Journal of Environmental Science and Health, Part B Pesticides, Food Contaminants, and Agricultural Wastes
ISSN: 0360-1234 (Print) 1532-4109 (Online) Journal homepage: http://www.tandfonline.com/loi/lesb20
Persistent organic pollutants (POPs) in populations of the clam Chione californiensis in coastal lagoons of the Gulf of California Héctor H. Vargas-González, Lía C. Méndez-Rodríguez, Jaqueline GarcíaHernández, Renato A. Mendoza-Salgado, Tania Zenteno-Savín & José A. Arreola-Lizárraga To cite this article: Héctor H. Vargas-González, Lía C. Méndez-Rodríguez, Jaqueline GarcíaHernández, Renato A. Mendoza-Salgado, Tania Zenteno-Savín & José A. Arreola-Lizárraga (2016): Persistent organic pollutants (POPs) in populations of the clam Chione californiensis in coastal lagoons of the Gulf of California, Journal of Environmental Science and Health, Part B To link to this article: http://dx.doi.org/10.1080/03601234.2016.1159455
Published online: 06 Apr 2016.
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Date: 07 April 2016, At: 11:12
JOURNAL OF ENVIRONMENTAL SCIENCE AND HEALTH, PART B 2016, VOL. 0, NO. 0, 1–11 http://dx.doi.org/10.1080/03601234.2016.1159455
Persistent organic pollutants (POPs) in populations of the clam Chione californiensis in coastal lagoons of the Gulf of California ctor H. Vargas-Gonzaleza, Lıa C. Mendez-Rodrıguezb, Jaqueline Garcıa-Hernandezc, Renato A. Mendoza-Salgadob, He Tania Zenteno-Savınb, and Jose A. Arreola-Lizarragaa
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a Northwestern Center for Biological Research (CIBNOR), Guaymas, SON, Mexico; bNorthwestern Center for Biological Research (CIBNOR), La Paz, BCS, Mexico; cCenter for Food and Development Research (CIAD), Guaymas, SON, Mexico
This study examines the potential public health risk due to the massive use of organochlorine pesticides (OCs) in agriculture in the Gulf of California. Specimens of the clam Chione californiensis were collected from three coastal lagoons (Yavaros, Altata and Reforma). Sites were classiﬁed as polluted/nonpolluted based on the presence/absence of OCs as an indicator of the persistence of these pollutants; in polluted sites, the time elapsed since pesticide application (past or recent) was estimated. Screening values (SV) for protecting human health as per the U.S. Environmental Protection Agency (EPA) were used for risk assessment. OCs detected were ranked according to frequency of occurrence as follows: g-chlordane (75%) > endrin (54%) > aldrin (48%) > heptachlor, and dichlorodiphenyl-trichloroethane (DDE) (37%) > b-heptachlor epoxide (30%) > lindane (a-BHC, d-BHC) and endosulphan I ( 6%). Speciﬁcally, OCs detected at the highest concentration were heptachlor in Yavaros (0.0168 mgg¡1) and Altata (0.0046 mgg¡1), and aldrin in Reforma (0.0019 mgg¡1). b-Heptachlor epoxide in Altata and Reforma was the only OC with a concentration exceeding the EPA Screening Value. From our results and based on the monthly consumption limit set forth by EPA, the maximum safe consumption of clams to avoid a carcinogenic risk derived from b-heptachlor epoxide in the ﬁshing villages of Yavaros and Altata is 4 servings per month (1 serving D 0.227 kg) by a 70-kg person. These ﬁndings suggest that concentrations of OCs and their isomers in C. californiensis populations reﬂect environmental persistence as well as recent inputs of OCs into coastal lagoons in the Gulf of California.
