The Potential of Talisay-Dagat (Terminalia Catappa L.) For Phytoremediation in Langihan Lagoon, Butuan City, Agusan Del Norte, Philippines
The Potential of Talisay-Dagat (Terminalia Catappa L.) For Phytoremediation in Langihan Lagoon, Butuan City, Agusan Del Norte, Philippines
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P-ISSN: 2339-0913
Jurnal Sylva Lestari E-ISSN: 2549-5747
1. Introduction
Heavy metal pollution has become a global problem (Mahar et al. 2016) that has attracted
considerable public attention (Li et al. 2019) and is increasing due to industrialization and the
disturbance of the natural nutrient cycles (Ali et al. 2013; Sumiahadi and Acar 2018) and stored in
soils from human activities and natural activities (Elnazer et al. 2015). The current state of
environmental contamination is extremely dangerous, endangering the fundamental foundation of
human existence (Motuzova et al. 2014). This is true when enterprises utilize the soil for the
discharge of treated liquid effluents, deposition of exhaust gas, and solid waste disposal (Adnan et
al. 2022; Gabarrón et al. 2017). The term “heavy metal” encompasses toxic elements like lead,
cadmium, chromium, nickel, copper, zinc, and mercury, posing biological risks to ecosystems.
The heavy metals found near hazardous waste sites can cause toxicity at low exposure levels (Jacob
et al. 2018). Although metals are necessary in small quantities, their presence in the ecosystem
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presents significant health and environmental hazards for all living things. Heavy metals
accumulate in plants from the soil because living things are unable to break them down, and trees
might experience long-term harm and effects from this (Nyangon et al. 2023).
In tropical countries like the Philippines, Terminalia catappa L., commonly known as
Talisay-dagat, is a versatile tree often planted for shade, ornamental, and edible nuts, yet it remains
underutilized for some purposes (Ladele et al. 2016). It is a fast-growing tree that naturally thrives
in coastal areas and belongs to the Combretaceae family. Although T. catappa has been extensively
studied, the majority of research has focused on its medicinal properties, including antitumor and
antioxidant properties (Pandya et al. 2013), including its wound healing applications (Chanda et
al. 2013), other research is about its potential as a biofuel (Khan et al. 2013), and as an indicator
for acid-based reactions (Iha et al. 2014).
Phytoremediation is a financially practical way to remediate. Phytoremediation technique
removes pollutants from the environment by utilizing plants and the microorganisms that live with
them (Kong and Glick 2017). According to the findings of Ullah et al. (2015), phytoremediation
is a financially viable way to remediate soil contaminated by metals by breaking down, stabilizing,
and/or eliminating the toxins (Pinto et al. 2014). According to Chibuike and Obiora (2014), it
works best when the contaminants are widespread and within the plant’s root zone. Considering
their extensive study history, using green plants to remediate contaminated soil appears to be a
promising solution to heavy metal issues (Sarwar et al. 2017). Phytoremediation was generally
acknowledged as an affordable method of restoring the environment supporting literature in the
field indicates that this technology is thought to be more economical and environmentally
beneficial than traditional methods for cleaning up contaminated places (Yadav et al. 2022).
According to Mahar et al. (2016), hyperaccumulation of metals appears to be an evolutionary
adaptation of plants to life.
In urban areas in Butuan City, particularly in Langihan Lagoon, Barangay Holy Redeemer,
it was observed that the area is more likely contaminated due to its proximity to the public market,
roadway, households of dwellers/communities, and the site was exposed to a variety of
anthropogenic activities. Thus, the present study aimed to determine the potential of T. catappa as
phytoremediation in mitigating soil contamination in Langihan Lagoon and to understand the
influence of heavy metals presence and concentration in the soil on the total absorption of T.
catappa.
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Fig. 1. The study site at Langihan Lagoon, Barangay Holy Redeemer, Butuan City, Caraga
Region, Philippines.
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of Agriculture, Caraga Region. The roots were put in an oven set at 70°C for 12 hours, the sample
was dried to a crisp and brittle texture where the analytical process took place at the Regional Soils
Laboratory of the Department of Agriculture, Caraga Region, using the Microwave-assisted aqua-
regia digestion and determination through ICP-OES. The aqua regia extraction was based on the
procedure recommended by the International Organization for Standardisation (ISO 1995). In this
process, 250 ml Pyrex digestion tubes were filled with a 3 g sample. The sample underwent an
initial pre-digestion step at room temperature for 16 hours using a 28 ml mixture of 37% HCl and
70% HNO3 in a 3:1 ratio. The suspension was then digested at 130°C for 2 hours using a reflux
condenser. The resulting suspension was filtered through an ashless Whatman 41 filter, diluted to
100 ml with 0.5 mol l−1 HNO3, and stored in polyethylene bottles at 4°C for analysis (Sastre et al.
2002).
