Environmental Biomonitoring of Terrestrial Ecosystems in The Philippines: A Critical Assessment and Evaluation
Environmental Biomonitoring of Terrestrial Ecosystems in The Philippines: A Critical Assessment and Evaluation
MELET B. MARIANO
https://orcid.org/0000-0003-0246-010X
marianobernabemelet23@gmail.com
De La Salle University
Taft Avenue, Malate, Manila, Philippines
JENNIFER P. LASCANO
https://orcid.org/0000-0002-1034-7783
jennifer_lascano@dlsu.edu.ph
De La Salle University
Taft Avenue, Malate, Manila, Philippines
LALAINE G. SARIANA
https://orcid.org/0000-0002-8493-0410
lalaine.sariana@cmu.edu.ph
De La Salle University
Taft Avenue, Malate, Manila, Philippines
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IAMURE International Journal of Ecology and Conservation
ZEBA F. ALAM
https://orcid.org/0000-0001-7769-2840
zeba.alam@dlsu.edu.ph
De La Salle University
Taft Avenue, Malate, Manila, Philippines
ABSTRACT
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KEYWORDS
INTRODUCTION
effects on the soil (Harris-Hellal et al., 2009; Müller et al., 2010). In humans, for
example, mercury (Hg) could induce harmful and fatal effects on the immune
system, reproduction, internal organs, and central nervous system (Dietz et al.,
2018).
Furthermore, substandard mining activities are aggravated by the absence of
proper ecological bio-monitoring in the affected areas that can lead to cautious
and accidental waste disposal (van Straaten, 2017). Despite its economic impact,
this remains an extremely controversial issue and concern due to its occurrences
on environmental deterioration and degradation amongst organisms exposed to
it (Cortes-Maramba et al., 2006). The increase of heavy metals on the soil in the
terrestrial environment (Getaneh & Alemayehu, 2016) is certainly deposited in
the rocky soil that could release in the terrestrial environment either by artificial
activities of people or by natural weathering in nature.
This scenario could give organisms an environmental threat due to their
increased potential to bio-accumulate and interfere with numerous biological,
environmental processes (Heikens et al., 2015). So, when the soil is exposed
to chemicals with heavy metals, there is a tendency for this to be stored and
accumulated within the living organs of organisms. These contaminants are
inevitable and raise major concern to all. In due time, it will bio-accumulate
within humans, mammals, and plants that can eventually compromise the
organisms. Although small amounts may give positive effects, excess volumes may
cause heavy metal toxicity that will lead living organisms to various problems.
For this reason, many recent studies revealed elevated content of mercury (Hg)
levels in living organisms (Cortes-Maramba et al., 2017), and the harmful effects
of mercury (Hg) on terrestrial organisms in the country is still insufficient and
lacking.
As contamination of heavy metals continues, dumpsites and landfills are
another major problem for environmental concerns due to its toxins released
to the soil. For instance, highly urbanized cities like Metro Manila in Luzon,
Cebu in the Visayas, and Davao in Mindanao has a big bulk of wastes thrown
in landfills that consist of dangerous metal-containing household wastes, factory
/ industrial, and hospital/laboratory (solid and liquid) wastes. Based on health
reports, heavy metals usually the content of combustible solid waste materials
have shown that cadmium (Cd) and chromium (Cr) are present in dumpsite
and landfill wastes (Riber et al., 2015). For instance, cadmium (Cd) enters the
environment biota through some activities like improper disposal of solid waste
in the surroundings, where heavy metal is toxic and has long and short biological
effects on living organisms (Sankaran & Ebbs 2017). For chromium (Cr), that
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is an essential element in trace amounts from the soil (Prasad & de Oliveira
Freitas, 2016). Still, the hexavalent form of chromium (Cr) is relatively toxic
and poisonous (Shanker et al., 2017). With this, the composition of solid waste
materials deposition on the living cell is found 30% of the total volume of heavy
metals including cadmium (Cd) and chromium (Cr) in wastes from the dumpsite
and landfill are in an available reactive form (Flyhammar et al., 2017).
