Arsenic in the top predators sailfish (Istiophorus platypterus) and dolphinfish (Coryphaena hippurus) off the southeastern Gulf of California

Abstract

Distribution of arsenic (As) in tissues and gonads of the Indo-Pacific sailfish Istiophorus platypterus and the dolphinfish Coryphaena hippurus from the SE Gulf of California was evaluated. The bioaccumulation patterns of As were the same in the two species. In I. platypterus, As levels (mg kg−1, wet weight) were gonads (7.4 ± 1.1) > liver (3.1 ± 0.1) > kidney (2.7 ± 0.1) > muscle (1.6 ± 0.1); in C. hippurus, As (mg kg−1) levels were gonads (4.3 ± 0.6) > liver (3.2 ± 0.2) > kidney (2.3 ± 0.1) > muscle (1.2 ± 0.1). Differences in As distribution could be attributed to the biological functions of tissues. The hypothesis was confirmed that biomagnification was evidenced by the fact that As levels were lower in prey species than in predators. Intake of muscle from either fish did not represent a risk to humans if recommended portions a week are not exceeded, adults as much as 1802.4 g and 2454.1 g and children 257.5 and 350.6 g, for sailfish and dolphinfish, respectively. In addition, the likelihood of developing cancer due to consumption of edible tissues from either of these top predators was in the acceptable range (6.4 × 10−5 to 27.3 × 10−6 for a population that consumes 50 g of muscle in a week) but if a conservative combined slope factor is used the probabilities to develop bladder and lung cancer increments from 1.1 × 10−3 to 9.1 × 10−5.

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Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Adams, D. (2009). Consistently low mercury concentrations in dolphinfish, Coryphaena hippurus, an oceanic pelagic predator. Environmental Research, 109(6), 697–701. https://doi.org/10.1016/j.envres.2009.05.004.

    CAS  Article  Google Scholar 

  2. Ai, Y., Li, X., Gao, Y., Zhang, M., Zhang, Y., Xhang, X., et al. (2019). In vitro bioaccessibility of potentially toxic metals (PTMs) in Baoji urban soil (NW China) from different functional areas and its implication for health risk assessment. Environmental Geochemistry and Health, 41, 1055–1073.

    CAS  Article  Google Scholar 

  3. Alejo-Plata, C., Gómez-Márquez, J. L., & Salgado-Ugarte, I. H. (2011). Sex ratios, size at sexual maturity, and spawning seasonality of dolphinfish (Coryphaena hippurus) caputured in the Gulf of Tehuantepec Mexico. Fisheries Research, 110(1), 207–216.

    Article  Google Scholar 

  4. Allen, G. R., & Robertson, D. R. (1994). Fishes of the tropical eastern Pacific. Hawaii: University of Hawaii Press.

    Google Scholar 

  5. Avigliano, E., Maichak de Carvalho, B., Invernizzi, M., Jasan, R., & Volpedo, A. V. (2019). Arsenic, selenium, and metals in a commercial and vulnerable fish from southwestern Atlantic estuaries: Distribution in water and tissues and public health risk assessment. Environmental Science and Pollution Research, 26(8), 7994–8006. https://doi.org/10.1007/s11356-019-04258-3.

    CAS  Article  Google Scholar 

  6. Avigliano, E., Schlotthauer, J., Maichak de Carvalho, B., Sigrist, M., & Volpedo, A. V. (2020). Inter-and intra-stock bioaccumulation of anionic arsenic species in an endangered catfish from South American estuaries: Risk assessment through consumption. Journal of Food Composition and Analysis, 87, 103404. https://doi.org/10.1016/j.jfca.2019.103404.

    CAS  Article  Google Scholar 

  7. Bergés-Tiznado, M. E., Páez-Osuna, F., Notti, A., & Regoli, F. (2013). Biomonitoring of arsenic through mangrove oyster (Crassostrea corteziensis Hertlein, 1951) from coastal lagoons (SE Gulf of California): Occurrence of arsenobetaine and other arseno-compounds. Environmental Monitoring and Assessment, 185(9), 7459–7468.

    Article  CAS  Google Scholar 

  8. Bergés-Tiznado, M. E., Márquez-Farías, F., Torres-Rojas, Y., Galván-Magaña, F., & Páez-Osuna, F. (2015). Mercury and selenium in tissues and stomach contents of the migratory sailfish, Istiophorus platypterus, from the Eastern Pacific: Concentration, biomagnification and dietary intake. Marine Pollution Bulletin, 101, 349–358.

