Scientific African 10 (2020) e00630

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Scientific African
journal homepage: www.elsevier.com/locate/sciaf

Search for autochthonous plants as accumulators and

translocators in a toxic metal-polluted coal mine soil in
Okaba, Nigeria
Eneojo Godwin Ameh a,∗, Daniel Oluwagbemiga Aina b
a
Federal University, Gusau, Zamfara, Faculty of Natural Sciences, Department of Geological Sciences, Nigeria
b
Kogi State University, Faculty of Natural Sciences, Department of Biological Sciences, P.M.B 1008 Anyigba, Nigeria

a r t i c l e i n f o a b s t r a c t

Article history: Increasing levels of toxic metals in soil due to natural processes (weathering of miner-
Received 4 September 2020 als, volcanic eruptions, and erosion) and anthropogenic activities (industrialization, urban-
Revised 22 October 2020
ization, and mining) are global problems. Coal mining activities pollute soils with toxic
Accepted 5 November 2020
metals. A valuable and inexpensive appealing technology known as phytoremediation can
be employed to remove and reduce the level of metal-pollution in soil. This study was
Keywords: conducted in a polluted coal mine soil within Okaba (Nigeria) to identify hyper accumula-
Okaba tor, phytoextractor and photo stabilizer plants based on the following indices: bioconcen-
Anambra basin tration factor (BCF), translocation factor (TF), and bioaccumulation coefficient (BAC). Both
Accumulation plant and soil samples were collected, prepared and digested using various acid concen-
Excluders trations and mixtures to achieve complete digestion. Heavy metal (As, Cd, Cr, and Cu) con-
Translocation
centrations from the digested samples were determined for both soil and plants in and
around the mine using EDX3600B X-ray Fluorescence Spectrometer. From this study, two
(2) plant species each have potential for phytoextraction and phytostabilization of As from
the soil. Also, Fuirena umbrellata Rottb and Selaginella myosurus were the only plants that
are suitable phytostabilizers of Cd. Arising from this study also, nine (9) plants species
have been identified as potential phytostabilizers of Cr. Only Hyptis Suaveolens Poit accu-
mulated >10 0 0mg/kg of Cu, and therefore, hyper accumulator of Cu while thirteen (13)
other species are suitable for phytostabilization of Cu. This study has shown that the na-
tive plants have the potential to naturally remove toxic metals from metal-polluted soils.
© 2020 The Authors. Published by Elsevier B.V. on behalf of African Institute of
Mathematical Sciences / Next Einstein Initiative.
This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/)

Introduction

Environmental pollution by heavy metals is a serious issue worldwide. It is associated with natural processes (e.g. weath-
ering of minerals, volcanic eruptions, and erosion, [5]) and anthropogenic activities (e.g. mining activities, industrial wastes
deposition and smelting of ores, [15]). Heavy metals are metals that have relatively high atomic and mass number > 20
and 5 g cm−3 . High toxic metal concentrations in soils as a result of these natural processes and anthropogenic activities

∗
Corresponding author.
E-mail address: [email protected] (E.G. Ameh).

https://doi.org/10.1016/j.sciaf.2020.e00630
2468-2276/© 2020 The Authors. Published by Elsevier B.V. on behalf of African Institute of Mathematical Sciences / Next Einstein Initiative. This is an
open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)
E.G. Ameh and D.O. Aina Scientific African 10 (2020) e00630

Fig. 1. Transfer of toxic heavy metals from soil to plants to humans and organism’s food to humans and their toxicity (After [2,3]).

release strong toxic effects referred to as environmental pollutants [9]. Accumulation of these metals in soils can raise the
risk of its access into food chain and consequently threatens human and animal’s health ([13]; Fig. 1). Heavy metals can be
classified as essential minerals (Copper, (Cu), Zinc (Zn), Chromium (Cr), Manganese (Mn), Nickel (Ni) and Iron (Fe) that are
required and important for normal plant development. However, when available in excess, they can adversely affect plant
development, processes involving photosynthesis and respiration [6]. The non-essential toxic metals Cd, Pb, Hg and As are
identified as very toxic with varied physiological and biochemical processes and of non-biological function in plants, yet are
toxic at low to moderate concentrations ([4,6]; Fig. 1).
Previous authors, although not limited to Fu and Wang [16], Venkatachalam et al. [38], Wang et al. [39] have documented
a number of physical, chemical and biological practices that can be utilized for heavy metal clean-up of contaminated soils.
These methods are mostly expensive and energy intensive, low efficiency, lengthy and complex treatments for a wide va-
riety of metals and formation of large amount of toxic sub-products [1]. Lately, phytoremediation (i.e. plant-mediated re-
mediation) is considered a tool for mitigating heavy metal contamination in soils. It is an environmentally friendly and
non-expensive practice [12]. Phytoextraction, phytostabilization, phytoevaporation, rhizofiltration and rhizodegradation are
diverse approaches encompassed within phytoremediation ([21,23]). Of all the approaches, phytoextractions received a note-
worthy importance in the field of environmental studies, because this technique is straight forward, fast and environmentally
friendly. It also enables plants to eliminate heavy metals from the soils within the environment by concentrating them in
their harvestable parts [40].
Due to stripping method of mining practice at Okaba coal mine, the presence of abandoned mine ponds and overburden
amid streams and farmlands provide real sources of metal contamination in the soil. In this study, BCF; TF and BAC were
all used to determine and identify plants that are suitable for phytoremediation [25,27,41,42]. Indigenous plants from the
surrounding mine area are usually used. This is because they are better in terms of their survival, growth, and reproduction
than foreign plants that may not be able to adapt to the new environment [26,42]. The aims of this study therefore, are to
determine the concentration of metals in native plants grown on soils contaminated by anthropogenic activities (coal mining
activities) and compare the concentration of metals in the aboveground biomass to those in roots and the soil. Other aims
of this research are also to evaluate, identify and recommend plant species that are suitable for phytoremediation purposes.
The following hypotheses were advanced to achieve the aims of this study (i) Coal mining activities can release toxic metals
into the soils and pollute the soils; (ii) indigenous plants can accumulate two or more metals from the soils and translocate

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E.G. Ameh and D.O. Aina Scientific African 10 (2020) e00630

Fig. 2. Geology and sample location map of the study area (modified after [29]).

same to the aboveground tissues, (iii) some of these plants could be hyperaccumulators, phytoextractors or stabilizers of the
toxic metals.

Materials and methods

Site characterization

The Nigeria coal measures occur within the Mamu (Lower Maastrichtian) and Nsukka Formations (Upper Maastrichtian
to Danian) [29,31]. The simple stratigraphic succession of Anambra Basin (Fig. 2) are the Nkporo shales (Campanian); Mamu
(Lower coal measures) Maastrichtian, Ajali sandstones and Nsukka Formation [10,29,31]. The coal-bearing sequence under
the current study is found in Mamu Formation (Lower Maastrichtian). In the Mamu Formation (Lower Coal Measures), coal
seams are found at several horizons with intercalations of shales/carbonaceous materials, mudstones, sandstones, and silt-
stones [30,31]. Conspicuous in the coal area are overburden, soil wastes, stream channels, abandoned mine ponds, and
agricultural land surrounded by villagers. The entire landscape has been devastated with no plan in place to reclaim the
soil. Consequently, the land and soils around the mine area are polluted and would require clean-up.

Plant and soil sampling

Twenty-one (21) plant species were collected from eight (8) different sampling points (Fig. 2). Each plant was collected
in duplicates making a total of Forty-two. Plants were collected based on availability and to represent the whole of the coal

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E.G. Ameh and D.O. Aina Scientific African 10 (2020) e00630

mine area. The plant species were carefully uprooted, rinsed with tap water, followed by deionized water and then separated
into roots, stems, and leaves [7,25,26,33,41]. The sampled plants were first oven-dried at 105 °C for 15 min to remove surface
water and then at 70 °C until constant weights were attained. The dried samples were ground to powder using a mortar and
pestle to enable it pass through a 100-mesh sieve [7,42]. The powdered plants were stored in a well-labeled polyethylene
bag for analysis.
Eighty-four (84) soil samples were collected (Fig. 2). Two soil samples were collected from the root zone of each plant
at 0–20 cm depth. Equal subsamples were collected from each sample, mixed thoroughly and homogenized to make a
composite. These composite soil samples were then dried in an oven for 6-h at 50 °C. The dried soil samples were grounded,
sieved through a 100-mesh and stored in a well-labeled polyethylene bags ready for analysis [11,26,41].