Presently, the extent of the biomarker in the terrestrial ecosystem responses
in the sensitivity of organisms is an initial cautionary alteration in organisms
to evaluate and monitor bio-environmental integrity and assess changes in the
terrestrial environment of organisms (Pascoe; Blanchet; Linder, 2018). With
this, the use and procedure of the biomarker approach in the lab experiments of
contaminated terrestrial environments have increased for many years, particularly
in the Philippines, where the terrestrial environments are massively engaged in
environmental activities like in Metro Manila, Cebu City, and Davao City. This
triggers the fact that biomarkers are a very important tool for environmental bio-
monitoring chemical exposure detection in living organisms. Its effect assessment
is useful decision-making of environmental management service activities
and protection to the ecosystem and protection of habitat implementation
on remediation procedures in the Philippines. The possibility of heavy metal
contamination of cadmium (Cd), chromium (Cr), mercury (Hg), Lead (Pb),
and zinc (Zn) in the mining areas, dumpsites, and landfills (Carmona, Cavite,
Philippines) are expected but undetermined.
As such, soil degradation in the environment poses severe environmental
problems that need to be resolved and determined. As an effect, heavy metals
such as lead (Pb) tend to persist in the upper layers of soil and metabolized or
absorbed in tissues. Thus, the high magnetization of heavy metals for certain
organic materials and its excessive amount may cause serious and severe organ
problems. So, the heavy metals could be of great concern to organisms because
they can react with chemicals which are essential for biological processes and
lab activity (Agrahari, Richa, Swati, Rai, & Singh, 2016). For instance, the
plants absorb the heavy metal (Pb) through their roots. The heavy metals tend
to concentrate mainly on leaves and in the outer part of the plant roots. So,
when organisms, including humans, eat the contaminated plants, a fraction of
lead (Pb) is entering inside the body organs like liver, kidney, and bones. Thus,
the lead (Pb) contamination in living organisms affects a wide range of sub-
lethal effects, and a higher-level could cause biological defects and death (Pain,
2016). More so, it is time for the health professionals and government agencies
of the country to increase concern for assessing and evaluating the protection and
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This study aims to identify the most suitable biomarkers for environmental
biomonitoring and to determine the different approaches for bioremediation in
the terrestrial ecosystem across Luzon, Visayas, and Mindanao that needs to be
developed and promulgated.
METHODOLOGY
three islands of the Philippines. Studies revealed that pollutants in the terrestrial
ecosystem are common to the three islands are chromium (Cr) and cadmium
(Cd). Other pollutants such as copper (Cu), zinc (Zn), lead (Pb), and mercury
(Hg) are present both in Luzon and Mindanao islands whereas; magnesium (Mg),
potassium (K), iron (Fe), manganese (Mn), and nickel (Ni) are only present in
Luzon island.
In Luzon, studies on environmental biomonitoring in the terrestrial
ecosystem (Ragragio et al., 2010; Juson et al., 2016; Navarrete et al., 2017;
Solidum, 2014; Cortez & Ching, 2014; Pfeiffer et al., 1990; & Ona et al., 2006)
revealed that the most prominent heavy metals which are found in the soil and
vegetation of Luzon are lead (Pb), copper (Cu), and zinc (Zn). Other metals
include cadmium (Cd), chromium (Cr), nickel (Ni), and mercury (Hg). These
pollutants come from various sources such as mining activities, industrial plants,
vehicular emissions, small factories, anthropogenic activities, land-use change,
urban wastes, and e-waste such as computers, batteries, appliances, and other
related waste products.
Other pollutants are airborne heavy metals from e-wastes such as cadmium
(Cd), copper (Cu), chromium (Cr), lead (Pb), and nickel (Ni), and essential
minerals like zinc (Zn), magnesium (Mg), potassium (K), iron (Fe), and
manganese (Mn) are found in landfills in Metro Manila (Alam et al., 2017).
The same heavy metals enumerated above, for instance, cadmium (Cd), nickel
(Ni), and lead (Pb), are also found in the nickel mining site in Mindoro Island
(Eufemio et al., 2016).
