Bioaccumulation of trace metals in farmed pacific oysters Crassostrea gigas from SW Gulf of California coast, Mexico

Accepted Manuscript Bioaccumulation of trace metals in farmed pacific oysters Crassostrea gigas from SW Gulf of California coast, Mexico

M.P. Jonathan, N.P. Muñoz-Sevilla, Andrés Martin Góngora-Gómez, Raquel Gabriela Luna Varela, S.B. Sujitha, D.C. Escobedo-Urías, P.F. Rodríguez-Espinosa, Lorena Elizabeth Campos Villegas PII:

S0045-6535(17)31320-6

DOI:

10.1016/j.chemosphere.2017.08.098

Reference:

CHEM 19796

To appear in:

Chemosphere

Received Date:

23 April 2017

Revised Date:

03 August 2017

Accepted Date:

18 August 2017

Please cite this article as: M.P. Jonathan, N.P. Muñoz-Sevilla, Andrés Martin Góngora-Gómez, Raquel Gabriela Luna Varela, S.B. Sujitha, D.C. Escobedo-Urías, P.F. Rodríguez-Espinosa, Lorena Elizabeth Campos Villegas, Bioaccumulation of trace metals in farmed pacific oysters Crassostrea gigas from SW Gulf of California coast, Mexico, Chemosphere (2017), doi: 10.1016/j. chemosphere.2017.08.098

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ACCEPTED MANUSCRIPT

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Bioaccumulation of trace metals in farmed pacific oysters

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Crassostrea gigas from SW Gulf of California coast, Mexico

3 4

M.P. Jonathana†, N.P. Muñoz-Sevillaa, Andrés Martin Góngora-Gómezb,

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Raquel Gabriela Luna Varelaa,c, S. B. Sujithaa, D.C Escobedo-Uríasb,

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P. F. Rodríguez-Espinosaa and Lorena Elizabeth Campos Villegasa

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aCentro

Interdisciplinario de Investigaciones y Estudios sobre Medio Ambiente y

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Desarrollo (CIIEMAD), Instituto Politécnico Nacional (IPN),

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Calle 30 de Junio de 1520, Barrio la Laguna Ticomán,

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Del. Gustavo A. Madero, C.P.07340, Ciudad de México (CDMX), México.

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bCentro

Interdisciplinario de Investigación para el Desarrollo Integral Regional

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(CIIDIR-IPN), Instituto Politécnico Nacional (IPN),

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Bulevar Juan de Dios Bátiz Paredes #250, Colonia San Joachin, Guasave, Sinaloa, México.

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cInstituto

de Ciencias del Mar y Limnologia, Universidad Nacional Autónoma de México

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(UNAM), Circuito Exterior s/n, Coyoacan, Ciudad Universitaria, 04510

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Ciudad de México (CDMX), México.

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†Corresponding

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†E-mail

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Keywords:

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author.

Tel.: +52 55 57296000 Ext: 52701

address: [email protected] Bioaccumulation; Crassostrea gigas; metals; cultivated oysters; toxicity; Mexico

Revised manuscript submitted to Chemosphere (Aug, 2017).

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Abstract

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The aim of the study was to evaluate the bioavailability of trace metals (Chromium,

3

Copper, Nickel, Lead, Zinc, Cadmium, Arsenic, and Mercury) in the commercially

4

consumed Crassostrea gigas oysters collected over a 12-month growth period (2011-12)

5

from an experimental cultivation farm in La Pitahaya, Sinaloa State, Mexico. Sediment and

6

water samples were also collected from four different zones adjacent to the cultivation area

7

to identify the concentration patterns metals. The results revealed that sewage disposals,

8

fertilizers used for agricultural practices and shrimp culture are the major sources for the

9

enrichment of certain toxic metals. The metal concentrations in oysters presented a

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decreasing order of abundance (all values in mg Kg-1): Zn (278.91 ± 93.03) > Cu (63.13±

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31.72) > Cr (22.29 ± 30.23) > Cd (14.54 ± 4.28) > Ni (9.41 ± 11.33) > Pb (2.22 ± 1.33) >

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As (0.58 ± 0.91) > Hg (0.04 ± 0.06). Bioconcentration Factor (BCF) and Biota Sediment

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Accumulation Factor (BSAFs) exhibited that C. gigas in the region are strong accumulators

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for Zn and Cd respectively. Thus, the present study proves to fulfill the gap in

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understanding the rate of bioaccumulation of metals in C. gigas which is regarded as the

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most sought after oyster species globally.