Received 21 July 2015
Introduction One of the major environmental problems in coastal areas around the world is pollution from nonbiodegradable or xenobiotic synthetic substances. Organochlorine (OC) pesticides are xenobiotics characterized by a high persistence in aquatic environments and a remarkable ampliﬁcation in food chains due to their solubility in adipose tissue, resulting from their chemical structure with a high proportion of Ar-Cl bonds that leads to a high hydrophobicity and low biodegradability.[4– 6] Most of these compounds are Persistent Organic Pollutants (POPs). Upon entering into the environment, pesticide residues are widely distributed because they can be transported beyond the point of discharge by wind and runoff. Coastal water bodies receive direct discharges from rivers, urban wastewater and agricultural drains, derived from the increase in human settlements and agroindustrial activities in coastal areas. Particularly, OC residues have been detected even more than a decade after its use was prohibited; for this reason, the presence of OCs in the environment derives not only from current pesticide use, but also from residues due to past use. Coastal lagoons and estuaries serve as OC sinks, where these substances persist because of a very slow degradation rate CONTACT Jose A. Arreola-Lizarraga Mexico. © 2016 Taylor & Francis Group, LLC
Persistent organic pollutants; organochlorine pesticides; coastal lagoons; clam pollution; Gulf of California
under the local conditions, and may remain there for a long time.[10, 11] OC half-lives range from 1 year (e.g., g-BCH lindane) up to 10 years (e.g., toxaphene). OCs are characterized by their potential to concentrate in sediments, even at low concentrations (< 1 mg¢L¡1) in the water column, and bioaccumulation in adipose tissues of ﬁsh and mollusks. Humans are usually at the top of the food chain, and accumulate the highest concentrations of these hydrophobic compounds present in aquatic and terrestrial systems. The potential risk to human health has been broadly documented (e.g., carcinogenic and mutagenic effects, reproductive disorders, hormone disrupters).[14, 15] OCs have been regarded as POPs since 2001 in the framework of the Stockholm Convention (SC). A group of 12 POPs has been named “dirty dozen,” nine of which are OCs: aldrin, chlordane, heptachlor, dieldrin, dichlorodiphenyl-trichloroethane (DDT), endrin, mirex, toxaphene, and hexachlorobenzene. Endosulphan was included in 2007, and lindane, in 2009. Historically, pesticides in Mexico have been used mainly in the northwestern states (Sonora and Sinaloa) where export agriculture prevails. The agricultural area cultivated in the past 20 years in this country amounts to
Centro de Investigaciones Biologicas del Noroeste, S. C. (CIBNOR, S.C.), 85454, Guaymas, SON,
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H. H. VARGAS-GONZALEZ ET AL.
20 million hectares, with 43% of this land being located in Sonora and Sinaloa. The main crops include maize, wheat, and sorghum, which altogether contribute 60% to national production. Agriculture releases agrochemicals to coastal lagoons, and the most frequent OC residues correspond to BHC, heptachlor, aldrin, endosulphan, and metoxichlor.[22–26] In some cases, pesticides prohibited by Stockholm Convention regulations (DDT, chlordane, aldrin, and endosulphan) have been found, and biochemical and physiological alterations have been reported in crustaceans, mollusks, ﬁsh, and turtles exposed to OCs.[25,27,28] POPs may be present in the biota living in eutrophic water bodies, causing losses in the ecological functions and ecosystem services supplied by coastal lagoons, which in turn lead to negative impacts on consumer health. Although the vast majority of OCs are no longer used or have been prohibited in many countries, they may still be detected in polluted sites due to their high persistence. Residual OC levels in a coastal water body depend on a number of factors, including the type and intensity of agriculture, as well as the pattern and intensity of rainfall in the region. The objective of this investigation was to identify the presence and quantity of OC pesticides in populations of the clam Chione californiensis in three coastal lagoons located in the Gulf of California. Our approach was to detect OCs and their bioavailable isomers as indicators of polluted sites, and determine whether pesticide application has occurred recently or in the past. We then tested for the presence of OCs in clam populations as an indicator of the persistence of these pollutants, to decide whether a preventive consumption alert is needed.
