Ocean and Coastal Management 184 (2020) 105003

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Ocean and Coastal Management

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Occurrences and ecotoxicological risks of trace metals in the San Benito

Archipelago, Eastern Pacific Ocean, Mexico
S.B. Sujitha a, M.P. Jonathan b, *, Lorena Elizabeth Campos Villegas b,
Claudia J. Herna �ndez-Camacho c
a
Centro Mexicano para la Producci� on m�
as Limpia (CMPþL), Instituto Polit�ecnico Nacional (IPN), Av. Acueducto s/n, Col. Barrio la Laguna Ticom� an, Gustavo A.
Madero, C.P. 07340, Ciudad de M�exico, Mexico
b
Centro Interdisciplinario de Investigaciones y Estudios sobre Medio Ambiente y Desarrollo (CIIEMAD), Instituto Polit�ecnico Nacional (IPN), Calle 30 de Junio de 1520,
Barrio la Laguna Ticom� an, Del. Gustavo A. Madero, C.P.07340, Ciudad de M�exico (CDMX), Mexico
c
Laboratorio de Ecología de Pinnípedos “Burney J. Le Boeuf”, Centro Interdisciplinario de Ciencias Marinas (CICIMAR), Instituto Polit�ecnico Nacional (IPN), Avenida
IPN, s/n Colonia Playa Palo de Santa Rita, C.P. 23096, La Paz, Baja California Sur, Mexico

A R T I C L E I N F O A B S T R A C T

Keywords: Trace metal concentrations (Fe, Mn, Cr, Cu, Ni, Co, Pb, Zn, Cd, As, Hg) were determined in water, sediment and
Bioaccumulation biota samples collected from the San Benito Islands off the Pacific Coast of Baja California, Mexico for a
Metals geochemical forensic study. Due to the proximity to the continental – oceanic crust interface and high biological
Toxicity
endemism, the islands demanded a profound geochemical survey for evaluating the presence and provenance of
Archipelago islands
San Benito
trace metals. Results suggested that the metals in the region are mainly originated from the geogenic sources (Fe,
Mexico Mn, Ni, Cr, Cu, Co), deep water circulation (Cd), atmospheric deposition (Pb) and hydrothermal processes (As).
Dissolved phase is the major metal carrier of Pb with an average value of 0.182 mg L 1, while Fe (1.60%), Mn
(335.42 mg kg 1), Ni (61.77 mg kg 1), Zn (32.36 mg kg 1) and Cr (28.7 mg kg 1) are mainly present in the
particulate phase. High values of Pb, As, Cd and Hg in biota with no biological functions are highly toxic and are
especially critical to those predators (Sea lions) in the region due to the process of biomagnification. For a
qualitative exposure assessment of trace metals, several indices namely Heavy metal Evaluation Index (HEI),
Nemerow Pollution Index (NPI), Bioconcentration Factor (BCF) and Biota Sediment Accumulation Factor (BSAF)
were calculated. The indices revealed that the overall pollution status of the region is “moderate”. This study
advocates a preliminary environmental surveillance in trace metal concentrations for implementing better
conservation strategies in maintaining and promoting the ecological richness and endemism of the islands.

1. Introduction specific characteristics of topographic and biological diversity, the San

Islands cover 2.7% of the earth’s surface and hotspots of cultural,
biological and geophysical riches that serve as globally connected lab­
oratories of environmental conservation, sustainable living and socio­
cultural innovation are of critical significance (Donlan et al., 2000). The
Baja California Pacific Islands Biosphere Reserve was created for the
substantial conservation of Mexico’s rich islands in biodiversity that
covers an area of 11,612 Km2 off the western coast of the Baja California
Peninsula, Mexico. The reserve includes six archipelagos: Coronado,
Todos Santos, San Jero �nimo, San Benito, Cedros and Bahia Magdalena,
comprising a total of 21 islands and 97 islets. Among these archipelagos,
because of the proximity to the continental-oceanic crust interface and
Benito Islands are of significant geological and environmental concern.
Due to the non-biodegradability, persistence and toxicity of metals,
many previous studies on metal concentrations in marine settings have
received innumerable attention in the last few decades (Lim et al., 2013;
Grinham et al., 2014; Shefer et al., 2015; Trevizani et al., 2016;
Zalervska and Danowska, 2017; Li et al., 2017a; Anbuselvan et al., 2018;
Castillo et al., 2019). In the oceans, trace metals reveal the biogeo­
chemical balances in water, sediment and biota, as well as the in­
teractions with the atmosphere (Libes, 1992; Raimundo et al., 2013).
Trace metals in coastal environments showed a multi-source mixing of
natural (erosion, weathering of rocks, volcanic processes, firing) and
anthropogenic activities (combustion of fossil fuels, mining, agriculture,