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1

Introduction

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Numerous studies on coastal regions have been focusing on metal contamination as

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it is regarded as one of the major concern in altering the ecological balance due to their vast

4

source, persistence, bioaccumulation, non-degradability and toxic effects on the biota

5

(Besada et al., 2011; Wang et al., 2013; Le et al., 2016). Although, many animal and plant

6

species are proposed for marine biomonitoring studies, bivalve mollusks which exhibit

7

several characters of ideal indicator organisms such as their sedentary nature, high

8

numerical abundance and life span are considered to be the best bioindicators for coastal

9

pollution studies (Green et al., 2000; Thèbault et al., 2008). Henceforth, since 1970’s a

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Worldwide scheme of using mussels and oysters for monitoring ocean health has been

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implemented (Goldberg, 1975; Watling and Watling, 1976; Phillips, 1977; Davies and

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Pirie, 1980).

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Pacific Oyster (Crassostrea gigas, Thunberg, 1793) through its potential for rapid

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growth and tolerance to environmental conditions is considered to be the most sophisticated

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of all the oyster species; the most pursued after species for cultivation. Intertidal oyster

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cultivation is one of most important aquaculture industry to satisfy the global demands for

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seafood consumption and Pacific oysters are the most dominant one (> 96 % by value and

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tonnage FAO, 2014).

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In México, the cultivation of C. gigas was introduced during the early 1973 and the

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major production was from the North western states, where the annual commercial

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production was 1600 tons (SAGARPA, 2010; Paez-Osuna et al., 2010). The net production

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of C. gigas in the region was gradually affected by human settlements, industrial

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developments, intensive agriculture activities, poultry and the construction of smaller dams 3

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across the minor rivers/channels feeding the lagoon (CENDEPESCA, 2012; Berges-

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Tiznado et al., 2013).

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Crassostrea gigas are marine bivalve mollusks, where both aqueous and dietary

4

exposures result in metal uptake and accumulation in the organism (Widmeyer et al., 2008).

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It is a highly selective suspension feeder which feed on phytoplankton, suspended

6

materials, sediments and aggregates consisting of high molecular weight substances,

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detritus, fecal pellets and microorganisms by filtering large volumes of seawater through

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their gills (Ward and Shumway, 2004, Liu and Deng, 2007). Oyster farms act as biological

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filters, whereas the seabed sediments are organically enriched and fine textured (Forrest et

10

al., 2009). Due to their sensitiveness and rapid response to pollutants, oysters prove to be

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sentinel organisms for marine eco-toxicological tests and coastal water quality (Knakievicz,

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2014). The relocation of metals from water column to sediment fractions and their

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subsequent bioavailability and toxicity to marine organisms primarily depends on their

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geochemical partitioning (Tessier et al., 1979; Luoma., 1989; Jara-Marini et al., 2013; Liu

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and Deng, 2007) and it has been proved that marine organisms are characterized by a

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greater spatial ability to accumulate metals compared to bottom sediments (Szefer et al.,

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2006). Henceforth, examining these species would give a comprehensive pollution status of

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the farmed oysters for human consumption.

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The main objective of the present study was to evaluate the concentrations of

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metals [Chromium (Cr), Copper (Cu), Nickel (Ni), Lead (Pb), Zinc (Zn), Cadmium (Cd),

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Arsenic (As), Mercury (Hg)] in Crassostrea gigas, water and sediments adjoining the

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oyster cultivation farm in the La Pitahaya channel, Sinaloa state, Northwest Mexico.

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Materials and Methods

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2.1

Study Area

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La Pitahaya channel is located between 25°18ʹ11ʺ N latitude and 108°30ʹ54ʺ W

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longitude along the Northwestern Pacific coast of Mexico in the city of Guasave, Sinaloa

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State forming the southern part of the larger lagoon system (Topolombompo and

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Navachiste) in Northern Mexico (Figure 1). Fish farming or aquaculture is considered to be

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the principal industry in Guasave. The State of Sinaloa is regarded as the “Agricultural

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Heart of Mexico” for its enormous production of agricultural products. The alluvial plains

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of northern and Central Sinaloa are among the most productive areas producing maize,

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soybean, sugarcane and vegetables. The channel has excessive sediment supply from Sierra

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Madre Occidental and effluents from anthropogenic activities (rural communities,

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agricultural and aquaculture practices).

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Geologically the region is dominated by Mesozoic granitic batholiths of the North

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American Cordillera with lacustrine sediments, where semitropical weathering is a major

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constraint of this region (Henry et al., 2003). The region is also overlaid by large volume of

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silicic igneous magmatism during late Miocene and basaltic andesites (Ferrari et al., 2007;

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Murray and Busty, 2015).

