Abstract
The bioaccumulation of arsenic (As) in the muscle, liver, kidneys, and brain of the shark Sphyrna lewini was measured in 40 juvenile specimens from southeast Gulf of California. Additionally, the biomagnification factor was calculated through prey items from stomach contents of the analyzed specimens. The concentrations of As (mg kg−1, wet weight) were higher in the muscle (10.1 ± 0.3) and liver (9.4 ± 0.5) than in the brain (4.5 ± 0.3) and kidneys (4.2 ± 0.2), which may be attributed to the biological functions of each tissue. Positive correlations were found between the levels of As in muscle and liver with the biological parameters of S. lewini. Hammerhead sharks feed mainly of teleost fishes with low As values (Clupeidae fishes, 1.1 ± 0.5; Sciaenidae fishes, 1.0 ± 0.6; Scomber japonicus, 1.2 ± 0.6; and Etropus crossotus 2.1 ± 0.4) compared with the predator, indicating biomagnification. Inorganic arsenic (Asi) in muscle was estimated as 3% of the total As, although muscle consumption is unlikely to represent a risk (HQ < 1) in humans. Moreover, the probabilities of developing cancer were estimated as low (3.99 × 10–5 to 3.32 × 10–6). To avoid health risks related to As, a weekly ration must not exceed 69.3 and 484.8 g in children and adults, respectively.
Similar content being viewed by others
Availability of Data and Material
The dataset generated during the current study are available from the corresponding author on reasonable request.
References
Allen GR, Robertson DR (1994) Fishes of the tropical eastern Pacific. University of Hawaii Press, Honolulu
Anislado-Tolentino V, Gallardo-Cabello M, Amezcua-Linares F, Robinson-Mendoza C (2008) Age and growth of the scalloped hammerhead shark, Sphyrna lewini (Griffith & Smith, 1834) from the Southern coast of Sinaloa, México. Hidrobiológica 18:31–40
Avigliano E, Maichak de Carvalho B, Invernizzi R, Olmedo M, Jasan R, Volpedo AV (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. Environ Sci Pollut Res 26:7994–8006
Barrera-García A, O’Hara T, Galván-Magaña F, Méndez-Rodríguez LC, Castellini M, Zenteno-Savín T (2012) Oxidative stress indicators and trace elements in the blue shark (Prionace glauca) off the east coast of the Mexican Pacific Ocean. Comp Biochem Physiol C Toxicol Pharmacol 156:59–66
Barrera-García A, O’Hara T, Galván-Magaña F, Méndez-Rodríguez LC, Castellini M, Zenteno-Savín T (2013) Trace elements and oxidative stress indicator in the liver and kidney of the blue shark (Prionace glauca). Comp Biochem Physiol A Molec Integr Physiol 165:483–490
Bergés-Tiznado ME, Páez-Osuna F, Notti A, Regoli F (2013) Arsenic and Arsenic Species in Cultured Oyster (Crassostrea gigas and C. corteziensis) from Coastal Lagoons of the SE Gulf of California. Mexico Biol Trace Element Res 151:43–49
Bergés-Tiznado ME, Márquez-Farías F, Lara-Mendoza R, Torres-Rojas Y, Galván-Magaña F, Bojórquez-Leyva H, Páez-Osuna F (2015) Mercury and selenium in muscle and target organs of Scalloped Hammerhead shark Sphyrna lewini of the SE Gulf of California: dietary intake, molar ratios, loads and human health risks. Arch Environ Contam Toxicol 69:440–452
Bizarro J, Smith W, Castillo-Géniz L, Ocampo-Torres L, Márquez-Farías F, Hueter R (2009) The seasonal importance of small coastal sharks and rays in the artisanal elasmobranch fishery of Sinaloa. Mexico Pan-Am J Aquat Sci 4(4):513–531
Boldrocchi G, Monticelli D, Omar YM, Bettinetti R (2019) Trace elements and POPs in two commercial shark species from Djibouti: Implications for human exposure. Sci Total Environ 669:637–648