* Corresponding author.
E-mail address: mpjonathan7@yahoo.com (M.P. Jonathan).

https://doi.org/10.1016/j.ocecoaman.2019.105003
Received 10 February 2019; Received in revised form 21 September 2019; Accepted 24 September 2019
Available online 7 October 2019
0964-5691/© 2019 Elsevier Ltd. All rights reserved.
S.B. Sujitha et al.
industrialization, and domestic sewage) mainly through river inputs,
estuaries, sewage pipes and atmosphere transmission (Pan and Wang,
2012). Additionally, hydrothermal venting also serves to be a significant
source and sink of trace metals in ocean (Resing et al., 2015). Metals in
the marine environment are principally present in three major reserves
namely water, sediment and biota determined by various physical,
chemical and biological factors. The distribution and behavior of metals
in seawater are regulated by the mixing and balance between water
bodies, suspended particle interaction, biological uptake, bioturbation
and diagenesis processes in sediments (Chester, 1990; Lapp and Balzer,
1993). Consequently, the bioaccumulation of metals in organisms is the
foremost step for an enhanced assessment of environment quality status
(Amaral and Rodrigues, 2005). Abnormal accumulation of metals in
marine sediments and biota have resulted in severe disruption of the
ecological biogeochemical processes and the functioning of local marine
organisms (Dorman et al., 2016). Concentrations of essential (Fe, Zn, Co,
Cu and Mn) and non-essential metals (As, Cd, Hg and Pb) in marine
organisms reflect their bioavailability in the environmental locale and
metabolic requirements of individual species (Raimundo et al., 2013).
Numerous studies (Aloupi and Angelidis, 2001; Dhaneesh et al., 2012;
Raimundo et al., 2013; Hwang et al., 2016; Li et al., 2017b; Conti et al.,
2017; Lu et al., 2019) on trace metal accumulation in different envi­
ronmental matrices have been conducted worldwide and the untiring
thrust lasts even today to fulfill the knowledge gap in providing con­
servation strategies in the field of environmental sciences. Subsequently,
the present study proves to be the pioneer work in terms of a baseline
geochemical assessment of the remote archipelago in the Pacific Ocean
for enhancing better conservation strategies.
The present study documents the presence of 11 trace metal con­
centrations (Fe, Mn, Cr, Cu, Ni, Co, Pb, Zn, Cd, As, Hg) in water, sedi­
ments and biotic samples collected from the San Benito Archipelago,
Eastern Pacific Ocean, Mexico, which will serve as a baseline data set for
any future investigation with reference to metal enrichments.
Fig. 1. Study area map indicating the sampling points in San Benito Islands off the coast of Baja California, Pacific Ocean, Mexico.
2
Ocean and Coastal Management 184 (2020) 105003
2. Materials and methods
2.1. Study area
The San Benito Islands, a group of three volcanic islands (west, east
and center) are located (28� 180 3000 N, 115� 340 0000 W) off the Pacific
coast of Baja California occupying an area of 5.7 km2 (Fig. 1). San Benito
West Island (3.5 km2) and San Benito East Island (1.1 km2) are separated
by 2 km and are similar both in vegetation and fauna. Endemism is high
on the San Benito Islands that shelters three endemic plant species, four
endemic land birds and one endemic land lizard (Junak and Philbrick,
1999). The northern elephant seal, Guadalupe fur seal and Californian
sea lion are permanent residents on the islands with stable abundance in
recent times (Elorriaga–Verplaneken et al., 2016). Not only endemism,
San Benito Islands highly support the ecological and evolutionary pro­
cesses that promote the differentiation of endemic forms (Lawlor, 1983;
Donlan et al., 2000) The region is highly influenced by the North Pacific
counterclockwise gyre systems and the Californian intermediate waters
with a temperature of 10–12 � C and a salinity of 33.9–34.4 (Talley,
1993), creating abundant productivity. The depth of the surrounding
waters ranges between 13 and 55 m (Esperon-Rodriguez and Gallo –
Reynosa, 2012). Proximity to the subduction zone, tectonic activity with
alternating marine sedimentation and volcanism characterize the late
cretaceous, tertiary and recent geologic history of the region. Further­
more, the islands contain complexly folded and sheared eugeosynclinal
sequences of greywacke chert, basalt, altered basalt and carbonates,
serpentinites and glaucophane rocks (Cohen et al., 1963). The vegeta­
tion is predominantly desertic shrubland and patches of kelp forests
(Aguirre-Mun ~ oz et al., 2013). Among the three islands, only the San
Benito west islands are habituated by the fishing population (approx. 70
persons) representing the fishing camp of Cooperativa Pescadores
Nacionales de Abulo �n (INEGI, 2013) of Ensenada, Baja California.
Moreover, these islands are considered to be one of the most ecologically
S.B. Sujitha et al. Ocean and Coastal Management 184 (2020) 105003

