Assessment of mercury bioaccumulation in a tropical elasmobranch assemblage
Andréia S. Campos
A * , Moisés F. Bezerra A B , Victor L. Moura A , Vicente V. Faria C , Carlos E. Rezende D , Wanderley R. Bastos E , Iuri Aparecida S. Oliveira E and Luiz D. Lacerda A
A
B
C
D
E
Abstract
Mercury (Hg) is a non-essential metal that can accumulate in aquatic biota, including top predators such as elasmobranchs (sharks and rays) and biomagnifying along the trophic web. This study provides data on Hg total, methylmercury (MeHg) and stable isotopes (δ13C and δ15N) for 13 elasmobranch taxa in the Equatorial Western Atlantic Ocean, relating biological and ecological properties with Hg concentrations and the estimated human consumption risk.
Elasmobranchs widely consume fish, making understanding Hg bioaccumulation crucial. Little is known about Hg distribution in their bodies beyond muscle tissue and the associated health risks for both animals and humans who consume them.
This study evaluated Hg, methyl-Hg (MeHg) and stable isotopes (δ13C and δ15N) in the muscle, liver and brain of 13 elasmobranch taxa landed by artisanal fisheries on the Western Equatorial Atlantic Ocean.
The study revealed that Hg concentrations were highest in muscle tissue, whereas the brain exhibited the greatest percentage of MeHg. Significant correlations between Hg levels and body size, as well as between muscle and brain Hg concentrations, were observed in sharks. Stable isotope values indicated dietary and habitat diversity, and a significant correlation between Hg (log10) and δ15N was found. Mercury concentrations exceeded thresholds for harmful effects in ~76% of the analysed taxa and were also detected in embryos. These taxa also surpassed the local consumption limits, highlighting a potential risk.
The results demonstrated bioaccumulation and biomagnification of Hg in the studied taxa. Muscle Hg was a good predictor of brain Hg levels as a result of the significant correlation between these variables. The high proportion of MeHg in the brain indicates rapid transport of Hg to this organ. Observed Hg concentrations in juveniles and adults may affect their health, whereas concentrations in embryos indicate possible transfer of Hg from the mother to the embryos. This study advises caution when consuming various elasmobranchs, depending on the consumer’s weight and meal frequency.
Keywords: contamination, fishing, Hg, human exposure, MeHg, rays, sharks, stable isotopes.
References
Abreu SN, Pereira E, Valeà C, Duarte AC (2000) Accumulation of mercury in Sea Bass from a contaminated lagoon (Ria de Aveiro, Portugal). Marine Pollution Bulletin 40, 293-297.
| Crossref | Google Scholar |
Adams DH, McMichael RH (1999) Mercury level in four species of sharks from the Atlantic coast. Fishery Bulletin 97, 372-379.
| Google Scholar |
Adams DH, Sonne C (2013) Mercury and histopathology of the vulnerable goliath grouper, Epinephelus itajara, in US waters: a multi-tissue approach. Environmental Research 126, 254-263.
| Crossref | Google Scholar | PubMed |
Agência Nacional de Vigilância Sanitária (1998) Regulamento Técnico. Princípios Gerais para o estabelecimento de Níveis Máximos de Contaminantes Químicos em Alimentos. (ANVISA) Available at https://bvsms.saude.gov.br/bvs/saudelegis/anvisa/1998/anexo/anexo_prt0685_27_08_1998.pdf [In Portuguese]
Amaral ACZ, Migotto AE (1980) Importância dos anelídeos poliquetas na alimentação da macrofauna demersal e epibentônica da região de Ubatuba. Boletim do Instituto Oceanográfico 29, 31-35 [In Portuguese].
| Crossref | Google Scholar |
Amorim-Lopes CA, Araujo NLF, Rocha L, Monteiro F, Rocha RCC, Saint’Pierre TD, Lutfi DS, Vianna M, Hauser-Davis RA (2019) Toxic and essential metals in Narcine brasiliensis (Elasmobranchii: Narcinidae): a baseline ecotoxicological study in the Southeast Atlantic and preliminary maternal transfer implications. Marine Pollution Bulletin 149, 110606.