Brusca RC (1980) Common intertidal invertebrates of the Gulf of California. The University of Arizona Press, Arizona
Cailliet GM, Goldman KJ (2004) Age determination and validation in Chondrichthyan fishes. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton FL, pp 399–447
Campbell LM, Norstrom RJ, Hobon KA, Muir DCG, Backus S, Fisk AT (2005) Mercury and other trace elements in a pelagic Artic marine food web (Northwater Polynya, Baffin Bay). Sci Total Environ 351–352:247–263
Castillo-Géniz L, Soriano-Veláquez SR, Villaseñor-Talavera R (2008) Pesquerías mexicanas de tiburón en el océano Pacífico. In: Machii T, Flores-Olivares J (eds) Pesquerías Latinoamericanas. Comisión Nacional de Acuacultura y Pesca, Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación, Mexico, pp 211–240
Castillo-Olguín E, Uribe-Acocer M, Díaz-Jaimes P (2012) Assessment of the population genetic structure of Sphyrna lewini to identify conservation units in the Mexican Pacific. Cienc Marinas 38:635–652
Chipps S, Garvey JE (2006) Assessment of diets and feeding patterns. In: Guy CS, Brown ML (eds) Analysis and interpretation of freshwater fisheries data. American Fisheries Society, Bethesda
Clarke KR, Gorley RN, Somerfield PJ, Warwick RM (2014) Change in marine communities: an approach to statistical analysis and interpretation, 3rd edn. PRIMER-e, Plymouth
Coiraton C, Amezcua F (2020) In utero elemental tags in vertebrae of the scalloped hammerhead shark Sphyrna lewini reveal migration patterns of pregnant females. Sci Rep 10:1799. https://doi.org/10.1038/s41598-020-58735-8
Coiraton C, Amezcua F, Ketchum JT (2020) New insights onto the migration patterns of the scalloped hammerhead shark Sphyrna lewini based on vertebral microchemistry. Mar Biol 167:58. https://doi.org/10.1007/s00227-020-3668-0
Colwell R (2006) Estimates: statistical estimation of species richness and shared species from samples, Version 8. http://viceroy.eeb.uconn.edu/EstimateS/
Compagno L (1984) FAO species catalogue. Vol. 4. Sharks of the world. An annotated and illustrated catalogue of shark species known to date. Part 2. Carcharhiniformes. FAO Fisheries Synopsis (125), volume 4. FAO, Rome
Davidson B, Cliff G (2002) The liver lipid acid profiles of seven Indian Ocean sharks species. Fish Physiol Biochem 26:171–175
De Gieter M, Leermakers M, Van Ryssen R, Noyen J, Goeyens L, Baeyens W (2002) Total and toxic arsenic levels in North Sea fish. Arch Environ Contam Toxicol 43:406–417
Drewniak T, Sklodowska A (2007) The role of bacteria in biogeochemical cycle of arsenic. Postep Mikrobiol 46:275–285
Duncan KM (2006) Estimation of daily energetic requirements in young scalloped hammerhead sharks, Shyrna lewini. Environ Biol Fish 76:139–149
Eisler R (2010) Compendium of Trace Metals and Marine Biota volume 2: vertebrates . Elsevier, London
EPA (2018) Environmental Protection Agency, Arsenic, inorganic (CASRN 7440–38–2). Environmental Protection Agency, Integrated Risk Information System. https://cfpub.epa.gov/ncea/iris/iris_documents/documents/subst/0278_summary.pdf. Accessed 22 May 2020
Evans DH, Piermarini PM, Choe KP (2004) Homeostasis: osmoregulation, pH regulation, and nitrogen excretion. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton FL, pp 247–268
Fisher W, Krupp F, Schneider W, Sommer C, Carpenter KE, Niem VH (1995) Guía FAO para la identificación de especies para los fines de la pesca. Pacífico Centro-Oriental, volume II: FAO, Rome