Aside from heavy metals, pesticides are also reported as pollutants in the
terrestrial ecosystem. The three major types of pesticides commonly used by
farmers in Benguet province according to chemical composition are pyrethroids,
organophosphates, and carbamates (Lu, 2009; Lu, 2010). The pyrethroids used
include cypermethrin, cyfluthrin, deltamethrin, cyphenothrin, fenvalerate, and
fluvalinate. Organophosphates such as malathion, parathion, diazinon, fenthion,
dichlorvos, chlorpyrifos, and ethion were also used as well as dithane a carbamate.
Also, both soils and crops have pesticidal residues. The most common
pesticide residue in crops is chlorpyrifos while in soils are endosulfan sulfate,
profenofos, chlorothalonil, T endo-sulfan, chlorpyrifos, cypermerthrin, and
cyhalothrin (Lu, 2010).
In the Visayas, the plants in the landfills of Cebu City are found to have
cadmium (Cd) and chromium (Cr) heavy metals (Nazareno et al., 2015).
In Mindanao, heavy metals include mercury (Hg), cadmium (Cd), copper
(Cu), zinc (Zn), and lead (Pb). These heavy metals come from gold mining
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(Appleton et al. 2006; Martinez et al. 2018; Maramba et 0al., 2006). Airborne
heavy metals such as mercury (Hg) and methylmercury are also found in gold
processing and refining plants (Akagi et al., 2000).
emerge when cells are not able to integrate whole or fragment chromosomes in
the daughter nuclei during cell division. Instead, these are combined in small
supplementary nuclei, where they persist throughout the cell (Viarengo et al.,
2007). In the study conducted in Northern Mindanao, a buccal micronucleus
test was used to inspect the damage in the genetic material caused by exhaust
exposure from vehicles. Female street sellers exposed to the exhaust from vehicles
have a notably higher incidence of micronucleated cells than females, which
are minimally or not exposed (Recoleto et al., 2017). There is no parallel study
found in Luzon and Visayas settings that focus on using the micronucleus test to
examine exposure to vehicular exhaust.
Humans
Humans have the possibility of being exposed to lead (Pb) environmentally
and occupationally. This may happen if the particles of lead produced from
burning resources that contain lead are inhaled during the shedding of leaded
paint, smelting, recycling and consuming leaded gasoline and aviation fuel.
Likewise, exposure may also occur through the ingestion of dust, water, and
food contaminated with lead. Additional sources of lead contaminants from
loosely regulated medicines and cosmetics (World Health Organization, 2018).
Biomonitoring of humans’ exposure to heavy metals such as Pb is an important
health care concern since it has detrimental effects, especially to children.
One of the biological specimens that can be collected easily and
inexpensively is the hair. Lead can be expelled through the hair. Because of this,
many recommended it to become a way of analyzing Pb exposure, especially
in developing countries where high-end laboratory facilities and materials are
limited (Schumacher et al., 1991). Though, there is an extensive call for the review
of the use of hair analysis in human biomonitoring because of some scientific
matters that need to be addressed before it becomes an effective biomonitoring
tool (Agency for Toxic Substances and Disease Registry, 1999).
One of the insistent ecological issues nowadays is the airborne lead as an
effect of growing numbers of vehicles as part of urbanization. Many organisms,
not just humans, tend to be continuously exposed to airborne lead. The
intensifying harmful problem of air pollution happening, not just in Manila but
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also to the other provinces of Luzon, such as in Cavite, is causing lifelong and
costly problems in human health.
In a study of hair lead bio-monitoring among school children in the province
of Cavite, Philippines who designed to investigate the status of trace lead in
pupils and determine if the socio-demographic profile, Body Mass Index (BMI),
means of transportation significantly impact the existence of airborne hair lead
absorption in them. To do this, concentrations of hair lead traces amongst school
children living in rural and urban places in the Cavite province (Israel & Asirot,
2015).
As a result, the traces of lead concentrations are in the hair of those children
attending classes in public schools that are relatively higher than children in
private schools. Also, students who live in rural places are lower hair lead traces
concentrations than those living in urban settings where hair lead concentrations
are high. The study found that there is a significant difference in hair lead
concentration between school children residing in urban and rural places and
those studying in private and public schools in Bacoor and Alfonso, Cavite. The
school children are constantly exposed to airborne lead, especially in areas where
there are many vehicles (Macawile et al., 2012).