| Crossref | Google Scholar |
Amorim-Lopes C, Willmer IQ, Araujo NLF, Pereira LHSS, Monteiro F, Rocha RCC, Saint’Pierre TD, Santos LN, Siciliano S, Vianna M, Hauser-Davis RA (2020) Mercury screening in highly consumed sharpnose sharks (Rhizoprionodon lalandii and R. porosus) caught artisanally in southeastern Brazil. Elementa Science of the Anthropocene 8, 022.
| Crossref | Google Scholar |
Asante KA, Agusa T, Mochizuki H, Ramu K, Inoue S, Kubodera T, Takahashi S, Subramanian A, Tanabe S (2008) Trace elements and stable isotopes (δ13C and δ15N) in shallow and deep-water organisms from the East China Sea. Environmental Pollution 156, 862-873.
| Crossref | Google Scholar | PubMed |
Baró-Camarasa I, Marmolejo-Rodríguez AJ, O’Hara TM, Castellini JM, Murillo-Cisneros DA, Martínez-Rincón RO, Elorriaga-Verplancken FR, Galván-Magaña F (2022) Mercury maternal transfer in two placental sharks and a yolk-sac ray from Baja California Sur, Mexico. Marine Pollution Bulletin 179, 113672.
| Crossref | Google Scholar | PubMed |
Barreto RR, Bornatowski H, Motta FDS, Santander-Neto J, Vianna GMDS, Lessa R (2017) Rethinking use and trade of pelagic sharks from Brazil. Marine Policy 85, 114-122.
| Crossref | Google Scholar |
Bastos WR, Dórea JG, Bernardi JVE, Lauthartte LC, Mussy MH, Hauser M, Dória CRC, Malm O (2015) Mercury in muscle and brain of catfish from the Madeira river, Amazon, Brazil. Ecotoxicology and Environmental Safety 118, 90-97.
| Crossref | Google Scholar | PubMed |
Bergés-Tiznado ME, Márquez-Farías F, Lara-Mendoza RE, Torres-Rojas YE, Galván-Magaña F, Bojórquez-Leyva H, Páez-Osuna F (2015) Mercury and selenium in muscle and target organs of scalloped hammerhead sharks Sphyrna lewini of the se gulf of California: dietary intake, molar ratios, loads, and human health risks. Archives of Environmental Contamination and Toxicology 69, 440-452.
| Crossref | Google Scholar | PubMed |
Bernardo C, Adachi AMCL, Cruz PV, Foresti F, Loose RH, Bornatowski H (2020) The label “Cação” is a shark or a ray and can be a threatened species! Elasmobranch trade in Southern Brazil unveiled by DNA barcoding. Marine Policy 116, 103920.
| Crossref | Google Scholar |
Bezerra MF, Lacerda LDD, Lima EHSM, Melo MTD (2013) Monitoring mercury in green sea turtles using keratinized carapace fragments (scutes). Marine Pollution Bulletin 77, 424-427.
| Crossref | Google Scholar | PubMed |
Bezerra MF, Lacerda LD, Chun-Ta L (2019) Trace metals and persistent organic pollutants contamination in batoids (Chondrichthyes: Batoidea): A systematic review. Environmental Pollution 248, 684-695.
| Crossref | Google Scholar | PubMed |
Bezerra MF, Goyanna FAA, Lacerda LD (2023) Risk assessment of human Hg exposure through consumption of fishery products in Ceará state, northeastern Brazil. Marine Pollution Bulletin 189, 114713.
| Crossref | Google Scholar | PubMed |
Bezerra MF, Barrios-Rodriguez CA, Rezende CE, Lópes-Castro MC, Lacerda LD (2024) Trophic ecology of sympatric sea turtles in the tropical Atlantic coast of Brazil. Marine Environmental Research 196, 106406.
| Crossref | Google Scholar | PubMed |
Bornatowski H, Abilhoa V, Freitas MO (2006) Sobre a alimentação de Narcine brasiliensis na Baía de Ubatuba-enseada, São Francisco do Sul, Santa Catarina, Brasil. Feeding of Narcine brasiliensis at Ubatuba-Enseada bay, São Francisco do Sul, Santa Catarina, Brazil. Estudos de Biologia 28(62), 57-60 [In Portuguese, with title, abstract and keywords in Portuguese and English].
