Abstract
In order to ascertain if Cu, Fe, and Zn are differentially accumulated in fish tissues, metal concentrations were measured in the muscle and liver of bycatch fish from the states of Sinaloa (189 specimens, 7 species) and Guerrero (152 individuals, 8 species) in the Mexican Pacific Coast during March and November 2011. Additionally, metal levels were compared with the maximum allowable limits set by international legislation and contrasted with similar ichthyofauna from other regions. Liver had more elevated concentrations of Cu (Sinaloa 28.3, Guerrero 16.3 μg g−1), Fe (Sinaloa 1098, Guerrero 636 μg g−1), and Zn (Sinaloa 226, Guerrero 186 μg g−1) than the muscle in fish from both studied areas. The relative abundances of analyzed metals in both tissues was Fe > Zn > Cu. As far as limits set by international legislation (Australia, India, New Zealand, Zambia), measured concentrations of Cu in the edible portion of fish were not found to be above the set values. In the case of Zn, the maximum allowable limits set by international legislation were exceeded by the Peruvian mojarra Diapterus peruvianus from Guerrero state (Mexican Pacific). No limits exist for Fe in the edible portion of fishery products in the national and international legislations.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
Introduction
A broad classification of metals divides them as essential, beneficial, or detrimental. Trace elements recognized as essential for biota, including human health, include iron, zinc, copper, chromium, iodine, cobalt, molybdenum, and selenium [1] as they are involved in important biological processes [2]. These elements play a functional and structural role in the human body [3]. Fish is a major source of iron in adults and children and a deficiency of it causes anemia. Fish is significant to the human diet due to its high protein content, low saturated fats, and abundant omega fatty acids known to support good health. On the other hand, trace metals can pose a risk to fish and humans, especially elements of elevated toxicity and facility to be biomagnified [4]. In this context, various studies on contamination of different fish species by trace metals have been conducted worldwide; in the specific case of bycatch fish, few studies have been carried out in Mexican waters [5, 6]. In the Mexican Pacific coast, shrimp fishery is an important source of bycatch resources, which include fish, crustaceans, and mollusks [7]. In terms of abundance, fish makes up the most sizeable group as it has been estimated that for every kilogram of shrimp, 10 kg of fish are caught [8, 9]. Fish muscle tissue is the most frequently used for analysis because it is a major target tissue for metal storage and it constitutes the main edible part of the fish [10].
Trace metals in the aquatic environment can affect aquatic biota and fish consumers, such as humans and other wildlife. These metals may enter the coastal ecosystem from different natural and anthropogenic sources, including industrial, aquaculture, agriculture, and domestic sewage, besides atmospheric precipitation [11–13]. The utilization of phosphorus-containing products such as fertilizers and detergents has also contributed to an increase of trace metals in water bodies. In aquatic ecosystems, trace metals have received considerable attention due to their toxicity and accumulation in fishes. The state of Sinaloa has a littoral of 656 km and an area of coastal lagoons of 221,600 ha [14]. Such coastal waters are of great ecological and economic relevance; the climate is sub-tropical-humid (AW type), with rainfall in summer and less than 10 °C of annual thermal oscillation [15]. In Mexico, the coast of Sinaloa is home to the highest concentration of aquatic farms, especially for shrimp production [16]; nevertheless, the intensive agriculture practiced in the surroundings of the state releases great quantities of agrochemicals [17], including fertilizers and fungicides containing metals. The coast of Guerrero has approximately 600 km of coastline, an amount that places it as the eighth longest state in the country, plus an area of 70,000 ha of inland waters and lagoons. In most of the state territory (82 %) the climate is warm and humid; the rest of the surface has dry, semi-dry, and temperate humid climate: the average annual temperature is 25 °C, the average minimum temperature is 18 °C, and maximum 32 °C; most of the rainfall occurs in summer, June through September; the average rainfall in the state is 1200 mm annually [18]. The aims of this study were as follows: (a) to determine Cu, Fe, and Zn distribution in the muscle and liver of bycath fish from selected sites of the Mexican Pacific coast; (b) to compare levels of Cu, Fe, and Zn with maximum permissible limits in fishery products set in the international legislation; and (c) to contrast metal levels in analyzed ichthyofauna with similar species worldwide.
