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Occurrences and ecotoxicological risks of trace metals in the San Benito Archipelago, Eastern Pacific Ocean, Mexico
Ocean and Coastal Management xxx (xxxx) xxx
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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, �ndez-Camacho c Claudia J. Herna 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 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 b
A R T I C L E I N F O
A B S T R A C T
Keywords: Bioaccumulation Metals Toxicity Archipelago islands San Benito Mexico
Trace metal concentrations (Fe, Mn, Cr, Cu, Ni, Co, Pb, Zn, Cd, As, Hg) were determined in water, sediment and biota samples collected from the San Benito Islands off the Pacific Coast of Baja California, Mexico for a geochemical forensic study. Due to the proximity to the continental – oceanic crust interface and high biological endemism, the islands demanded a profound geochemical survey for evaluating the presence and provenance of trace metals. Results suggested that the metals in the region are mainly originated from the geogenic sources (Fe, 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 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, �nimo, San Benito, Cedros and Bahia Magdalena, Todos Santos, San Jero comprising a total of 21 islands and 97 islets. Among these archipelagos, because of the proximity to the continental-oceanic crust interface and
specific characteristics of topographic and biological diversity, the San 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: [email protected] (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 0964-5691/© 2019 Elsevier Ltd. All rights reserved.
Please cite this article as: S.B. Sujitha, Ocean and Coastal Management, https://doi.org/10.1016/j.ocecoaman.2019.105003
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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.
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 ~ oz et al., 2013). Among the three islands, only the San (Aguirre-Mun Benito west islands are habituated by the fishing population (approx. 70 persons) representing the fishing camp of Cooperativa Pescadores �n (INEGI, 2013) of Ensenada, Baja California. Nacionales de Abulo Moreover, these islands are considered to be one of the most ecologically
Fig. 1. Study area map indicating the sampling points in San Benito Islands off the coast of Baja California, Pacific Ocean, Mexico. 2
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intact non polar archipelagos in the world (Donlan et al., 2002).
Table 1 Classifications of HEI and NPI used for the present study.
2.2. Sampling and analyses Nearly 25 surface water (Fig. 1) and 11 biota samples were acquired from the San Benito Islands during November 2016, whereas only 2 sediment samples in triplicate were collected due to the rocky terrain, remoteness of the island and the practical difficulties during the field work. Biotic samples (11 nos.) included marine macrophytes (Eisenia arborea, Phyllospadix sp) and organisms (Crabs: Calappidae, Loxo rhynchus grandis; Fishes: Gymnothorax mordax, Halichoeres semicinctus, Hypsypops rubicundus, Paralabrax nebulifer, Caulolatilus affinis, Balistes polylepis and Semicossyphus pulcher). Trace metal clean procedures were strictly followed during sampling and the seawater samples were procured in pre-cleaned low density 1 L polyethylene bottles, subsequently acidified (pH < 2) using HNO3 (High purity J.T Baker) and refrigerated until further analysis. Trace metals in seawater were determined by direct aspiration Flame Atomic Absorp tion Spectrometry (Kramer, 2011; Sujitha et al., 2018) and lanthanum oxides were added to each sample to avoid spectral and non-spectral interferences. Biotic samples were taxonomically identified and thereafter washed 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 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 for 4 h in a hot plate and filtered through a 0.45μ membrane up to 50 ml for the determination of metals. Thereafter, concentrations of metals (Fe, Mn, Cr, Cu, Ni, Co, Pb, Zn and Cd) in water, sediments and biotic samples were determined using an Atomic Absorption Spectrometer (PerkinElmer Model AAnalyst100, CIIEMAD, IPN, Mexico) following the method EPA 7000B; US EPA, 2007). Estimation of Hg and As was carried out using the cold vapor technique and hydride generation respectively (EPA, 1979). Suitable Standard Reference Materials (SRM) for all the three com ponents [(Quality control Standard 21 for water); (Inorganics in marine sediments NIST 2702 for sediments) and (CRM-TMF Trace metals in fishes for biota)] were used. The recovery percentages of metals in 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 (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 (102) respectively. Quality and accuracy was guaranteed for the entire experimental procedure.