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Table 1. Criteria for hyperaccumulator, excluder and/or indicator type of plant (Adriano 2001;
Baker et al. 2000; Ndeda and Manohar 2014; Santos et al. 2021; Yoon et al. 2006)
Hyperaccumulator Excluder/Regulator Indicator
- Ratio of heavy metal concentrations - High levels of heavy - Metal levels in the tissues
of TF > 1 metals in the roots but reflect the levels in the
- Ratio of heavy metal concentrations with TF quotients < 1 sediments
of EF > 1 - Indicators are plant species
- Pb, Cu, Co, Cr, and Ni have > 1000 that correspondingly respond
µg/g or 10.000 µg/g of Fe, Mn, and to metal concentrations in
Zn or Cd > 50 µg/g in any soils
aboveground tissue in their natural
habitat without suffering toxic
effects
According to WHO (1996), the permissible limit of Ni in the soil is 35 ppm, 100 ppm for Cr
and 36 ppm for Cu. Microorganisms, animals, and plants are all extremely hazardous to heavy
metals such as N, Cr, and Cu. Due to increased anthropogenic and geological processes, heavy
metal-polluted soils are becoming more commonplace worldwide (Chibuike and Obiora 2014).
Furthermore, heavy metals Ni, Cr, and Cu are necessary for plants to complete their life cycle
because they cannot obtain another nutrient that can substitute them (Harasim and Filipek 2015).
Contaminated land must be cleaned up and made free of heavy metals to improve the ecosystem
for all living organisms (Dixit et al. 2015).
Given the presence of heavy metals in nature, this topic has received a lot of attention. In a
study conducted by Fazil et al. (2023) at Mardan Industrial Estate, their presented results point to
the potential application of the identified twenty-one plant species for heavy metal remediation in
contaminated areas, particularly for Ni present in soil. This is to offer a viable path for ensuring
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absorptions in leaf samples (Table 4). Ni follows with a mean concentration of 11.21 ppm and a
standard deviation of 5.82 ppm, while Cr shows a mean concentration of 3.54 ppm, measuring a
dispersion of 1.66 ppm. According to WHO (1996), the permissible limit of plants for Cu is 10
ppm, Ni is 10 ppm, and Cr is 1.30 ppm, Ni and Cr exceed the permissible value as also used by
Iqbal et al. (2011).
Matakala et al. (2023) studied the Combretum molle (Combretaceae) and other native species
found in tailing dams effectively restricting the root-to-shoot translocation of heavy metals. This
indicates the potential suitability of some plants with the same family, such as T. catappa for Cu
phytoremediation as these elements are essential to plants’ growth and development. In addition,
Cu was highest in leaves as observed in the results because it is essential to the growth of plants.
Cu belongs to the eight micronutrients needed for the plant growth (Shabbir et al. 2020) in low
concentrations (Hajar et al. 2014). However, Cu has been distinguished to move several toxic
effects on various biophysiochemical processes (Ameh and Sayes 2019).
There are very few studies of hyperaccumulation of nickel particularly in tropical regions,
and the Ni hyperaccumulation by plants is not well understood. Some data are concentrated on
only a few species and metals (Pollard et al. 2014). In the presence of Ni, the contents of mineral
nutrients in plant organs may increase, decrease, or stay even (Bhalerao et al. 2015). Safari et al.
(2018) studied Conocarpus erectus (Combretaceae) and found that this species can capture Ni
from the air and absorb it from contaminated soils. Cr is a non-essential heavy metal for living
systems, considered one of the most toxic elements that has detrimental effects on plants and
animals (Handa et al. 2018) and Cu is transported and absorbed in reduced form (Mir et al. 2021).
Based on the study of Kapoor et al. (2022), Cr has two forms (mobile and immobile), and further
studies are required to overcome Cr contamination and suitable remediation strategies.
3.2.3. Heavy metal uptake and translocation of T. catappa through TF, BCF, and EF calculations
The translocation factor (TF) explains the distribution of heavy metals, specifically Ni, Cu
and Cr among the soil and the roots of T. catappa. The TF and BCF factors should be greater than
one to be a hyperaccumulator (Baker et al. 2000; Ndeda and Manohar 2014; Santos et al. 2021;
Yoon et al. 2006). Cu obtained the highest BCF value (0.13), followed by Ni with a BCF value
(0.04), and Cr obtained the lowest BCF value (0.04) (Table 5). Ni having a BCF value of 0.04
explains that a limited portion of the heavy metals are present in the soil taken by the roots (Table
5). Meanwhile, the Cu of BCF value of (0.13) indicates a higher uptake of Cu by the roots of T.
catappa. The BCF value of 0.04 indicates that Cr is taken up by roots although to a lesser extent
than Cu and Ni. The study of Tauqeer et al. (2019) suggests that Conocarpus erectus
(Combretaceae) can stabilize Ni and Cr with a BCF value of less than 1. Since there is limited data
about the ability of the Combretaceae family particularly T. catappa to stabilize heavy metals in
the soil a similar study could be one of the possible supports for this claim. Ni and Cu exhibit TF
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values greater than one. Ni has a TF value of 1.22, and Cu has a TF values of 1.60. The values
explain the potential of T. catappa as a hyperaccumulator for Ni and Cu while a potential excluder
for Cr with TF of 0.57. Hyperaccumulator (extreme accumulator) can thrive and tolerate heavily
contaminated soils; in contrast, excluders can survive through a restriction mechanism as
influenced by species and genotypes, even among crops sensitivity and tolerance vary (Adriano
2001). Furthermore, Cu obtained a high EF value (0.20) followed by Ni (0.05) and Cr (0.02), this
indicates that these heavy metals were accumulated by the plant.