| Crossref | Google Scholar |
Bornatowski H, Braga RR, Kalinowski C, Vitule JRS (2015) “Buying a pig in a poke”: the problem of elasmobranch meat consumption in southern Brazil. Ethnobiology Letters 6, 196-202.
| Crossref | Google Scholar |
Bornatowski H, Braga RR, Barreto RP (2018) Elasmobranchs consumption in Brazil: impacts and consequences. Coastal Research Library 22, 251-262.
| Crossref | Google Scholar |
Botto F, Gaitán E, Mianzan H, Acha M, Giberto D, Schiariti A, Iribarne O (2011) Origin of resources and trophic pathways in a large SW Atlantic estuary: an evaluation using stable isotopes. Estuarine, Coastal and Shelf Science 92, 70-77.
| Crossref | Google Scholar |
Braccini JM (2008) Feeding ecology of two high-order predators from south-eastern Australia: the coastal broadnose and the deepwater sharpnose sevengill sharks. Marine Ecology Progress Series 371, 273-284.
| Crossref | Google Scholar |
Branco V, Vale C, Canário J, Santos MN (2007) Mercury and selenium in blue shark (Prionace glauca, L. 1758) and swordfish (Xiphias gladius, L. 1758) from two areas of the Atlantic Ocean. Environmental Pollution 150, 373-380.
| Crossref | Google Scholar | PubMed |
Coelho KKF, Lima FS, Wosnick N, Nunes AROP, Silva APC, Gava TT, Brito RMS, Ferreira LJS, Duailibe ICFS, Dias HN, Almeida ZS, Nunes JLS (2021) Research trends on elasmobranchs from the Brazilian Amazon Coast: a four-decade review. Biota Neotropica 21, e20211218.
| Crossref | Google Scholar |
Collins AB, Heupel MR, Hueter RE, Motta PJ (2007) Hard prey specialists or opportunistic generalists? An examination of the diet of the cownose ray, Rhinoptera bonasus. Marine and Freshwater Research 58, 135-144.
| Crossref | Google Scholar |
Depew DC, Basu N, Burgess NM, Campbell LM, Devlin EW, Drevnick PE, Hammerschmidt CR, Murphy CA, Sandheinrich MB, Wiener JG (2012) Toxicity of dietary methylmercury to fish: derivation of ecologically meaningful threshold concentrations. Environmental Toxicology and Chemistry 31, 1536-1547.
| Crossref | Google Scholar | PubMed |
Dillon T, Beckvar N, Kern J (2010) Residue-based mercury dose-response in fish: an analysis using lethality-equivalent test endpoints. Environmental Toxicology and Chemistry 29, 2559-2565.
| Crossref | Google Scholar | PubMed |
Dias ACL, Gimarães JRD, Malm O, Costa PAS (2008) Total mercury in muscle of the shark Prionace glauca (Linnaeus, 1758) and swordfish Xiphias gladius Linnaeus, 1758, from the south-southeast coast of Brazil and the implications for public health. Cadernos de Saúde Pública 24, 2063-2070.
| Crossref | Google Scholar | PubMed |
Dulvy NK, Fowler SL, Musick JA, Cavanagh RD, Kyne PM, Harrison LR, Carlson JK, Davidson LNK, Fordham SV, Francis MP, Pollock CM, Simpfendorfer CA, Burgess GH, Carpenter KE, Compagno LJV, Ebert DA, Gibson C, Heupel MR, Livingstone SR, Sanciangco JC, Stevens JD, Valenti S, White WT (2014) Extinction risk and conservation of the world’s sharks and rays. Elife 3, e00590.
| Crossref | Google Scholar | PubMed |
Dulvy NK, Pacoureau N, Rigby CL, Pollom RA, Jabado RW, Ebert DA, Finucci B, Pollock CM, Cheok J, Derrick DH, Herman KB, Sherman CS, VanderWright WJ, Lawson JM, Walls RHL, Carlson JK, Charvet P, Bineesh KK, Fernando D, Ralph JM, Matsushiba JH, Hilton-Taylor C, Fordham SV, Simpfendorfer CA (2021) Overfishing drives over one-third of all sharks and rays toward a global extinction crisis. Current Biology 31, 4773-4787.