Materials and Methods
Fish samplings were conducted in the Mexican Pacific; in the state of Sinaloa, 189 specimens of 7 species were collected; in Guerrero, the number of individuals was 152 and they belong to 8 species. According to a national survey on environmental impacts in Mexican coastal cities, in Sinaloa coasts, the factors that mostly affect the aquatic environment are tourism and recreational activities and habitat destruction; such activities may contribute to the occurrence of trace metals. In Guerrero state, the main environmental impacts are represented by wastewater discharges, tourism, and recreation and habitat destruction [19].
Bycatch fish were collected during shrimp trawling operations in the continental shelf of the states of Sinaloa (Fig. 1a) and Guerrero (Fig. 1b) according to their fishing plans. Fish from Sinaloa were obtained during March 2011 and fish samples from Guerrero were collected in November 2011, at a depth range of 30–46 m. In the laboratory, fish were identified and total length and weight recorded. Muscle tissue from the median dorsal portion and the liver were used for analysis. Samples were frozen at −20 °C and lyophilized for 72 h (−52 °C and 60 × 10−3 mbar) in a Labconco Freeze-dry-System-FreeZone 6; then, they were ground in an agate mortar with pestle (Fisher-Scientific). Powdered samples (0.25 g) were acid digested in duplicates (5 mL of concentrated nitric acid-trace metal grade, Baker) using capped Teflon vials (Savillex™) on a hot plate (Barnstead Thermolyne) during 3 h (120 °C). Digested samples were stored in polyethylene containers for further analysis. For metal analysis, an atomic absorption spectrophotometer (Varian SpectrAA220) was used. For Zn and Fe, flame atomic absorption spectrophotometry was used (FAAS); the working conditions were as follows: wavelengths (nm) 248.3 (Fe) and 213.9 (Zn) and lamp current was 10 mA for both elements. In the case of Cu, measurements were made by graphite furnace atomic absorption spectrophotometry (GF-AAS); the working conditions were wavelength 324.7 nm and temperature for sample atomization was 2100 °C. The accuracy and precision of metal measurements were ensured using blanks and certified reference material for trace metals (liver DOLT-4, NRC-Canada). Elemental recoveries were estimated as the ratio of measured concentrations with respect to the corresponding value in the certificate of the reference material. Measured concentrations (n = 8) of Fe (1650 μg g−1), Cu (33.7 μg g−1), and Zn (127.5 μg g−1) in the reference material were comparable to certified levels (Fe 1833 μg g−1, Cu 31.2 μg g−1, and Zn 116 μg g−1). Recovery percentages were appropriate (Fe 90 %, Cu 108 %, Zn 110 %). The limits of detection of Cu, Fe, and Zn were 0.01, 0.19, and 0.48 μg g−1, respectively. Metal concentrations are reported in microgram per gram on a dry weight basis; for comparisons with legal limits of metals in fishery products (reported as μg g−1 on a wet weight basis) conversions of concentrations from dry weight to wet weight were made considering an average humidity of 72 % in the muscle tissue of analyzed fish. Comparisons of elemental concentrations in a given tissue were made by a one-way analysis of variance (ANOVA-Kruskal-Wallis test); in the case of significant differences, a Dunn’s test was used. A p < 0.05 level was considered of statistical significance. All statistical analyses were performed using GraphPad Prism 4.0.