Fowler J, Cohen L (1990) Practical statistics for field biology. Wiley, West Sussex, England
Froese R, Pauly D (2019a) Fish base. Sphyrna lewini (Griffith & Smith, 1834) Scalloped hammerhead. https://www.fishbase.de/summary/Sphyrna-lewini.html. Accessed 9 Nov 2020
Froese R, Pauly D (2019b) Fish base. Etropus crossutus (Jordan & Gilbert, 1882) Fringed flounder. https://www.fishbase.de/summary/Etropus-crossotus.html. Accessed 9 Nov 2020
Garcia-Barcia L, Argiro J, Babcock EA, Cai Y, Shea SKH (2020) Mercury and arsenic in processed fins from nine of the most traded shark species in the Hong Kong and China dried seafood markets: The potential health risks of shark fin soup. Mar Pollut Bull 157:111281. https://doi.org/10.1016/j.marpolbul.2020.111281
Gray J (2002) Biomagnification in marine systems: the perspective of an ecologist. Mar Pollut Bull 45:46–52
Haman K, Norton T, Thomas A, Dove A, Tseng F (2012) Baseline health parameters and species comparisons among free-ranging Atlantic Sharpnose (Rhizoprionodon Terraenovae), Bonnethead (Sphyrna tiburo) and Spiny dogfish (Squalus Acanthias) sharks in Georgia, Florida and Washington, USA. J Wildlife Dis 48:295–306
Harris D (2003) Análisis Químico Cuantitativo, tercera edición. Reverté, Spain
Hurtado-Banda R, Gomez-Alvarez A, Márquez-Farías F, Cordoba-Figueroa M, Navarro-García G, Medina-Juárez L (2012) Total mercury in liver and muscle tissue of two coastal sharks from the Northwest of Mexico. Bull Environ Contam Toxicol 88(6):971–975
Kalantzi I, Pergantis SA, Black KD, Shimmield TM, Papageorgiou N, Tsapakis M, Karakassis I (2015) Metals in tissues of seabass and seabream reared in sites with toxic and anoxic substrata and risk assessment for consumers. Food Chem 194:659–670
Kojadinovic J, Potier M, Le Corre M, Cosson R, Bustamante P (2006) Mercury content in commercial pelagic fish from the Western Indian Ocean. Sci Total Environ 366:688–700
La Torre GL, Cicero N, Bartolomeo G, Rando R, Vadalà R, Santini A, Durazzo A, Lucarini M, Dugo G, Salvo A (2020) Assessment and monitoring of fish quality from a coastal ecosystem under high anthropic pressure: a case of study in southern Italy. Int J Environ Res Public Health 17:3285. https://doi.org/10.3390/ijerph17093285
Lluch-Cota S, Aragón-Noriega E, Arreguín-Sánchez F, Aurioles-Gamboa D, Bautista-Romero J, Brusca R, Cervantes-Duarte R, Cortés-Altamirano R, Del-Monte-Luna P, Esquivel-Herrera A, Fernández G, Hendrickx M, Hernández-Vázquez S, Herrera-Cervantes H, Kahru M, Lavín M, Llunch-Belda D, Llunch-Cota D, López-Martínez J, Marione S, Nevárez-Martínez M, Ortega-García S, Palacios-Castro E, Parés-Sierra A, Ponce-Díaz G, Ramírez-Rodríguez M, Salinas-Zavala, C, Schwartzlose R, Sierra-Beltran A (2007) The Gulf of California: Review of ecosystem status and sustainability challenges. Progr Oceanogr 731–26
Lowe C (2001) Metabolic rates of juvenile scalloped hammerhead sharks (Sphyrna lewini). Mar Biol 139:447–453
Luvonga C, Rimmer CA, Yu LL, Lee SB (2020) Organoarsenicals in seafood: occurrence, dietary exposure, toxicity and risk assessment considerations: a review. J Agric Food Chem 68:943–960
Lynch HN, Greenberg GI, Pollock MC, Lewis AS (2014) A comprehensive evaluation of inorganic arsenic in food and considerations for dietary intake analyses. Sci Total Environ 496:299–313
Mandal BK, Suzuki KT (2002) Arsenic around the world: a review. Talanta 16:201–235
Merly L, Lange L, Meyër M, Hewitt AM, Koen P, Fisher C, Muler J, Schilack V, Wentzel M, Hammerschlag N (2019) Blood plasma levels of heavy metals and trace elements in white sharks (Carcharodon carcharias) and potential health consequences. Mar Pollut Bull 142:85–92