    Article  CAS  Google Scholar 

  9. Bergés-Tiznado, M. E., Márquez-Farías, F., Osuna-Martínez, C. C., Torres-Rojas, Y., Galván-Magaña, F., & Páez-Osuna, F. (2019). Patterns of mercury and selenium in tissues and stomach contents of the dolphinfish Coryphaena hippurus, from the SE Gulf of California, Mexico: Concentration, biomagnification and dietary intake. Marine Pollution Bulletin, 138, 84–92.

    Article  CAS  Google Scholar 

  10. Brusca, R. C. (1980). Common intertidal invertebrates of the Gulf of California. Tucson: The University of Arizona Press.

    Google Scholar 

  11. Campaore, W. F., Dumoulin, A., & Rousseau, D. P. L. (2020). Metals and metalloid in gold mine pit lakes and fish intake risk assessment, Burkina Faso. Environmental Geochemical and Health, 42, 563–577.

    Article  CAS  Google Scholar 

  12. Cerdenares-Ladrón de Guevara, G., Morales-Bojórquez, E., & Rodríguez-Sánchez, R. (2011). Age and growth of the sailfish Istiophorus platypterus (Istiophoridae) in the Gulf of Tehuantepec Mexico. Marine Biology Research, 7(5), 488–499.

    Article  Google Scholar 

  13. Chang, S. K., & Maunder, M. N. (2012). Aging material matters in the estimation of Von Bertalanffy growth parameters for dolphinfish (Coryphaena hippurus). Fisheries Research, 119–120, 147–153.

    Article  Google Scholar 

  14. Cheng, Z., Chen, K., Li, K., Nie, X., Wu, S., Wong, C., et al. (2013). Arsenic contamination in the freshwater fish ponds of Pearl River Delta: bioaccumulation and health risk assessment. Environmental Science and Pollution Research, 20(7), 4484–4495.

    CAS  Article  Google Scholar 

  15. Chipps, S., & Garvey, J. E. (2006). Assessment of diets and feeding patterns. In C. S. Guy & M. L. Brown (Eds.), Analysis and interpretation of freshwater fisheries data (pp. 473–514). Bethesda: American Fisheries Society.

    Google Scholar 

  16. Clarke, K. R., & Warwick, R. M. (2001). Change in marine communities: An approach to statistical analysis and interpretation. Plymouth: PRIMER-E.

    Google Scholar 

  17. Colwell, R. (2019). Estimates: Statistical Estimation of Species Richness and Shared Species from Samples, Version 9. http://viceroy.eeb.uconn.edu/EstimateS/. Accessed 3 September 2019.

  18. Cui, D., Zhang, P., Li, H., Zhang, Z., Song, Y., & Yang, Z. (2020). The dynamic effects of different inorganic arsenic species in crucian carp (Carassius auratus) iver during chronic dietborne exposure: Bioaccumulation, biotransformation and oxidative stress. Science of the Total Environment, 727, 138737. https://doi.org/10.1016/j.scitotenv.2020.138737.

    CAS  Article  Google Scholar 

  19. Di Bella, G., Bua, G. D., Fede, M. R., Mottese, A. F., Potortì, A. G., Cicero, N., et al. (2020). Potentially toxic elements in Xiphias gladius from Mediterranean Sea and risks related to human consumption. Marine Pollution Bulletin, 159, 111512. https://doi.org/10.1016/j.marpolbul.2020.111512.

    CAS  Article  Google Scholar 

  20. Donets, M. M., & Tsygankov, V. Y. (2019). Trace elements in commercial marine organisms from the Russian part of the northwest Pacific (2010–2018). Environmental Chemistry Letters, 17, 1727–1740.

    CAS  Article  Google Scholar 

  21. EPA. (2010). Toxicological Review of Inorganic arsenic (CAS No. 7440–38–2). U.S. Environmental Protection Agency. Washington, DC. https://cfpub.epa.gov/ncea/iris_drafts/recordisplay.cfm?deid=219111. Accessed 22 May 2020.

  22. EPA. (2017). Arsenic, inorganic (CASRN 7440–38–2). Integrated Risk Information System. https://cfpub.epa.gov/ncea/iris2/chemicalLanding.cfm?&substance_nmbr=278. Accessed 22 May 2020.

  23. Falco, G., Llobet, J. M., Bocio, A., & Domingo, J. L. (2006). Daily intake of arsenic, cadmium, mercury and lead by consumption of edible marine species. Journal of Agriculture and Food Chemistry, 54, 6106–6112.

    CAS  Article  Google Scholar 

  24. FAO. (2020a) División de Pesca. Species fact sheets. Coryphaena hippurus (Linnaeus, 1758). http://www.fao.org/fishery/species/3130/es. Accessed 10 April 2020.