Result and Discussion
The main contributors of metals in fish are food and surrounding water, with diet being the dominant source [20]. When elements are ingested, they are distributed all over the fish body and bound to diverse sites in tissues and organs, which implies that metals are distributed differentially. For the three analyzed elements, liver showed more elevated concentrations than muscle. The highest metal concentrations were measured in the liver of fish from both areas. As far as relative abundances of analyzed elements, the sequence of average concentrations in muscle and liver of fish from both areas was Fe > Zn > Cu. Metal concentrations in the muscle and liver of fish species from Sinaloa are presented in Table 1; the highest mean Cu concentration was found in the liver of Micropogonias ectenes (64.0 μg g−1) and the lowest concentration was present in the muscle of Larimus argenteus (0.92 μg g−1). In the case of Fe, the highest value was measured in the liver of L. argenteus (1886 μg g−1) while the lowest was found in the muscle of Trachinotus kennedyi (43.5 μg g−1). For Zn the highest level was detected in the liver of T. kennedyi (495.2 μg g−1); the smallest concentration was found in the muscle of M. ectenes (20.3 μg g−1). In fish from Guerrero state, the highest average Cu concentration was found in the liver of Haemulopsis axillaris (31.3 μg g−1); the lowest value (0.82 μg g−1) was in A. dendritica muscle (Table 2). In the case of Fe, the highest value was detected in the liver of Diapterus peruvianus (945 μg g−1) while the lowest was found in the muscle of Ancylopsetta dendritica (26.8 μg g−1). For Zn, the highest level was measured in T. kennedyi liver (299 μg g−1); the lowest concentration was found in the muscle of Hemicaranx leucurus (24.0 μg g−1). At low levels, metals like Cu, Fe, and Zn are essential for enzymatic activity and diverse biological processes in fish [21]; although essential elements are required for fish metabolism, they may become toxic at elevated levels. Some of the toxic effects of essential metals on fish include the alteration of physiological activities and biochemical parameters in blood [22]. Metals such as Cu, Fe, and Zn are essential since they play important structural and functional roles in biological systems [23]. In this context, Fe is mostly found in hemoglobin and hemosiderin in fish liver [24]. On the other hand, it has been found that Zn can accumulate less in fish muscle, whereas fish liver is able to store Cu in higher amounts compared to muscle and gills [25] because this organ works as a Cu deposit [26]. Mexican legislation does not set maximum permissible levels of Cu, Fe, and Zn in fishery products, so legal limits of Cu and Zn from other countries were used as guideline values (Table 3). Limits for Fe in the international legislations do not exist. For comparative reasons, only the species with the highest values of Cu and Zn in muscle tissue were included; it can be seen that legal limits of Cu were not exceeded. With regard to Zn, D. peruvianus from Guerrero exceeded all the maximum permissible limits in legislation from all the areas studied [27]. Taking into account that the Peruvian mojarra D. peruvianus is widely consumed in Mexico and that the level of Zn in this species from both sampling areas exceeded the legal limits, it is necessary to monitor Zn availability through D. peruvianus. In order to contrast our results with studies from other areas, levels of Cu, Fe, and Zn were compared among similar fish species of the families Mullidae and Carangidae (Table 4). In Mullidae, only a study with Mullus surmuletus from Spain was published [28]; levels of Cu and Zn were an order of magnitude higher in our study. As far as Carangidae, the reported studies matched three species of Trachurus. Levels of Cu, Fe and Zn in T. kennedyi from Sinaloa and Guerrero (this study) were comparable to concentrations reported in fish from Spain [28, 29]. In contrast, Cu and Zn concentrations in our study were higher than reported values in Trachurus trachurus from Nigeria. It is worth mentioning that samples from the Edo State in Nigeria [30] were purchased in local markets as smoked fish, which implies that samples might have been caught in different areas. Moreover, the thermal process may alter the elemental composition as compared to raw tissue so conclusions should be made with caution.