Materials and methods Study area The Yavaros, Altata and Reforma lagoons are located in the Gulf of California eastern coast. Their main morphometric and hydrological characteristics are shown in Table 1. Yavaros lagoon is located in a semi-arid region with a mean annual precipitation of 224 mm. It is inﬂuenced by human activities around the Mayo river basin, where irrigated agriculture accounts for 77%; rainfed agriculture, 16%; urban areas, 6%; and shrimp farming, 1%. Altata lagoon is located in a subhumid region with a mean annual precipitation of 653 mm. Irrigated agriculture represents 62%; rainfed agriculture, 27%; urban areas, 9%; and shrimp farming, 2%. Reforma lagoon is located in a sub-humid region with a mean annual precipitation of 653 mm. It is inﬂuenced by the Sinaloa and Mocorito Table 1. Morphometric and hydrological characteristics of the coastal lagoons studied. Characteristics
Surface Volume Mean depth Tidal amplitude Type of tide
72 km2 220 Mm3 2m 1.03 m Mixed semidiurnal
283 km2 848 Mm3 3m 1.14 m Mixed semidiurnal
578 km2 1732 Mm3 3m 1.10 m Mixed semidiurnal
river basins, where irrigated agriculture accounts for 63%; rainfed agriculture, 28%; urban areas, 6%; and shrimp farming, 3%. The primary economic activity in the study area is agriculture, and agricultural wastewater is the main source of pollution entering these lagoon systems. The lagoons of interest are located in Mexico’s two most important agricultural regions: area II, where the so-called Green Revolution started, in the Mayo Valley (southern Sonora), with the Yavaros lagoon located adjacent to Irrigation District #038 (ID-038); area III, currently known as Mexico’s agricultural heartland, in the Culiacan Guasave and Mocorito Valleys in northern Sinaloa (ID-010, ID-063 and ID-074), where Altata and Reforma lagoons are located (Fig. A1). In the Mayo valley and northern Sinaloa, cotton and tobacco were the main agricultural products grown in the late 1930s and early 1940s. From 1950 to 1978, DDT was used intensively in cotton crops, which quickly led to a marked resistance of cotton pests. As a result, in a few years, starting in the 1980s, this culture proved unaffordable; since 2007, cotton cultivation was discontinued in northern Sinaloa, and cultivated areas were reduced in southern Sonora. Crops that use the largest amount of OCs and that could be affecting the lagoons studied are shown in Table 2. Agricultural areas where Yavaros, Altata and Reforma are located (II and III, Fig. A1) accounted for 43% of the total cultivated area in Mexico; ID-010, ID-038, ID063 and ID-074 contributed »481,400 ha to the total harvested area in crop year 2008–2009, being within the top eight major irrigation districts. Table 2 shows the cultivated area for the main crops, which use the highest volume of pesticides. Both agricultural regions consume large quantities of pesticides of all sorts; crops that use the highest volume of pesticides include maize, cotton, potato, chili, tomato, beans, wheat, avocado, coffee and tobacco, in quantities ranging from 395 up to 13,163 tons of pesticides (as commercial formulations) per year. Sampling and sample processing OC concentrations were measured in the clam Chione californiensis, which is ﬁshed locally for self-consumption. Sampling was carried out in seven sites in each lagoon during the main irrigation season of the autumn-winter cycle. Clams were collected, and seven composite samples were taken, including three clams each, of each length class from each coastal lagoon. The size of collected clams ranged between 30 mm and 78 mm, with a mean of 43 mm and a standard deviation of 9.5 mm Eighty eight percent of samples were distributed in ﬁve length classes (29–33.9; 34– 38.9; 39–43.9; 44–48.9 y 49–53.9 mm). Clams were preserved and stored frozen until analysis. Seventeen highly persistent organochlorine pesticides (OCs) related to a number of adverse effects on the aquatic biota[35, 36] were assayed in adipose tissue of collected clams; these included DDT (and its derivatives), hexachlorocyclohexane (BHC and its isomers), chlordane compounds (CHLs), cyclodienes (aldrin, endrin, dieldrin, endosulphan I and endosulphan II), and methoxychlor. Three grams of adipose tissue were
JOURNAL OF ENVIRONMENTAL SCIENCE AND HEALTH, PART B
Table 2. Cultivated area for the main crops using the highest volume of pesticides in ID-038, ID-063, ID-074, and ID-010 adjacent to the lagoons studied (annual and perennial, crop year 2007–2009. Modality: rainfed C irrigation). Yavaros (ID-038) Crop
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Maize Cotton Wheat Chile Tomato Bean Potato Safﬂower Tomatillo Vegetables Total Grand Total % Crops OC % Main Crops
Cultivated surface Cultivated surface area 2007/08 (Ha) area 2008/09 (Ha) 4704 49 65426 86 333 1135 6965 4084 493 2673 85948 88328
5317 0 72432 225 400 2819 6395 2359 703 2578 93228 94512 90.9% 98.0%
Reforma (ID-063 – ID-074)