At present, there is no parallel study found in Visayas and Mindanao that
focus on hair as a medium for biomarkers of lead and other heavy metals (Gupta
et al., 2000).
Plants
Plants can also be used as a biomarker of exposure. Zea mays (corn) used to
measure the presence of heavy metals such as Cd, Cu, Pb, and Zn in dumpsite
soil in Manila (Cortez et al., 2014). A. sessilis and E. indica, common plants
in Park and Wildlife Areas in Quezon City) are used to assess the presence of
Chromium in landfill areas (Navarette et al., 2017).
Lichens
Lichens refer to the symbiotic relationship between algae and fungi. They
have particular requirements for their habitat. In the study of Phlyctis argena
Spreng, flot lichen is biomonitoring of airborne heavy metals near a nickel
mining site in Mindoro Island, Philippines, Phlyctis argena, or white paint
lichen is collected and used to analyze the presence of cadmium, nickel, and lead.
The performance of P. argena as an effective biomonitoring tool is also assessed.
Samples are collected near a nickel mining area and along a roadside in Barangay
Villa Cerveza, Municipality of Victoria in the Island of Mindoro. Heavy metals in
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white paint lichens were analyzed using Flame Atomic Absorption Spectrometer.
As a result, among cadmium (Cd), nickel (Ni) and lead (Pb), nickel was the most
plentiful metal in the two (2) sampling places.
The study concluded that Phlyctis argena (white paint lichen) is useful
as a bioindicator of airborne heavy metals such as cadmium, nickel, and lead.
However, the bioaccumulation levels of these heavy metals depend on several
parameters, such as season and climatological circumstances (frequency of
rainfall occurrence, temperature, wind speed, and wind direction) (Eufemio et
al., 2016).
Many existing literatures show that lichens are good bioindicators of
pollutants such as heavy metals. In detecting airborne heavy metals, it is said that
lichen species such as white paint lichen have a necessary characteristic of being a
reliable bioindicator and an effective tool for biomonitoring. It is because of their
capability to accumulate heavy metal and chemical pollutants in the atmosphere
in their tissues without the organism dying because of hostile effects on its growth
or survival (Zverina et al., 2014; Beeby, 2001; Sarret et al., 1998; Nash, 1989).
Lichen species depend on their nourishment on atmospheric particles due
to their plain anatomy and the absence of a fully developed root structure.
Consequently, atmospheric pollutants or airborne heavy metals easily
bioaccumulate on its tissues (Bargagli et al., 2002). The absence of the waxy,
outside cuticle, enables the absorption and retention of atmospheric particles
(Sloof, 1995; Nash, 1996). Thus, in a long period, the metal ions present in the
atmosphere and its rudimentary composition reflects on the lichens (Adamo et
al., 2003). Furthermore, lichen species distribution is widespread in many places.
These characteristics of lichens make them an effective bioindicator, and reliable
biomonitoring means.
and Portulaca oleracea (Common purslane) are potential for absorbing a high
amount of copper. Amaranthus spinosus (Spiny amaranth), Achyrantes aspera
(Chaff-flower), Portulaca oleracea (Common purslane), and Alternanthera sessilis
(Dwarf copperleaf ) are reported to absorb a high amount of lead. Eleusine indica
(Wiregrass) and Amaranthus spinosus (Spiny amaranth) absorb a high amount
of zinc. Crassocephalum crepidiodes (Fireweed), Portulaca oleracea (Common
purslane), Alternanthera sessilis (Dwarf copperleaf ), and Cyperus alternifolius
(Umbrella sedge) absorb a high amount of cadmium. Amaranthus spinosus (Spiny
amaranth) and Blumea sp. absorb a high amount of nickel. Paz-Alberto & Sigua
(2007) reported mustard, tomato, and Vetiveria zizanioides L. (Vitever grass) as
potential phytoremediators for ethidium bromide, a mutagenic agent commonly
used in the molecular biology laboratory for Agarose Gel Electrophoresis.
Generally, the country must regulate and make remediation in soil strategies
for reducing metal bio-availability equated with possible reduced risk for long
term solution (Martin & Ruby, 2004) so that in the scenario of heavy metals’
contaminating the soils, the chemical form of these contaminants in the soil will
intensely impact in the selection of the proper remediation treatment method.