intact non polar archipelagos in the world (Donlan et al., 2002). Table 1
Classifications of HEI and NPI used for the present study.
Index Class Description
2.2. Sampling and analyses
Heavy metal Evaluation Index <400 Low contamination
(HEI) 400–800 Medium contamination
Nearly 25 surface water (Fig. 1) and 11 biota samples were acquired
˃ 800 High contamination
from the San Benito Islands during November 2016, whereas only 2 Nemerow Pollution Index (NPI) <0.7 Non polluted sediments
sediment samples in triplicate were collected due to the rocky terrain, 0.7 < NPI < 1 Nearly polluted
remoteness of the island and the practical difficulties during the field 1 < NPI < 2 Lightly polluted
2 < NPI < 3 Moderately polluted
work.
NPI > 3 Seriously polluted
Biotic samples (11 nos.) included marine macrophytes (Eisenia sediments
arborea, Phyllospadix sp) and organisms (Crabs: Calappidae, Loxo­
rhynchus grandis; Fishes: Gymnothorax mordax, Halichoeres semicinctus,
Hypsypops rubicundus, Paralabrax nebulifer, Caulolatilus affinis, Balistes The Nemerow Pollution Index reveals the comprehensive status of
polylepis and Semicossyphus pulcher). trace metal pollution at a particular site and can be calculated by using
Trace metal clean procedures were strictly followed during sampling the formula (Yan et al., 2016),
and the seawater samples were procured in pre-cleaned low density 1 L sffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
polyethylene bottles, subsequently acidified (pH < 2) using HNO3 (High ðCFÞ2 þ ðCFmax Þ2
NPI ¼
purity J.T Baker) and refrigerated until further analysis. Trace metals in 2
seawater were determined by direct aspiration Flame Atomic Absorp­
tion Spectrometry (Kramer, 2011; Sujitha et al., 2018) and lanthanum where CF is the arithmetic mean of contamination factor of all trace
oxides were added to each sample to avoid spectral and non-spectral metals and CFmax is the maximum CF factor value among the trace
interferences. metals. The NPI values are categorized into five different classes
Biotic samples were taxonomically identified and thereafter washed (Table 1).
with deionized water; oven dried at 60 � C for three days and homoge­
nized using an agate mortar. Consequently, 1 g of each dried powdered c) Bioconcentration Factor (BCF)
sample (sediment & biota) was digested using (high purity J.T. Baker)
3 ml HNO3 þ 2 ml HCl þ10 ml H2O2 (Portman, 1976; EPA 3010), heated Bioconcentration is defined as the accumulation of metals by or­
for 4 h in a hot plate and filtered through a 0.45μ membrane up to 50 ml ganisms from the ambient waters via respiratory or dermal absorption
for the determination of metals. Thereafter, concentrations of metals (Jitar et al., 2015). It is well known that only freely dissolved metal
(Fe, Mn, Cr, Cu, Ni, Co, Pb, Zn and Cd) in water, sediments and biotic concentrations are only highly bioavailable and pass through biological