  25. FAO. (2020b). Fisheries and Resources Monitoring System. Stock status report 2018 Indo-Pacific sailfish-Indian Ocean. http://firms.fao.org/firms/resource/10039/en. Accessed 14 August 2020.

  26. Fang, T., Lu, W., Cui, K., Li, J., Yang, K., Zhao, X., et al. (2019). Distribution, bioaccumulation and trophic transfer of trace metals in the food web of Chaohu lake, Anhui, China. Chemospere, 218, 1122–1130.

    Article  Google Scholar 

  27. Ferrante, M., Napoli, S., Grasso, A., Zccarelo, P., Cristaldi, A., & Copat, C. (2019). Systematic review of arsenic in fresh seafood from the Mediterranean Sea and European Atlantic coasts: A health risk assessment. Food and Chemical Toxicology, 126, 322–331.

    CAS  Article  Google Scholar 

  28. Fisher, W., Krupp, F., Schneider, W., Sommer, C., Carpenter, K. E., & Niem, V. H. (1995). Guía FAO para la identificación de especies para los fines de la pesca Pacífico Centro-Oriental, volumen II. Rome: FAO.

    Google Scholar 

  29. Froese, R., & Pauly, D. (2019a). Fish Base. Istiophorus platypterus (Shaw, 1792) Indo-Pacific sailfish. http://www.fishbase.org/summary/Istiophorus-platypterus.html. Accessed 14 August 2020.

  30. Froese, R., & Pauly, D. (2019b) Fish Base. Coryphaena hippurus (Linnaeus, 1758) Common dolphinfish. https://www.fishbase.de/summary/Coryphaena-hippurus.html. Accessed 14 August 2020.

  31. Fuentes-Gandara, F., Pinedo-Hernández, J., Marrugo-Negrete, J., & Díez, S. (2018). Human health impacts of exposure to metals through extreme consumption of fish from the Colombian Caribbean Sea. Environmental Geochemical and Health, 40, 229–242.

    CAS  Article  Google Scholar 

  32. García-Hernández, J., Cadena-Cárdenas, L., Bentancourt-Lozano, M., García-de-la-Parra, L., García-Rico, L., & Márquez-Farías, F. (2007). Total mercury content found in edible tissues of top predator fish from the Gulf of California Mexico. Toxicological and Environmental Chemistry, 89(3), 507–522.

    Article  CAS  Google Scholar 

  33. Gray, J. (2002). Biomagnification in marine systems: The perspective of an ecologist. Marine Pollution Bulletin, 45, 46–52.

    CAS  Article  Google Scholar 

  34. Hinton, M., & Maunder, M. (2014). Status of sailfish in the Eastern Pacific Ocean in 2011 and outlook for the future. Stock Assessment Report. Inter-American Tropical Tuna Commission, 14, 224–251.

    Google Scholar 

  35. Idrisi, N., Capo, T., Luthy, S., & Serafy, J. (2002). Behavior, oxygen consumption and survival of stressed juvenile sailfish (Istiophorus platypterus) in captivity. Marine and Freshwater Behaviour and Physiology, 36, 51–57.

    Article  CAS  Google Scholar 

  36. John-Kiran, P., Annapurn, A. Y., & Sree-Ramulu, K. (2017). Heavy metals in sailfish Istiophorus platypterus from Visakhapatnam fishing harbour, East Coast of India. Global Journal of Research Analysis, 6(12), 449–452.

    Google Scholar 

  37. Juncos, R., Arcagni, M., Squadrone, S., Rizzo, A., Arribére, A., Barriga, J. P., et al. (2019). Interspecific differences in the bioaccumulation of arsenic of three Patagonian top predator fish: Organ distribution and arsenic speciation. Ecotoxicology and Environmental Safety, 168, 431–442.

    CAS  Article  Google Scholar 

  38. La Torre, G. L., Cicero, N., Bartolomeo, G., Rando, R., Vadalà, R., Santini, A., et al. (2020). Assessment and monitoring of fish quality from a coastal ecosystem under high anthropic pressure: A case of study in southern Italy. International Journal of Environmental Research and Public Health, 17(9), 3285. https://doi.org/10.3390/ijerph17093285.

    CAS  Article  Google Scholar 

  39. Liao, W., Zhao, W., Wu, Y., Rong, N., Liu, X., Li, K., et al. (2020). Multiple metal(loid)s bioaccessibility from cooked seafood and health risk assessment. Environmental Geochemical and Health, 21, 4037–4050.