| Crossref | Google Scholar | PubMed |
Ehnert-Russo S, Gelsleichter J (2020) Mercury accumulation and effects in the brain of the Atlantic sharpnose shark (Rhizoprionodon terraenovae). Archives of Environmental Contamination and Toxicology 78, 267-283.
| Crossref | Google Scholar | PubMed |
Endo T, Hisamichi Y, Haraguchi K, Kato Y, Ohta C, Koga N (2008) Hg, Zn and Cu levels in the muscle and liver of tiger sharks (Galeocerdo cuvier) from the coast of Ishigaki Island, Japan: relationship between metal concentrations and body length. Marine Pollution Bulletin 56, 1774-1780.
| Crossref | Google Scholar | PubMed |
Estupiñán-Montaño C, Pacheco-Triviño F, Cedeño-Figueroa LG, Galván-Magaña F, Estupiñán-Ortiz JF (2018) Diet of three shark species in the Ecuadorian Pacific, Carcharhinus falciformis, Carcharhinus limbatus and Nasolamia velox. Journal of the Marine Biological Association of the United Kingdom 98, 927-935.
| Crossref | Google Scholar |
France RL (1995) Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Marine Ecology Progress Series 124, 307-312.
| Crossref | Google Scholar |
Frías-Espericueta MG, Zamora-Sarabia FKG, Márquez-Farías JF, Osuna-López JI, Ruelas-Inzunza J, Voltolina D (2015) Total mercury in female Pacific sharpnose sharks Rhizoprionodon longurio and their embryos. Latin American Journal of Aquatic Research 43, 534-538.
| Crossref | Google Scholar |
Frisk MG, Miller TJ, Fogarty MJ (2001) Estimation and analysis of biological parameters in elasmobranch fishes: a comparative life history study. Canadian Journal of Fisheries and Aquatic Sciences 58, 969-981.
| Crossref | Google Scholar |
Gelsleichter J, Musick JA, Nichols S (1999) Food habits of the smooth dogfish, Mustelus canis, dusky shark, Carcharhinus obscurus, Atlantic sharpnose shark, Rhizoprionodon terraenovae, and the sand tiger, Carcharias taurus, from the northwest Atlantic Ocean. Environmental Biology of Fishes 54, 205-217.
| Crossref | Google Scholar |
Gibb H, O’Leary KG (2014) Mercury exposure and health impacts among individuals in the artisanal and small-scale gold mining community: a comprehensive review. Environmental Health Perspectives 122, 667-672.
| Crossref | Google Scholar | PubMed |
Goericke R, Fry B (1994) Variations of marine plankton δ13C with latitude, temperature, and dissolved CO2 in the world ocean. Global Biogeochemical Cycles 8, 85-90.
| Crossref | Google Scholar |
Gomes UL, Santos HRS, Gadig OBF, Signori CN, Vicente MM (2019) Guia para identificação dos tubarões, raias e quimeras do Rio de Janeiro (Chondrichthyes: Elasmobranchii e Holocephali). Identification guide of sharks, batoids and chimaeroids from Rio de Janeiro State (Chondrichthyes: Elasmobrachii e Holocephali). Guía para identificación de tiburones, rayas y quimeras del Estado de Rio de Janeiro (Chondrichthyes: Elasmobrachii e Holocephali). Revista Nordestina de Biologia 27, 171-368 [In Portuguese, with title, abstract and keywords in Portuguese, English and Spanish].
| Crossref | Google Scholar |
Grippo MA, Heath AG (2003) The effect of mercury on the feeding behavior of fathead minnows (Pimephales promelas). Ecotoxicology & Environmental Safety 55, 187-198.
| Crossref | Google Scholar | PubMed |
Havelková M, Dušek L, Némethová D, Poleszczuk G, Svobodová Z (2008) Comparison of mercury distribution between liver and muscle – a biomonitoring of fish from lightly and heavily contaminated localities. Sensors 8, 4095-4109.