samples were determined using an Atomic Absorption Spectrometer membranes (Arnot and Gobas, 2006). However, for the present study
(PerkinElmer Model AAnalyst100, CIIEMAD, IPN, Mexico) following the BCF is calculated using the total metal concentrations in seawater for a
method EPA 7000B; US EPA, 2007). Estimation of Hg and As was carried comprehensive status on the accumulation of metals from bulk water
out using the cold vapor technique and hydride generation respectively phase. BCF (unitless) is calculated by using the formula:
(EPA, 1979). Co
Suitable Standard Reference Materials (SRM) for all the three com­ BCF ¼
Cwd
ponents [(Quality control Standard 21 for water); (Inorganics in marine
sediments NIST 2702 for sediments) and (CRM-TMF Trace metals in where Co is the metal concentration in the organism and Cwd is the metal
fishes for biota)] were used. The recovery percentages of metals in concentration in water.
seawater and biota was (all values in %): Fe (104.34), Mn (101.91), Cr
(102.14), Cu (89.40), Ni (89.20), Co (95.74), Pb (95.65), Zn (95.32), Cd d) Biota Sediment Accumulation Factor (BSAF)
(97.66), As (88.61); Fe (98.40), Mn (106.50), Cr (102), Cu (101.60), Ni
(100.10), Co (88), Pb (98.07), Zn (97.33), Cd (106), As (103.33), Hg Biota Sediment Accumulation Factor (BSAF) is best suited for
(102) respectively. Quality and accuracy was guaranteed for the entire describing the bioaccumulation of metals from sediments in benthos
experimental procedure. food webs with non-equilibrium conditions (Ankley et al., 1992). BSAF
can be calculated using the formula,
2.3. Data analyses Co
BSAF ¼
Cs
The determined concentrations of trace metals were also assessed
based on several indices such as where Co is the metal concentration in the organism and Cs is the metal
concentration in the surficial sediments.
a) Heavy metal Evaluation Index (HEI)
3. Results and discussion
Heavy metal Evaluation Index (HEI) estimates the overall water
quality based on trace metal concentrations (Edet and Offiong, 2002; 3.1. Seawater
Prasanna et al., 2012) and is calculated using the formula:
The average metal concentrations in the seawater were observed to
be in the decreasing order of (all values in mg L 1): Pb
Xn
Hc
HEI ¼
i¼1
Hmac (0.182 � 0.024) > Fe (0.169 � 0.042) > Ni (0.154 � 0.016) > Co
(0.135 � 0.012) > As (0.118 � 0.065) > Cr (0.047 � 0.002) > Cd
where Hc is the monitored value and Hmac is the maximum allowable (0.029 � 0.004) > Cu (0.029 � 0.005) > Mn (0.025 � 0.002). The most
concentration of the ith parameter respectively and the resultant values important pathways by which trace metals reach the ocean include at­
are described based on three different classes (Table 1). mospheric deposition of mineral dust, submarine hydrothermalism and
sediment dissolution along continental margins (Horner et al., 2015).
b) Nemerow Pollution Index (NPI)