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2.2

Sampling and analytical procedures

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The entire experimental hatchery setup was stationed at La Pitahaya channel

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(Station no. 3) at a depth of 1.5 m above the water level and was controlled by CIIDIR, IPN

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Research Center in Guasave, Sinaloa State, Mexico. Samples were collected from four

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different points for a one year period during March 2011 to March 2012. 1) El Chicote

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(discharge zone from aqua culture ponds); 2) La Piedra (domestic discharge point); 3) La 5

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Pithaya channel (cultivation of Crassostrea gigas) and 4) La Bocanita (estuarine point in

2

contact with open sea) (Figure 1). At each sampling point, water and sediment samples

3

were collected, whereas oysters were collected from the experimental oyster cultivation in

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La Pitahaya. Long line cultivation method was adopted where NeisterTM plastic baskets (50

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cm × 50 cm × 10 cm: w × l × d) were used. Soft oyster tissues from twelve samples (as

6

triplicates) were collected from the cultivated oyster farms each month of the study period.

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Samples were also procured during the last week of July 2011 to evaluate the metal

8

concentration patterns due to the impact of heavy inflow of river water after a major rainfall

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event.

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Twenty-eight surface sediment and water samples (seven from each site) were

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collected from the four different sites (mentioned above) during the cultivation period of C.

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gigas. The water samples were treated with nitric acid and frozen until further analysis of

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determination of dissolved metals. The surface sediment samples were collected using a

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Van Veen grab sampler and the samples were oven dried at 60 °C for 24 hours and

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powdered upto 63 µm using an agate mortar. For the total and acid leachable analysis, 1 g

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of each sediment sample was digested using HNO3 + HCl + HF + H3BO4 in an automated

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microwave digester (Loring et al., 1992) and HNO3 + HCl + H2O2 for the determination of

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Cr, Cu, Ni, Pb, Zn, Cd, As and Hg respectively. Evaluating the leachable fraction in

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sediments is carried out as it often extracts the metal fraction that is considered as external

20

(or) absorbed metals and is highly bioavailable (Agemian and Chau, 1976; Taliadouri,

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1995; Janakiraman et al., 2007; Jonathan et al., 2010). The collected oyster samples were

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also oven dried at 60 °C for 24 hours and were homogenized using an agate mortar and

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consequently digested using HNO3+ HCl + H2O2 for further analysis. The concentrations of 6

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metals (Cr, Cu, Ni, Pb, Zn, Cd, As and Hg) in water, sediments and oysters were

2

determined using a Perkin Elmer Model AAnalyst100 atomic absorption spectrometer

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(Portman, 1976; EPA 3010a, 1992). Cold vapor and hydride generation techniques were

4

used to estimate Hg and As concentrations respectively. Quality and accuracy of the

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experimental procedure and the equipment was ensured using a Certified reference material

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for water (Quality Control Standard 21), sediments (CRM – River sediment solution B) and

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oysters (CRM – Oyster tissue) after every five samples (Table 1).

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2.3

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i. Bioconcentration factor

Data Processing

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Bioconcentration is the process by which a chemical compound is absorbed by an

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organism from the ambient environment only through its respiratory and dermal surfaces.

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The degree to which bioconcentration occurs is stated as Bioconcentration Factor (BCF)

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which is calculated by using the formula (Arnot and Gobas, 2006), BCF = Concentration of

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metal in the organism/ Concentration of metal in water

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ii. Biota Sediment Accumulation Factor (BSAF)

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Biota Sediment Accumulation Factor refers to the bioavailable concentration

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reflecting operationally the efficiency of sentinel organisms as bioconcentrators of any

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given metal. Henceforth, to estimate the proportion in which the metal occurs in an

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organism, BSAFs are used which is calculated by the ratio between the concentrations of a

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pollutant in an organism to the concentration in sediment aggregates (Thomann et al.,

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1995), where BSAF = Concentration of metal in organism/Concentration of metal in

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sediment.

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iii. Statistical Analysis 7

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Correlation matrices (p ˃ 0.05) were generated for the concentrations of metals in

2

water, sediments and C. gigas using Statistica version 12.0 for a better understanding of the

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interrelationship of different metals.

4 5

3

Results and Discussion

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3.1

Metals in water

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The average dissolved metal concentrations (Table 2) were observed to be in the

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decreasing order of (all values in mg L-1): Ni (0.094) > Pb (0.072) > Cu (0.029) > Cd

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(0.019) > Zn (0.019) > Cr (0.010) > As (0.0002) > Hg (0.0002). Seasonally, average metal

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concentrations in water were high during the rainy season (July 2011 to October 2011) and

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ranged between 0.030 - 0.036 mg L-1. The high values of Ni (0.087 – 0.105 mg L-1) are

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influenced by the digenetic remobilization of the benthic sediments (Lares et al., 2009) and

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domestic wastewater effluents (Cempel and Nikel, 2006). Significant positive correlations

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between Ni vs Cr (r2 = 0.65; p < 0.05) indicate strong local influences and mobilization of

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trace metals from biogenic particles or sediments (Achterberg and Van Den Berg, 1997),

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whereas Ni vs Hg (r2 = 0.63; p < 0.05) exhibit the effects from sewage sludges (Basta et al.,

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2005).

