Water and Environment Journal.

Print ISSN 1747-6585

Evaluation of the accumulation of heavy metals in water,

sediments and plants of a coastal zone of Mexico
Juan Miguel Gómez-Bernal 1
, Esther Aurora Ruiz-Huerta 2
, María Aurora Armienta Hernández 3
,
Patricia Ramírez Romero 1
& Margarita Elizabeth Gallegos-Martínez 1

 Departamento de Hidrobiología, División de Ciencias Básicas y de la Salud, Universidad Autónoma Metropolitana Unidad Iztapalapa, Iztapalapa,
1

Mexico; 2 Departamento de Peligros y Riesgos por fenómenos Naturales, Instituto de Geofísica Unidad Michoacán, Universidad Nacional Autónoma de México,
Michoacán, Mexico; and 3 Departamento de Recursos Naturales, Instituto de Geofísica, Universidad Nacional Autónoma de México, Coyoacan, Mexico

Keywords
accumulation; coastal zones; heavy metals;
mangrove; seagrass; sediments.
Correspondence
Juan Miguel Gómez-Bernal, Departamento de
Hidrobiología, División de Ciencias Básicas y
de la Salud, Universidad Autónoma
Metropolitana Unidad Iztapalapa, Iztapalapa
09340, Mexico.
Email: gupi02@yahoo.com.mx
doi:10.1111/wej.12655
Abstract
A preliminary environmental assessment of four heavy metals (Mn, Pb, Zn and
Fe) on the coast of Campeche, Mexico was carried out. Surface sediments (0–
10 cm), water and plants were collected in four sites of the coastline to obtain
information about the levels and spatial distribution of the selected elements.
The bioconcentration factor (BCF) was calculated for plants, where the BCF of
Mn (3.375–3.558) and Zn (0.291–0.888) were high for Conocarpus erectus (button
mangrove) and the BCF of Fe ranged from 0.022 to 0.023 in Laguncularia rac-
emosa (white mangrove). This study showed that a significant source of metal
contamination in the coastline of Campeche could be the discharge of municipal
sewage. The relationship among metals, water, sediments and plants revealed a
distinct behaviour of metals transportation in the marine environment. Mangroves
operated as excluder species for nonessential metals (Pb) and accumulators for
essential metals (Zn). Results showed that mangroves could be employed as a
phytostabiliser of heavy metals.

Introduction biodiversity and as an effective sink for wastewater.