Mohammed A, Mohammed T (2017) Mercury, arsenic, cadmium and lead in two commercial shark species (Sphyrna lewini and Caraharinus porosus) in Trinidad and Tobago. Mar Pollut Bull 119:214–218
Nance HA, Klimley P, Galván-Magaña F, Martínez-Ortíz J, Marko PB (2011) Demographic processes underlying subtle patterns of population structure in the Scalloped hammerhead shark Sphyrna lewini. PlosOne 6:e21459
Páez-Osuna F, Álvarez-Borrego S, Ruíz-Fernández AC, García-Hernández J, Jara-Marini ME, Bergés-Tiznado ME, Piñón-Gimate A, Alonso-Rodríguez R, Soto-Jiménez MF, Frías-Espericueta MG, Ruelas-Inzunza JR, Green-Ruíz CR, Osuna-Martínez CC, Sánchez-Cabeza JA (2017) Environmental status of the Gulf of California: a pollution review. Earth-Sci Rev 166:185–205
Powell JH, Powell RE, Fielder DR (1981) Trace element concentrations in tropical marine fish at Bougainville Island, Papua New Guinea. Water Air Soil Pollut 16:143–158
Rahman MA, Hasegawa H, Lim RP (2012) Bioaccumulation, biotransformation and trophic transfer of arsenic in the aquatic food chain. Environ Res 116:118–135
Rigby CL, Dulvy NK, Barreto R, Carlson J, Fernando D, Fordham S, Francis MP, Herman K, Jabado RW, Liu KM, Marshall A, Pacoureau N, Romanov E, Sherley RB, Winker H (2019) Sphyrna lewini. The IUCN Red List of Threatened Species 2019:e.T39385A2918526
Sele V, Sloth JJ, Lundebye AK, Larsen EH, Berntssen MHG, Amlund H (2012) Arsenolipids in marine oils and fats: a review of occurrence, chemistry and future research needs. Food Chem 133:618–630
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
Šlejkovec Z, Stajnko A, Falnoga I, Lipej L, Mazej D, Horvat M, Faganeli J (2014) Bioaccumulation of arsenic species in rays from the Northern Adriatic Sea. Int J Molec Sci 15:22073–22091
Storelli M, Marcotrigiano G (2004) Interspecific variation in total arsenic body concentrations in elasmobranch fish from the Mediterranean Sea. Mar Pollut Bull 48:1145–1167
Storelli M, Ceci E, Storelli A, Marcotrigiano G (2003) Polychlorinated biphenyl, heavy metal and methylmercury residues in hammerhead sharks: contaminant status and assessment. Mar Pollut Bull 46:1035–1039
Storelli M, Cuttone G, Marcotigiano G (2011) Distribution of trace elements in the tissue of smooth hound Mustelus mustelus (Linnaeus, 1978) from the southern-eastern waters of Mediterranean Sea (Italy). Environ Monitor Assess 174:271–281
Suhendrayatna AO, Nakajima T, Maeda S (2001) Metabolism and organ distribution of arsenic in the freshwater fish Tilapia mossambica. Appl Organometallic Chem 15:566–571
Taylor V, Goodale B, Raab A, Schwerdtle T, Reimer K, Conklin S, Karagas MR, Francesconi KA (2017) Human exposure to organic arsenic species from seafood. Sci Total Environ 580:266–282
Thomson DA, Findley LT, Kerstitch AN (2000) Reef fishes of Sea of Cortez. University of Texas, Austin, The Rocky-Shore fishes of the Gulf of California
Torres P, Tristao da Cunha R, Maia R, dos Santos RA (2014) Trophic ecology and bioindicator potential of the North Atlantic tope shark. Sci Total Environ 481:574–581
Torres-Rojas YE, Hernández-Herrera A, Galván-Magaña F, Alatorre-Ramírez VG (2010) Stomach content analysis of juvenile, scalloped hammerhead shark Sphyrna lewini captured off the coast of Mazatlán, Mexico. Aquat Ecol 44:301–308
Torres-Rojas YE, Páez-Osuna F, Hernández-Herrera A, Galván-Magaña F, Aguiñiga-García S, Villalobos-Ortíz H, Sampson L (2014) Feeding grounds of juvenile scalloped hammerhead sharks (Sphyrna lewini) in the south-eastern Gulf of California. Hydrobiologia 726:81–94