| Crossref | Google Scholar | PubMed |
Henriques MC, Carvalho I, Santos C, Herdeiro MT, Fardilha M, Pavlaki MD, Loureiro S (2023) Unveiling the molecular mechanisms and developmental consequences of mercury (Hg) toxicity in zebrafish embryo-larvae: a comprehensive approach. Neurotoxicology and Teratology 100, 107302.
| Crossref | Google Scholar | PubMed |
Heupel MR, Knip DM, Colin A, Simpfendorfer CA, Dulvy NK (2014) Sizing up the ecological role of sharks as predators. Marine Ecology Progress Series 495, 291-298.
| Crossref | Google Scholar |
Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120, 314-326.
| Crossref | Google Scholar | PubMed |
Hussey NE, Brush J, McCarthy ID, Fisk AT (2010) δ15N and δ13C diet-tissue discrimination factors for large sharks under semi-controlled conditions. Comparative Biochemistry and Physiology 155, 445-453.
| Crossref | Google Scholar | PubMed |
Hussey NE, MacNeil MA, Olin JA, McMeans BC, Kinney MJ, Chapman DD, Fisk AT (2012) Stable isotopes and elasmobranchs: tissue types, methods, applications and assumptions. Journal of Fish Biology 80, 1449-1484.
| Crossref | Google Scholar | PubMed |
Instituto Brasileiro de Geografia e Estatística (2011) Pesquisa de Orçamentos Familiares 2008–2009: análise do consumo alimentar pessoal no Brasil. Rio de Janeiro. (IBGE, Diretoria de Pesquisas, Coordenação de Trabalho e Rendimento) Available at https://biblioteca.ibge.gov.br/visualizacao/livros/liv50063.pdf [In Portuguese]
Jezierska B, Ługowska K, Witeska M (2009) The effects of heavy metals on embryonic development of fish (a review). Fish Physiology and Biochemistry 35, 625-640.
| Crossref | Google Scholar | PubMed |
Julio TG, Moura VL, Lacerda LD, Lessa RPT (2022) Mercury concentrations in coastal Elasmobranchs (Hypanus guttatus and Rhizoprionodon porosus) and human exposure in Pernambuco, northeastern Brazil. Anais da Academia Brasileira de Ciências 94, e20220045.
| Crossref | Google Scholar | PubMed |
Kidd K, Clayden M, Jardine T (2012) Bioaccumulation and biomagnification of mercury through food webs. In ‘Environmental Chemistry and Toxicology of Mercury’. (Eds G Liu, Y Cai and N O’Driscoll) pp. 453–499. (Wiley) 10.1002/9781118146644.ch14
Kim KH, Kabir E, Jahan SA (2016) A review on the distribution of Hg in the environment and its human health impacts. Journal of Hazardous Materials 306, 376-385.
| Crossref | Google Scholar | PubMed |
Krey A, Kwan M, Chan HM (2014) In vivo and in vitro changes in neurochemical parameters related to mercury concentrations from specific brain regions of polar bears (Ursus maritimus). Environmental Toxicology and Chemistry 33, 2463-2471.
| Crossref | Google Scholar | PubMed |
Kružíková K, Kenšová R, Sedláčková L, Jarkovský J, Poleszczuk G, Svobodová Z (2013) The correlation between fish mercury liver/muscle ratio and high and low levels of mercury contamination in Czech localities. International Journal of Electrochemical Science 8, 45-56.
| Crossref | Google Scholar |
Lacerda LD, Paraquetti HHM, Marins RV, Rezende CE, Zalmon IR, Gomes MP, Farias VV (2000) Mercury content in shark species from the south-eastern Brazilian coast. Revista Brasileira de Biologia 60, 571-576.
| Crossref | Google Scholar | PubMed |
Lacerda LD, Bezerra MF, Costa BGB, Braga TM, Goyanna FAA (2016) Mercury distribution in fish commercialized at the Mucuripe Market, Fortaleza, Ceará State, Brazil. Arquivos de Ciências do Mar 49, 50-54.
