.107	0.148	0.074	0.050	0.100	0.012	0.006
BIC	0.029	0.418	0.339	3.011	1.864	3.101	2.666	1.286	0.019	0.005	0.689
BOC	0.017	0.211	1.147	1.641	0.466	0.002	0.109	0.873	0.106	0.209	0.820
IC	0.045	0.222	0.268	0.591	1.802	0.050	2.036	0.066	1.847	1.143	1.500
OC	0.019	0.351	0.297	3.021	2.326	0.025	0.035	0.258	0.083	0.711	0.003

Table 3: Concentration of Hg²⁺ Taken up  by The Plants in mg/kg

Innoculant	Eh1	Eh2	Eh3	Ac1	Ac2	Ec1	Ec2	Ec3	Sd1	Sd2	Sd3
H	0.273	0.357	0.841	0.018	0.000	0.061	0.009	0.023	Dd	0.560	0.000
BH	0.135	0.175	0.236	0.001	0.004	0.045	0.077	0.080	Dd	0.001	0.007
BIH	0.138	0.171	0.169	0.006	0.013	0.050	0.052	0.050	Dd	1.302	0.000
BOH	0.113	0.169	0.122	0.019	0.011	0.050	0.077	0.065	Dd	0.024	0.182
IH	0.096	0.136	0.098	0.002	0.005	0.020	0.056	0.080	Dd	0.732	0.587
OH	0.092	0.116	0.127	0.015	0.001	0.030	0.050	0.087	Dd	1.021	0.872

Table 4: Concentration  of As³⁺ Taken up  by The Plants in mg/kg

Innoculant	Eh1	Eh2	Eh3	Ac1	Ac2	Ec1	Ec2	Ec3	Sd1	Sd2	Sd3
A	0.002	0.008	0.009	5.342	0.000	Dd	11.316	13.342	Dd	0.981	0.201
BA	0.004	0.009	0.196	Dd	Dd	Dd	5.639	10.166	Dd	0.005	0.002
BIA	0.005	0.007	0.027	Dd	Dd	Dd	18.340	11.130	Dd	1.809	0.812
BOA	Dd	Dd	Dd	Dd	Dd	Dd	2.753	10.907	Dd	0.501	1.311
IA	Dd	Dd	Dd	1.233	Dd	Dd	12.241	14.232	Dd	0.862	0.000
OA	0.014	0.019	0.015	Dd	Dd	Dd	6.817	10.913	Dd	0.000	0.221

pH of the soil = 6.3

CODES

Eh1, Eh2 and Eh3 = leaf, stem and root of Euphorbia heterophylla respectively.

Ac1 and Ac2 = shoot and root of Axonopus compressus respectively,

Ec1, Ec2 and Ec3 = leaf, stem and root of Emilia coccinea respectively

Sd1, Sd2 and Sd3 = leaf, stem and root of Scoparia dulcis respectively

P= lead, C= Cadmium, A= Arsenic, H= Mercury, O= Organic fertilizer, I= Inorganic fertilizer