Altata (ID-010) Crop Maize Cotton Wheat Chile Tomato Bean Sugar cane Sorghum Chickpea Vegetables Total Grand Total % Crops OC % Main Crops
Cultivated surface Cultivated surface area 2007–08 (Ha) area 2008/09 (Ha) 152177 0 1115 2959 5050 11939 5174 11084 5963 8276 203737 207405
extracted using HPLC-grade solvents such as pentane, hexane and dichloromethane; subsequently, extracts were puriﬁed in a column packed with sodium sulfate, using FlorisilTM (Fisher Scientiﬁc International, Hampton NH, USA), hexane and dichloromethane as carriers according to an adaptation of the technique described by Gardner et al. The puriﬁed extract was evaporated and reconstituted with 2,2,4-trimethylpentane (isooctane) as eluent (Piscataway, NJ, USA). One microliter of the extract was injected to a gas chromatograph (Network GC System, 6890 N) coupled to an electron-capture detector (DCE Niquel63, model G23977-65505, Agilent Technologies, Inc., Palo Alto, CA, USA) with an automatic injection system and a capillary column (30 m £ 0.25 mm £ 0.25 mm; 5% phenylmethyl silicone) (HP-5MS Agilent Wilmington, DE, USA). Concentrations of individual OCs were calculated from the peak area of each analyte in the sample relative to the respective standard curve. The relative recovery of the surrogate standard (1,2,3,4-TCDD) was used for correcting the results of sample extract concentration for in-process losses according to the internal standard 1,7,8 -TriCDD (dioxins acquired from AccuStandar, New Haven, CT, USA). Total OC concentration was obtained as the sum of DDTs, CHLs, BHCs and cyclodienes, as follows: the sum of DDT compounds (and derivatives) was calculated as the sum of the concentrations of DDT, dichlorodiphenyldichloroethylene (DDE) and dichlorodiphenyldichloroethane (DDD). Hexachlorocyclohexane and its isomers (BHCs) were calculated as the sum of the concentrations of a-BHC, ß-BHC, g-BHC and d-BHC. Chlordane compounds (CHLs) were calculated as the sum of the concentrations of g-chlordane, heptachlor and heptachlor epoxide, when these were detected. With regard to the molecular structure, these were grouped into cyclodienes (aldrin, dieldrin, endrin, endrin sulphate, endosulphan I and endosulphan II) and were also determined. The detection limits with the electron-capture detector ranged from 0.000005 mgg¡1 (a-BHC, g-BHC, aldrin, endrin, endrin sulphate, endosulphan II, dieldrin, g-chlordane, heptachlor epoxide, DDE and DDT and DDD) to 0.00001 mgg¡1 (ß-BHC, d-BHC, heptachlor, endosulphan I, methoxychlor) according to the pesticide. The results were
153095 0 3526 2321 5411 15172 4092 13934 8210 7903 213664 217391 85.3% 98.3%
Crop Maize Cotton Wheat Chile Tomato Bean Potato Sorghum Chickpea Vegetables Total Grand Total % Crops OC % Main Crops
Cultivated surface Cultivated surface area 2007–08 (Ha) area 2008/09 (Ha) 113733 0 4894 288 1762 14148 1310 7146 14639 2656 160576 162093
100196 0 15416 202 1900 16777 1232 14536 15781 1128 167168 169611 82.0% 98.8%
expressed in mg¢g¡1 wet weight of adipose tissue for comparison with FDA and EPA standards. A ﬁve-point calibration curve (0.005 to 1.0 mg¢mL¡1, r2 0.99) was generated to quantify each pesticide of interest (CLP Organochlorine Pesticide mix, Supelco 47426-u, Bellefonte, PA, USA). In order to measure accuracy, analytical blanks were injected to each set of 10 samples to determine the method’s background interference; likewise, samples were spiked to check the effectiveness, recovery of the extraction, as well as cleaning with FlorisilTM . The average recovery of the extraction was 78%. The limits of quantiﬁcation (LoQ) for OCs ranged between 5 and 10 ng¢g¡1 of lipids. Comparison of results vs. regulations Results were contrasted with action levels set by the U.S. Food and Drug Administration (FDA) and with tolerances recommended by the U.S. Environmental Protection Agency (EPA), responsible for the regulation of pesticides used in agriculture. These limits of residual pesticides in food, namely agricultural products, ﬁsh and shellﬁsh exposed to pollutants, are called “tolerances” in the United States. EPA has deﬁned the Screening Value (SV) as the concentration of a chemical pollutant in ﬁsh tissue that is of potential concern for public health; it is used as a threshold for comparison against the concentrations found in similar matrices. SV is calculated considering both carcinogenic and non-carcinogenic effects of the chemical pollutant. In order to issue recommendations regarding the maximum safe consumption of clams in kilogram per month, SV ﬁgures were used for a population of subsistence ﬁshers (selfconsumption). This is because FDA action levels are 1 to 2 orders of magnitude lower than potential monthly consumption limits based on health risks (chronic systemic and carcinogenic effects) issued by EPA SV.[35, 38] Also, ﬁgures were compared with Mexican regulatory standards applicable for ﬁsh and shellﬁsh consumption, which set forth that these products shall not contain residues of pesticides such as aldrin, dieldrin, endrin, heptachlor, kapone or