| Crossref | Google Scholar |
Lacerda LD, Moura VL, Oliveira RW, Carmo KLC, Nunes JLS, Freitas AS, Bezerra MF (2024) Mercury (Hg) concentration in fish commercialized in the São Luís fish market (MA) and potential exposure of consumers. Anais da Academia Brasileira de Ciências 96, e20230238.
| Crossref | Google Scholar | PubMed |
Lavoie RA, Jardine TD, Chumchal MM, Kidd KA, Campbell LM (2013) Biomagnification of mercury in aquatic food webs: a worldwide meta-analysis. Environmental Science and Technology 47, 13385-13394.
| Crossref | Google Scholar | PubMed |
Layman CA, Arrington DA, Montaña CG, Post DM (2007) Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88, 42-48.
| Crossref | Google Scholar | PubMed |
Li Z, Pethybridge HR, Gong Y, Wu F, Dai X, Li Y (2022) Effect of body size, feeding ecology and maternal transfer on mercury accumulation of vulnerable silky shark Carcharhinus falciformis in the eastern tropical pacific. Environmental Pollution 309, 119751.
| Crossref | Google Scholar | PubMed |
Licata P, Trombetta D, Cristani M, Naccari C, Martino D, Calò M, Naccari F (2005) Heavy metals in liver and muscle of bluefin tuna (Thunnus thynnus) caught in the straits of Messina (Sicily, Italy). Environmental Monitoring and Assessment 107, 239-248.
| Crossref | Google Scholar | PubMed |
Lyons K, Lowe CG (2013) Mechanisms of maternal transfer of organochlorine contaminants and mercury in the common thresher shark (Alopias vulpinus). Canadian Journal of Fisheries and Aquatic Sciences 70, 1667-1672.
| Crossref | Google Scholar |
Lyons K, Carlisle AB, Lowe CG (2017) Influence of ontogeny and environmental exposure on mercury accumulation in muscle and liver of male Round Stingrays. Marine Environmental Research 130, 30-37.
| Crossref | Google Scholar | PubMed |
Matulik AG, Kerstetter DW, Hammerschlag N, Divoll T, Hammerschmidt CR, Evers DC (2017) Bioaccumulation and biomagnification of mercury and methylmercury in four sympatric coastal sharks in a protected subtropical lagoon. Marine Pollution Bulletin 116, 357-364.
| Crossref | Google Scholar | PubMed |
Moura VL, Rabelo JN, Bezerra MF, Silva GB, Faria VV, Rezende CE, Bastos WR, Lacerda LD (2020) Ecological and biological factors associated to mercury accumulation in batoids (Chondrichthyes: Batoidea) from northeastern Brazil. Marine Pollution Bulletin 161, 111761.
| Crossref | Google Scholar | PubMed |
Nam DH, Adams DH, Reyier EA, Basu N (2011) Mercury and selenium levels in lemon sharks (Negaprion brevirostris) in relation to a harmful red tide event. Environmental Monitoring and Assessment 176, 549-559.
| Crossref | Google Scholar | PubMed |
Newman MC, Xu X, Cotton CF, Tom KR (2011) High mercury concentrations reflect trophic ecology of three deep-water chondrichthyans. Archives of Environmental Contamination and Toxicology 60, 618-625.
| Crossref | Google Scholar | PubMed |
Niedermüller S, Ainsworth G, Juan S, García R, Ospina-Alvarez A, Pita P, Villasante S (2021) The shark and ray meat network: a deep dive into a global affair. (World Wildlife Fund: Rome, Italy) Available at https://sharks.panda.org/images/downloads/392/WWF_MMI_Global_shark__ray_meat_trade_report_2021_lowres.pdf
Nomaki H, Ogawa NO, Ohkouchi N, Suga H, Toyofuku T, Shimanaga M, Nakatsuka T, Kitazato H (2008) Benthic foraminifera as trophic links between phytodetritus and benthic metazoans: carbon and nitrogen isotopic evidence. Marine Ecology Progress Series 357, 153-164.