Torres-Rojas YE, Páez-Osuna F, Camalich J, Galván-Magaña F (2015) Diet and trophic level of scalloped hammerhead shark (Sphyrna lewini) from the Gulf of California and Gulf of Tehuantepec, Mexico. Iranian J Fish Sci 14:767–785
Trevizani TH, Petti MAV, Ribeiro AP, Corbisier TN, Figueira RCL (2018) Heavy metal concentrations in the benthic trophic web of Martel Inlet, Admiralty Bay (King George Island, Antarctica). Mar Pollut Bull 130:198–205
Vannuccini S (1999) Shark utilization, marketing and trade. FAO Fisheries Technical Paper. No. 389. FAO, Rome
Vélez-Alavez M, Labrada-Martagón V, Méndez-Rodriguez LC, Galván-Magaña F, Zenteno-Savín T (2013) Oxidative stress indicators and trace element concentrations in tissues of mako shark. Comp Biochem Physiol A Molec Integr Physiol 165:508–514
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-encosed marine coastal area (Stagnone di Marsala, Sicily, Mediterranean). Arch Environ Contam Toxicol 65:642–653
WHO (2001) Environmental Health Criteria 224 Arsenic and Arsenic compounds. World Health Organization, Geneva. http://www.inchem.org/documents/ehc/ehc/ehc224.htm. Accessed 22 Feb 2019
Wolff CA (1982) A beak key for eight eastern tropical Pacific cephalopods species, with relationship between their beak dimensions and size. Fish Bull 80:357–370
Zar J (2010) Biostatistical analysis, 5th edn. Prentice Hall Pearson, New Jersey
Zhang W, Wang W (2012) Large-scale spatial and interspecies differences in trace elements and stable isotopes in marine wild fish from Chinese waters. J Hazard Mater 215–216:65–74
Zhang W, Zhiqiang G, Song D, Du S, Zhang L (2018) Arsenic speciation in wild marine organisms and a health risk assessment in a subtropical bay of China. Sci Total Environ 626:621–629
Acknowledgements
This study was supported partially 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 “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). Special thanks are extended to H. Bojórquez-Leyva for the assistance in the analytical work.
Funding
The funding source for this work came from UNAM (Universidad Nacional Autónoma de México) through their grant “Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica” (PAPIIT) IN208213 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).
Author information
Authors and Affiliations
Contributions
All authors contributed to the conception and design of the study. The conceptualization, funding acquisition, resources material, and review and editing of the manuscript was performed by FP-O. MEB-T wrote the original draft and was in charge of the investigation, methodology, validation and formal analysis. JFM-F, DV, and VD performed formal analysis, and reviewed and edited the manuscript.
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that they have no conflict of interest.
Ethics Approval
This study did not involve human or animal participant experiments.
Consent to Participate
Not applicable.
Consent for Publication
All authors consent to the publication of this manuscript.
Code Availability
Not applicable.
Rights and permissions
About this article
Cite this article
Bergés-Tiznado, M.E., Vélez, D., Devesa, V. et al. Arsenic in Tissues and Prey Species of the Scalloped Hammerhead (Sphyrna lewini) from the SE Gulf of California. Arch Environ Contam Toxicol 80, 624–633 (2021). https://doi.org/10.1007/s00244-021-00830-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00244-021-00830-6