Plant and soil extraction

1.0 g of dry weight powdered plants were placed in a tube treated with 5 ml of a 5:1 mixture of aqua regia (HNO3 :
HCL) and Perchloric acid (HCLO4 ) and digested in an OI- analytical model 7295 microwave digestion system until complete
digestion was attained [11,42]. 1.0g of soil samples were digested in a 1:2:2 (V/V/V) HNO3 : HCL: HCLO4 mixture to achieve
total metal content extraction from the soil [26,28]. After cooling, the contents in the tube were filtered, centrifuged, de-
canted, diluted to 50 mL [26,42]. Metal concentrations in soil and plant samples were analyzed using the EDX3600B X-ray
Fluorescence Spectrometer (Sky ray Instruments Inc., USA) at the Centre for Nanotechnology and Advanced Material, Na-
tional Agency for Science and Engineering Infrastructure (World Bank Assisted Project), Akure, Nigeria. The analytical range
of elements with EDX3600B were between (Mg, Z = 12) and Uranium (U, Z = 92) (Plate 21) with high resolution, high ac-
curacy of 0.05%, and detection limits of 0.01ppm. For quality assurance, blanks and duplicates were also used with few trace
elements to ensure precision and accuracy. The differences between measured and certified values for analyzed metals were
within 5%. The internal standard applied to all measured elements and the recoveries of all elements were in the range of
97.50–100%.

Data evaluation and analysis

2.4.1 Bioconcentration factor (BCF): This is the ratio of metal concentration (mg/kg) in the root to the metal concentration
in soil [28,42].
2.4.2 Translocation factor (TF): This is defined as the ratio of metal concentration (mg/kg) in shoots to the metal concen-
tration in roots [26,36,42].
2.4.3 Biological accumulation coefficient (BAC): This is the concentration of metals in plant shoots divided by the metal
concentration in soil [26].
2.4.4 One-way analysis of variance (ANOVA) was performed to confirm data variability and validity using SPSS software
(20.0, SPSS, Inc., Chocago, IL, USA). The analysed results showed that all the data acquired were significant at P < 0.05
(Tables 1d, 2c, 3c and 4c). The descriptive statistics were also carried-out using the same SPSS.

Results and discussion

Arsenic (As)

The concentrations of As in soil from the study area ranged from 0.00 mg/kg to 1.40 mg/kg (Table 1a). These concen-
trations of As from Okaba coal area are lower than 05–20 mg/kg in the world average soil ([19]; 2001) and other standard
limits for unpolluted soils (Table 1b and c). Imperata cylindrica Linn showed the highest concentration value of 2.10mg/kg
in roots, followed by Urena lobata Linn (1.10mg/kg) and Uraria Picta (0.87 mg/kg) while the least concentration value of
0.00mg/kg was recorded in ABH,MCJ,SAB, SL, SAL and SVL.
Interestingly, ACL, EAH, FUR, GL, HIS, HP, ICL, LF, MCJ accumulated more As in their roots in nineteen (19) locations
compared to eighteen (18) locations where As concentrations were more (SM, SAL,SVL, SPB and ULL) in the soils. This
relatively higher As accumulation in roots is consistent with the work of Wu et al. [41]. The concentration of As in the
shoots of sampled species followed this order, Imperata cylindrica L. (2.52 mg/kg) > Uraria picta (0.65 mg/kg) >Urena lobata
Linn (0.45 mg/kg) >Eclipta alba (L) Hassk (0.40mg/kg). The least concentration value of 0.00mg/kg was observed in Aspila
bussei O. Hoffin. In eighteen (18) locations out of forty-two (42), plant species such as DV, EAH,GL,HP, ICL, MCJ, SM, SAB, SL,
SAL,SVL, SPB and ULL accumulated more As in their shoots than in roots (Table 1a and Fig. 3a). These higher accumulation
and translocation of As into the shoots implies tolerance of these native plants to As. The major mechanism in tolerance
species of plant appears to be compartmentalization of metal ions, which is sequestration in the vacuolar compartment,
which excludes them from cellular sites where cell division and respiration occur (Singh et al., 2010; [27]).
The ability of plants to accumulate metals in their roots is known as bioconcentration factor (BCF). The highest BCF
was recorded in Urena lobata Linn (3.67), followed by Selaginella mysosurus (SW) (2.67), Gleichenia linearis (2.36) and the
least value of (0.00) was recorded in ACL, ABH, FUR,HP, MCJ, PM, SAB, SL, SAL, SVL and SPB at various locations (Table 1a and
Fig. 3b). The TF ranged from 0.00 to 2.20. The highest value of TF (2.20) was recorded in Imperata cylindrica linn, followed by
2.10 in Hyptis suaveolens Poit, followed by 2.08 in Monechma ciliatum Jacq. and 2.00 in Urena lobata The least TF value of 0.00

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E.G. Ameh and D.O. Aina Scientific African 10 (2020) e00630

Table 1a
Concentration (mg/kg) of Arsenic in soils and plant tissues.

Plant species site no Soil Root Shoot BCF TF BAC

Ageratum conyzoides Linn ∗ ACL 6 0.00 0.10 0.02 0.00 0.20 0.00
Average values 5 0.14 0.11 0.02 0.79 0.18 0.14
0.07 0.11 0.02 0.79 0.19 0.14
Aspila bussei O. Hoffin ∗ ABH 8 0.00 0.00 0.00 0.00 0.00 0.00
Average values 7 0.12 0.01 0.01 0.08 1.00 0.08
0.06 0.01 0.01 0.04 0.50 0.04
Desmodium velutinum ∗ DV 3 1.40 0.11 0.20 0.08 1.82 0.14
Average values 2 0.30 0.20 0.36 0.67 1.80 1.20
0.85 0.16 0.28 0.38 1.81 0.67
Eclipta alba (L) Hassk ∗ EAH 4 0.21 0.22 0.40 1.05 1.82 1.90
Average values 5 0.14 0.26 0.32 1.86 1.23 2.29
0.16 0.24 0.36 1.46 1.53 2.10
Triumfetta rhiomdoidea Jacq. ∗ TRJ 3 1.40 0.31 0.22 0.22 0.71 0.16
Average values 1 0.42 0.32 0.16 0.76 0.50 0.38
0.91 0.32 0.19 0.49 0.61 0.27
Fuirena umbrellata Rottb ∗ FUR 4 0.21 0.14 0.10 0.67 0.71 0.48
Average values 6 0.00 0.11 0.04 0.00 0.36 0.00
0.21 0.13 0.07 0.67 0.54 0.24
Gleichenia linearis (Burns) ∗ GL 5 0.14 0.33 0.32 2.36 0.97 2.29
Average values 7 0.12 0.25 0.26 2.08 1.04 2.17
0.13 0.29 0.29 2.22 1.01 2.23
∗
Hyparrhenia involucrate stapf HIS 2 0.30 0.30 0.12 1.00 0.40 0.40
Average values 1 0.42 0.50 0.32 1.19 0.64 0.76
0.25 0.40 0.22 1.10 0.52 0.58
Hyptis suaveolens Poit ∗ HP 6 0.00 0.10 0.21 0.00 2.10 0.00
Average values 8 0.00 0.12 0.04 0.00 0.33 0.00
0.00 0.11 0.13 0.00 1.22 0.00
Imperata cylindrica (Linn) ∗ ICL 2 0.30 0.20 0.44 0.67 2.20 1.47
Average values 3 1.40 2.10 2.52 1.50 1.20 1.80
0.85 1.15 1.48 1.09 1.70 1.64
∗
Leptochloa filiformis LF 1 0.42 0.14 0.12 0.33 0.86 0.29
Average values 2 0.30 0.31 0.22 1.03 0.71 0.73
0.36 0.23 0.17 0.68 0.79 0.51
Monechma ciliatum Jacq. ∗ MCJ 7 0.12 0.00 0.01 0.00 0.00 0.08
Average values 6 0.00 0.12 0.25 0.00 2.08 0.00
0.06 0.06 0.13 0.00 1.04 0.04
Panicum maximum Jacq. ∗ PM 1 0.42 0.10 0.01 0.24 0.10 0.02
Average values 8 0.00 0.10 0.01 0.00 0.10 0.00
0.21 0.10 0.01 0.12 0.10 0.01
∗
Selaginella myosurus SM 5 0.14 0.21 0.22 1.50 1.04 1.57
Average values 7 0.12 0.32 0.36 2.67 1.10 3.00
0.13 0.27 0.29 2.09 1.07 2.29
Sida acuta Burm. F. ∗ SAB 6 0.00 0.00 0.01 0.00 0.00 0.00
Average values 4 0.21 0.10 0.02 0.48 0.20 0.09
0.21 0.05 0.02 0.24 0.10 0.05
Sida linifolia juss.excav. ∗ SL 8 0.00 0.00 0.02 0.00 0.00 0.00
Average values 5 0.14 0.04 0.03 0.29 0.75 0.21
0.07 0.02 0.03 0.29 0.75 0.21
Schwenckia ammericana Linn ∗ SAL 7 0.12 0.00 0.23 0.00 0.00 1.92
Average values 4 0.21 0.34 0.26 1.62 0.76 1.24
0.17 0.17 0.25 0.31 0.28 1.66
Spermacoce verticillata Linn ∗ SVL 8 0.00 0.00 0.10 0.00 0.00 0.00
Average values 2 0.30 0.40 0.32 1.33 0.80 1.07
0.15 0.20 0.21 0.67 0.40 0,53
Sporobolus pyramidalis Beauv ∗ SPB 1 0.42 0.20 0.21 0.48 1.05 0.50
Average values 6 0.00 0.02 0.01 0.00 0.50 0.00
0.21 0.11 0.11 0.24 0.78 0.25
∗
Urena lobata Linn ULL 7 0.12 0.10 0.26 0.83 2.00 1.67
Average values 2 0.30 1.10 0.45 3.67 0.41 1.50
0.21 0.60 0.33 2.25 1.21 1.59
Uraria Picta ∗ UP 3 1.40 0.87 0.65 0.62 0.75 0.46
Average values 5 0.14 0.12 0.11 0.86 0.92 0.79
0.77 0.50 0.38 0.74 0.84 0.63
∗
coded form of each plant.