The coastal zones of Mexico have been subjected for sev-
eral years to humans pressure by the direct or indirect
deposit of wastes, thereby contributing to the detriment
of their ecological values. Therefore, it is essential to per-
form analyses on sediments, plants and water in order to
assess the quality of coastal environments. These environ-
ments are potentially at risk because of high concentrations
of metals in sediments (Jayaprakash et al., 2015). Similarly,
other pollutants that modify the quality of water are organic
matter, nutrients, fats and oils, detergents and pesticides,
among others, which can affect the environment (Ramos
et al., 2003). Sediments can be important indicators for
monitoring contaminants in aquatic environments (Atgin
et al., 2000). Sediments pollution with various types of
hazardous and toxic substances has been reported (Fukue
et al., 1999; Zabetoglou et al., 2002); trace elements and
hydrocarbons, among others, can accumulate via disposal
of liquid effluents. Therefore, the evaluation of metal dis-
tribution in surface sediments is useful to assess pollution
in the marine environment (Bellucci et al., 2002; Buccolieri
et al., 2006).
Mangroves prosper along the coastline throughout most
of the tropical and subtropical zones (Lin, 1999). This forest
play essential ecological roles in coastline protection,
606
Mangroves may be under aerobic and anaerobic conditions,
contribute considerably to metals removal from wastewater
and can increase the content of heavy metals in sediments
(Wang et al., 2011). The ability of some plant species to
accumulate high concentrations of heavy metals in roots,
stem, leaves or fruits, represents an important strategy in
the remediation of sites polluted by heavy metals. The
identification of plants growing in metals polluted sites
represents an interesting model for studying heavy metal
mechanisms of tolerance and accumulation. This accumula-
tion of heavy metals depends on the concentration and
availability of the soil type, solubility in water and plant
species. Some plant species have developed strategies for
avoiding toxic concentrations buildup of metals within the
cell. These heavy metals cannot be degraded in the envi-
ronment, so they are continuously deposited in water bodies
and soil. Although some metals are absorbed and accu-
mulated by plants, these can be stored in leaves, stem
and roots, which represents an essential strategy in the
remediation of contaminated sites with heavy metals.
Metals are dangerous pollutants for their toxicity, persis-
tence in nature and ability to be incorporated into food
chains (Sakan et al., 2009); these enter the environment
in two ways: from natural and anthropogenic sources. The
bioconcentration factor is used to establish the translocation
Water and Environment Journal 35 (2021) 606–616 © 2020 CIWEM.
J. Gómez-Bernal et al.
and the magnitude of metal pollution in the environment.
The identification of plants growing in contaminated sites
with heavy metals represents an interesting model for
researching metals mechanisms of tolerance, accumulation
and removal. Some studies have been carried out in
Campeche on water quality for human consumption and
some studies about sediments and organisms. However, the
impact of metals in plants growing in the coastal zone has
not been assessed (Vázquez et al., 1992; Gold et al., 1993).
The aquatic ecosystem gets affected by the decay of plants
and vegetation, atmospheric particulates and discharge of
municipal waste. Mangrove and seagrass plants comprise a
group of plants that dominate the coastlines of many tropi-
cal and subtropical regions. Campeche is a region that has
a complex ecosystem and is influenced by anthropogenic
activities, including tourism (boat rides, seafood restaurants),
fishing, as well as commercial and domestic wastewater
discharges. The present study aimed to determine the con-
centration, distribution and source of selected metals (Mn,
Pb, Zn and Fe) in sediments, water and plants of a coastal
zone in Campeche, México to assess the contamination status
as well as the possible influence of anthropogenic activities
Fig. 1. Distribution of sample points of water, sediments and plants species in the coastline of Campeche, México. [Colour figure can be viewed at
wileyonlinelibrary.com]
Water and Environment Journal 35 (2021) 606–616 © 2020 CIWEM.
Evaluation of the accumulation of heavy metals in water, sediments and plants of Mexico
and to compare the metals contamination levels with others
sites in Mexico.
Materials and methods
Study area
Plants were collected in a coastal zone (along 2.850 km)
of Campeche, Mexico (Fig. 1). Campeche is a city located
at 19.84 latitude and −90.53 longitude and 4 meters above
sea level. Approximately 899 931 inhabitants live in
Campeche. The annual temperature varies between 26.4°C
and 27.8°C, and the range of annual precipitation is 800–
1100 mm (Rico-Gray, 1982). The composition of the rocks
in the study area are limestones, which are divided into
three: the calcareous armor, soft sub-superficial limestone
and coastal calcareous sand. The compositions of the
dominant soils of Campeche are vertisol, letosol and phae-
ozem. The coastal vegetation of this area includes coastal
dune vegetation, mangrove swamp, low flood forest, pasture
land, tular and medium forest sub-caducifolia (Barrera, 1982;
Rico-Gray, 1982; Durán, 1987; Yáñez-Arancibia, 1996). The
607
Evaluation of the accumulation of heavy metals in water, sediments and plants of Mexico J. Gómez-Bernal et al.

Table 1  Water’s physicochemical parameters in the sample points and maximum limits (mg/L) of pollutants in wastewater discharges into water and
national properties (NOM-001-SEMARNAT-1996)

Sampling point pH Ω µs/cm CO2−

3 HCO−3 SO2−
4 Cl− F− Na+ K+

P1-1 7.88 40 900 19.5 183 2344.1 17 350 0.822 6750 311
P1-2 7.91 41 000 16.5 192.15 2286.3 17 500 0.819 6700 310.5
P2-1 7.5 23 100 326.96 1066.5 10 087 0.553 6185 237
P2-2 7.77 32 800 275.72 1788.1 13 400 0.69 6215 245.3
P3-1 8.13 39 100 25.2 175.68 2260.7 15 362 0.784 6200 292.5
P3-2 8.19 39 100 21.6 180.56 2237 16 550 0.806 6280 290
P4-1 7.97 2570 419.38 102.69 650.5 0.232 329 14.05
P4-2 8.12 3040 18 381.25 103.33 830.5 0.204 329.5 14.03

Sampling point Ca2+ Mg2+ Balance NO3− Mn Zn Cd Cu Fe

P1-1 376.66 1048.74 −14.2 * ND ND ND ND ND

P1-2 405.63 1042.48 −14.7 * ND ND ND ND ND
P2-1 328.37 814.07 4 18.7 ND ND ND ND ND
P2-2 347.68 831.64 −7.3 * ND ND ND ND ND
P3-1 415.3 1001.5 −11.9 * ND ND ND ND ND
P3-2 405.63 995.63 −14.87 * ND ND ND ND 0.14
P4-1 146.8 56.22 −1.4 * ND ND ND ND 0.1
P4-2 160.32 51.54 −8.3 * ND ND ND ND 0.19
permissible maximum 10 0.1 4
limits