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containing pesticides and fertilizers that are used in the study region for agricultural

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purposes (EPA, 2001). Likewise, the average concentrations (all values in mg L-1) of

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dissolved Cu (0.029), Cd (0.019), Zn (0.019) and Cr (0.010) are probably sourced from the

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discharge of untreated domestic and municipal sewage effluents, pesticides and fertilizers,

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from increased agricultural activity adjoining the study area (Cuevas et al., 2006), which is

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well supported by the positive correlations between Cu vs Cd (r2 = 0.73; p < 0.05) and Cr

High concentrations of Pb (0.072 mg L-1) are mainly sourced from the lead

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vs As (r2 = 0.61; p < 0.05). Apart from the anthropogenic sources, similarity in the

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temporal variations of dissolved Cd (March – December, 2011) is a good indicator of

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upwelling process off the coast of Gulf of California and it is also associated with the

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organic matter production and remineralization (Sañudo-Wilhelmy and Flegal, 1991; Jara-

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Marini et al., 2013). Following the recommended marine water quality criteria for the

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protection of aquatic life and human health, the concentrations of Cu, Cd, Ni, Zn and Pb

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were higher than that of the maximum permissible acute and chronic concentrations

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prescribed by USEPA, 2009 and Diario Oficial de la Federación, Mexico 2014.

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3.2

Metals in sediments

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The concentration of total and leachable metals exhibited almost similar distribution

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patterns in the four sampling stations representing the influences from natural and external

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inputs. El Chicote (discharge zone from aquaculture ponds) presented higher metal

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concentrations (all values in mg Kg-1): Cu (36), Pb (32), Cd (5), As (4.35), Hg (0.24), due

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to the impact of sewage effluents. Similarly, in the cultivation site La Pithaya also

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presented higher metal concentrations (all values in mg Kg-1): Zn (132.30), Cr (46), Ni

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(37.12), Cd (5) because oyster farms act as biological filters where the sea bed sediments

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are organically enriched, fine textured and anoxic in nature adsorbing high levels of metals

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(Forrest and Creese, 2006). Conversely, the station La Bocanita (near the mouth) presented

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lower metal concentrations (all values in mg Kg-1): Ni (10), Pb (7), Cr (6), Cu (4), Hg

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(0.01) due to the differences in grain size, tidal mixing and degradation of organic matter

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(Baeyens et al., 2005) at the mouth. The average concentrations of leachable metals (Table

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3) were found to be in the decreasing order of (all values in mg Kg-1): Zn (76.27) > Cr

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(26.40) > Ni (24.30) > Cu (21.69) > Pb (19.55) > As (2.79) > Cd (1.14) > Hg (0.15). 9

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Naturally, the presence of Pb-Zn ore mine in the upstream regions of the study area (~80

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Km in the eastern side) and the dominancy of alluviums and nature of fluvial gravels are

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the possible sources for the accumulation of metals (Duskin and Clark, 1973).

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presence of Late Cretaceous and Late Tertiary sedimentary sequences of the region that are

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dominant in calcareous limestone with metamorphosed mafic intrusions also source the

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bioavailable elements like Cu, Zn, and Cd mainly due to the calcareous composition that

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are highly prone to erosion and dissolution processes (Ortega-Guitérrez et al., 1979; Henry

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et al., 2003; McDowell et al., 2001). In addition, epithermal mineralization, intense

9

alteration and weathering processes of the rocks also result in high concentrations of metals

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in the sediments of the study area (eg. Murray and Busty, 2015). High values of Cu (36 mg

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Kg-1), Pb (32 mg Kg-1), Cd (5 mg Kg-1) and As (4.35 mg Kg-1) observed in the sediments at

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El Chicote are due to its location near aquaculture ponds where these metals are used in

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algicides and pesticides (Egna and Boyd, 1997). Strong inter-metallic relationships (p <

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0.05) observed between Cu vs Ni (r2= 0.88), Zn (r2= 0.94), Pb (r2 = 0.88), is attributed to

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the influence of sewage sludges, manures, agrochemicals and phosphate fertilizers from

16

extensive agricultural practices and the similar geochemical pathways of the analyzed

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metals (Yuan et al., 2011; Lu et al., 2012). Likewise, the elevated levels of Zn (132.30 mg

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Kg-1) in the cultivated farms of oysters are sourced from the discharges of agricultural

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drains in the area (Green Ruiz and Páez-Osuna, 2001). Positive relationship between Ni vs

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Pb (r2 = 0.80), Pb vs Zn (r2 = 0.93) also represent the influences from untreated sewage

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effluents from domestic, agriculture and shrimp culture practices that alter the estuarine

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conditions (Alloway, 1990; Leoni and Sartori,1997; Wongetal, 2007).