Index
Class
Description
Heavy metal Evaluation Index (HEI)
<400 400–800 ˃ 800 <0.7 0.7 < NPI < 1 1 < NPI < 2 2 < NPI < 3 NPI > 3
Low contamination Medium contamination High contamination Non polluted sediments Nearly polluted Lightly polluted Moderately polluted Seriously polluted sediments
Nemerow Pollution Index (NPI)
The Nemerow Pollution Index reveals the comprehensive status of trace metal pollution at a particular site and can be calculated by using the formula (Yan et al., 2016), sffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi ðCFÞ2 þ ðCFmax Þ2 NPI ¼ 2 where CF is the arithmetic mean of contamination factor of all trace metals and CFmax is the maximum CF factor value among the trace metals. The NPI values are categorized into five different classes (Table 1). c) Bioconcentration Factor (BCF) Bioconcentration is defined as the accumulation of metals by or ganisms from the ambient waters via respiratory or dermal absorption (Jitar et al., 2015). It is well known that only freely dissolved metal concentrations are only highly bioavailable and pass through biological membranes (Arnot and Gobas, 2006). However, for the present study BCF is calculated using the total metal concentrations in seawater for a comprehensive status on the accumulation of metals from bulk water phase. BCF (unitless) is calculated by using the formula: BCF ¼
Co Cwd
where Co is the metal concentration in the organism and Cwd is the metal concentration in water. d) Biota Sediment Accumulation Factor (BSAF) Biota Sediment Accumulation Factor (BSAF) is best suited for describing the bioaccumulation of metals from sediments in benthos food webs with non-equilibrium conditions (Ankley et al., 1992). BSAF can be calculated using the formula,
2.3. Data analyses
BSAF ¼
The determined concentrations of trace metals were also assessed based on several indices such as
Co Cs
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; Prasanna et al., 2012) and is calculated using the formula:
3.1. Seawater The average metal concentrations in the seawater were observed to be in the decreasing order of (all values in mg L 1): Pb (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 (0.029 � 0.004) > Cu (0.029 � 0.005) > Mn (0.025 � 0.002). The most important pathways by which trace metals reach the ocean include at mospheric deposition of mineral dust, submarine hydrothermalism and sediment dissolution along continental margins (Horner et al., 2015).
n X Hc HEI ¼ Hmac i¼1
where Hc is the monitored value and Hmac is the maximum allowable concentration of the ith parameter respectively and the resultant values are described based on three different classes (Table 1). b) Nemerow Pollution Index (NPI) 3
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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).
(3.44 � 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 ~ oz and Salamanca, 2003). (Mun 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
3.2. Sediments
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 �mez, 2013). However, crabs (40.13 mg kg 1 dry sediments (Redondo-Go wt.) presented two-fold higher levels of metals than fishes
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
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
Mn
1.00 – – – 0.44 – 0.47 – –
1.00 0.44 – – – – – –
Cr
Cu
1.00 – – – – –
1.00 0.66 – 0.51 –
Ni
Co
Pb
Cd
As
1.00 – – – –
1.00 – – –
1.00 – –
1.00 –
1.00
b. Biota Fe Mn Cr Cu Ni Co Pb Zn Cd As Hg
Fe
Mn
Cr
Cu
Ni
Co
Pb
Zn
Cd
As
Hg
1.00 – – 0.88 0.81 0.83 0.83 – 0.90 – –
1.00 – – – – – – – – –
1.00 – 0.70 – – – – – –
1.00 0.74 0.80 0.83 – 0.99 – –
1.00 0.99 0.98 – 0.83 – –
1.00 1.00 – 0.88 – –
1.00 – 0.90 – –
1.00 – 0.94 –
1.00 – –
1.00 –
1.00
p < 0.05 4
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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. Water (mg/L) Present Study Permissible Limits SEMARNAT, 2010b Sediment (mg/kg) Present Study Crustal average NASCc UCCd Sediment Quality Guidelines TECe PEC Ecotoxicological Values LELf SEL ERLg ERM Biota (mg/kg) Present study Macrophytes Crabs Fishes Permissible limits in fishes WHO, 1985 FEPA, 2003 a b c d e f g
Fe
Mn
Cr
Cu
Ni
Co
Pb
Zn
Cd