main economic activities are oil extraction, tourism, wood
industry, agriculture and fishing.
Sampling sites
Four sampling sites were selected in the coastline area of
Campeche: close to a retail store (P1), boat area (P2),
restaurant area (P3) and mangrove area (P4) (Fig. 1). The
selection of each sampling point was designed according
to the following methods: sediment collection was carried
out where the most abundant plant species were observed
in each sampling point at a depth of 10 cm, water samples
were taken next to one side of the plants (Fig. 1). Leaves
were collected from the plant samples for species identi-
fication by the Metropolitan Herbarium at the Universidad
Autónoma Metropolitana-Iztapalapa in November of 2017
(UAM-I).
Analytical methods
Water samples were collected in 250 mL polyethylene bot-
tles previously washed with HCl (1 N) and rinsed with
deionized water. Temperature and pH were measured with
portable multiparametric equipment (HANNA, HI 9829).
Water samples were also collected at each point acidifying
with HNO3 (0.1 M), filtered through a 0.45 μm pore mem-
brane and stored under refrigeration until laboratory analy-
sis. The analysis of main cations and anions were carried
out using the described techniques by Armienta et al.
(1987) and APHA (2005). Metals concentrations were deter-
mined by atomic absorption spectrometry (Perkin Elmer
AAnalyst 200).
Sediment samples were dried, homogenized and sieved
through 0.063 mm. Half a gram of each sample was weighed,
10 mL aqua-regia (HNO3 and HCl 3:1) were added and the
mixture was digested during 30 min in a microwave oven
CEM, MARSXpress. The digestions were taken to 100 mL
with deionized water and filtered through Whatman 40
paper. Triplicates of each sample were treated in this way.
Concentrations of Mn, Pb, Zn and Fe in sediments were
determined by flame atomic absorption spectrometry
(Perkin Elmer AAnalyst 200). High purity standards (Certified
reference materials NIST traceable) and NIST Montana soil
2711 were used for calibration. The percentage of heavy
metals recovery of the certified reference material Montana
soil was: 81.87% for Mn, 93.76% for Pb, 79% for Zn and
82.72% for Fe.
Four plant samples were randomly collected; these were
carefully washed in the laboratory with running tap water,
followed by three rinses with deionized water (18 MΩcm-1,
Milli-Q Millipore) and a rinse of tri-distilled water. All plants
were carefully divided into roots and leaves. A dry weight
of the collected plants was obtained after heating at 60°C
for 75 h in an oven; samples were then crushed, sieved
(<325  μm), homogenized and weighed. The digestion of
plant parts was performed by adding concentrated HNO3
to 0.5 g of each part and heating during 30 min in a
microwave oven CEM, MARSXpress. The accuracy of the