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The

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The bioavailable fraction of metals in sediments were calculated using total and

2

leachable metal concentrations and it presented the following sequence (all values in %):

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Cu (84) > Zn (71) > Cr (60) > As (46) > Ni (42) > Pb (36) > Cd (25) > Hg (11). The high

4

bioavailability of Cu and Zn in the cultivation sites are related to their use in antifouling

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and feeding products (Burridge et al., 2008), whereas Cr is from the use of antibiotics in the

6

farming sector (Shamsuzzaman and Biswas, 2012). Moreover, the cultivation centers are

7

dominated with organic rich fine layers in the bottom sediments, which are anoxic in nature

8

accumulating more bioavailable trace metals than the surrounding regions (eg. Forrest and

9

Creese, 2006).

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The potential harmful effects of studied metals were also compared with Sediment

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Quality Guidelines (SQGs) and Ecotoxicological values such as Lowest effect level (LEL),

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Severe Effect Level (SEL), Effect Range Low (ERL) and Effect Range Medium (ERM)

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(Table 3). The concentrations of Cd, Cr, Ni and Zn were higher than the values of

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Threshold Effect Concentration (TEC) indicating adverse effects on the biota (MacDonald

15

et al., 2000). Likewise, the metals Cu, Cd, Cr, Ni, Pb and Zn were found to be higher than

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that of the values of LEL and ERL suggesting probable risks to the biological community

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(USEPA, 2001; Long et al., 1995).

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3.1

Metals in cultivated (C. gigas) oysters

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Bioaccumulation patterns of metals in C. gigas are depicted in figure 2a-h. In spite

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of seasonal fluctuations, the calculated average values of metal concentrations in oysters

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presented a decreasing trend of Zn > Cu > Cr > Cd > Ni > Pb > As > Hg. High average

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concentration of Zn (279 mg Kg-1) observed in C. gigas is attributed to the fact that

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mollusks possess high affinity in the accumulation of Zn (Paez-Osuna & Osuna-Martinez, 11

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2011) for numerous aspects of cellular metabolism by hundreds of critical enzymes

2

(USDA, 2011) and it is generally agreed that the highest concentrations of zinc in marine

3

biota are found in the tissues of filter-feeding mollusks, especially oysters (Eisler, 2000).

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Strong positive correlation between Zn vs Cd (r2 = 0.98; p < 0.05) indicate their similar

5

physicochemical properties and binding empathies to the same proteins in the tissues

6

(Brzoska and Moniuszko-Jakoniuk, 2001). Cu levels varied between 26 – 142 mg Kg-1 with

7

an average of 63.13 mg Kg-1 and were found to be lesser than the values observed by Paez-

8

Osuna et al., 1991 (67 mg Kg-1) and Frias-Espericueta et al., 2005 (76.5 mg Kg-1) in C.

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corteziensis along the Mexican Pacific coast. Cu concentrations found in oysters are

10

associated to higher assimilation efficiencies, bioavailability and its source from feeding

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products (Wang, 2002). Average chromium levels were observed to be 22.29 (mg Kg-1)

12

which is due to the impact of sewage outfalls and the ability of oysters to accumulate Cr far

13

in excess from the seawater (Maanan, 2007). High values of Ni (42.60 mg Kg-1) in the

14

oysters show that the uptake of Ni is directly proportional to the nickel concentrations

15

either through ingestion or filtration process (Haidari et al., 2013). The strong positive

16

correlation (Table 5) between Cr vs Ni (r2 = 0.96; p < 0.05) indicate that they are

17

bioavailable with a similar source from the geologic formations and sewage sludges from

18

agricultural soils (Gonnelli and Renella, 2012). Cadmium levels ranged between 9.00 mg

19

Kg-1 (November 2011) to 21.40 mg Kg-1 (July 2011) and presented a balanced

20

concentration during the entire period of cultivation, because of their natural presence in

21

waters and influence of agricultural effluents (Jara-Marini et al., 2013), particularly

22

phosphate fertilizers (UNEP, 2000) from the adjoining areas. Seasonal behavior of Pb

23

varied during the cultivation period from 4.60 mg Kg-1 in October 2011 to 0.8 mg Kg-1 in 12

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November 2011, which is owed to the high influxes from the aquaculture and industrial

2

complexes of the region (Luoma and Rainbow, 2005). Less concentration of As (0.19 mg