H. H. VARGAS-GONZALEZ ET AL.
others prohibited in the Ofﬁcial Catalog of Pesticides. Statistical analysis OC concentrations between lagoons were compared using an Analysis of Variance; results were displayed using box and whisker graphs. In addition, a frequency analysis of pesticides in the lagoons of study was performed. The statistical package Statgraphics plus 4.1 was used.
Results and discussion
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Organochlorine pesticides Table 3 shows the total, median, upper and lower OC concentration levels detected in Chione californiensis, in a wetweight basis (mg¢g¡1), during the high farming (January, 2009) for each lagoon system. Of the 17 OCs analyzed, 53% were detected in at least one sample from one study site (Fig. 1); these were detected with a higher frequency (47%) in Yavaros, followed by Altata (29%) and Reforma (24%). The rest of OCs, including endosulphan II, b-BHC, g-BHC, dieldrin, DDD, DDT, endrin sulphate and methoxychlor, were below the detection limit of the chromatography technique used. The most frequent pesticide was g-chlordane, found in clams from the three lagoons, with an average frequency of 75%, followed by endrin, with an average frequency of 54%. Aldrin was detected in clams from all sites sampled in Yavaros. Signiﬁcant differences in OC levels were observed both between lagoons and between pesticides (Fig. 2). The highest concentrations were recorded in Yavaros (»0.0200 mg.g¡1),
whereas Altata and Reforma showed lower median concentrations (»0.00200 mg.g¡1). In Yavaros, heptachlor was the OC with the highest concentration (0.0168 mg.g¡1); in Altata, it was also heptachlor (0.00460 mg.g¡1); in Reforma, aldrin (0.00181 mg.g¡1). Heptachlor and its isomer b-heptachlor epoxide were detected in Yavaros and Altata. In Yavaros, except for heptachlor and aldrin, median OC concentrations were also below 0.00200 mg.g¡1. Extreme OC concentrations were measured in one site of each lagoon (e.g. a-BHC, g-BHC in Yavaros; heptachlor, endosulphan I, in Altata). In Reforma, both median and average g-chlordane concentrations were similar between sampling sites, indicating a broad distribution of this OC across the lagoon. Comparison of results versus regulations Table 4 shows the comparison of action levels of the Food and Drug Administration (FDA) and recommended tolerances issued by the Environmental Protection Agency (EPA) and Mexican standards. EPA recommends values typically 2 to 120 times lower than those issued by FDA; therefore, the former are more conservative than the corresponding FDA action or tolerance level. The concentrations recorded for the 17 OCs tested are lower than the values established by FDA; b-heptachlor epoxide in Altata and Reforma is the only OC with a concentration exceeding the EPA (SV) assessment level. Based on the monthly consumption limit established by EPA, the maximum safe consumption of clams to avoid a carcinogenic risk derived from b-heptachlor epoxide in the ﬁshing villages of Yavaros and Altata is 4 servings per month (1 serving D 0.227 kg) by a 70-kg person.
Table 3. Concentration of OCs, in mg.g¡1(wet weight), in populations of the clam Chione californiensis in Yavaros, Altata, and Reforma lagoons. Yavaros Pesticide OC a-BHC b-BHC g-BHC b d-BHC Heptachlor Aldrin b-Heptachlora epoxide g-chlordane Endosulphan I Dieldrin DDE Endrin Endosulphan II DDD DDT Endrin sulphate Methoxychlor