    Article  CAS  Google Scholar 

  40. Mandal, B., & Suzuki, K. (2002). Arsenic around the world: A review. Talanta, 58, 201–235.

    CAS  Article  Google Scholar 

  41. Marín, S., Pardo, O., Sánchez, A., Sánchez, Y., Vélez, D., Devesa, V., et al. (2018). Assessment of metal levels in foodstuffs from the Region of Valencia (Spain). Toxicology Reports, 5, 654–670.

    Article  CAS  Google Scholar 

  42. Mehouel, F., Bouayad, L., Berber, A., Van-Hauteghem, I., & Van-de-Wiele, M. (2019). Analysis and risk assessment of arsenic, cadmium and lead in two fish species (Sardina pilchardus and Xiphias gladius) from Algerian coastal water. Food Additives & Contaminants: Part A, 36(10), 1515–1521.

    CAS  Article  Google Scholar 

  43. Milošković, A., & Simić, V. (2015). Arsenic and other trace elements in five edible fish species in relation to fish size and weight and potential health risks for human consumption. Polish Journal of Environmental Studies, 24, 199–206.

    Article  CAS  Google Scholar 

  44. Moreno-Sierra, D., Bergés-Tiznado, M. E., Márquez-Farías, F., Torres-Rojas, Y. E., Ruelas-Inzunza, J. R., & Páez-Osuna, F. (2016). Trace metals in target tissues and stomach contents of the top predator sailfish Istiophorus platypterus from the Eastern Pacific: concentrations and contrasting behavior of biomagnification. Environmental Science and Pollution Research, 23, 23791–23803.

    CAS  Article  Google Scholar 

  45. Nakamura, I (1985) FAO Species Catalogue Vol 5 Billfishes of the World an annotated and illustrated catalogue of marlins, sailfishes, spearfishes and swordfishes known to date. United Nations Development Programme Food and Agricuature Organization of the United Nations, Rome

  46. NRC-CNRC. (2008). DOLT-4 Dogfish liver certified reference material for trace metals. Ottawa: National Research Council Canada–Conseil National de Recherches Canada.

    Google Scholar 

  47. Rahman, M. M., Shehzad, M. T., Nayak, A. K., Sharma, S., Yeasmin, M., Samanta, S., et al. (2020). Health risks from trace elements in muscles of some commonly available fish in Australia and India. Environmental Science and Pollution Research, 27, 21000–21012.

    CAS  Article  Google Scholar 

  48. Ramírez-Pérez, J., Quiñonez-Velázquez, C., Abitia-Cárdenas, L., & Melo-Barrera, F. N. (2011). Age and growth of sailfish Istiophorus platypterus (Shaw in Shaw and Nodder, 1792) from Mazatlan, Sinaloa, Mexico. Environmental Biology of Fishes, 92, 187–196.

    Article  Google Scholar 

  49. Ravenscroft, P., Brammer, H., & Richards, K. (2009). Arsenic pollution: A global synthesis. Oxford, UK: Wiley-Blackwell.

    Google Scholar 

  50. Schwenke, K. L., & Buckel, J. A. (2008). Age, growth and reproduction of dolphinfish (Coryphaena hippurus) caught off the coast of North Carolina. Fishery Bulletin, 106, 82–92.

    Google Scholar 

  51. Sele, V., Sloth, J., Lundeye, A. K., Larsen, E., Berntssen, M., & Amlund, H. (2012). Arsenolipids in marine oils and fats: A review of occurrence, chemistry and future research needs. Food Chemistry, 133, 618–630.

    CAS  Article  Google Scholar 

  52. SEMARNAT (2020). Secretaria del Medio Ambiente y Recursos Naturales. Consulta temática. Consumo Nacional aparente por destino y especie. http://dgeiawf.semarnat.gob.mx:8080/ibi_apps/WFServlet?IBIF_ex=D2_PESCA03_02&IBIC_user=dgeia_mce&IBIC_pass=dgeia_mce&NOMBREANIO=*. Accessed 10 July 2020.

  53. Šlejkovec, Z., Stajnko, A., Falnoga, I., Lipej, L., Mazej, D., Horvat, M., et al. (2014). Bioaccumulation of arsenic species in rays from the Northherrn Adriatic Sea. International Journal of Molecular Sciences, 15(12), 22073–22091.

    Article  CAS  Google Scholar 

  54. Soto-Jiménez, M. F., Amezcua, F., & González-Ledesma, R. (2010). Nonessential metals in striped marlin and indo-pacific sailfish in the southeast Gulf of California, Mexico: Concentrations and assessment of human health risk. Archives of Environmental Contamination and Toxicology, 58(3), 810–818.