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E.G. Ameh and D.O. Aina Scientific African 10 (2020) e00630

Table 1b
Summary statistics of As in soil and plant tissues.

Variables Minimum Maximum Mean Std. Deviation

Soil .00 1.40 .28 .39

Root .00 2.10 .25 .36
Shoot .00 2.52 .24 .39
BCF .00 3.67 .74 .85
TF .00 2.20 .79 .65
BAC .00 3.00 .73 .84

Table 1c
Standard trace/toxic metal limits in unpolluted soils.

Hansford, T
Shacklette and
Josphine, G. Kabata- Pendias,
Elements (mg/kg) [21], 2001 Boerngen, 1984) [7] [35] [10] 2001

As 05-20 - - 5.0 5.0 5.0

Cu 20-100 20.0 20.0 28.0

- -
Cd 05-30 - - - - -

Cr - 200.00 60.00 92.0 80.0

42.0

Table 1d
ANOVA analysis of data.

Variables Sum of Squares df Mean Square F Sig.

Root Between Groups .63 13 .05 .52 .04

Within Groups .66 7 .09
Total 1.29 20
Shoot Between Groups 1.12 13 .09 .77 .02
Within Groups .79 7 .11
Total 1.91 20
TF Between Groups 4.06 13 .31 1.45 .00
Within Groups 1.51 7 .22
Total 5.56 20
BAC Between Groups 10.52 13 .81 3.15 .01
Within Groups 1.80 7 .26
Total 12.32 20
BCF Between Groups 7.76 13 .60 1.81 .002
Within Groups 2.31 7 .33
Total 10.07 20
∗
Data significant at P<0.05.

was recorded in ABS, MCJ, SAB, SAL, and SVL. The BAC is the ability of the shoot/stem of plants to accumulate metals [26,33].
The BAC in the study area ranged from 0.00 to 3.00 (Table 1a and Fig. 3b). It’s highest in Selaginella myosurus (SW) plant
species with BAC of 3.00 while Gleichenia linearis (Burns) and Eclipta alba (L) Hassk recorded 2.29 and Imperata cylindrica
(Linn) recorded 1.80. The least BAC value of 0.00 was observed at various locations in ACL, ABH, FUR, HP, MCJ, PM, SAB, SL,
SVL and SPB.
According to Baker and Brooks [7] and Yoon et al. [42], hyperaccumulators are plants that can accumulate > 10 0 0 mg/kg
As in their shoots. Based on this criterion, no plant species was a hyperaccumulator of As. Plant species with values of BCF
and TF >1 are said to be suitable for phytoextraction while plant species with BCF>1 and TF<1 are suitable for phytostabi-
lization [25,26,42]. In this study, Eclipta alba (L) Hassk, Gleichenia linearis, Imperata cylindrica (Linn), and Selaginella myosurus
(SW) showed BCF, TF and BAC values > 1 (Table 1a and Fig. 3b), suggesting that these plant species are suitable for phy-
toextraction of As from the contaminated coal mine soil. This finding is in agreement with the work of Mellem et al. [24] in
which they recorded BCF and TF > 1 from A. dubius plant species for As. It is also interesting to note that Hyparrhenia
involucrata Stapf, Leptochloa filiformis, Schwenckia Americana Linn, Spermacoce verticillata Linn, and Urena lobata Linn have BCF
> 1 but TF values < 1 (Table 1a and Fig. 3b). These plant species are also useful in phytoremediation processes as they act
as phytostabilizers, thereby restricting As mobility and further soil contamination. This is consistent with the work of Wu
et al. [41] where BCFs > 1 and TFs < 1 were observed for A. Corniculatum, signifying good potentials for As phytostabiliza-
tion. The mean values of BCF, TF and BAC (Table 1b) were all higher than the mean values of As found in the soil, root, and
shoot. These imply that the native plants were more adapted to the soil and showed tolerant to As pollution.

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E.G. Ameh and D.O. Aina Scientific African 10 (2020) e00630

Fig. 3a. Average concentrations (mg/kg) of As in soil and sampled plant species.

Fig. 3b. Average variations of As in sampled plant tissues.

Fig. 4a. Average concentration (mg/kg) of Cd in soils and sampled plant tissues.

Cadmium (Cd)

The highest concentration of Cd in soil was 3.10 mg/kg and the least value was 0. /kg. This recorded value is below
the limit of 05–30 mg/kg for unpolluted soils ([19,20]; Table 1c). The accumulated Cd in roots of plant species varied from
0.00 mg/kg to 1.45 mg/kg with Spermacoce verticillata Linn recording the highest value of 1.45 mg/kg. This is followed by
1.41 mg/kg and 1.20 mg/kg accumulations in the roots of Selaginella mysorus and Panicum maximum respectively (Table 2a
and b). The least Cd value of 0.00 mg/kg was recorded in ACL, HP, ICL, LF, PM, SL, and SPB at various locations. The accu-
mulated Cd in plant’s roots in the study area is lower than the 5.20–9.13 mg/kg recorded in Eichhornia crassipes in a similar
study [36].

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E.G. Ameh and D.O. Aina Scientific African 10 (2020) e00630

Table 2a
Concentration of Cd (mg/kg) in soils and plant tissues.