According to Thakur et al. (2016), a hyperaccumulator can accumulate and absorb heavy
metals in high concentrations in the aboveground tissues without affecting physiological
processes. Matakala et al. (2023) studied the Combretum molle (Combretaceae) and other native
species found in tailing dams, which have the potential for phytostabilization of Cu, Cr, and Ni.
Nyenda et al. (2023) also supported this study, which recommended planting C. molle, C. zeyheri,
and C. apiculatum (Combretaceae) for tailings with high Ni. Adriano (2001) explains
bioavailabilty in the soil-plant system and explains that plant species and genotypes influence the
sensitivity or tolerance of plants to excess metals. Rascio and Nava-Izzo (2011) discusses the
phenomena of hyperaccumulation in plants, especially in response to heavy metal contamination,
which further supports the observations of values BCF > 1. The EF analysis of Ni, Cu, and Cr
revealed relatively low EF values with 0.05, 0.20, and 0.02, respectively, indicating a limited
absorption of these heavy metals in the plant tissues compared to the soil. The study of Lorestani
et al. (2011) showed that none of the collected plants were suitable for phytoextraction of Cu, these
plants were found naturally in heavy metal-contaminated soil.
This suggests that the plant species are not significantly accumulating these metals with
concentrations in the leaves being notably lower than in the soil samples. Printarakul and
Meeinkuirt (2022) conducted a related study on heavy metal accumulation in bryophytes, where
they found Cu exhibiting a low EF value of (0.9) in bryophyte tissues, suggesting minimal
enrichment. The study highlights that the sources of heavy metals in the bryophyte community are
primarily lithological rather than anthropogenic, providing valuable insights into the limited
accumulation of Ni, Cu, and Cr in the studied plant species. The results show that based on TF,
BCF, and EF equations, only TF shows the effectivity of restricting the root-shoot ratio
translocation of Ni and Cu (TF > 1). Plants with more than one bioconcentration factor and
translocation factor of greater than one can be used in phytoextraction (Santos et al. 2021).
Furthermore, if the plant's bioconcentration factor is higher than one and its translocation factor is
lower than one, the plant has the potential for phytostabilization (Yoon et al. 2006). The
phytoextraction process involves the movement of heavy metals to the plant's harvestable parts,
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such as the shoots (Yoon et al. 2006). In contrast, phytostabilization relies on the plant's ability to
limit the transfer of metals from the roots to the shoots (Yoon et al. 2006).
70
60
50 y = -0.79x + 82.24
40 r² = 0.48
30
20
10
0
15 17 19 21 23 25 27 29 31 33
Cu absorption of T. catappa (ppm)
Fig. 2. Relationship between Cu absorption (root and shoot) of eight T. catappa and soil Cu
concentration.
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environmental conditions, and plant type. Furthermore, the study also emphasizes that the multiple
factors should also be considered, suggesting the need for broader data to better understand the
acquisition of Ni in the environment.
400
Ni concentration in soil (ppm)
350
300 y = -1.2648x + 242.41
r² = 0.0122
250
200
150
100
50
0
10 15 20 25 30 35 40
Ni absorption of T. catappa (ppm)
Fig. 3. Relationship between Ni absorption (root and shoot) of eight T. catappa and soil Ni
concentration.
250
200
(ppm)
150
y = 1.71x + 144
100 r² = 0.008
50
0
4 6 8 10 12 14 16
Fig. 4. Relationship between Cr absorption (root and shoot) of eight T. catappa and soil Cr
concentration.
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4. Conclusions
The study shows that T. catappa is a potential hyperaccumulator for Ni and Cu based on TF
value > 1 and a potential excluder for Cr where TF value < 1. Based on regression analysis the
total absorption of Ni, Cu, and Cr by T. catappa shows no correlation and no statistically
significant impact on the presence and concentration of heavy metals in the soil (r2 < 0.5). This
may be because of the few tree samples in the study and the environmental factors. Also, these
findings emphasize the complexity of heavy metal absorption, indicating that factors beyond T.
catappa influence soil metal concentrations. T. catappa shows potential for hyperaccumulation
based on its ability to translocate metals to its shoots, but it may not be effective in overall
accumulation and soil uptake. Further research is needed to comprehensively understand the
mechanisms involved, considering metal availability, as well as comparing with other known
hyperaccumulators would be beneficial to fully understand and leverage the T. catappa
phytoremediation capabilities. More information from this will help explore the potential of tree
species for phytoremediation.
Acknowledgments
The authors would like to express gratitude to the Caraga State University (CSU), the
Regional Soils Laboratory, Department of Agriculture, and Barangay Holy Redeemer, Butuan City
for their invaluable support for the completion of this study.
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