| Crossref | Google Scholar |
Núñez-Nogueira G (2005) Concentration of essential and non-essential metals in two shark species commonly caught in Mexican (Gulf of Mexico) coastline. In ‘Golfo de México Contaminación e Impacto Ambiental: Diagnóstico y Tendencias’. (Eds AV Botello, J Rendón von Osten, G Gold-Bouchot, C Agráz-Hernández) pp. 451–474. (Universidad Autónoma de Campeche, Universidad Autónoma Campeche, Universidad Nacional Autónoma de México, Instituto Nacional de Ecología) Available at https://www.researchgate.net/publication/235917351
Pacoureau N, Rigby CL, Kyne PM, Sherley RB, Winker H, Carlson JK, Fordham SV, Barreto R, Fernando D, Francis MP, Jabado RW, Herman KB, Liu KM, Marshall AD, Pollom RA, Romanov EV, Simpfendorfer CA, Yin JS, Kindsvater HK, Kindsvater HK, Dulvy NK (2021) Half a century of global decline in oceanic sharks and rays. Nature 589, 567-571.
| Crossref | Google Scholar | PubMed |
Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annual Review of Ecology, Evolution, and Systematics 18, 293-320.
| Crossref | Google Scholar |
Pinheiro WM, Santander-Neto J, Arthaud IDB, Faria VV (2023) Size and sex composition of three carcharhiniform sharks landed by a coastal artisanal fleet from the northeastern coast of Brazil. Neotropical Ichthyology 21, 230005.
| Crossref | Google Scholar |
Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703-718.
| Crossref | Google Scholar |
Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montaña CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152, 179-189.
| Crossref | Google Scholar | PubMed |
Queiroz APN, Araújo MLG, Hussey NE, Lessa RP (2023) Trophic ecology of three stingrays (Myliobatoidei: Dasyatidae) off the Brazilian north‐eastern coast: habitat use and resource partitioning. Journal of Fish Biology 102, 27-43.
| Crossref | Google Scholar | PubMed |
Rodrigues ACM, Gravato C, Galvão D, Silva VS, Soares AMVM, Gonçalves JMS, Ellis JR, Vieira RP (2022) Ecophysiological effects of mercury bioaccumulation and biochemical stress in the deep-water mesopredator Etmopterus spinax (Elasmobranchii; Etmopteridae). Journal of Hazardous Materials 423, 127245.
| Crossref | Google Scholar | PubMed |
Roubie E, Karavoltsos S, Sakellari A, Katsikatsos N, Dassenakis M, Megalofonou P (2024) Trace metals distribution in tissues of 10 different shark species from the eastern Mediterranean Sea. Fishes 9, 77.
| Crossref | Google Scholar |
Rua-Ibarz A, Bolea-Fernandez E, Maage A, Frantzen S, Sanden M, Vanhaecke F (2019) Tracing mercury pollution along the norwegian coast via elemental, speciation, and isotopic analysis of liver and muscle tissue of deep-water marine fish (Brosme brosme). Environmental Science and Technology 53, 1776-1785.
| Crossref | Google Scholar | PubMed |
Sandheinrich MB, Miller KM (2006) Effects of dietary methylmercury on reproductive behavior of fathead minnows (Pimephales promelas). Environmental Toxicology and Chemistry 25, 3053-3057.
| Crossref | Google Scholar | PubMed |
Santander-Neto J, Faria VV (2020) Sharks and rays caught by a small-scale fisheries in the western equatorial Atlantic. Journal of Applied Ichthyology 36, 830-833.
| Crossref | Google Scholar |
Scheuhammer A, Braune B, Chan HM, Frouin H, Krey A, Letcher R, Loseto L, Noël M, Ostertag S, Ross P, Wayland M (2015) Recent progress on our understanding of the biological effects of mercury in fish and wildlife in the Canadian Arctic. Science of the Total Environment 509–510, 91-103.
| Crossref | Google Scholar | PubMed |
Shibuya A, Rosa RS (2019) Stomach contents of the Caribbean sharpnose shark Rhizoprionodon porosus (Poey, 1864) (Elasmobranchii: Carcharhinidae) from the coast of Paraíba, Brazil. Revista Nordestina de Biologia 27, 81-90.
| Crossref | Google Scholar |
Shiffman DS, Gallagher AJ, Boyle MD, Hammerschlag-Peyer CM, Hammerschlag N (2012) Stable isotope analysis as a tool for elasmobranch conservation research: a primer for non-specialists. Marine and Freshwater Research 63, 635-643.