Dd= Died

The results of the analyses showed that generally, the order of the metal ions absorption by the four plants follows the order; As> Cd> Hg> Pb.  Euphorbia heterophylla absorbed more of Cadmium and Mercury relative to Lead and Arsenic in the order; Cadmium>Mercury>Lead>Arsenic. Inorganic fertilizer application decreased the absorption of Pb²⁺ by Euphorbia heterophylla both at pH of 6.3 and 7 which was against the report of  Chu et al., 2018 that organic and inorganic fertilizer applications increased  lead absorption by Polygonum hydropiper L,⁴¹ Also organic manure application increased the absorption of the Pb²⁺ only in neutral condition(BP-BOP=0.205mg/kg-0.532mg/kg). Since the roots absorbed most of the metal ion except in BP, both organic and inorganic fertilizers can strengthen phytostabilization rate of E. heterophylla  to Pb, this is in line with the reports  Mendes  et al., 2006,⁴⁰ also that phytostabilization technique was good in remediating Pb from the soil.⁵ The reduction of lead concentration absorbed by the plant when the pH was increased from 6.3 to 7 was in line with the report of Traunfeld and Clement, 2001.⁴² Axonopus compressus, absorbed cadmium and arsenic relative to lead and mercury. Inorganic and organic fertilizer applications in A. compressus increased the uptake of lead ion both in acidic and neutral mediums. Those plants inoculated with inorganic fertilizers showed the absorption of the metal ion more in shoot regions, showing the inorganic fertilizers can strengthen the phytoextraction rate of the plant while organic fertilizer application can enhance the phytostabilization rate of the metal ion by the plant since most were absorbed in root.  Emilia coccinea generally absorbed As³⁺ and Cd²⁺ relative to Pb²⁺ and Hg²⁺. Application of inorganic fertilizer in neutral condition increased the absorption of lead, but decreased the absorption of lead in acidic condition. Fertilizer application enhanced phytostabilization of the metal ion by the plant since most of the ions were found in the roots. Scoparia dulcis absorbed more cadmium and arsenic relative to mercury and lead. Application of NPK fertilizer at pH of both 6.3 and 7 increased the absorption of lead by S. dulcis, but application of organic manure decreased the absorption. Increase in the pH decreased the absorption in line with Traunfeld and Clement, 2001.⁴² Generally the order of lead absorption by all the plants is as follows; Ac > Ec > Eh > Sd.   The order of absorption of Cd²⁺ by the plants is as follows; Ac > Ec> Sd > Eh.  Application of both organic and inorganic fertilizers increased the absorption of Cd²⁺ by  E. heterophylla  both at pH of 6.3 and 7- This is in line with the reports of  Sampanpanish and Wanapan, 2016 and Roberts, 2014  which stated that concentrations of Cd were found to increase when the application rate of fertilizer increased and fertilization increases the risk of Cd movement into the food chain,^43,44 most absorption occurred when organic manure was applied at pH of 7(1.375mg/kg)- This is in line with report of  Grant and Sheppard, 2008 that higher soil organic matter content will increase Cd adsorption.⁴⁵ Application of organic manure at pH of 7 and application of inorganic fertilizer at pH of 6.3 strengthened the phytostabilization rate of E. heterophylla. Application of both organic and inorganic fertilizers increased the absorption of Cd²⁺ by  A. compressus. Absorption occurred most when inoculated with organic fertilizer at pH of 6.3 (total = 5.347mg/kg). Application of organic manure enhanced phytoextraction of the metal ion at both pH of 6.3 and 7. Increase in the pH decreased the absorption of the ion – this is in line with the findings of Hattori et al., 2006 which stated that decrease in  pH increased the absorption of Cd.⁴⁶ Generally application of fertilizers decreased the absorption of Cd²⁺ by Emilia coccinea except with inorganic fertilizer at pH of 7. Also application of both fertilizers increased the absorption of cadmium, absorption was most when inorganic fertilizer was applied in neutral condition (7.053mg/kg)- This could be as result of Phosphorous fertilizer being the major anthropogenic source of Cd.⁴⁵ Increase in pH increased absorption. Application of inorganic fertilizer at both pH enhanced phytoextraction while application of organic fertilizer at pH of 7 enhanced phytostabilization. Scoparia dulcis absorbed most Cd²⁺when inorganic fertilizer was applied at pH of 6.3(total= 4.422mg/kg). Application of inorganic fertilizer at both pH increased the uptake of the metal ion by the plant, but only increased with organic fertilizer at pH of 7. Acidic condition strengthened phytoextraction. Increase in pH decreased the absorption of Hg²⁺ by E. heterophylla, A. compressus, S. dulcis , but increased the absorption with  E. coccinea. Application of both organic and inorganic fertilizers decreased the absorption of Hg²⁺ by E. heterophylla, E. coccinea and A. compressus (when inoculated at pH of 6.3)- This is against the findings of  Atafar et al., 2010.³¹ Application of the both fertilizers increased the absorption of the metal ion by S. dulcis and A. compressus (when inoculated at pH of  7). Increase in pH decreased the absorption of As³⁺ with S. dulcis  and E. coccinea and A. compressus, but increased absorption of the ion with E. heterophylla. E. coccinea showed a very good phytoremediating potential against As³⁺, it could be regarded as an arsenic hyperaccumulator . Though there were abscissions of the leaves of E. coccinea and S. dulcis. It was not supprising to see that As inoculation resulted in phytotoxicity of some parts of all the plants used which is in line with the report of  Kim, 2019 that As is phytotoxic⁴⁷ . Highest absorption of arsenic by E. coccinea was observed on addition of inorganic fertilizers at pH of 7(total =29.510 mg/kg) and 6.3(total= 26.473 mg/kg) which is against the report of Pigna et al., 2010 that P fertilization prevented As uptake.⁴⁸ Application of NPK fertilizer increased the absorption of As at both pH with E. coccinea, at only pH of 7 with S. dulcis. Application of organic manure decreased the absorption of ion at both pH with E. coccinea, increased absorption at pH of 6.3 with E. heterophylla and at pH of 7 with S. dulcis.

Conclusion

Heavy metal pollution of environment has been increasing with increase in industrialization and urbanization. Phytoremediation being green and inexpensive technique, capable of cleaning up of these metals from the environment was employed in this research. From this work, it could be concluded that application of fertilizers affected the metals’ uptake by the plants used. Though As was phytotoxic at some pH to some parts, E. coccinea showed very good phytoremediating potential against As and so could be used in an environment polluted by As³⁺.

Acknowledgement

We acknowledge the Nnamdi Azikiwe University Central Laboratory for providing the facilities for this research. We also thank the Botany Department of Nnamdi Azikiwe University for assisting in the plants’ identification.

Conflict of Interest

We wish to state that there is no conflict of interests in this work.

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