Concluding Remarks
In general, bioaccumulation of Cu, Fe, and Zn in fish from both areas followed the order liver > muscle. The average concentrations of the analyzed elements in both tissues was Fe > Zn > Cu. With respect to the maximum permissible limits in fishery products for human consumption, Cu concentrations in the edible portion of fish were not exceeded; Zn levels were above those allowed by international legislation [27] in the muscle of the Peruvian mojarra D. peruvianus from Guerrero. Concentrations of Fe in studied fish were not compared because no legal limits exist in the national and international legislations. The studied fish belong to families Mullidae and Carangidae; in the case of Mullidae, our fish had Cu and Zn levels higher than M. surmuletus from Spain [28]. Regarding Carangidae, our fish had higher levels of Cu and Zn than similar fish from Nigeria [30] but comparable to levels reported in fish from Spain.
References
WHO/FAO/IAEA (1996) Trace elements in human nutrition and health. World Health Organization, Geneva
Perelló G, Martí-Cid R, Llobet JM, Domingo JL (2008) Effects of various cooking processes on the concentrations of arsenic, cadmium, mercury, and lead in foods. J Agric Food Chem 56(23):11262–11269
Mendil D, Demirci Z, Tuzen M, Soylak M (2010) Seasonal investigation of trace element contents in commercially valuable fish species from the Black Sea, Turkey. Food Chem Toxicol 48(3):865–870
Ordiano-Flores A, Rosiles-Martínez R, Galván-Magaña F (2012) Biomagnification of mercury and its antagonistic interaction with selenium in yellowfin tuna Thunnus albacares in the trophic web of Baja California Sur, Mexico. Ecotoxicol Saf 86:182–187
Ruelas-Inzunza J, Sánchez-Osuna K, Amezcua-Martínez F, Spanopoulos-Zarco P, Manzano-Luna L (2012) Mercury levels in selected bycatch fish species from industrial shrimp-trawl fishery in the SE Gulf of California. Mar Pollut Bull 64:2857–2859
Spanopoulos-Zarco P, Ruelas-Inzunza J, Jara-Marini ME, Meza-Montenegro M (2015) Bioaccumulation of arsenic and selenium in bycatch fishes Diapterus peruvianus, Pseudupeneus grandisquamis and Trachinotus kennedyi from shrimp trawling in the continental shelf of Guerrero, México. Environ Monit Assess 187:700
Madrid-Vera J, Amezcua F, Morales-Bojórquez E (2007) An assessment approach to estimate biomass of fish communities from bycatch data in a tropical shrimp-trawl fishery. Fish Res 83:81–89
Alverson DL, Freeberg MH, Pope JG, Murawski SA (1994) A global assessment of fisheries bycatch and discards. FAO Fish Tech Pap 339:1–233
Rábago-Quiroz CH, López-Martínez J, Herrera-Valdivia E, Nevarez-Martínez MO, Rodríguez-Romero J (2008) Population dynamics and spatial distribution of flatfish species in shrimp trawl bycatch in the Gulf of California. Hydrobiol 18(3):177–188
Kumar B, Mukherjee DP, Kumar S, Mishra M, Prakash D, Singh SK, Sharma CS (2011) Bioaccumulation of heavy metals in muscle tissue of fishes from selected aquaculture ponds in East Kolkata wetlands. Annals Biol Res 2(5):125–134
Förstner U, Wittmann GTW (1983) Metal pollution in the aquatic environment. Springer-Verlag, Berlin
Callender E (2005) Heavy metals in the environment-historical trends. In: Holland HD, Turekian KK (eds) Treatise on geochemistry. Elsevier, Amsterdam, pp. 67–106
Páez-Osuna F, Osuna-Martínez C (2015) Bioavailability of cadmium, copper, mercury, lead and zinc in subtropical coastal lagoons from the southeast Gulf of California using mangrove oysters (Crassostrea corteziensis and Crassostrea palmula). Arch Environ Contam Toxicol 68:305–316