608 Water and Environment Journal 35 (2021) 606–616 © 2020 CIWEM.

J. Gómez-Bernal et al.
procedure was determined by analysing the certified refer-
ence material peach leaves (SRM 1547). Concentrations of
Mn, Pb, Zn and Fe in plants were determined by flame
atomic absorption spectrometry (Perkin Elmer AAnalyst
200). The percentage of recovery in heavy metals of the
certified reference material of peach leaves was 96.62%
for Mn, 122.70% for Zn and 73.79% for Fe. The QA/QC
protocol included the regular control of standards by routine
analysis of SRMs; determination and minimization of sample
contamination by frequent analysis of blank samples and
control of uncertainty induced because of detection limits
of Mn ( 0.1 mg/L), Pb (0.2 mg/L), Zn (0.05 mg/L) and Fe
(0.3 mg/L).
The metals concentration values were used to estimate
the Bioconcentration Factor (BCF). The BCF was defined
as the average of the concentration of the metal in plant
tissues divided by the concentration of the metal in soil
(Ruiz-Huerta and Armienta-Hernández, 2012; Gómez-Bernal
et al., 2014).
BCF = Concentration of metals in roots/Concentration
of metals in the sediments.
Statistical methods
SPSS 17 software was used for all statistical analysis (SPSS
Inc. Released 2008). A correlation matrix was created with
data on physicochemical parameters in water, heavy metals
in sediments and plants; P < 0.05 was used to determine
statistical significance.
Results and discussion
Physicochemical parameters values are presented in
Table 1. The pH of the water ranged from 7.5 to 8.19,
complying with Mexican threshold values for the protec-
tion of aquatic life in freshwater and wetlands (LFDMA,
2019), which is 6.5 to 8.5, also with USEPA´s (1986) ambi-
ent quality criteria that establishes mean pH values
between 6.5 and 9.0 for the protection of aquatic life.
The carbonates (CO2− 3 ) varied from 16.5 to 25.2 mg/L and
bicarbonates (HCO−3 ) from 175.68 to 419.38 mg/L (Table 1).
These parameters are important for a variety of biological
processes. The sulphates (SO2− 4 ) in water ranged from
102.69 to 2344.1 mg/L. Chlorides varied from 650.5 to
17 350 mg/L. Fluoride ranged from 0.204 to 0.822 mg/L,
complying with the protection of aquatic life freshwater
and wetlands (LFDMA, 2019), which is 1 mg/L. Sodium
in water varied from 329 to 6750 mg/L and potassium
from 14.03 to 311 mg/L. Calcium (Ca2+) ranged from 146.8
to 415.3 mg/L and magnesium from 51.54 mg/L to
1048.74 mg/L. Nitrates (NO−3 ) varied from the below the
detection limit to 18.7 mg/L in only one sample (Table 1).
The concentrations of heavy metals in water for Cu, Cd,
Water and Environment Journal 35 (2021) 606–616 © 2020 CIWEM.
Evaluation of the accumulation of heavy metals in water, sediments and plants of Mexico
Mn and Zn were below the detection limit complying
with the protection of aquatic life freshwater and wetlands
(LFDMA, 2019), which is 0.02 mg/L for Zn, 0.004 mg/L
Cd, 0.05 mg/L Cu. The range of Fe was from 0.1 to
0.19 mg/L in only three sampled points, complying with
the protection of aquatic life freshwater and wetlands
(LFDMA, 2019), which is 1 mg/L. The limit for Zn proposed
by WHO (1980) is 5 and 0.02 mg/L by LFDMA (2019).
The limits proposed by WHO (1980) and LFDMA (2019)
were not exceeded.
The highest values of sulphates, chlorides, fluorides,
sodium, potassium and manganese were observed at sam-
pling point P1 and those of pH, carbonates and calcium
at sampling point P3. Sampling point P4 presented the
highest bicarbonate concentrations. In contrast, the P2
sampling site had no high concentrations, which can be
assumed was because of the transit of boats that move
the water and remove the sediments. For the sampling
point P1, the anthropogenic activity could be the factor
influencing the measured parameters. These parameters
could be originated mainly from domestic sewage, industrial
wastewater and agricultural fertilizers.
Ayala-Pérez and Can-González (2009) reported the tem-
poral and spatial behaviour of temperature, salinity, dis-
solved oxygen and pH in the littoral portion of Campeche.
The temperature registered its maximum values in August
and the minimum values in December (35.48°C and
23.85°C, respectively). Salinity ranged between 26.17 UPS
and 42.17 UPS (with minimum values in October and
maximum values in May), for dissolved oxygen minimum
values of 3.24 mg/L and maximum values of 12.87 mg/L
(in June and May, respectively) were recorded; finally,
the pH presented values between 7.61 in September and
8.55 in July, finding the highest values near the man-
groves. In our study, the highest values were found in
sampling point P3, where T. testudinum grows in a waste-
water discharge area.
Previous studies of the coastal zone of Campeche have
focused on the determination of hydrocarbons, polychlorin-
ated biphenyls (BPCs) and organochlorine pesticides (Rivera
et al., 2012). Thus, to have a better evaluation of the
contamination status of this area, it was necessary to carry
out the quantification of metals in different environmental
matrixes.
Chemical determinations were carried out to understand
the accumulation mechanisms of metals in the coastline,
where mangrove, seagrass and other aquatic plants grow;
with these numbers, the BCFs were calculated to evaluate
the relationship between sediments and plant species.
Metals’ contents are reported in Table 2 expressed as mil-
ligram per kilogram on a dry basis except for Fe (these
values are reported as percentages). Mn ranged at the
sediment sampling points from 32.99 to 589.76 mg kg−1.
609
Evaluation of the accumulation of heavy metals in water, sediments and plants of Mexico J. Gómez-Bernal et al.