    Article  CAS  Google Scholar 

  55. Storelli, M., Giacominelli-Stuffler, R., Storelli, A., & Marcotrigiano, G. (2005). Accumulation of mercury, cadmium, lead and arsenic in swordfish and bluefin tuna from the Mediterranean Sea: A comparative study. Marine Pollution Bulletin, 50(9), 993–1018.

    Article  CAS  Google Scholar 

  56. Sujitha, S. B., Jonathan, M. P., Aurioles-Gamboa, D., Campos Villegas, L. E., Bohórquez-Herrera, J., & Hernández-Camacho, C. J. (2019). Trace elements in marine organisms of Magdalena Bay, Pacific coast of Mexico: Bioaccumulation in a pristine environment. Environmental Geochemical and Health, 41(3), 1075–1089.

    CAS  Article  Google Scholar 

  57. Tripp-Valdez, A., García-De León, F., Ortega-García, S., Lluch-Cota, D., López-Martínez, J., & Cruz, P. (2010). Population genetic structure of dolphinfish (Coryphaena hippurus) in the Gulf of California, using microsatellite loci. Fisheries Research, 105(3), 172–177.

    Article  Google Scholar 

  58. Varol, M., Kaya, G. K., & Sünbül, M. R. (2019). Evaluation of health risks from exposure to arsenic and heavy metals through consumption of ten fish species. Environmental Science and Pollution Research, 26(32), 33311–33320.

    CAS  Article  Google Scholar 

  59. Varol, M., & Sünbül, M. R. (2020). Macroelements and toxic trace elements in muscle and liver of fish species from the largest three reservoirs in Turkey and human risk assessment based on the worst-case scenarios. Environmental Research, 184, 109298. https://doi.org/10.1016/j.envres.2020.109298.

    CAS  Article  Google Scholar 

  60. Vizzini, S., Costa, S., Tramati, C., Gianguzza, P., & Mazzola, A. (2013). Trophic transfer of trace elements in an isotopically constructed food chain from a semi-enclosed marine coastal area (Stagnone di Marsala, Sicily, Mediterranean). Archives of Environmental Contamination and Toxicology, 65(4), 642–653.

    CAS  Article  Google Scholar 

  61. Zar, J. (2010). Biostatistical analysis (5th ed.). New Jersey: Prentice Hall Pearson.

    Google Scholar 

  62. Zhang, W., & Wang, W. (2012). Large-scale spatial and interspecies differences in trace elements and stable isotopes in marine wild fish from Chinese waters. Journal of Hazardous Materials, 215–216, 65–74.

    Article  CAS  Google Scholar 

  63. Zhang, W., Guo, Z., Song, D., Du, S., & Zhang, L. (2018). Arsenic speciation in wild marine organisms and a health risk assessment in a subtropical bay of China. Science of the Total Environment, 626, 621–629.

    CAS  Article  Google Scholar 

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Acknowledgements

Authors thanks to H. Bojórquez-Leyva for assistance in analytical work.

Funding

Study supported by the Dirección General de Asuntos del Personal Académico, Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica and the Universidad Nacional Autónoma de México (DGAPA-PAPIIT-UNAM) Project IN200619 titled “Metales y metaloides en ríos y presas de cuencas mineras de Sinaloa: identificando contaminación y riesgos para la salud”; and DGIP-UAS (Dirección General de Investigación y Posgrado-Universidad Autónoma de Sinaloa) (Grant number: IN208213).

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All authors contributed to this work. FPO and MEBT conceived the ideas and designed the research; MEBT contributed to formal analysis; FPO contributed to funding acquisition; MEBT and JFMF contributed to methodology; MEBT, CCOM and JFMF contributed to investigation; MEBT and JFMF contributed to methodology; FPO and JFMF contributed to resources and supervision; MEBT and CCOM contributed to writing—original draft; FPO, MEBT, CCOM and JFMF contributed to writing—review and editing.

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Correspondence to Federico Páez-Osuna.

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Bergés-Tiznado, M.E., Márquez-Farías, J.F., Osuna-Martínez, C.C. et al. Arsenic in the top predators sailfish (Istiophorus platypterus) and dolphinfish (Coryphaena hippurus) off the southeastern Gulf of California. Environ Geochem Health (2021). https://doi.org/10.1007/s10653-021-00836-y

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Keywords

  • Biomagnification
  • Health risk
  • Muscle
  • Gonads
  • Eastern Pacific
  • Inorganic arsenic