Páez Osuna F, Ramírez-Reséndiz G, Ruiz-Fernández AC, Soto-Jiménez MF (2007) La contaminación por nitrógeno y fósforo en Sinaloa: flujos, fuentes, efectos y opciones de manejo. In: Páez-Osuna F (ed) Serie Lagunas Costeras de Sinaloa. El Colegio de Sinaloa, UNAM, SEMARNAT, CONACYT, Mexico pp. 71–81
García E (1973) Modificaciones al sistema de clasificación climática de Köppen para adaptarla a las condiciones de la República Mexicana. Instituto de Geografía UNAM, México
Hernández-Covarrubias V, Chávez-Herrera D, Melchor-Aragón J, Villegas-Hernández F, Muñoz-Rubí H, Osuna-Zamora M (2012) Fauna de acompañamiento de camarón en la ribera adyacente a la boca sur de Santa María la Reforma Sinaloa. Instituto Nacional de la Pesca, Mexico
Carvalho FP, Fowler SW, Gónzalez-Farías F, Mee LD, Readman JW (1996) Agrochemical residues in the Altata-Ensenada del Pabellón coastal lagoon (Sinaloa, México): a need for integrated coastal zone management. Int J Environ Health Res 6(3):209–220
www.inegi.org.mx
Ortiz-Solano L, Granados-Barba A, Solís-Weiss V, García-Salgado MA (2005) Environmental evaluation and development problems of the Mexican coastal zone. Ocean Coast Manag 48:161–176
Pentreath RJ (1977) The accumulation from water of 65Zn, 54Mn, 58Co and 59Fe by the mussel, Mytilus edulis. J Mar Biol Assoc UK 53:127–143
AL-Weher SM (2008) Levels of heavy metal Cd, Cu and Zn in three fish species collected from the northern Jordan Valley, Jordan. Jordan J Biol Sci 1(1):41–46
Nemesok JG, Huphes ZGM (1988) The effects of copper sulphate on some biochemical parameters of rainbow trout. Environ Pollut 49:77–85
Ozden O, Erkan N, Ulusoy S (2010) Determination of mineral composition in three commercial fish species (Solea solea, Mulus surmuletus, and Merlangius merlangus). Environ Monit Assess 170(1–4):353–363
MJ K (2001) Practical handbbok of marine science. CRC Press, Boca Raton
Abbas HH, Zaghloul KH, Mousa MA (2002) Effect of some heavy metal pollutants on some biochemical and histopathological changes in blue tilapia; Oreochromis aureus. Egyp J Agric Res 80:1395–1411
Salanki I, Katalin VB, Berta E (1982) Heavy metals in animals of Lake Balaton. Water Res 16(7):1147–1152
Nauen C (1983) Compilation of legal limits for hazardous substances in fish and fishery products. FAO Fish Circ 764:1–102
Olmedo P, Hernández AF, Pla A, Femia P, Navas-Acien A, Gil F (2013) Determination of essential elements (copper, manganese, selenium and zinc) in fish and shellfish samples. Risk and nutritional assessment and mercury selenium balance. Food Chem Toxicol 62:299–307
Rivas A, Peña-Rivas L, Ortega E, López-Martínez C, Olea-Serrano F, Lorenzo ML (2014) Mineral element contents in commercially valuable fish species in Spain. Sci World J 1–7
Daniel EO, Ugwueze AU, Igbegu HE (2013) Microbiological quality and some heavy metals analysis of smoked fish sold in Benin City, Edo State, Nigeria. World J Fish and Mar Sci 5(3):239–243
Acknowledgments
We acknowledge partial financial support by the Ministry of Public Education (Project REDES PROMEP/103.5/13/9335). We thank G. Ramírez-Reséndiz for map elaboration.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Spanopoulos-Zarco, P., Ruelas-Inzunza, J., Aramburo-Moran, I. et al. Differential Tissue Accumulation of Copper, Iron, and Zinc in Bycatch Fish from the Mexican Pacific. Biol Trace Elem Res 176, 201–206 (2017). https://doi.org/10.1007/s12011-016-0800-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12011-016-0800-6