3
S.B. Sujitha et al. Ocean and Coastal Management 184 (2020) 105003

Likewise, high concentrations of Pb (0.135–0.219 mg L 1) in this region
is mostly anthropogenic, mainly sourced by industrial emissions, coal
combustion, and leaded gasolines globally (Zurbrick et al., 2017). The
dissolved concentrations of Fe (0.124–0.270 mg L 1) and Ni
(0.130–0.154 mg L 1) are influenced by the sediment dissolution pro­
cess (Severmann et al., 2010) and mineral dusts from the San Benito
Islands that are rich in greywackes and ultramafic rocks, which is also
clearly supported by the positive correlation of Fe vs Ni (r2 ¼ 0.44;
p < 0.05). However, negative correlations (Table 2) found between Fe vs
Pb (r2 ¼ 0.47; p < 0.05) suggest their diverse origins from natural and
anthropogenic activities respectively. Although Fe, Ni and Cr are mainly
sourced from the adjacent rocks of the islands, the average concentra­
tions of Cr were observed to be comparatively less (0.047 mg L 1) due to
the incorporation of dissolved Cr in siliceous and carbonated biogenic
particles in the surface waters (Guertin et al., 2005). Dissolved Co levels
(0.114–0.155 mg L 1) are possibly from the cobalt rich Fe–Mn crusts on
the Californian continental margins (Hein et al., 2000). High average As
concentrations (0.118 mg L 1) are due to the arsenic flux from hydro­
thermal systems and their concentrations are greatly controlled by the
biological activities in the ocean (Flora, 2015). Less average concen­
trations of Cd (0.029 mg L 1), Cu (0.029 mg L 1) and Mn (0.025 mg L 1)
are probably originated from deep-water circulation and upwelling
phenomenon (Conrad et al., 2017), and represent nutrient like distri­
butions due to their biological functions in marine phytoplanktons (Lane
and Morel, 2000; Martínez-Finley et al., 2013). Significant positive
correlation (Table 2) between Cu vs Pb (r2 ¼ 0.51; p < 0.05) indicate an
aeolian source similar to that of Pb (Leinen et al., 1994), whereas Ni vs
Cu (r2 ¼ 0.66; p < 0.05) indicate their source derived from manganese
nodules present in the Pacific Ocean (Wegorzewski and Kuhn, 2014).
Dissolved metal concentrations of Pb, Ni, As, and Cd (Table 3) were
found to be higher than that of the permissible limits set forth by the
Mexican Government (Diario Oficial de la Federacion, Mexico, 2014).
3.2. Sediments
Concentrations of metals in sediments presented an order of (all
values in mg Kg 1): Fe (16000 � 12000) > Mn (335.42 � 203.54) > Ni
(61.77 � 4.24) > Pb (35.43 � 20.01) > Zn (32.36 � 12.58) > Cr
(28.7 � 6.07) > Co (21.11 � 0.23) > Cu (18.04 � 12.45) > Cd
(3.44 � 1.99) > As (1.28 � 0.25) > Hg (0.01 � 0.01). According to
Bonatti et al. (1972), sediments of San Benito Archipelago are generally
originated from diagenetic and hydrothermal venting processes (Guegen
et al., 2016). The average Fe (16000 mg kg 1) and Mn (335.42 mg kg 1)
levels are possibly due to the volcanic seamounts that normally consists
of Fe–Mn crusts and formed through slow accumulation of seawater
derived Fe–Mn oxyhydroxides colloids on hard substrates (Koschinsky
and Halbach, 1995). Even though, Fe and Mn are frequent constituents
of sedimentary deposits with similar chemical behavior, very often, the
variations in the concentrations of both the elements are ascribed to the
dominance of iron in a homogenous mass in the form of a manganiferous
iron (Penrose, 1893; Vishwakarma et al., 2018). Additionally, several
studies (Benner, 2011; Winckler et al., 2016; Ratnarajah et al., 2018)
also suggest that Fe levels are linked to the biological productivity of a
region. Concentrations of Ni (61.77 mg kg 1), Cr (28.77 mg kg 1), Co
(21.11 mg kg 1) are derived from the Fe–Mg rich mafic and ultramafic
rocks in the volcanic islands (Neall and Trewick, 2008). Elevated Pb
(35.43 mg kg 1), Zn (32.36 mg kg 1) and Cu (18.04 mg kg 1) concen­
trations are acquired from the marine-volcanic association of Pb–Zn
deposits (Misra, 2000) predominant in the region, however anthropo­
genic Pb is also found in the sediments due to atmospheric inputs
(Mun ~ oz and Salamanca, 2003).
The probable harmful effects of metal concentrations in sediments
were compared with the Sediment Quality Guidelines (SQGs) and Eco­
toxicological values such as Lowest Effect Level (LEL), Severe Effect
Level (SEL), Effect Range Low (ERL) and Effect Range Medium (ERM)
(Table 3). The concentrations of Ni and Cd were higher than that of the
values of Threshold Effect Concentration (TEC) signifying adverse ef­
fects on the biota (MacDonald et al., 2000). Similarly, Cr, Cu, Ni, Pb, Cd
were also higher than the values of LEL and ERL suggesting possible risks
to the biota.
3.3. Biota
The macrophytes, Phyllospadix sp (527.13 mg kg 1 dry wt.) and
Eisenia arborea (56.95 mg kg 1 dry wt.) presented high metal concen­
trations as they accumulate metals at a linear rate from the underlying
sediments (Redondo-Go �mez, 2013). However, crabs (40.13 mg kg 1 dry
wt.) presented two-fold higher levels of metals than fishes