The highest concentration was found in P3-2 only rarely. SQuiRTs does not propose a limit for Mn in
(589.76 mg kg−1) (Table 2). Total metal dry weight concen- sediments.
trations were compared with marine sediment screening Zn concentrations did not exceed Alloway’s (1995) pro-
values reported by NOAA SQuiRTs, which are associated posed limit of 70 to 400 mg kg−1 in soils in any of the
with several probabilities of adverse biological effects sampling points. The concentration of Zn in the present
(Buchman, 1999). Threshold Effects Levels (TELs) represent study was lower than the proposed TEL (124 000 mg kg−1)
the level below which adverse effects are expected to occur for sediments (Buchman, 1999). The sampling site with the
highest concentration of Zn was P4-2 (159.92 mg kg−1)
Table 2  Concentrations of Mn, Pb, Zn (mg kg−1) and Fe (%) in sediments of (Table 2). Pb concentrations ranged from 15 to 23.99 mg kg−1
the coastline to Campeche, México in the sediments (Table 2); these values did not exceed the
Sampling point Mn Pb Zn Fe (%) SQuiRT limit of 30 240 ppm; neither Alloway’s (1995) limit
for soils of 100 to 400 mg kg−1. The highest Pb concentra-
P1-1 52.97 21.49 94.94 3.77
tion was found at sample points P3-2 (23.99 mg kg−1) (Table 2).
P1-2 56.98 20.49 94.97 4.12
Fe concentration varied from 4.20 to 18.37% in sediments.
P2-1 36.99 23.49 67.47 5.00
P2-2 32.99 21.50 59.99 4.62 The highest concentration was found at sampling point
P3-1 68.47 23.49 134.93 18.37 P3-1 (18.37%) (Table 2); this could be related to the con-
P3-2 589.76 23.99 109.96 13.24 centrations present in the water (Table 1). Iron and man-
P4-1 57.49 15.00 134.99 3.75 ganese in the water can form complex hydroxy compounds
P4-2 69.47 16.99 159.92 4.20
that may eventually precipitate (Riley and Chester, 1971).
Standard 510.05 118.51 337.53 32.50
SQuiRTs proposed a limit for 30 240 mg kg−1 in Fe in sedi-
Recovery 81.87% 93.76% 79.00% 82.72%
ments, which was exceeded in all samples (Buchman, 1999).

Fig. 2. Distribution maps of concentration of heavy metals (mg kg−1), Fe (%) in sediments of the coastline of Campeche, México. [Colour figure can be
viewed at wileyonlinelibrary.com]

610 Water and Environment Journal 35 (2021) 606–616 © 2020 CIWEM.

J. Gómez-Bernal et al.
The distribution patterns of heavy metals shown in Fig. 2
(Mn, Pb, Zn and Fe), were depicted through the interpola-
tion of metal concentrations using Surfer 15.0 software.
As shown, heavy metals concentrations increase towards
the central part (P3) of the study area (Fig. 2). This behav-
iour could be because of the City´s wastewater discharge,
where pH and carbonates play an essential role as sinks
for Mn, Pb and Fe.
Raj and Jayaprakash (2008) found in marine sediments
of Bay of Bengal at Ennore, southeast coast of India values
of Mn (248–460 µg/g), Pb (24.9–40 µg/g) and Zn (71.3–
201 µg/g) higher than this study, except for Fe (1.7–3.7%),
in all sampling points (Table 2). These authors showed that
the primary sources of metal contamination in the Ennore
shelf are land-based anthropogenic ones, such as industrial
and municipal wastewater discharges and run-off. Jonathan
et al. (2004) found the following values in the Gulf of Mannar
for Mn (305 µg/g), Pb (16 µg/g), Zn (73 µg/g) and Fe (1.26%).
In China shelf sea, Zhao and Yan (1992) found the follow-
ing concentrations of Mn (530 µg/g), Pb (20 µg/g), Zn
(65 µg/g) and Fe (3.1%). In Tokio Bay, Fukushima et al.
(1992) found values for Mn (1098 µg/g), Pb (50.68 µg/g),
Fig. 3. Distribution maps of the studied vegetable species in México. (a) Avicennia germinans; (b) Laguncularia racemosa; (c) Conocarpus erectus and (d)
Thalassia testudinum. [Colour figure can be viewed at wileyonlinelibrary.com]
Water and Environment Journal 35 (2021) 606–616 © 2020 CIWEM.
Evaluation of the accumulation of heavy metals in water, sediments and plants of Mexico
Zn (322 µg/g) and Fe (3.77%). The previous studies show
similar characteristics to those found for the Campeche
coastline, except for Fe that in this study was higher at
all sampling sites. The distribution of heavy metals depends
on their physical and chemical properties and those of
the environment; they can be mobilized and transported
in the ecosystems causing damage to the biota; therefore,
metals monitoring and control are necessary to protect
and preserve the environment, as well as to define mitiga-
tion policies and actions for conservation. These monitoring
of heavy metals concentrations in the organs of living
organisms could provide direct information of the contami-
nants fraction with direct ecotoxicological relevance, for
example, the bioavailable forms, and also could detect
early signs of environmental disturbance in coastal zones
in mexico altering the distribution of the vegetation and
being able to reduce it (Fig. 3).
The plants collected in sampling point P1were identified
as Laguncularia racemosa (mangrove); Conocarpus erectus
(mangrove) in P2; Thalassia testudinum (seagrass) in P3
and Avicennia germinans (mangrove) in P4. All mangrove
species are subject to special protection in Mexico,
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Table 3  Concentrations of Mn, Pb, Zn (mg kg−1) and Fe (%) in plants of the coastline to Campeche, México

Sampling points Plants Mn Pb Zn Fe (%)