Plant species Site no Soil Root Shoot BCF TF BAC

Ageratum conyzoides Linn ∗ ACL 6 0.16 0.00 0.20 0.00 0.00 1.25
Average value 5 0.12 0.01 0.02 0.08 2.00 0.17
0.14 0.005 0.11 0.04 1.00 1.34
Aspila bussei O. Hoffin ∗ ABH 8 3.10 0.11 0.21 0.04 1.91 0.07
Average value 7 1.40 0.25 0.26 0.18 1.04 0.19
2.25 0.18 0.24 0.11 1.48 0.13
Desmodium velutinum ∗ DV 3 2.15 0.01 0.00 0.00 0.00 0.00
Average value 2 1.30 0.20 0.31 0.15 1.55 0.19
1.73 0.11 0.16 0.08 0.78 0.10
∗
Eclipta alba (L) Hassk EAH 4 0.29 0.22 0.21 0.76 0.95 0.72
Average value 5 0.12 0.25 0.14 2.08 0.56 1.17
0.21 0.24 0.18 1.42 0.76 0.95
Triumfetta rhiomdoidea Jacq. ∗ TRJ 3 2.15 0.03 0.04 0.01 1.33 0.02
Average value 1 0.21 0.06 0.04 0.29 0.67 0.19
1.18 0.05 0.04 0.15 1.00 0.11
Fuirena umbrellata Rottb ∗ FUR 4 0.29 0.31 0.22 1.07 0.71 0.76
Average value 6 0.16 0.26 0.18 1.63 0.69 1.13
0.23 0.29 0.20 1.35 0.70 0.95
∗
Gleichenia linearis (Burns) GL 5 0.12 0.01 0.01 0.08 1.00 0.08
Average value 7 1.40 0.65 0.84 0.46 1.29 0.57
0.76 0.33 0.43 0.27 1.15 0.33
∗
Hyparrhenia involucrate stapf HIS 2 1.30 0.01 0.00 0.01 0.00 0.00
Average value 1 0.21 0.02 0.06 0.09 0.50 0.05
0.76 0.02 0.03 0.05 0.25 0.03
Hyptis suaveolens Poit ∗ HP 6 0.16 0.00 0.08 0.00 0.00 0.50
Average value 8 3.10 0.75 0.85 0.24 1.13 0.27
1.63 0.38 0.47 0.12 0.57 0.39
∗
Imperata cylindrica (Linn) ICL 2 1.30 0.00 0.02 0.00 0.00 0.02
Average value 3 2.15 0.84 2.00 0.39 2.38 0.93
2.20 0.42 1.01 0.20 1.19 0.48
∗
Leptochloa filiformis LF 1 0.21 0.00 0.15 0.00 0.00 0.71
Average value 2 1.30 0.78 0.86 0.60 1.10 0.66
0.76 0.39 0.51 0.30 0.55 0.69
Monechma ciliatum Jacq. ∗ MCJ 7 1.40 0.04 0.05 0.03 1.25 0.04
Average value 6 0.16 0.01 0.01 0.06 1.00 0.06
0.78 0.03 0.03 0.05 1.13 0.05
Panicum maximum Jacq. ∗ PM 1 0.21 0.00 0.12 0.00 0.00 0.57
Average value 8 3.10 1.20 1.01 0.39 0.84 0.33
1.66 0.60 0.57 0.20 0.42 0.45
Selaginella myosurus ∗ SM 5 0.12 0.21 0.16 1.75 0.76 1.33
Average value 7 1.40 1.41 1.08 1.01 0.77 0.77
0.76 0.81 0.62 1.38 0.77 1.00
Sida acuta Burm. F. ∗ SAB 6 0.16 0.10 0.20 0.63 2.00 1.25
Average value 4 0.29 0.06 0.16 0.21 2.67 0.55
0.23 0.08 0.18 0.42 2.34 0.90
Sida linifolia juss.excav. ∗ SL 8 3.10 0.00 0.07 0.00 0.00 0.02
Average value 5 0.12 0.16 0.02 1.33 0.13 0.17
1.61 0.08 0.05 0.67 0.07 0.10
Schwenckia ammericana Linn ∗ SAL 7 1.40 0.04 0.06 0.03 1.50 0.04
Average value 4 0.29 0.30 0.32 1.03 1.07 1.10
0.85 0.17 0.19 0.53 1.29 0.57
Spermacoce verticillata Linn ∗ SVL 8 3.10 0.12 0.20 0.04 1.67 0.06
Average value 2 1.30 1.45 1.02 1.12 0.68 0.78
2.20 0.79 0.61 0.58 1.18 0.42
Sporobolus pyramidalis Beauv ∗ SPB 1 0.21 0.00 0.02 0.00 0.00 0.10
Average value 6 0.16 0.09 0.10 0.56 1.11 0.63
0.19 0.05 0.06 0.28 0.56 0.37
Urena lobata Linn ∗ ULL 7 1.40 0.03 0.04 0.02 1.33 0.03
Average value 2 1.30 0.02 0.03 0.02 1.50 0.02
1.35 0.03 0.04 0.02 1.42 0.03
Uraria Picta ∗ UP 3 2.15 0.04 0.02 0.02 0.50 0.01
Average values 5 0.12 0.08 0.10 0.67 1.25 0.83
1.14 0.06 0.06 0.35 0.88 0.42
∗
coded form of each plant.

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E.G. Ameh and D.O. Aina Scientific African 10 (2020) e00630

Table 2b
Summary statistics of Cd in soil and plant tissues.

Variables Minimum Maximum Mean Std. Deviation

Soil .12 3.10 1.05 1.02

Root .00 1.45 .24 .38
Shoot .00 2.00 .27 .41
BCF .00 2.08 .41 .55
TF .00 2.67 .92 .70
BAC .00 1.33 .44 .43

Table 2c
ANOVA analysis of data.

Variables Sum of Squares Df Mean Square F Sig.

Root Between .81 15 .05 .66 .01

Groups
Within .41 5 .08
Groups
Total 1.22 20
Shoot Between 5.23 15 .35 6.26 .00
Groups
Within .28 5 .06
Groups
Total 5.51 20
TF Between 15628.74 15 1041.92 .00
Groups 2933.90
Within 1.78 5 .36
Groups
Total 15630.52 20
BAC Between 2.33 15 .16 1.44 .04
Groups
Within .54 5 .11
Groups
Total 2.87 20
BCF Between 2.42 15 .16 .51 .00
Groups
Within 1.57 5 .32
Groups
Total 3.99 20
∗
data significant at P<0.05.

Fig. 4b. Average variation of Cd in soil and plant tissues.

The concentration of Cd in shoots ranged from 0.00 to 2.00 mg/kg (Table 2b and Fig. 4a). The highest accumulation was
observed in Imperata cylindrica Linn (2.00 mg/kg), followed by Selaginella myosurus (1.08 mg/kg) and Spermacoce verticillata
linn (1.02 mg/kg). Desmodium velutinum and Hyparrhenia involucrate Stapf recorded least value of 0.00 mg/kg.
Accumulated Cd in the shoot of plant’s species under investigation is lower than the > 100 mg/kg in Marigold shoot and
5.91 mg/kg in Panicum antidotale shoot (Rungruang et al., 2011; [36]). One of the criteria for a hyperaccumulator plant is
the ability of the plant to accumulate Cd > 10 0.0 0 mg/kg [14,34] in its above-ground level. Based on this criterion, no plant
species in this study meets this requirement as a hyperaccumulator of Cd (Table 2a).

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E.G. Ameh and D.O. Aina Scientific African 10 (2020) e00630

Fig. 5a. Average concentration (mg/kg) of Cr in soil and sampled plant tissues.

Fig. 5b. Average variations of Cr in sampled plant tissues.