Table 2
Correlation matrix of metal concentrations in water and biota of San Benito Islands off the coast of Baja California, Pacific Ocean, Mexico.
a. Water

Fe Mn Cr Cu Ni Co Pb Cd As

Fe 1.00
Mn – 1.00
Cr – 0.44 1.00
Cu – – – 1.00
Ni 0.44 – 0.66 1.00
Co – – – – – 1.00
Pb 0.47 – – 0.51 – – 1.00
Cd – – – – – – 1.00
As – – – – – – – – 1.00

b. Biota

Fe Mn Cr Cu Ni Co Pb Zn Cd As Hg

Fe 1.00
Mn – 1.00
Cr – – 1.00
Cu 0.88 – – 1.00
Ni 0.81 – 0.70 0.74 1.00
Co 0.83 – – 0.80 0.99 1.00
Pb 0.83 – – 0.83 0.98 1.00 1.00
Zn – – – – – – – 1.00
Cd 0.90 – – 0.99 0.83 0.88 0.90 – 1.00
As – – – – – – – 0.94 – 1.00
Hg – – – – – – – – – – 1.00

p < 0.05

4
S.B. Sujitha et al. Ocean and Coastal Management 184 (2020) 105003

Table 3
Comparison values of average metal concentrations in water, sediment and biota samples from San Benito Islands with that of the maximum permissible limits.
Fe Mn Cr Cu Ni Co Pb Zn Cd As Hg

Water (mg/L)
Present Study 0.169 0.025 0.047 0.029 0.154 0.135 0.182 – 0.029 0.118 –
Permissible Limits
SEMARNAT, 2010b 0.050 0.020 0.010 0.010 0.002 – 0.010 0.020 0.0002 0.010 –
Sediment (mg/kg)
Present Study 1.60a 335.42 28.77 18.04 61.77 21.11 35.43 32.36 3.44 1.28 0.01
Crustal average
NASCc 3.95a 500 125 – 58 25.7 – – – 28.4 –
UCCd 3.49a 542 85 14 19 35 17 52 0.102 2 0.056
Sediment Quality Guidelines
TECe – – 43.4 31.6 22.7 – 35.8 121 0.99 9.79 0.18
PEC – – 111 149 48.6 – 128 459 4.98 33 1.06
Ecotoxicological Values
LELf 2.0a 460 26 16 16 – 31 120 0.6 6 0.2
SEL 4.0a 1100 110 110 75 – 250 820 10 33 2
ERLg – – 81 34 20.9 – 46.7 150 1.2 8.2 0.15
ERM – – 370 270 51.6 – 218 410 9.6 70 0.71
Biota (mg/kg)
Present study
Macrophytes 2997.55 70.86 32.47 6.82 35.85 8.04 18.52 27.65 4.92 9.55 0.24
Crabs 208.69 7.60 11.78 30.32 32.90 22.28 59.03 48.21 9.56 10.93 0.10
Fishes 89.99 9.08 6.70 3.94 8.44 5.24 11.52 94.27 1.69 14.42 0.49
Permissible limits in fishes
WHO, 1985 – 0.5 0.15 3 0.6 – 2 10–75 – – –
FEPA, 2003 – 0.5 0.15 1.3 0.5 – 2 75 – – –
a
Values represented in %.
b
SEMARNAT, 2010
c
Gromet et al. (1984).
d
Wedepohl (1995).
e
MacDonald et al., 2000.
f
USEPA, 2001.
g
Long et al. (1995).

Fig. 2. Metal concentrations in the marine macrophytes, crabs and fishes collected from San Benito Islands off the coast of Baja California, Pacific Ocean, Mexico.