3

Kg-1) was observed during the rainy season due to the dilution effect of rains (Song et al.,

4

2015), whereas the high value of 3.46 mg Kg-1 in December 2011 is attributed to the

5

wastewater discharges and differences in the temperature and salinity values also induce the

6

accumulation of As (Lango–Reynoso et al., 2010). However, As values in the present study

7

were comparatively less than 23 mg Kg-1 reported for C. virginica by Hernandez et al.,

8

2005 in Bahia Cienfuegos of Cuba. The filter feeders presented Hg values that ranged

9

between (0.01 – 0.02 mg Kg-1) sourced mainly from domestic waste discharges, however

10

minor levels of Hg are highly toxic as they undergo rapid biomagnification in the marine

11

food web (Hobson and Welch 1992; Dehn et al., 2006). Cr, Cu, Pb in the studied C. gigas

12

species exhibited two to three-fold increase when compared to the maximum permissible

13

limits (Table 4) put forth by FDA, 1993, whereas Cd levels were extremely high than the

14

permissible limits considered by various organizations worldwide.

15

In the present study, dimensions and weight of each farmed species of C. gigas was

16

measured to analyze the performance and state of oyster during its growing period. The

17

results revealed a progressive trend where the length, width and weight of each species

18

indicated a steady growth during the entire study. At the start of the study (June 2011), the

19

species marked a total length of 92.92 cm, width of 10.53 cm and it weighed only 15.26 g,

20

whereas at the end of the study (March 2012), the oysters presented a steady increase in the

21

total length of 203.72 cm, width of 30.21 cm and weight of 168.95 g. Correlation studies

22

(Table 5) exhibited strong positive relationship between length vs width (r2 = 0.99; p <

23

0.05), weight (r2 = 0.98; p < 0.05) indicating isometric growth of the farmed oyster species. 13

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However, Cd, Cr, Ni, Pb and Zn presented negative correlations with the biometry data

2

supporting to the fact that small oysters are usually labelled to contain higher metal

3

concentrations than the larger ones (Shulkin et al., 2003; Liu and Deng, 2007) because

4

younger bivalves exhibit faster growth rates allowing rapid turnover of cellular materials

5

and larger surface to volume ratio resulting in more heavy metal uptake and incorporation

6

into the tissues (Cheung and Wong, 1992).

7

4

Data Assessment

8

4.1

Bioconcentration Factor (BCF)

9

BCF values in C. gigas exhibited an order (Figure 3a) of Zn (15641) > As (3326) >

10

Cr (2310) > Cu (2157) > Cd (734) > Hg (282) > Ni (94) > Pb (29). BCF values > 1000 for

11

Zn, As, Cr and Cu denote significant and slow accumulation, potentiality for chronic effects

12

and food chain accumulation (Kwok et al., 2014; Jayaprakash et al., 2015). High BCF

13

values also indicate that oysters uptake free metal ions from solution more efficiently via

14

dermal organs.

15

4.2

Biota sediment accumulation factor (BSAF)

16

The biota sediment accumulation factor (BSAF) presented the following order

17

(Figure 2b): Cd > Zn > Cu > Hg > Cr > Ni > Pb > As. On an average, BSAFs were found to

18

be 12.38 for Cd, 3.89 for Zn, 3.52 for Cu and 2.88 for Hg reflecting high level absorbing

19

capacity of these metals in the soft tissues of oysters (Figure 3b). The high bioavailability

20

of Cd is due to the fact that they are mostly associated with the exchangeable carbonates

21

and organic phases in the biota and thus they are readily available to the organisms (Soto-

22

Jiménez et al., 2001). Based on the results, C. gigas is considered to be strong accumulators

23

for Cd and moderate accumulators for Zn, Cu and Hg. 14

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1

5

Conclusion

2

This study exhibited the fact that anthropogenic influences such as sewage wastes

3

from agricultural fields, shrimp culture and domestic sludges govern the concentration

4

patterns of metals (Cu, Cd, Cr, Ni, Pb, Zn, As, Hg) in water, sediments and cultivated C.

5

gigas. The concentration levels of metals in oysters are integrated measures of the

6

availability of each metal to the oyster species over time and are interspecies specific in

7

terms of their physiological and metabolic needs. Cd levels observed in the present study

8

exceeded the permissible limits for human consumption established by public health

9

standards globally. This study also proves to be a baseline for developing remediation

10

techniques in aquaculture sites for sustainable cultivation strategies and it is evident that a

11

continuous monitoring system is obligatory in the cultivation sites for healthy production of

12

seafood.