The BCF in the area varied from 0.00 to 2.08 mg/kg (Table 2a). The highest BCF (2.08) was observed in Eclipta alba (L)
Hassk, followed by Selaginella myosurus (1.75) and Fuirena umbrellata Rottb (1.63). Five (5) other plants at different locations
recorded least BCF value of 0.00. The TF recorded varied from 0.00 to 2.67 (Table 2a and Fig. 4b). The highest TF (2.67)
was observed in Sida acuta Burm, this is followed by Imperata cylindrica linn (2.38) and Ageratum conyzoides linn (2.00).
Nine (9) plants out of 21 recorded least value of 0.00. Of all the plant species, only Schwenckia Americana linn recorded BCF
(1.03) and TF (1.07) in location (4) and it is the only plant under investigation that is suitable for phytoextraction of Cd.
This is a clear indication that almost all the plants cannot store and transfer Cd to their above-ground tissues. On the other
hand, Eclipta alba (L) Hassk at location 5, Fuirena umbrellata Rottb, Selaginella myosurus, Sida linifolia juss. excav. at location
5 and Spermacoce verticillata linn at location 2 recorded BCF > 1 and TF < 1(Table 2a and Fig. 4b). These five species are
potential plants for Cd stabilization in the area under investigation. This BCF>1 and TF<1 suggests that only five species can
remove Cd from soil and store in their roots. These findings are in agreement with the result of B. chinensis used for both
phytoextraction and phytostabilization of Cd [17,37]. The obtained mean values of BCF, TF, and BAC (Fig. 4b) for Cd indicated
that most plants had little or no tolerance to the presence of Cd in the soil. This is because few of these plants have BCF,
TF and BAC >1. This implies that most of these plants under investigation possess little ability to store and transfer Cd to
above ground tissues (Singh et al., 2010; [27])

Chromium (Cr)

The concentration of Cr in the soil ranged from 0.11 to 35.00 mg/kg. Eleven soil locations recorded least value of
0.11 mg/kg (Table 3a and Table 3b). The obtained value is lower than the toxic metal limits reported by Kabata-Pendias
and Pendias [19]; Baker and Brooks [7] and Shacklette et al. [35] in unpolluted soils (Table 1c).
On the other hand, Cr accumulation in roots of plant species varied from 0.00 to 63.00 mg/kg (Table 3a and Table 3b). The
Sida acuta Burm recorded the highest value of 63.00 mg/kg in the roots. The least value of 0.00 mg/kg was accumulated in
Gleichenia linearis (Burns) and Spermacoce verticillata linn. This is higher than 7.20 mg/kg reported by Singh et al. [36] for
Malvestrum coromandilianum roots but lower than 16 to 310 mg/kg observed in roots from another study carried-out by [24].
The observed low concentrations of Cr in soils could be due to the ability of these plant species to accumulate Cr in their
roots. The Cr content in the shoots ranged from 0.00 to 70.08 mg/kg (Table 3a and Fig. 5a). The highest accumulated value

10
E.G. Ameh and D.O. Aina Scientific African 10 (2020) e00630

Table 3a
Concentration of Cr (mg/kg) in soils and plant tissues.

Plant species Site no Soil Root Shoot BCF TF BAC

∗
Ageratum conyzoides Linn ACL 6 35.00 62.00 25.10 1.77 0.40 0.72
Average value 5 0.11 0.21 0.16 1.91 0.76 1.45
17.56 31.11 12.63 1.84 0.58 1.09
Aspila bussei O. Hoffin ∗ ABH 8 0.11 0.20 0.10 1.82 0.50 0.91
Average value 7 0.31 0.52 0.75 1.68 1.44 2.42
0.21 0.36 0.43 1.75 0.97 1.67
Desmodium velutinum ∗ DV 3 0.12 0.10 0.08 0.83 0.80 0.67
Average value 2 0.22 6.10 0.10 2.77 0.02 0.45
0.17 3.10 0.09 1.80 0.41 0.56
Eclipta alba (L) Hassk ∗ EAH 4 0.12 0.17 0.10 1.42 0.59 0.83
Average value 5 0.11 0.20 0.04 1.82 0.20 0.36
0.12 0.19 0.07 1.62 0.40 0.60
Triumfetta rhiomdoidea Jacq. ∗ TRJ 3 0.12 0.24 0.01 2.00 0.04 0.08
Average value 1 0.51 0.86 1.00 1.69 1.16 1.96
0.32 0.55 0.51 1.85 0.60 1.02
Fuirerina umbrellata Rottb ∗ FUR 4 0.12 0.21 0.34 1.75 1.62 2.83
Average value 6 35.00 12.02 20.15 0.34 1.68 0.58
17.57 6.12 10.25 1.05 1.65 1.71
Gleichenia linearis (Burns) ∗ GL 5 0.11 0.00 0.15 0.00 0.00 1.36
Average value 7 0.31 0.01 0.00 0.03 0.00 0.00
0.21 0.01 0.15 0.03 0.00 1.36
Hyparrhenia involucrate stapf ∗ HIS 2 0.22 0.30 0.20 1.36 0.67 0.91
Average value 1 0.51 0.96 0.73 1.88 0.76 1.43
0.37 0.63 0.47 1.62 0.72 1.17
∗
Hyptis suaveolens Poit HP 6 35.00 58.00 30.02 1.66 0.52 0.86
Average value 8 0.11 0.16 0.06 1.45 0.38 0.55
17.50 29.08 15.04 1.56 0.45 0.71
Imperata cylindrica (Linn) ∗ ICL 2 0.22 0.01 0.00 0.05 0.00 0.00
Average value 3 0.12 0.03 0.01 0.25 0.33 0.08
0.17 0.02 0.005 0.15 0.33 0.08
Leptochloa filiformis ∗ LF 1 0.51 0.43 0.58 0.84 1.35 1.14
Average value 2 0.22 0.19 0.31 0.86 1.63 1.41
0.37 0.31 0.45 0.85 1.49 1.28
Monechma ciliatum Jacq. ∗ MCJ 7 0.31 0.05 0.00 0.16 0.00 0.00
Average value 6 35.00 51.82 30.02 1.48 0.58 0.86
17.66 29.94 15.01 0.82 0.58 0.86
Panicum maximum Jacq. ∗ PM 1 0.51 0.40 0.01 0.78 0.03 0.02
Average value 8 0.11 0.01 0.00 0.09 0.00 0.00
0.31 0.21 0.01 0.44 0.03 0.02
Selaginella myosurus ∗ SM 5 0.11 0.21 0.14 1.91 0.67 1.27
Average value 7 0.31 0.48 0.56 1.55 1.17 1.82
0.21 0.35 0.35 1.73 0.92 1.55
Sida acuta Burm. F. ∗ SAB 6 35.00 63.00 50.04 1.80 0.79 1.43
Average value 4 0.12 0.35 0.14 2.92 0.40 1.17
17.56 31.68 25.09 2.36 0.60 1.30
Sida linifolia juss.excav ∗ SL 8 0.11 0.01 0.01 0.09 1.00 0.09
Average value . 5 0.11 0.10 0.11 0.91 1.10 1.00
0.11 0.06 0.06 0.50 1.05 0.55
∗
Schwenckia ammericana Linn SAL 7 0.31 0.16 0.10 0.52 0.63 0.32
Average value 4 0.12 0.10 0.03 0.83 0.30 0.25
0.22 0.13 0.07 0.68 0.47 0.29
∗
Spermacoce verticillata Linn SVL 8 0.11 0.00 0.11 0.00 0.00 1.00
Average value 2 0.22 0.35 0.28 1.59 0.80 1.27
0.17 0.35 0.20 1.59 0.40 1.14
Sporobolus pyramidalis Beauv ∗ SPB 1 0.51 0.13 0.27 0.25 2.25 0.53
Average value 6 35.00 60.18 70.08 1.72 1.16 2.00
17.76 30.16 35.18 0.99 1.71 1.27
∗
Urena lobata Linn ULL 7 0.31 0.06 0.01 0.19 0.17 0.03
Average value 2 0.22 0.33 0.12 1.50 0.36 0.55
0.27 0.20 0.07 0.85 0.27 0.29
Uraria Picta ∗ UP 3 0.12 0.31 0.18 2.58 0.50 1.50
Average value 5 0.11 0.20 0.13 1.82 0.65 1.18
0.12 0.26 0.16 2.22 0.58 1.34
∗
coded form of each plant.

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E.G. Ameh and D.O. Aina Scientific African 10 (2020) e00630

Table 3b
Summary statistics of Cr in soil and plant tissues.

Variables Minimum Maximum Mean Std. Deviation

Soil .11 35.00 5.2 12.32

Root .00 63.00 7.65 19.26
Shoot .00 70.08 5.57 14.79
BCF .00 2.92 1.21 .81
TF .00 2.25 .65 .55
BAC .00 2.83 .89 .70

Table 3c
ANOVA analysis of data.

Variables Sum of Squares df Mean Square F Sig.