5
S.B. Sujitha et al. Ocean and Coastal Management 184 (2020) 105003

(22.34 mg kg 1 dry wt.) because of the differences in morphological
characteristics and living conditions (Rainbow and Luoma, 2011).
The average concentrations of metals (Fig. 2) presented a decreasing
order of (mg Kg 1 dry wt.);
1. Surf grass (Phyllospadix sp): Fe (5471.81) > Mn (128.99) > Ni
(56.12) > Cr (51.16) > Zn (40.10) > Pb (20.72) > Co (10.46) > Cu
(10.06) > Cd (6.40) > As (2.40) > Hg (0.18).
2. Kelps (Eisenia arborea): Fe (523.24) > As (16.69) > Pb (16.33) > Ni
(15.58) > Zn (15.20) > Cr (13.77) > Mn (12.73) > Co (5.62) > Cu
(3.57) > Cd (3.45) > Hg (0.29).
3. Crabs: Fe (208.69) > Pb (59.03) > Zn (48.21) > Ni (32.50) > Cu
(30.32) > Co (22.28) > Cr (11.78) > As (10.93) > Cd (9.56) > Mn
(7.60) > Hg (0.10).
4. Fishes: Zn (94.27) > Fe (89.99) > As (14.42) > Pb (11.32) > Mn
(9.08) > Ni (8.44) > Cr (6.70) > Co (5.24) > Cu (3.94) > Cd
(1.69) > Hg (0.49).
The hierarchical orders of metal levels in immobile surf grass and
crabs were found to be similar to that of the metal concentrations in
sediments because of their strong association with the underlying sedi­
ment beds. High Fe content observed in all the samples are due to its
vital role in the regulation of homeostasis and metabolism of both plants
and animals (Bury et al., 2001). Elevated As content (16.69 mg kg 1 dry
wt.) in kelps is due to the phosphate uptake systems of plants mainly in
the form of arsenate that is relatively less toxic (Fourqurean et al., 1993).
The higher levels of trace metals in the marine macrophytes are due to
their affinities for metal accumulation through numerous physiological
mechanisms (Valitutto et al., 2006). High average concentrations of Pb
(59.03 mg kg 1 dry wt.) in crabs is due to the dissolution of CaCO3
followed by micro-precipitation of PbCO3 on the surface of crab shells
(Lee et al., 1997), while Zn levels (94.27 mg Kg-1 dry wt.) in fishes are
mainly due to waterborne exposure for which gills act as a major site of
uptake and accumulation for various biological needs (Niyogi et al.,
2016). Strong positive correlations between Zn vs As (r2 ¼ 0.94;
p < 0.05) suggest significant branchial uptake of both the elements from
the aqueous medium (Glover and Hogstrand, 2002; Meader et al., 2004).
Likewise, significant positive correlations (Table 2) amongst Co vs Pb
(r2 ¼ 1.00; p < 0.05) indicate a synergistic effect where Co facilitates the
uptake of Pb and vice versa (Batool and Javed, 2015). The positive
relationship between Fe vs Cu when p < 0.05, (r2 ¼ 0.88), Ni (r2 ¼ 0.81),
Co (r2 ¼ 0.83), Pb (r2 ¼ 0.83) and Cd (r2 ¼ 0.90) suggest that Fe acts as
natural metal scavenger which adsorb other trace metals along with
them (Jayaprakash et al., 2015). In general, Balistes polylepis (Finescale
Trigger fish) presented the highest total concentrations of metals
(456.27 mg kg 1 dry wt.) primarily due to its dietary characteristics that
include sedentary crustaceans and mollusks. Mn, Cr, Ni, Cd and As
values from the present study exhibited six-tenfold greater values than
the maximum allowable limits (Table 3), whereas Pb concentrations
were extremely higher than the limits put forth by various government
agencies.
b) Nemerow Pollution Index (NPI)
NPI values were calculated to assess the pollution status of the region
in terms of the metal concentrations in sediments. In the present study,
NPI was found to be 1.6 signifying lightly polluted sediments (Yan et al.,
2016) due to its geogenic setting with volcanic seamounts and its
proximity to the interface of continental-oceanic crust.
c) Bioconcentration Factor (BCF)
In general, BCF values presented an order of (Fig. 3a): Fe
(6501) > Mn (1157) > Cu (472) > Cr (361) > Cd (186) > Ni (167) > Pb
(163) > As (98.57) > Co (87.82). BCF value greater than 5000 for Fe is
considered to be highly bioaccumulative than other metals, according to
the guidelines in Annex XIII of the REACH regulation 1907/2006 (EC,
2006). Correspondingly, except Fe and Mn no other elements presented
chronic effects and food chain accumulation (Kwok et al., 2014).
However, diverse organisms thriving in the same habitat presented
varying accumulation rates [Marine macrophytes (2460) > Crabs
(440) > Fishes (168)] due to the differences in physiological character­
istics of each group.
d) Biota Sediment Accumulation Factor (BSAF)
In general, BSAF values presented an order of (Fig. 3b): As
(9.09) > Hg (2.51) > Zn (1.75) > Cd (1.57) > Pb (0.84) > Cu (0.76) > Cr
(0.59) > Co (0.56) > Ni (0.42) > Mn (0.09) > Fe (0.07). High BSAF
values for As and Hg suggest possible acute and chronic toxicity to
marine biota due to the ingestion of particulate matter, dietary intake
and also membrane facilitated transport (Mamindy-Pajany et al., 2013).
The calculated BSAF values can be categorized into macro-concentrator
(BSAF > 2), micro-concentrator (1 < BSAF < 2) and deconcentrator
(BSAF >1), according to Dallinger, 1993). Therefore, the studied species
of San Benito Islands with an average BSAF value of 1.66 are considered
to be micro-concentrators of trace metals.
4. Conclusion
Over the last few decades, scientists all over the world has increas­
ingly sought a multidisciplinary approach in the field of environmental