| Crossref | Google Scholar |
Simpfendorfer CA, Goodreid AB, McAuley RB (2001) Size, sex and geographic variation in the diet of the tiger shark, Galeocerdo cuvier, from Western Australian waters. Environmental Biology of Fishes 61, 37-46.
| Crossref | Google Scholar |
Sousa MC, Martins IM, Hanazaki N (2016) Trophic relationships between people and resources: fish consumption in an artisanal fishers neighborhood in southern Brazil. Ethnobiology and Conservation 5(4), 1-16.
| Crossref | Google Scholar |
Storelli MM, Giacominelli-Stuffler R, Marcotrigiano G (2002) Mercury accumulation and speciation in muscle tissue of different species of sharks from Mediterranean Sea, Italy. Bulletin of Environmental Contamination and Toxicology 68, 201-210.
| Crossref | Google Scholar | PubMed |
Storelli A, Barone G, Garofalo R, Busco A, Storelli MM (2022) Determination of mercury, methylmercury and selenium concentrations in elasmobranch meat: fish consumption safety. International Journal of Environmental Research and Public Health 19, 788.
| Crossref | Google Scholar | PubMed |
Taylor DL, Kutil NJ, Malek AJ, Collie JS (2014) Mercury bioaccumulation in cartilaginous fishes from southern New England coastal waters: contamination from a trophic ecology and human health perspective. Marine Environmental Research 99, 20-33.
| Crossref | Google Scholar | PubMed |
Tiktak GP, Butcher D, Lawrence PJ, Norrey J, Bradley L, Shaw K, Preziosi R, Megson D (2020) Are concentrations of pollutants in sharks, rays and skates (Elasmobranchii) a cause for concern? A systematic review. Marine Pollution Bulletin 160, 111701.
| Crossref | Google Scholar | PubMed |
Torres P, Rodrigues A, Soares L, Garcia P (2016) Metal concentrations in two commercial tuna species from an active volcanic region in the Mid-Atlantic Ocean. Archives of Environmental Contamination and Toxicology 70, 341-347.
| Crossref | Google Scholar | PubMed |
United States Environmental Protection Agency (2022) Regional screening levels for chemical contaminants at superfund sites. (USEPA: Washington, DC, USA) Available at https://www.epa.gov/risk/regional-screening-levels-rsls-users-guide#special
Vianna M, Arfelli CA, Amorim AF (2000) Feeding of Mustelus canis (Elasmobranchii, Triakidae) caught off south-southeast coast of Brazil. Boletim do Instituto de Pesca 26, 79-84.
| Google Scholar |
Walker TI (1988) Mercury concentrations in edible tissues of elasmobranchs, teleosts, crustaceans and molluscs from south-eastern Australian Waters. Marine and Freshwater Research 39, 39-49.
| Crossref | Google Scholar |
Wosnick N, Chaves AP, Leite RD, Nunes JLS, Saint’Pierre TD, Willmer IQ, Hauser-Davis RA (2021a) Nurse sharks, space rockets and cargo ships: metals and oxidative stress in a benthic, resident and large-sized mesopredator, Ginglymostoma cirratum. Environmental Pollution 288, 117784.
| Crossref | Google Scholar |
Wosnick N, Niella Y, Hammerschlag N, Chaves AP, Hauser-Davis RA, Rocha RCC, Jorge MB, Oliveira RWS, Nunes JLS (2021b) Negative metal bioaccumulation impacts on systemic shark health and homeostatic balance. Marine Pollution Bulletin 168, 112398.
| Crossref | Google Scholar |
Yeakel JD, Bhat U, Smith EAE, Newsome SD (2016) Exploring the isotopic niche: isotopic variance, physiological incorporation, and the temporal dynamics of foraging. Frontiers in Ecology and Evolution 4, 1.
| Crossref | Google Scholar |
Zheng W, Aschner M, Ghersi-Egea JF (2003) Brain barrier systems: a new frontier in metal neurotoxicological research. Toxicology and Applied Pharmacology 192, 1-11.
| Crossref | Google Scholar | PubMed |