Root Between 2946.07 12 245.51 4.55 .02

Groups
Within 431.90 8 53.99
Groups
Total 3377.97 20
Shoot Between 2312.05 12 192.67 12.13 .01
Groups
Within 127.11 8 15.89
Groups
Total 2439.17 20
TF Between 2.63 12 .22 .98 .00
Groups
Within 1.79 8 .22
Groups
Total 4.41 20
BAC Between 4.12 12 .34 2.52 .01
Groups
Within 1.09 8 .14
Groups
Total 5.21 20
BCF Between 4.09 12 .34 .56 .00
Groups
Within 4.91 8 .61
Groups
Total 9.00 20
∗
data significant at P<0.05.

of Cr (70.08 mg/kg) in shoots was observed in Sporobolus pyramidalis Beauv and the least value of 0.00 mg/kg was recorded
in Gleichenia linearis Burns and Imperata cylindrical linn at various locations. The result of Cr accumulated in roots from this
research is consistent with the 17–126 mg/kg recorded in plant roots by Mellem et al. [24]. The soil to roots and roots to
shoots accumulation and translocation (Table 3a and Table 3b and Fig. 5a) suggests that the plants were also tolerant to the
upward transfer of Cr from the soil and consequently abating pollution in the study area (Singh et al., 2010; [27]).
No plant species accumulated > 10 0 0 mg/kg of Cr in the study area and as such no hyper accumulator of Cr among
the plants ([7,42]; Nazir et al., 2013). From the values of BCF, TF and BAC>1, only five species (ABH, TRJ, FUR, SM and SPB)
are suitable for phytoextraction of Cr at various locations. Also, based on the values of BCF>1, TF and BAC<1, thirteen (13)
species (ACL, ABH, DV, EAH, TRJ, HIS, HP, MCJ, SM, SAB, SVL, ULL and UP) are suitable for phytostabilization of Cr at various
locations. Based on these indices, BCF, TF and BAC (Table 3a and Fig. 5b), it is clear that most plants could not transfer Cr
from their roots to the above-ground tissues. This implies that five sampled plants were suitable for phytoextraction and
thirteen (13) for stabilization of Cr in the soils. This also means that most plants were excluders of Cr and not tolerant to Cr.
Transport of non essential elements is similar to cell wall immobilization of the epidermal layers. Thus, these plants absorb
and store these elements in the tissues, especially the roots system [41].

Copper (Cu)

Copper is an essential plant nutrient, therefore, higher concentrations of Cu in soils and its accumulation in roots and
shoots are expected [42]. Copper concentrations in the soils varied from 462.00 mg/kg to 648.00 mg/kg (Table 4a). This
recorded range of Cu exceeded the unpolluted standard limit of toxic elements in soil [7,19,20]. This is an indication that
coal mining activities have polluted the soil around the mine (Table 1c). Similar works carried out by Lorestani et al. [22] and
Nazir et al. [26] revealed lower ranges of 330.8–575.7 mg/kg and 8.88–357.39 mg/kg respectively for Cu in soils. Yoon et al.
[42] and Mkumbo et al. [25] recorded 20–990 mg/kg and 30.7–3625 mg/kg respectively in separate but similar studies with
Cu.

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E.G. Ameh and D.O. Aina Scientific African 10 (2020) e00630

Table 4a
Concentration of Cu (mg/kg) in soils and plant tissues.

Plant species Site no Soil Root Shoot BCF TF BAC

Ageratum conyzoides Linn ∗ ACL 6 594.00 6217.00 585.00 10.47 0.09 0.98
Average values 5 624.00 500.00 613.00 0.80 1.23 0.98
609.00 3359.50 599.00 5.64 0.66 0.99
∗
Aspila bussei O. Hoffin ABH 8 544.00 664.00 701.00 1.22 1.10 1.29
7 648.00 675.00 465.00 1.04 0.69 0.72
596.00 669.50 583.00 1.13 0.90 1.01
∗
Desmodium velutinum DV 3 629.00 834.00 720.00 1.33 0.86 1.14
Average values 2 544.00 506.00 436.00 0.93 0.86 0.80
586.50 670.00 578.00 1.13 0.86 0.97
Eclipta alba (L) Hassk ∗ EAH 4 462.00 318.00 501.00 0.69 1.58 1.08
Average values 5 624.00 604.00 595.00 0.97 0.99 0.95
543.00 461.00 548.00 0.83 1.29 1.02
Triumfetta rhiomdoidea Jacq.∗ TRJ 3 629.00 4462.00 804.00 7.09 0.18 1.28
Average values 1 645.00 700.00 750.00 1.09 1.07 0.08
639.00 2581.00 777.00 4.09 0.63 0.68
Fuirerina umbrellata Rottb ∗ FUR 4 462.00 856.00 896.00 1.85 1.05 1.94
Average values 6 594.00 1000.00 489.00 1.68 0.49 0.82
528.00 928.00 692.50 1.77 0.77 1.38
Gleichenia linearis (Burns) ∗ GL 5 624.00 573.00 399.00 0.92 0.70 0.64
Average values 7 648.00 428.00 386.00 0.66 0.90 0.60
636.00 500.50 392.50 0.79 0.80 0.62
Hyparrhenia involucrate stapf ∗ HIS 2 544.00 677.00 704.00 1.24 1.04 1.29
Average values 1 645.00 565.00 508.00 0.88 0.50 0.79
594.50 621.00 606.00 1.06 0.77 1.04
Hyptis suaveolens Poit ∗ HP 6 594.00 959.00 1001.00 1.61 1.04 1.69
Average values 8 544.00 807.00 1020.00 1.48 1.26 1.88
569.00 883.00 1010.50 1.55 1.15 1.79
Imperata cylindrica (Linn) ∗ ICL 2 544.00 573.00 468.00 1.05 0.82 0.86
Average values 3 629.00 802.00 511.00 1.28 0.64 0.81
586.50 687.50 489.50 1.17 0.73 0.84
∗
Leptochloa filiformis LF 1 645.00 563.00 554.00 0.87 0.98 0.86
Average values 2 544.00 388.00 337.00 0.71 0.87 0.62
594.50 475.50 445.50 0.79 0.93 0.74
∗
Monechma ciliatum Jacq. MCJ 7 648.00 876.00 944.00 1.35 1.08 1.46
Average values 6 594.00 1004.00 1000.00 1.69 0.99 1.68
621.00 940.00 972.00 1.52 1.04 1.57
∗
Panicum maximum Jacq. PM 1 645.00 703.00 601.00 1.09 0.85 0.93
Average values 8 544.00 682.00 569.00 1.25 0.83 1.05
594.50 692.50 585.00 1.17 0.84 0.99
Selaginella myosurus ∗ SM 5 624.00 701.00 603.00 1.12 0.86 0.97
Average values 7 648.00 902.00 863.00 1.39 0.96 1.33
636.00 801.50 733.00 1.26 0.91 1.15
Sida acuta Burm. F. ∗ SAB 6 594.00 807.00 825.00 1.36 1.02 1.39
Average values 4 462.00 788.00 515.00 1.71 0.65 1.11
528.00 797.50 670.00 1.54 0.84 1.25
∗
Sida linifolia juss.excav. SL 8 544.00 517.00 430.00 0.95 0.83 0.79
Average values 5 624.00 485.00 561.00 0.78 1.16 0.90
584.00 509.00 495.50 0.87 1.00 0.85
Schwenckia ammericana Linn ∗ SAL 7 648.00 893.00 692.00 1.38 0.77 1.07
Average values 4 462.00 882.00 910.00 1.91 1.03 1.97
555.00 887.50 801.00 1.65 0.90 1.52
Spermacoce verticillata Linn ∗ SVL 8 544.00 821.00 421.00 1.51 0.51 0.77
Average values 2 544.00 774.00 387.00 1.42 0.50 0.71
544.00 797.50 404.00 1.47 0.51 0.74
Sporobolus pyramidalis Beauv ∗ SPB 1 645.00 881.00 895.00 1.37 1.02 1.39
Average values 6 594.00 809.00 998.00 1.36 1.23 1.68
619.50 854.00 946.50 1.37 1.13 1.54
Urena lobata Linn ∗ ULL 7 648.00 919.00 466.00 1.42 0.51 0.72
Average values 2 544.00 862.00 519.00 1.58 0.60 0.95
596.00 890.50 492.50 1.50 0.56 0.84
Uraria Picta ∗ UP 3 629.00 795.00 600.00 1.26 0.75 0.95
Average values 5 624.00 587.00 513.00 1.37 0.87 0.82
626.50 691.00 556.50 1.32 0.81 0.89
∗
coded form of each plant.