P1-1 Laguncularia racemosa 22.46 ND 17.47 0.087

P1-2 Laguncularia racemosa 22.44 ND 17.45 0.092
P2-1 Conocarpus erectus 124.81 ND 59.91 0.076
P2-2 Conocarpus erectus 117.38 ND 17.48 0.75
P3-1 Thalassia testudinum 63.75 ND 25.00 0.096
P3-2 Thalassia testudinum 76.14 ND 28.71 0.106
P4-1 Avicennia germinans 29.90 ND 18.69 0.030
P4-2 Avicennia germinans 29.89 ND 24.91 0.036
Standard Peach leaves 94.49 ND 22.05 0.162

ND, not detectable.

according to NOM-059-SEMANART-2010. Mangrove ecosys- Zinc is an essential element that is related to physiologi-
tems are highly productive and large quantities of nutrients cal and metabolic processes in all plants. However, in high
are deposited on the coastal coastline, these forest, stabilize concentrations, it can be toxic. The normal range in plants
the coastal zone and provide security for seagrasses and proposed by Reeves and Baker (2000) is of 20–400 mg kg−1,
a variety of fish, that have commercial importance. Some which was not exceeded at any sampling point. Zn ranged
studies have found metals (Cu, Zn, Pb, Fe, Mn and Cd) in the studied plants from 17.45 to 59.91 mg kg−1. C. erec-
accumulated predominantly in the root tissues, rather than tus presented the highest Zn in sampling point P2-1 with
in the foliage of numerous mangrove species such as 59.91 mg kg−1 (Table 3). This accumulation of Zn is higher
Avicennia spp., Aegiceras spp., Rhizophora spp. and than that measured in sediments (Table 2). The possible
Kandelia spp. (Said and Zaidi, 1994; Lacerda, 1997; Peters physiological mechanism responsible for variations in uptake
et al., 1997; Chen et al., 2003) collected at other sites. and translocation at the root level include processes at
Iron is an essential element for plants (Wintz et al., 2002) the root´s rhizosphere.
and plays a vital role in enzymatic processes such as chlo- In contrast, the high concentration of Zn in sediment
rophyll and protein biosynthesis as well as in cellular res- from sampling point P4-2 (159.92 mg kg−1) was not observed
piration. On the contrary, excessive accumulation of this in plant accumulation (24.91 mg kg−1) (Table 3). This behav-
element damages tissues through free radicals production iour indicates the low availability of Zn to the plants at
(Bienfait, 1988; Engin et al., 2015). Markert (1992) proposed the sampling point (Table 2). The concentration of Pb in
5–200 mg kg−1 as phytotoxic concentrations for Fe; this plants was below the detection limit at all points.
range was exceeded in the sampled aquatic plants. The potential exposure to metals contaminated sediments
Maximum concentrations of Fe occurred in points P3-1 and was not reflected in mangroves; they appear to be highly
P3-2 (0.096 and 0.106%, respectively) in the leaves of T. resistant to metals; therefore, the concentrations of metals
testudinum (Table 3), these high Fe concentrations may required to impart significant adverse effects on mangroves
be because of the reduction of Fe (III) to Fe (II) in the may be several orders of magnitude higher than those
rhizosphere as a product of microbial activity in the envi- that can be accumulated by these plants. This tolerance
ronment, increasing Fe bioavailability. The low accumulation has been attributed in part to the ability of mangroves to
of Fe in A. germinans leaves (0.030 to 0.036%) could be exclude metals uptake at the root restricting its accumula-
because of the large number of plants growing in the area. tion in the shoot (MacFarlane and Burchett, 2002). However,
Manganese is an essential element for plants and is used the absence of monitoring and control of contaminats at
in photosynthesis and many redox enzymatic processes
Table 4 Bioconcentration factors of heavy metals in plants growing in
(Carranza-Álvarez et al., 2008), in contrast with Pb, Cd or
the coastline in Campeche, México
Cr. However, Mn concentrations over 300 mg kg−1 are toxic
for plants (Kabata-Pendias and Pendias, 2001); this value was BCF Mn Pb Zn Fe
not exceeded at the sampling points. The highest concentra-
L. racemosa 0.424 0.000 0.184 0.023
tions of Mn occurred in points P2-1 and P2-2 (124.81 mg kg−1 L. racemosa 0.394 0.000 0.184 0.022
and 117.38 mg kg−1, respectively) in the leaves of C. erectus C. erectus 3.375 0.000 0.888 0.015
(Table 3), these Mn values are higher than those measured C. erectus 3.558 0.000 0.291 0.016
in sediments (Table 2). In contrast, at sampling point P3-2, T. testudinum 0.931 0.000 0.185 0.005
the high concentration of Mn in the sediment (589.76 mg kg−1) T. testudinum 0.129 0.000 0.261 0.008
A. germinans 0.520 0.000 0.138 0.008
was not reflected in the concentrations measured in the
A. germinans 0.430 0.000 0.156 0.009
plant, although these are not low (Table 3).