As
Hg
0.169
0.025
0.047
0.029
0.154
0.135
0.182
–
0.029
0.118
–
0.050
0.020
0.010
0.010
0.002
–
0.010
0.020
0.0002
0.010
–
1.60a
335.42
28.77
18.04
61.77
21.11
35.43
32.36
3.44
1.28
0.01
3.95a 3.49a
500 542
125 85
– 14
58 19
25.7 35
– 17
– 52
– 0.102
28.4 2
– 0.056
– –
– –
43.4 111
31.6 149
22.7 48.6
– –
35.8 128
121 459
0.99 4.98
9.79 33
0.18 1.06
2.0a 4.0a – –
460 1100 – –
26 110 81 370
16 110 34 270
16 75 20.9 51.6
– – – –
31 250 46.7 218
120 820 150 410
0.6 10 1.2 9.6
6 33 8.2 70
0.2 2 0.15 0.71
2997.55 208.69 89.99
70.86 7.60 9.08
32.47 11.78 6.70
6.82 30.32 3.94
35.85 32.90 8.44
8.04 22.28 5.24
18.52 59.03 11.52
27.65 48.21 94.27
4.92 9.56 1.69
9.55 10.93 14.42
0.24 0.10 0.49
– –
0.5 0.5
0.15 0.15
3 1.3
0.6 0.5
– –
2 2
10–75 75
– –
– –
– –
Values represented in %. SEMARNAT, 2010 Gromet et al. (1984). Wedepohl (1995). MacDonald et al., 2000. USEPA, 2001. 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
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(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.);
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.
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).
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.
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.
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 islands showed higher HEI values due to the impact of fishing activities all year round than the center and east San Benito.
Fig. 3. a–b Bioconcentration Factor (BCF) and Biota Sediment Accumulation Factor (BSAF) in the biota from San Benito Islands off the coast of Baja Cali fornia, Pacific Ocean, Mexico. 6
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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.
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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, �ndez-Camacho c Claudia J. Herna 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 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 b
A R T I C L E I N F O
A B S T R A C T
Keywords: Bioaccumulation Metals Toxicity Archipelago islands San Benito Mexico
Trace metal concentrations (Fe, Mn, Cr, Cu, Ni, Co, Pb, Zn, Cd, As, Hg) were determined in water, sediment and biota samples collected from the San Benito Islands off the Pacific Coast of Baja California, Mexico for a geochemical forensic study. Due to the proximity to the continental – oceanic crust interface and high biological endemism, the islands demanded a profound geochemical survey for evaluating the presence and provenance of trace metals. Results suggested that the metals in the region are mainly originated from the geogenic sources (Fe, 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 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, �nimo, San Benito, Cedros and Bahia Magdalena, Todos Santos, San Jero comprising a total of 21 islands and 97 islets. Among these archipelagos, because of the proximity to the continental-oceanic crust interface and
specific characteristics of topographic and biological diversity, the San 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: [email protected] (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 0964-5691/© 2019 Elsevier Ltd. All rights reserved.
Please cite this article as: S.B. Sujitha, Ocean and Coastal Management, https://doi.org/10.1016/j.ocecoaman.2019.105003
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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.
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 ~ oz et al., 2013). Among the three islands, only the San (Aguirre-Mun Benito west islands are habituated by the fishing population (approx. 70 persons) representing the fishing camp of Cooperativa Pescadores �n (INEGI, 2013) of Ensenada, Baja California. Nacionales de Abulo Moreover, these islands are considered to be one of the most ecologically
Fig. 1. Study area map indicating the sampling points in San Benito Islands off the coast of Baja California, Pacific Ocean, Mexico. 2
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intact non polar archipelagos in the world (Donlan et al., 2002).
Table 1 Classifications of HEI and NPI used for the present study.