13 14 15 16 17 18 19 20 21 22 23 15

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1

Acknowledgements

2

Funding from Secretaria de Investigación Posgradate (SIP), Instituto Politécnico Nacional

3

(IPN), Mexico for this project is greatly acknowledged. Authors from IPN thank COFAA

4

and EDI for their support. MPJ, NPMS and PFRE thank Sistema Nacional de

5

Investigadores (SNI), CONACyT, México. RGLV and SBS thanks CONACyT for the

6

research fellowship. This article is the 92nd partial contribution from Earth System Science

7

Group (ESSG), Chennai, India (Participating members: MPJ & SBS).

16

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References Achterberg, E. P., Van den Berg, C. M. G., 1997. Chemical speciation of chromium and nickel in the Western Mediterranean. Deep Sea Res. II, 44(3-4), 693 – 720. Agemian, H., Chau, A.S.Y., 1976. Evaluation of extraction techniques for determination of metals in aquatic sediments. Analyst 101, 761-767. Alloway, B.J., 1990. Heavy Metals in Soils. Blackie, London, p. 363. Arnot, J. A., Gobas, F. A. P. C., 2006. A review of Bioconcentration Factor (BCF) and Bioaccumulation Factor (BAF) assessments for organic chemical in aquatic organisms. Environ. Rev., 14, 257 – 297. Baeyens, W., Leermakers, M., DeGieter, M., Nguyen, H. L., Parmentier, K., Panutrakul, S., Elskens, M., 2005. Overview of trace metal contamination in the Scheldt estuary and effect of regulatory measures. Hydrobiologia, 540, 141-154. Basta, N. T., Ryan, J. A., Chaney, R. L., 2005. Trace element chemistry in residual treated soil: Key concepts and metal bioavailability. J Environ. Quality., 34 (1), 49-63. Berges–Tiznado, M.E., Paéz-Osuna, F., Notti, A., Regoli, F., 2013. Arsenic and arsenic species in cultured oyster (Crassostrea gigas and Crassostrea corteziensis) from coastal lagoons of the SE Gulf of California, Mexico. Biol. Trace elem. Res., 151, 43-49. Besada, V., Manuel Andrade, J., Schultze, F., Jose González, J., 2011. Monitoring of heavy metals (Mytilus galloprovincialis) from the Spanish North Atlantic coast. Cont. Shelf Res., 31, 457-465. Brzoska, M. M., Moniuszko-Jakoniuk, J., 2001. Interactions between cadmium and zinc in the organisms. Food Chem. Toxicol., 39, 967-980. 17

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List of tables Table 1

Recovery percentages of analyzed metals in water, sediment and oyster.

Table 2

Comparison of the studied metal concentrations in water with that of the maximum permissible limits.

Table 3

Comparison of studied metal concentrations with that of crustal average, Sediment Quality Guidelines and Ecotoxicological values.

Table 4

Comparison of the studied metal concentrations in C. gigas with that of the maximum permissible limits set forth by various organizations.

Table 5

Correlation matrix for biometric measurements and metal concentrations in C. gigas from La Pitahaya channel, SW Gulf of California, Mexico

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List of figures Figure 1

Study area map indicating the four different sites of sample collection and the artificial experimental cultivation site in La Pitahaya Channel in SW Gulf of California, México.

Figure 2a-h

Metal concentration pattern in oysters (C. gigas) during the entire cultivation period from La Pitahaya Channel in SW Gulf of California, México.

Figure 3a-b

Bioconcentration Factor (BCF) and Biota Sediment Accumulation Factor (BSAF) in oysters (C. gigas) from the La Pitahaya Channel in SW Gulf of California, México.

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Research Highlights 

Elevated metal levels in oyster species (C. gigas) from a cultivation site in SW Gulf of California Coast, Mexico



High affinities of oyster to accumulate Zn and Cd from the ambient water and sediment fractions



Impact of effluents from agriculture, aquaculture and domestic waste disposals.

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Table 1

Recovery percentages of analyzed metals in water, sediment and oyster

Elements Cu Cd Cr Ni Pb Zn As Hg All values in %

Water 101.8 96.1 96 95.6 106.6 100.2 95.2 95.3

Sediment 98.1 94 85.9 91.62 95.05 104.6 87.5 92

Oyster 98.8 95.4 120 110.5 110.9 102.4 96 103.8

ACCEPTED MANUSCRIPT Table 2

Comparison of the studied metal concentrations in water with that of the maximum permissible limits

Present study Min - Max Mean ± SD

Cu

Cd

Cr

Ni

Pb

Zn

As

Hg

0.0230.045 0.027

0.016 – 0.023 0.019

0.009 – 0.011 0.010

0.087 – 0.105 0.094

0.056 – 0.084 0.072

0.011 – 0.031 0.019

0.0001 – 0.0002 0.0002

0.00010.0003 0.0002

± 0.007

± 0.002

±0.001

± 0.007

± 0.010

± 0.008

±0.00004

± 0.0001

Permissible limits 0.010 0.0002 0.010 0.002 0.010 0.020 0.040 0.0001 Mexico1 2 USEPA Acute Conc. 0.005 0.033 1.100 0.074 0.210 0.090 0.069 0.002 Chronic Conc. 0.003 0.008 0.050 0.008 0.008 0.081 0.036 0.001 All values in mg L-1; 1Diario Oficial de la Federación, 2014; 2US Environmental Protection Agency, 2009.