612 Water and Environment Journal 35 (2021) 606–616 © 2020 CIWEM.

 Table 5  Correlation matrix (r) of physicochemical parameters in water, heavy metals in the sediments (S) and plants (P) of the coastline of Campeche, Mexico. Significant r values have been highlighted in
bold

pH Ω µs/cm CO2−
3 HCO−3 SO2−
4 Cl− F− Na+ K+ Ca2+ Mg2+ FeP MnP PbP ZnP FeS MnS PbS ZnS

pH 1
Ω µs/cm −0.008 1
J. Gómez-Bernal et al.

CO2−
3
0.565 0.31 1

HCO−3 −0.22 −.966** −0.416 1

SO2−
4
0.068 .996** 0.339 −.979** 1

Cl− −0.043 .998** 0.247 −.957** .991** 1

F− −0.023 .999** 0.309 −.960** .994** .998** 1

Water and Environment Journal 35 (2021) 606–616 © 2020 CIWEM.

Na+ −0.297 .948** 0.283 −.852** .918** .955** .952** 1

K+ −0.161 .983** 0.298 −.922** .965** .987** .985** .986** 1

Ca2+ −0.05 .982** 0.406 −.943** .969** .980** .982** .964** .987** 1

Mg2+ −0.158 .981** 0.316 −.921** .963** .985** .984** .987** 1.000** .989** 1

FeP 0.039 .959** 0.442 −.946** .950** .960** .962** .930** .962** .984** .965** 1

MnP −0.546 0.15 0.788 0.02 0.09 0.152 0.163 0.391 0.257 0.265 0.267 0.253 1
PbP

ZnP −0.557 −0.119 0.559 0.195 −0.186 −0.091 −0.102 0.149 0.053 0.037 0.063 0.08 0.627 1

FeS 0.534 0.419 .935* −0.534 0.447 0.376 0.416 0.314 0.38 0.5 0.393 0.556 0.176 0.066 1
MnS 0.511 0.265 0.25 −0.354 0.286 0.274 0.282 0.171 0.22 0.289 0.23 0.44 0.095 0.046 0.47 1

PbS −0.172 .809* 0.713 −.760* .778* .810* .814* .890** .867** .886** .875** .905** 0.576 0.414 0.569 0.371 1

ZnS .780* −0.508 0.217 0.276 −0.447 −0.538 −0.525 −.711* −0.601 −0.518 −0.599 −0.449 −0.649 −0.293 0.268 0.097 −0.536 1

a
It can not be calculated because at least one variable is constant.
*The correlation is significant at the 0.05 level (bilateral); **The correlation is significant at the 0.01 level (bilateral).