2.2. Sampling and analyses Nearly 25 surface water (Fig. 1) and 11 biota samples were acquired from the San Benito Islands during November 2016, whereas only 2 sediment samples in triplicate were collected due to the rocky terrain, remoteness of the island and the practical difficulties during the field work. Biotic samples (11 nos.) included marine macrophytes (Eisenia arborea, Phyllospadix sp) and organisms (Crabs: Calappidae, Loxo rhynchus grandis; Fishes: Gymnothorax mordax, Halichoeres semicinctus, Hypsypops rubicundus, Paralabrax nebulifer, Caulolatilus affinis, Balistes polylepis and Semicossyphus pulcher). Trace metal clean procedures were strictly followed during sampling and the seawater samples were procured in pre-cleaned low density 1 L polyethylene bottles, subsequently acidified (pH < 2) using HNO3 (High purity J.T Baker) and refrigerated until further analysis. Trace metals in seawater were determined by direct aspiration Flame Atomic Absorp tion Spectrometry (Kramer, 2011; Sujitha et al., 2018) and lanthanum oxides were added to each sample to avoid spectral and non-spectral interferences. Biotic samples were taxonomically identified and thereafter washed 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 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 for 4 h in a hot plate and filtered through a 0.45μ membrane up to 50 ml for the determination of metals. Thereafter, concentrations of metals (Fe, Mn, Cr, Cu, Ni, Co, Pb, Zn and Cd) in water, sediments and biotic samples were determined using an Atomic Absorption Spectrometer (PerkinElmer Model AAnalyst100, CIIEMAD, IPN, Mexico) following the method EPA 7000B; US EPA, 2007). Estimation of Hg and As was carried out using the cold vapor technique and hydride generation respectively (EPA, 1979). Suitable Standard Reference Materials (SRM) for all the three com ponents [(Quality control Standard 21 for water); (Inorganics in marine sediments NIST 2702 for sediments) and (CRM-TMF Trace metals in fishes for biota)] were used. The recovery percentages of metals in 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 (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 (102) respectively. Quality and accuracy was guaranteed for the entire experimental procedure.
Index
Class
Description
Heavy metal Evaluation Index (HEI)
<400 400–800 ˃ 800 <0.7 0.7 < NPI < 1 1 < NPI < 2 2 < NPI < 3 NPI > 3
Low contamination Medium contamination High contamination Non polluted sediments Nearly polluted Lightly polluted Moderately polluted Seriously polluted sediments
Nemerow Pollution Index (NPI)
The Nemerow Pollution Index reveals the comprehensive status of trace metal pollution at a particular site and can be calculated by using the formula (Yan et al., 2016), sffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi ðCFÞ2 þ ðCFmax Þ2 NPI ¼ 2 where CF is the arithmetic mean of contamination factor of all trace metals and CFmax is the maximum CF factor value among the trace metals. The NPI values are categorized into five different classes (Table 1). c) Bioconcentration Factor (BCF) Bioconcentration is defined as the accumulation of metals by or ganisms from the ambient waters via respiratory or dermal absorption (Jitar et al., 2015). It is well known that only freely dissolved metal concentrations are only highly bioavailable and pass through biological membranes (Arnot and Gobas, 2006). However, for the present study BCF is calculated using the total metal concentrations in seawater for a comprehensive status on the accumulation of metals from bulk water phase. BCF (unitless) is calculated by using the formula: BCF ¼
Co Cwd
where Co is the metal concentration in the organism and Cwd is the metal concentration in water. d) Biota Sediment Accumulation Factor (BSAF) Biota Sediment Accumulation Factor (BSAF) is best suited for describing the bioaccumulation of metals from sediments in benthos food webs with non-equilibrium conditions (Ankley et al., 1992). BSAF can be calculated using the formula,
2.3. Data analyses
BSAF ¼
The determined concentrations of trace metals were also assessed based on several indices such as
Co Cs
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; Prasanna et al., 2012) and is calculated using the formula:
3.1. Seawater The average metal concentrations in the seawater were observed to be in the decreasing order of (all values in mg L 1): Pb (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 (0.029 � 0.004) > Cu (0.029 � 0.005) > Mn (0.025 � 0.002). The most important pathways by which trace metals reach the ocean include at mospheric deposition of mineral dust, submarine hydrothermalism and sediment dissolution along continental margins (Horner et al., 2015).
n X Hc HEI ¼ Hmac i¼1
where Hc is the monitored value and Hmac is the maximum allowable concentration of the ith parameter respectively and the resultant values are described based on three different classes (Table 1). b) Nemerow Pollution Index (NPI) 3
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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).