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E.G. Ameh and D.O. Aina Scientific African 10 (2020) e00630

Table 4b
Summary statistics of Cu in soil and plant tissues.

Variables Minimum Maximum Mean Std. Deviation

Soil 462.00 648.00 5.90 57.85

Root 318.00 6217.00 9.37 1029.90
Shoot 337.00 1020.00 6.37 198.90
BCF .66 10.47 1.60 1.70
TF .09 1.58 .86 .29
BAC .08 1.97 1.07 .41

Table 4c
ANOVA analysis of data.

Variables Sum of Squares df Mean Square F Sig.

Root Between Groups 9780275.04 14 698591.07 40.76 .00

Within Groups 102846.42 6 17141.07
Total 9883121.45 20
Shoot Between Groups 565251.24 14 40375.09 2.97 .04
Within Groups 81455.00 6 13575.83
Total 646706.24 20
TF Between Groups .66 14 .05 3.24 .00
Within Groups .09 6 .02
Total .75 20
BAC Between Groups 1.89 14 .14 3.63 .01
Within Groups .22 6 .04
Total 2.12 20
BCF Between Groups 26.10 14 1.86 39.58 .00
Within Groups .28 6 .05
Total 26.38 20
∗
data significant at P < 0.05.

Fig. 6a. Average concentration (mg/kg) of Cu in soil and sampled plant tissues.

The accumulated Cu in roots of plant species ranged from 318.00 mg/kg to 6217 mg/kg (Table 4a and b and Fig. 6a).
While Eclipta alba (L) Hassk accumulated the least value of 318.00 mg/kg, Ageratum conyzoides linn, recorded the highest
value (6217 mg/kg) of Cu in their roots respectively.
This range of Cu accumulation in roots is higher than those obtained from similar works by Yoon et al. [42] and Lorestani
et al. [22] where 10–460 mg/kg of Cu was accumulated in P. nodiflora L and 18.8–475 mg/kg was accumulated in E. macro-
clada accordingly. The range of Cu accumulation in shoots varied from 337.00 mg/kg in Leptochloa filifirmis to 1020 mg/kg
in Hyptis suaveolens Poit (Table 4a and Table 4b and Fig. 6a). These observed values of Cu accumulation in roots and shoots
are higher compared to other similar studies carried-out by Yoon et al. [42]; Lorestani et al. [22] and Nazir et al. [26]. From
this result, eight (8) plant species can remove excess Cu from the soil and store in their aboveground tissues. Plants species
that accumulate >10 0 0 mg/kg of Cu in their shoots are said to be hyper accumulator plants [7,26,33,42]. From this study,
Hyptis Suaveolens Poit accumulated > 10 0 0 mg/kg of Cu (e.g. locations 6 and 8) and therefore, could be rightly adjudged to
be a hyper accumulator of Cu (Table 4a and Fig. 6a). For HP, the storage in root from the soil is not only high but was also
able to transfer Cu to the shoots. This plant apart from being a ready tool for phytoremediation can also serve as source
of Cu. This finding is consistent with Sporobolus sp. that accumulated above 10 0 0 mg/kg of Cu as documented by [25] but
contrary to findings by other workers, where a lower accumulation of Cu was recorded in the plant shoots [26,42]. From
these results, it shows that some of the native plants have higher tolerance for Cu and as such suitable for phytoremediation

14
E.G. Ameh and D.O. Aina Scientific African 10 (2020) e00630

Fig. 6b. Average variations of Cu in sampled plant tissues.

purposes. This is evident from the ability of some of these plants to accumulate Cu in their roots and transfer same to the
shoots (Singh et al., 2010; [27]).
The lowest BCF (0.66) for Cu was recorded in Gleichenia linearis (Location 7) while the highest (10.47) was in Ageratum
conyzoides linn (Location 6) (Table 4a and Fig. 6b). The highest TF (1.58) was observed in Eclipta alba (L) Hassk (Location
4) while the least TF (0.09) was recorded in Ageratum conyzoides linn (Location 6) (Fig. 6b). The BAC values ranged from
0.08 in Triumfetta rhimboidea Jacq to 1.97 in Schwenckia Americana linn (Table 4a and Fig. 6b). From this study (Table 4a),
Aspilia bussei O. Hoffin (Location 8), Triumfetta rhimboidea (Location 1), Fuirena umbrellata Rottb (Location 4), Hyparrhenia
involucrata Stapf (Location 2); Hyptis suaveolens Poit (Locations 6 and 8), Monechma ciliatum Jacq. (Location 7), Sida acuta
Burm. F. (Location 6), Schwenckia ammericana linn (Location 4) and Sporobolus pyramidalis Beauv are all phytoextractors of
Cu.
Most of the plant species have BCF > 1 and TF <1 (Table 4a and Fig. 6b). This means that these plants can accumulate
Cu but cannot translocate the same to their shoots. In other words, they have potential as Cu stabilizers and therefore are
excluders [18]. This study is consistent with similar research work of Yoon et al. [42], where they reported that most plants
were accumulators of Cu but could not translocate same. The high values of BCF (10.47) and TF (1.58) obtained from this
study did not compare favourably with documented values of BCF = 1.6 and TF = 5.6 by Yoon et al. [42] in R. fruticosus
for Cu. This BCF and TF values are indication of high accumulation of Cu in roots and translocation of same to the shoots
by few of the plants under investigation. It is evidence, therefore, that some of the plants can remove Cu from the polluted
coal mine soil.

Conclusion

Only Hyptis Suaveolens Poit has the potential as a hyper accumulator of Cu. The majority of the plants under investi-
gation have potential for phytoextraction and stabilization. It, therefore, means that most of these plants are suitable for
phytoremediation of metal-polluted soils around Okaba coal. From this study, phytoremediation of Okaba soil is therefore
recommended.

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable

Author contributions

EA carried out the design, sample collection, analysis, interpretation and writing. DA carried out the sample identification
and collection, sample preparation and analysis and correction of grammatical errors. Both authors read and approve the
final manuscript for publication.

Declaration of Competing Interest

The authors declare that they have no competing interest.

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E.G. Ameh and D.O. Aina Scientific African 10 (2020) e00630

Data for reference

All data generated or analysed during this study are included in this article.

Acknowledgments

The authors are grateful to the field team, the laboratory technicians, and all anonymous reviewers for the grammatical
corrections.

Funding

No funding was received from any individual, institution or organization for this research.