613
Evaluation of the accumulation of heavy metals in water, sediments and plants of Mexico
Evaluation of the accumulation of heavy metals in water, sediments and plants of Mexico
the coastal environments, urbanization and industrialization
are putting mangroves at risk because there is no real
implementation in the regulations. In addition to this, the
few research studies of mangroves and coastal areas in
Mexico. Therefore, this study provides a guideline to con-
tinue investigating the importance of coastal ecosystems
in Mexico and to apply the laws (Fig. 3).
Table 4 shows the bioconcentration factor (BCF) of all the
studied plants. The highest BCFs were obtained in C. erectus
for Mn in points P2-2 and, P2-1 (3.558 and 3.375, respec-
tively); and, for Zn (0.888 and 0.291) in L. racemose. Different
plant uptake rates explain the Zn bioaccumulation differences
and physical processes such as root intrusion, water and
ion fluxes and their relations with the metal solubilization
kinetics in sediment and biological differences among plants
(age, height, diameter). All plants also presented the highest
Fe BCF at points P1-1 and P1-2 (0.023 and 0.022, respec-
tively) (Table 4). The previous BCFs indicate the accumulation
of metals, mainly Mn in C. erectus (Table 4). A high biocon-
centration factor for metals at low external concentrations
is essential for phytoremediation because this process is a
more efficient cost option than other conventional techniques
for treating large volumes of wastewater with low concentra-
tions of contaminants. C. erectus can act as a filter for the
capture of Mn and Zn from anthropogenic activities and
thereby improve the quality of water and sediments. All of
these results confirm the ability of mangrove species and
seagrasses to accumulate heavy metals in different parts of
the plant. However, it seems to depend significantly on the
specific type of aquatic plants species and the physicochemi-
cal characteristics of the sediments.
Albers and Camardese (1993) reported that macrophytes,
compared with other plant species, accumulate metals with
a similar capacity. Also, seagrasses have a high metal bio-
accumulative capacity since they interact directly with both
the water column through the leaves and the sediment
pore water through the roots (Ralph et al., 2006).
Mejías et al. (2013) studied three species of mangrove
at Las Cucharillas Marsh in Puerto Rico; these are Rhizophora
mangle, Laguncularia racemose and Avicennia germinans.
The study suggests that A. germinans is the only species
to significantly bioconcentrate Hg (10%), Al (5%) and Fe (5%).
Usman et al. (2013) reported the ability of A. marina
to bioaccumulate heavy metals on the coast of the Red
Sea, Saudi Arabia; Cd, Cr, Cu, Ni and Zn had BCF values
of leaf range from 0.12–2.36, 0.33–6.43, 1.25–9.08, 0–1.02
and 0.20–4.71, respectively. These results suggest that A.
marina can bio-accumulate Cu and Cr.
Table 5 shows the correlation of sediments and plants
metal content with water’s physicochemical parameters,
indicating a high negative correlation between CO2− 3 and
Ec (−0.966); and HCO−3 negatively with conductivity and all
the main anions and cations. The other ions were positively
614
J. Gómez-Bernal et al.
correlated among them (Table 5). In the plants, Fe presented
a high correlation with many of the physicochemical param-
eters, with Ec (0.959), HCO−3 (−0.946), SO2−
4 (0.950), Cl (0.960),
−
F (0.962), Na (0.930), K (0.962), Ca (0.984) and Mg2+
− + + 2+
(0.965) (Table 5).
In sediments, the correlation matrix showed a high cor-
relation between Fe and CO2− 3 (0.935); Pb with Ec (0.809),
HCO−3 (−0.760), SO2− 4 (0.778), Cl− (0.810), F− (0.814), Na+
(0.890), K (0.867), Ca (0.886), Mg2+ (0.875) and Fe in
+ 2+
plants (0.905); Zn with pH (0.780) and Na+ (−0.711) (Table 5).
The correlation of Pb with physicochemical parameters in
water reveals a significant source of contamination, reflect-
ing a common origin: the wastewater effluents. This influ-
ence was significant in P2-1 by the presence of nitrates
in water. The differences in correlations between the metals
in sediments, plants and water depend on physical, chemi-
cal and biological processes in the aquatic environment
as well as discharging of contaminants through anthropo-
genic activities and their effects on the portioning of metals
in the aquatic system (Kumar et al., 2010).
Conclusions
(1) The direct discharge of untreated wastewater in the
coastal zone is the leading cause of pollution. In the
City of Campeche, the sanitary infrastructure for the
collection and treatment of municipal waters is insuffi-
cient. At point P3, the highest values for Mn, Pb and
Fe were found in a residential area nearby, which could
explain these values; in P4 Zn concentrations were high
and this can be correlated with the plants’ metabolic
processes because it is a natural nonpolluted zone. In
the case of the plants, the P2 point was the highest
for Mn and Zn and P3 for Fe. The BFC was high in
C. erectus for Mn and Zn and in L. racemosa for Fe.
(2) C. erectus could be used in phytoremediation of Mn
and Zn contaminated coastal zones. The studied plants
did not accumulate Pb in their tissues, which suggests
that they are plants that exclude this metal because
there was evidence of Pb in sediments. Therefore, pro-
tection, restoration and conservation of coastal ecosys-
tems must be encouraged, as well as enforcing the
existing wastewater discharges criteria. This study con-
tributes to the knowledge of the patterns of metal accu-
mulation and translocation in mangroves. More research
should be done concerning the transport of pollutants
by groundwater in the coastal zone of Campeche.
Acknowledgements
Dr. Gomez-Bernal appreciates the postdoctoral fellowship
at the Posgrado en Energía y Medio Ambiente (PEMA),
Universidad Autónoma Metropolitana Unidad Iztapalapa,
Water and Environment Journal 35 (2021) 606–616 © 2020 CIWEM.
J. Gómez-Bernal et al. Evaluation of the accumulation of heavy metals in water, sediments and plants of Mexico
granted by the Consejo Nacional de Ciencia y Tecnología
(CONACYT) for the development of this research, Santana
Carrillo Jorge, MSc, for his technical support in processing
and taxonomy of the plants´ samples and to Alejandra
Aguayo and Olivia Cruz for their technical support in pro-
cessing sediments and water samples. We express sincere
thanks to the Journal Editor and reviewers for their con-
structive comments and helpful suggestions, which have
greatly improved the quality of the article.
Declaration of competing interest
The authors declare that they have no known competing
financial interests or personal relationships that could
have appeared to influence the work reported in this
paper.
To submit a comment on this article please go to http://
mc.manuscriptcentral.com/wej. For further information please see the
Author Guidelines at wileyonlinelibrary.com
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