(3.44 � 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 ~ oz and Salamanca, 2003). (Mun 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
3.2. Sediments
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 �mez, 2013). However, crabs (40.13 mg kg 1 dry sediments (Redondo-Go wt.) presented two-fold higher levels of metals than fishes
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
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
Mn
1.00 – – – 0.44 – 0.47 – –
1.00 0.44 – – – – – –
Cr
Cu
1.00 – – – – –
1.00 0.66 – 0.51 –
Ni
Co
Pb
Cd
As
1.00 – – – –
1.00 – – –
1.00 – –
1.00 –
1.00
b. Biota Fe Mn Cr Cu Ni Co Pb Zn Cd As Hg
Fe
Mn
Cr
Cu
Ni
Co
Pb
Zn
Cd
As
Hg
1.00 – – 0.88 0.81 0.83 0.83 – 0.90 – –
1.00 – – – – – – – – –
1.00 – 0.70 – – – – – –
1.00 0.74 0.80 0.83 – 0.99 – –
1.00 0.99 0.98 – 0.83 – –
1.00 1.00 – 0.88 – –
1.00 – 0.90 – –
1.00 – 0.94 –
1.00 – –
1.00 –
1.00
p < 0.05 4
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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. Water (mg/L) Present Study Permissible Limits SEMARNAT, 2010b Sediment (mg/kg) Present Study Crustal average NASCc UCCd Sediment Quality Guidelines TECe PEC Ecotoxicological Values LELf SEL ERLg ERM Biota (mg/kg) Present study Macrophytes Crabs Fishes Permissible limits in fishes WHO, 1985 FEPA, 2003 a b c d e f g
Fe
Mn
Cr
Cu
Ni
Co
Pb
Zn
Cd
As
Hg
0.169
0.025
0.047
0.029
0.154
0.135
0.182
–
0.029
0.118
–
0.050
0.020
0.010
0.010
0.002
–
0.010
0.020
0.0002
0.010
–
1.60a
335.42
28.77
18.04
61.77
21.11
35.43
32.36
3.44
1.28
0.01
3.95a 3.49a
500 542
125 85
– 14
58 19
25.7 35
– 17
– 52
– 0.102
28.4 2
– 0.056
– –
– –
43.4 111
31.6 149
22.7 48.6
– –
35.8 128
121 459
0.99 4.98
9.79 33
0.18 1.06
2.0a 4.0a – –
460 1100 – –
26 110 81 370
16 110 34 270
16 75 20.9 51.6
– – – –
31 250 46.7 218
120 820 150 410
0.6 10 1.2 9.6
6 33 8.2 70
0.2 2 0.15 0.71
2997.55 208.69 89.99
70.86 7.60 9.08
32.47 11.78 6.70
6.82 30.32 3.94
35.85 32.90 8.44
8.04 22.28 5.24
18.52 59.03 11.52
27.65 48.21 94.27
4.92 9.56 1.69
9.55 10.93 14.42
0.24 0.10 0.49
– –
0.5 0.5
0.15 0.15
3 1.3
0.6 0.5
– –
2 2
10–75 75
– –
– –
– –
Values represented in %. SEMARNAT, 2010 Gromet et al. (1984). Wedepohl (1995). MacDonald et al., 2000. USEPA, 2001. 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
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(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.);
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.
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).
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.
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.
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 islands showed higher HEI values due to the impact of fishing activities all year round than the center and east San Benito.
Fig. 3. a–b Bioconcentration Factor (BCF) and Biota Sediment Accumulation Factor (BSAF) in the biota from San Benito Islands off the coast of Baja Cali fornia, Pacific Ocean, Mexico. 6
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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.
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