Table 3 Comparison of studied metal concentrations with that of crustal average, Sediment Quality Guidelines and Ecotoxicological values.

Present study (Total metals) Min- Max Mean ± SD Leachable metals Min- Max Mean ± SD Crustal Average NASC1 UCC2 Sediment Quality Guidelines3 TEC PEC Ecotoxicological values LEL4 SEL ERL5 ERM 1Gromet

Cu

Cd

Cr

Ni

Pb

Zn

As

Hg

6.50 - 46 25.74 ± 11.18

3-5 4.23 ± 0.66

29 - 67 44.92 ± 9.18

33.50 - 72 54.61 ± 11.10

36 – 71.05 54.05 ± 10.14

42 – 146.39 95.10 ± 27.48

0.80 – 5.50 3.47 ± 0.99

0.02 – 0.50 0.20 ± 0.15

4 -36 21.69 ± 10.09

0-5 1.14 ± 0.58

6 - 46 26.40 ± 9.91

10 - 37.12 24.30 ± 7.92

7 – 32. 19.55 ± 6.68

22-132.30 76.27 ± 26.11

0 - 4.35 2.79 ± 1.28

0.01 – 0.24 0.15 ± 0.08

14

0.102

125 85

58 19

17

52

28.4 2

0.056

31.6 149

0.99 4.98

43.4 111

22.7 48.6

35.8 128

121 459

9.79 33

0.18 1.06

16 110 34 270

0.6 10 1.2 9.6

26 110 81 370

16 75 20.9 57.6

31 250 46.7 218

120 820 150 410

6 33 8.2 70

0.2 2 0.15 0.71

et al., 1984; 2Wedepohl, 1995; 3MacDonald et al.,2000; 4USEPA, 2001; 5Long et al.,1995. NASC - North American Shale Composite; UCC - Upper Continental Crust; TEC – Threshold Effect Concentration; PEC – Probable Effect Concentration; LEL – Lowest Effect Level; SEL – Severe Effect Level; ERL – Effect Range Low; ERM – Effect Range Medium. All values represented in mg Kg-1

Table 4

Comparison of the studied metal concentrations in C. gigas with that of the maximum permissible limits set forth by various organizations. Cu

Cd

Cr

Ni

Pb

Zn

As

Hg

Present study 26.33 - 85.33 4.07 – 21.33 0.33 – 104 1 – 42.33 < LDM – 4.67 95.10 – 416.67 0.07-0.42 0.003 – 0.03 Min- Max 63.37 ± 31.72 14.54 ± 4.28 22.29 ± 30.23 9.41± 11.33 2.22 ± 1.33 278.91 ± 93.03 0.58 ± 0.91 0.04 ± 0.06 Mean ± SD Permissible limits Spain, 19851 20 1 3 4 0.5 Mexico, 19932 0.5 1 2–4 1 3 FDA, 1993 4 13 80 1.7 1 EEC, 19954 2 3 1 -1 1 2 3 All values in mg Kg ; Standard quality guidelines for bivalve mollusks (FAO, 1989); Secretaria de Salud, 1993 (NOM-031-SSA1-1993); U.S Food and Drug Administration, 1993; 4European Economic Community (Codex Alimentarius, 1995)

Table 5

Correlation matrix for biometric measurements and metal concentrations in C. gigas from La Pitahaya channel, SW Gulf of California, Mexico.

Length Width Weight Cu Cd Cr Ni Pb Zn As Hg p < 0.05

Length 1.00 0.99 0.98 0.40 -0.65 -0.40 -0.40 -0.78 0.71

Width 1.00 0.98 0.41 -0.64 -0.48 -0.49 -0.76 0.48 0.78

Weight 1.00 0.53 -0.52 -0.50 -0.47 -0.67 0.72

Cu

1.00 0.44 -0.64 -0.65 0.46 0.51

Cd

1.00 0.98 -0.53 -

Cr

1.00 0.96 -0.86

Ni

1.00 -0.57 -0.91

Pb

1.00 -

Zn

1.00 -0.51 -

As

1.00 0.74

Hg

1.00