With this, various technologies exist nowadays for the soil remediation of heavy
metal in the polluted soil environment (Gupta et al., 2000). Some of the most
applicable bioremediations in the country are the immobilization techniques,
soil washing, and chemical extractants for soil washing, phytoremediation, and
photostabilization.
Immobilization techniques
This technique employs practical approaches in the remediation of
contaminated soils of heavy metal in the area of concern. This scientific technique
is probably used and applied in the areas with highly contaminated soil to
eradicate heavy metal from its origin. Its storage is linked with high ecological
risk because its alterations of organic and inorganic materials have hastened
the decrease of soil toxicity to the affected ground/area. Its prime role in this
manner is to immobilize the ground where the alter of soil metals’ origin is more
geochemically unchanging through precipitation, sorption, and complexation
methods/processes (Hashimoto, 2009).
Recent studies have shown possible low-cost industrial/manufacturing
chemical residues (Boisson et al., 2015; Lombi, 2002; Anoduadi, 2009) to
restrain heavy metals in the polluted/contaminated terrestrial environment due
to the bulk of soil environment and the limits of present methodical techniques
where the halt mechanisms are not yet simplified by concern field, which
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Soil washing
In this technique, there is a quantity of heavy metals have been declined
in the mined soil (Dermonth et al., 2008). As conferred in this evaluation, this
technique could employ physical and chemical processes to remove heavy metal
toxins from soils. In the process of the soil washing method, the soil particles in
the site with bulk metal contamination will be removed from the soil portion.
With this, metal pollutants will be vanished from the soil particles by aqueous
chemical substances and retrieved from a solution on the dense substrate, and a
mixture of chemicals (compound) (Dermonth et al., 2008). In many situations,
the detached soil impurities then drive to harmful waste in landfills. So, in
extracting the bulk of impurity from the terrestrial environment, a big portion is
retained in the soil that could be usually recycled in the area being remediated,
or the user of the new area as fill, and secure proper disposal of somewhat
inexpensively as non-hazardous waste materials in the site.
So, soil washing is mainly and commonly used in the so-called soil
remediation method since it totally removes the metal contaminants from the
soil and henceforth warrants the quick clean-up of a terrestrial contaminated site
(Wood et al., 2015). With specific and appropriate soil criteria, it reduces long-
term accountability, with effective and lucrative soil solution, and it may yield
recyclable material (GOC, 2016). For its disadvantages, the metal contaminants
could be moved to different sites, or the concerned agencies must strictly monitor
and evaluate the threat of diffusing chemically contaminated soil. Thus, soil
excavation is a relative option when involved huge volumes of soil need to be
removed, or proper toxic disposal of waste is required.
solutions varies significantly in various soil types because acidic chemicals degrade
soil crystallinity structure at a lengthy time frame. In this regard, when damaging
washes are less, the organic acids and chelating components or agents are frequently
recommended as substitutes for the conventional use of acid (Yu et al., 2014).
The usual organic acids, including of this technique are formic, aconitic,
oxalic, acetic, malonic, itric, fumaric, and succinic acids are usual and natural
products of exudated roots and microbial secretions residue decomposition in
the terrestrial environment (Naidu et al., 2016). For metal dissolution of carbon-
based acids is possible to become a mobile metal portion existing in the soil biota
(Labanowski, 2008). Chelating agents of carbon-based acids could extricate the
interchangeable reducible portions of metals by chemical extractant procedures
(Dermonth, 2008). In chelating agent mixture for activating heavy metals, it
is evaluated that the remaining uncertainties are the optimal option for this
application. So, in the quantification and identification of co-existing metal in
the organisms of soil (before and after), treatment is important to design the
efficacy of this method (Kirpichtchikova, 2006). Presently, the changes in heavy
metals in the uptake in a sandy loam soil before and after washing with chelating
agent organic acids showed citric acid. EDTA seemed to bid better possibilities
for remediating the permeable soil structure (Wuana, 2010).