References

[1] V.S. Adki, J.P. Jadhav, V.A. Bapat, Nopalea cochenillifera, a potential chromium (vi) hyperaccumulator plant, Environ. Sci. Pollut. Res. 20 (2013)
1173–1180.
[2] H. Ali, E. Khan, What are heavy metals? Long-standing controversy over the scientific use of the term ‘heavy metals’ - proposal of a comprehensive
definition, Toxicol. Environ. Chem. 100 (2018) 6–19.
[3] H. Ali, E. Khan, Trophic transfer, bioaccumulation and biomagnification of non-essential hazardous heavy metals and metalloids in food chains/webs:
concepts and implications for wildlife and human health, Hum. Ecol. Risk Assess. (2018) 1469398, https://doi.org/10.1080/10807039.2018 .
[4] B. Alloway, Trace Metals and Metalloids in Soils and Their Bioavailability: Heavy Metals in Soils, Springer Press, London, 2012.
[5] V. Antoniadis, E. Levizou, S.M. Shaheen, Y.S. Ok, A. Sebastian, C. Baum, M.N. Prasad, W.W. Wenzel, J. Rinklebe, Trace elements in the soil-plant interface:
phytoavailability, translocation, and phytoremediation – a review, Earth Sci. Rev. (2017) 2017.
[6] B. Asgari, M. Ghorbanpour, S. Nikabadi, Heavy metals in contaminated environment: destiny of secondary metabolite biosynthesis, oxidative status
and phytoextraction in medicinal plants, Ecotoxicol. Environ. Saf. 145 (2017) 377–390.
[7] A.J.M Baker, R.R. Brooks, Terrestrial higher plants which hyper accumulate metallic elements- a review of their distribution, ecology, and phytochem-
istry, Biol. Recovery 1 (1989) 81–126.
[8] HJM Bowen, in: Environmental Chemistry of the Elements, Academic Press, London, 1979, p. 333pp.
[9] A. Chehregani, B. Malayeri, R. Golmohammadi, Effect of heavy metals on the developmental stages of ovules and embryonic sac in Euphorbia cheiran-
denia, Pak. J. Biol. Sci. 8 (2005) 622–625.
[10] Edited by SIL Coker, Azubuike A. Elueze (Ed.) Nigerian Mining and geosciences Society, 2003. Edited by.
[11] V. Cudic, D. Stojiljkovic, A. Jovovic, Phytoremediation potential of wild plants growing on soil contaminated with heavy metals, Arh. Hig Rada Toksikol.
Vol.67 (2016) 229–239.
[12] Z. Deng, L. Cao, Fungal endophytes and their interactions with plants in phytoremediation: a review, Chemosphere 168 (2017) 1100–1106.
[13] S. Fahimirad, M. Hatami, Heavy metal-mediated changes in growth and phytochemicals of edible and medicinal plants, in: M Ghorbanpourm, A Varma
(Eds.), Medicinal Plants and Environmental Challenges, first ed., Springer International Publishing AG, Germany, 2017, pp. 259–277.
[14] H.F. Farrag, Y.M. Al-Sodany, F.G. Otiby, Phytoremediation and accumulation characteristics of heavy metal by some plants in Wadi Alargy-Wetland,
Taif-KSA, World Appl. Sci. J. 28 (5) (2013) 644–653.
[15] N.X. Feng, J. Yu, H.M. Zhao, Y.T. Cheng, C.H. Mo, Q.Y. Cai, Y.W. Li, H. Li, M.H. Wong, Efficient phytoremediation of organic contaminants in soils using
plant-endophyte partnerships, Sci. Total Environ. 583 (2017) 352–368.
[16] F. Fu, Q. Wang, Removal of heavy metal ions from wastewaters: a review, J. Environ. Manag. 92 (2011) 407–418.
[17] A. Hamzah, R.I. Hapsari, E.I. Wisnubroto, Phytoremediation of Cadmium-contaminated agricultural land using indigenous plants, Int. J. Environ. Res. 2
(1) (2015) 8–14.
[18] M.E. Hosman, S.S. El-Feky, M.I. Elshahawy, E.M. Shaker, Mechanism of phytoremediation potential of Flax (linum usitatissimum L.) to Pb, Cd, and Zn,
Asian J. Plant Sci. Res. 7 (4) (2017) 30–40.
[19] A. Kabata-Pendias, H. Pendias, Trace Elements in Soils and Plants, CRC Inc, Boca Raton, FL, 1992.
[20] A Kabata-Pendias, H. Pendias, Trace Elements in Soils and Plants, third ed., CRC Press, Boca Raton, 2001.
[21] J.N. Liu, Q.X. Zhou, T. Sun, L.Q. Ma, S. Wang, Growth responses of three ornamental plants to Cd and Cd–Pb stress and their metal accumulation
characteristics, J Hazard Mater 151 (2008) 261–267.
[22] B. Lorestani, M. Cheraghi, N. Yousefi, Phytoremediation potential of native plants growing on a heavy metals contaminated soil of copper mine in Iran.
5 (5) (2011) 299–304.
[23] A. Mahar, P. Wang, A. Ali, M.K. Awasthi, A.H. Lahori, Q. Wang, R. Li, Z. Zhang, Challenges and opportunities in the phytoremediation of heavy metals
contaminated soils: a review, Ecotoxicol. Environ. Saf. 126 (2016) 111–121.
[24] J.J. Mellem, H. Baijnath, B. Odhav, Bioaccumulation of Cr, Hg, As, Pb, Cu, and Ni with the ability for hyperaccumulation by Amaranthus dubius, Afr. J.
Agric. Res. 7 (4) (2012) 591–596.
[25] S. Mkumbo, W. Mwegoha, G. Renman, Assessment of the phytoremediation potential for Pb, Zn, and Cu of indigenous plants growing in a gold mining
area in Tanzania, Int. J. Environ. Sci. 2 (4) (2012) 2425–2434.
[26] A. Nazir, R.N. Malik, M. Ajaib, N. Khan, M.F. Siddiqui, Hyperaccumulators of heavy metals of industrial areas of Islamabad and Rawalpindi, Pak. J. Bot.
43 (4) (2011) 1923–1933.
[27] S. Netty, T. Wardiyati, M.D. Maghfoer, E. Handayanto, Bioaccumulation of Nickel by fine wild plant species on nickel contaminated soil, IOSR J. Eng. 3
(5) (2013) 01–06.
[28] R. Nirola, M. Megharaj, T. Palanisami, R. Aryal, K. Venkateswarlu, R. Naidu, Evaluation of metal uptake factors of native trees colonizing an abandoned
copper mine - a quest for phytostabilization, J. Sustain. Min. 14 (2015) 115–123.
[29] P.U. Obianuju, Palynological study of the Okaba coal mine section in the Anambra Basin, Southeastern Nigeria, J. Min. Geol. 41 (issue 2) (2005)
193–203.
[30] J.E. Ogala, M.I Akaegbobi, O.O. Omo-Irabo, R.B. Finkelman, Statistical analysis of the geochemical distribution of major and trace elements of the
Maastrichtian coal measures in the Anambra basin, Nigeria, Petrol. Coal 51 (4) (2009) 260–269 .pp.
[31] O.A. Okunlola, O. Idowu, The geochemistry of claystone-shale deposits from the Maastrichtian Patti Formation, Southern Bida Basin, Nigeria, Earth Sci.
Res. J. 16 (2) (2012) 57–67.
[32] RL Rudnick, S Gao, Composition of the continental crust, in: HD Holland, KK Turekian (Eds.), Treatise on geochemistry 3: Rudnick, RL. (eds), The crust,
Elsevier-Pergamon, Oxford, 2003, pp. 1–64.

16
E.G. Ameh and D.O. Aina Scientific African 10 (2020) e00630

[33] A.A. Sagiroglu, S.O. Sen, Hyperaccumlator plants of the Keban mining district and their possible impact on the environment, Pol. J. Environ. Stud. 15
(2) (2006) 317–325.
[34] M. Sakizadeh, F.M. Sharafabadi, E. Shayegan, H. Ghorbani, Concentration and soil-to-plant transfer factor of Selenium in soil and plant species from an
arid area, in: World Multidisciplinary Earth Sciences Symposium, (WMESS, 2016) Vol. 44, 2016, pp. 1–7.
[35] HT Shacklette, G Josphine, JG Boerngen, The Average Content of Elements in the Soil, US Geological Survey Paper 1270, 1984.
[36] N. Singh, M. Kaur, J.K. Katnoria, Analysis of bioaccumulation of metals in the aquatic environment of Beas River Basin: a case study from Kanli wetland,
GeoHealth 1 (2017) 93–105.
[37] R. Sudmoon, L Neeratanaphan, P. Thamsenanupap, T. Tanee, Hyperaccumu location of Cadmium and DNA changes in popular vegetable, Brassica
chinensis L, Int. J. Environ. Res. 9 (2) (2015) 433–438.
[38] P. Venkatachalam, N. Jayalakshmi, N. Geetha, S.V. Sahi, N.C. Sharma, E.R Rene, S.K Sarkar, P.J. Favas, Accumulation efficiency, genotoxicity and antioxi-
dant defense mechanisms in medicinal plant Acalypha indica L. under lead stress, Chemosphere 171 (2017) 544–553.
[39] L. Wang, B. Ji, Y. Hu, R. Liu, W. Sun, A review on in situ phytoremediation of mine tailings, Chemosphere 184 (2017) 594–600.
[40] S. Wang, J. Liu, The effectiveness and risk comparison of EDTA with EGTA in enhancing Cd phytoextraction by Mirabilis Jalapa L, Environ. Monit. Assess.
186 (2014) 751–759.
[41] G.-R. Wu, H.-L. Hong, C.-L. Yan, Arsenic accumulation and translocation in mangrove (Aegiceras corniculatum L.) grown in Arsenic contaminated soils,
Int. J. Environ. Res. Public Health 12 (2015) 7244–7253.
[42] J. Yoon, Xinde Ceo, Qixing Zhou, Len Q. Ma, Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site, Sci. Total Environ.
368 (2006) 456–464.

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