3.4. Data assessment

a) Heavy metal Evaluation Index (HEI)

HEI provides the overall water quality of the region in terms of trace
metals. The mean HEI values for all the sampling stations ranged be­
tween (Stn 4: 224.25 – Stn 1: 304.45; western islands) with a mean value
of 255.08 indicating that the region is less contaminated based on the
classification, when HEI < 400 (Edet and Offiong, 2002). Low concen­
trations of trace metals in seawater are attributed to the active biological
uptake, hydrodynamics and passive scavenging onto either biotic or
abiotic components (Chester, 1990). However, the samples of western Fig. 3. a–b Bioconcentration Factor (BCF) and Biota Sediment Accumulation
islands showed higher HEI values due to the impact of fishing activities Factor (BSAF) in the biota from San Benito Islands off the coast of Baja Cali­
all year round than the center and east San Benito. fornia, Pacific Ocean, Mexico.

6
S.B. Sujitha et al.
sciences, and thus the present study highlights the execution of a
geochemical study for efficient management and biomonitoring de­
cisions. Thus it proves to be distinct as it raises awareness of the origin of
trace metals from geogenic sources, deep-water circulation, atmospheric
deposition and hydrothermal processes. Dissolved phase is the major
metal carrier of Pb, while Fe, Mn, Ni, Zn and Cr are mainly present in the
particulate phase. Bioaccumulation pattern in marine biota clearly ex­
hibits trace metal partitioning (Fe, Zn, Mn, Ni) based on the essentiality
of each element for various physiological functioning, however, high Pb
levels in the biota can lead to toxicity. Presence of toxic levels of trace
metals in marine environment will definitely lead to imbalances in the
food chain due to the process of biomagnification and indirectly affects
human health. As the San Benito Islands prove to be a testament for
endemism, evolutionary processes and fishing practices, profound water
quality and biomonitoring surveillances must be carried out frequently
based on the careful documentation of existing biological diversity for
the establishment of competent management strategies.
Acknowledgement
This work is part of the Multidisciplinary project SIP-IPN Nos.
20160133, 20160055, 20170463, 20170489 and the authors wish to
acknowledge for the financial assistance provided by SIP, IPN. Authors
SBS, MPJ, and CJHC thank the Sistema Nacional de Investigadores
(SNI), CONACyT, COFAA, EDI, Mexico. SBS thanks the CONACYT
project no. 274276 “Fase I De La Remediacio �n de Areas
� Contaminadas
Con Hidrocarburos En La Refinería Gral. La �zaro Ca�rdenas” for the
postdoctoral fellowship. This article is the 100th contribution (partial)
from Earth System Science Group (ESSG), Chennai, India (Participating
members: MPJ & SBS).
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.ocecoaman.2019.105003.
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