Phytoremediation
In this technique, the use of related microbiota, vegetation, and agronomic
methods to remove environmental soil contaminants are a friendly and harmless
way (Cunningham et al., 2015). The knowledge of this technique in metal bio-
accumulating plants in the contaminated/affected sites to remove dangerous
metals compounds was introduced before. Still, its idea has been applied to
wastewater discharges (Henry et al., 2000). So, the medium could degrade organic
impurities or eliminate and stabilize heavy metal impurities. With this, the
techniques /methods applied in phytoremediation metal pollutants are somewhat
dissimilar from other methods/techniques in the remediated areas with organic
contaminants. Because of the new technology application, phytoremediation is
still typically in its testing stages. Though it has been confirmed conclusively in
some places of different contaminants, phytoremediation is a powerful method
in removing soil contaminants. It is efficient and applicable to a traditionally
remedial method as a vital phase of the remedial soil process.
Its advantages compared to conventional remediation show more
economically practical with using similar tools. This phytoremediation
technique is less disrupting to the soil environment without involving new plant
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Phytostabilization
In the technique of phytostabilization, the prime concern is the use of
plants to halt the sediment in soil (USAPE, 2015), where toxin in the soil will be
absorbed by plant roots (rhizosphere). It believes that this reduces the mobility
of preventing soil impurities migration from the groundwater to reduce bio-
availability of the impurity hence avoiding its spread in the food web. When
phytostabilization is in plants, it can reduce the volume of H2O penetrating
through soil ground that may cause the formation of hazardous soil as a result, and
avoid soil corrosion and can circulation of toxic metal in the other sites (Raskin
& Ensley, 2000). This technique may occur in the process of absorption or metal
reduction. This is very beneficial because of the clean-up of heavy metals (Jadia
& Fulekar, 2009). This may use to re-establish a plant environment on bared
areas because of its metal contamination. When the environment of tolerant
organisms has been established, the possibility of wearing away is reduced. So, in
this regard, the phytostabilization is very important because the disposal of toxic
material is not required with very good protection of surface soil.
CONCLUSIONS
Based on the results of this review paper, findings show that the concentrations
of heavy metals (Hg, Cd, Cr, Cu, Pb, Mg, Fe, Zn) in terrestrial ecosystem
varies in the different parts of the country. Mercury (Hg) is the most hazardous
element in the sites where mining lies neither terrestrial nor water ecosystem. The
contamination in soil is hazardous and severe compared to other heavy metals.
These ecological pollutants are found to be heavy metals that occur in the soil and
in the plant body, airborne heavy metals, and pesticides that come from various
sources. These pollutants are present in the Philippines’ three islands in Luzon,
Visayas, and Mindanao, where most metallic mines are actively operational.
As mentioned in the findings, pesticides are also reported as pollutants in the
terrestrial ecosystem in Benguet, Luzon, and crop pesticidal residues. For plants
in Cebu, landfills found heavy metals of cadmium (Cd) and chromium (Cr). In
Mindanao, most heavy metals include mercury (Hg), cadmium (Cd), copper
(Cu), zinc (Zn), and lead (Pb). These heavy metals come from gold mining,
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IAMURE International Journal of Ecology and Conservation
including airborne heavy metals like mercury (Hg) and methylmercury found in
gold processing and refining plants.
With the complexity of pollutants present in the Philippines, the choice of
appropriate specific biomarkers for terrestrial biomonitoring varies in different
regions. Hence, identifying the single most suitable biomarker for the same
pollutant that would apply to all regions still needs further investigations even
though the most commonly used biomarker would be far from ideal. Still,
the combinations of several biomarkers for a particular pollutant may give
complementary data.
Lastly, the role of the phytoremediation strategy of advanced technology
(immobilization techniques, soil washing, and chemical extractants for soil
washing, phytoremediation), photostabilization (plants), and phytoremediation
species absorb a high amount heavy metal. Thus, bioaccumulation of heavy
metals by agents plays a vital role in the elimination of contaminants from the
soil because they possess unique remarkable metabolic (species) and absorption
capabilities that enable them to decrease or remove heavy metal contamination.
In conclusion, the country must regulate and make remediation in soil strategies
for reducing metal bio-availability equated with possible reduced risk for long
term solutions and improve knowledge in the environmental contamination in
a global vision.
RECOMMENDATIONS
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