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Mercury concentrations in coastal Elasmobranchs (Hypanus guttatus and Rhizoprionodon porosus) and human exposure in Pernambuco, Northeastern Brazil

Abstract

Elasmobranchs are long-lived predatory fish that show high Hg concentrations generally reflecting environmental levels, notwithstanding they are widely consumed in Brazil increasing Hg exposure to humans. This study reports on Hg concentrations in largely consumed sharks (Rhizoprionodon porosus) and rays (Hypanus guttatus) from the Pernambuco coast, NE Brazil and the risk associated with their consumption. Muscle tissue concentrations of Hg in H. guttatus and R. porosus varied from 40 to 1,020 ng.g-1 w.w. (median = 125; mean = 124 ± 48 ng.g-1 w.w.) in sharks and from 129 to 2,130 ng.g-1 w.w. (median = 976; mean = 919 ± 139 ng.g-1 w.w.) in rays. Concentrations of Hg positively correlated with size in sharks, but not in rays. Concentrations reflect the local environmental contamination of a large urban center and industrial park concentrated in a short extension of mangrove-dominated coastline (50 km) and are higher compared to other Brazilian sites where Hg concentrations in these species have been reported. Sharks had a risk coefficient (HQ) range of 0.04 to 1.1, not surpassing the reference level of exposure. On the other hand, rays’ HQ ranged from 0.14 to 2.3, and exceeds the reference level of exposure and suggests adverse effects to consumers.

Key words
trace metal; bioaccumulation; stingray; shark; age; human exposure

INTRODUCTION

The quality of aquatic ecosystems plays an outstanding role in maintaining seafood resources, especially in high diversity zones as coastal and estuarine waters used for feeding and rearing of marine fish (Lotze et al. 2006LOTZE HK ET AL. 2006. Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312: 1806-1809., Woodland et al. 2011WOODLAND RJ, SECOR DH, FABRIZIO MC & WILBERG MJ. 2011. Comparing the nursery role of inner continental shelf and estuarine habitats for temperate marine fishes. Estuar Coast Shelf Sci 99: 61-73.). Anthropogenic pressures like urbanization, industrialization, port activities, and tourism over coastal environments have increased eutrophication and pollution (Nixon 1995NIXON SW. 1995. Coastal marine eutrophication: a definition, social causes, and future concerns. Ophelia 41: 199-219., Kemp et al. 2005KEMP WM, BOYNTON WR, ADOLF JE & BOESCH DF. 2005. Eutrophication of Chesapeake Bay: historical trends and ecological interactions. Mar Ecol Progr Ser 303: 1-29.), resulting in habitat degradation, fragmentation of native populations, biodiversity loss, as well as high levels of pollutants, including highly toxic mercury (Hg) (Levin et al. 2001LEVIN LA, BOSCH DF, COVICH A & DAHM C. 2001. The function of marine critical transition zones and the importance of sediment biodiversity. Ecosystems 4: 430-451., Meyer & Medeiros 2017MEYER U & MEDEIROS C. 2017. Mercury in the Santa Cruz Channel, NE Brazil - A potential risk.Trop Oceanogr 45: 58-75.).

Trace concentrations of Hg occurs naturally in the environment, but abnormal concentrations are due to anthropogenic actions, mostly from chemical and electro-electronic industry, solid waste disposal, mining, and burning of fossil fuels. These activities increase Hg concentrations particularly in coastal ecosystems (Ferreira et al. 2004FERREIRA AG, FARIA VV, CARVALHO CEV, LESSA RPT & SILVA FMS. 2004. Total mercury in the night shark, Carcharhinus signatus in the western equatorial Atlantic Ocean. Brazil Arch Biol Technol 47: 629-634., Fitzgerald et al. 2007FITZGERALD WF, LAMBORG CH & HAMMERSCHMIDT CR. 2007. Marine biogeochemical cycling of mercury. Chem Rev 107: 641-662.). Owing to its high toxicity, strong bioaccumulation and biomagnification through food chains, Hg is recognized as one of the most potentially hazardous pollutant in the marine environment (Dias et al. 2008DIAS ACL, GUIMARÃES JRD, MALM O & COSTA PAS. 2008. Mercúrio total em músculo de cação Prionace glauca (Linnaeus, 1758) e de espadarte Xiphias gladius Linnaeus, 1758, na costa sul-sudeste do Brasil e suas implicações para a saúde pública. Cad Saúd Públ 24: 2063-2070.). Therefore, the use of long-lived, high trophic level aquatic organisms represents an essential tool to monitor changes in Hg environmental levels, as well as Hg exposure to humans consuming them (Verhaert et al. 2019VERHAERT V ET AL. 2019. Bioaccumulation and trophic transfer of total mercury in the subtropical Olifants River Basin, South Africa. Chemosphere 216: 832-843.).

Elasmobranchs, a long-lived, predatory group of fish, often show high Hg concentrations (Wang & Wang 2019WANG X & WANG W-X. 2019. The three ‘B’ of fish mercury in China: Bioaccumulation, biodynamics and biotransformation. Environ Pollut 250: 216-232., Bezerra et al. 2019BEZERRA MF, LACERDA LD & LAI CT. 2019. Trace metals and persistent organic pollutants contamination in batoids (Chondrichthyes: Batoidea): A systematic review. Environ Pollut 248: 684-695.). Characteristics like slow growth, late maturation, and high trophic level presented by elasmobranchs contribute to increasing the accumulation of contaminants (Gelsleichter & Walker 2010GELSLEICHTER J & WALKER CJ. 2010. Pollutant exposure and effects in sharks and their relatives. In: Carrier JC, Musick JA & Heithaus MR (Eds), Sharks and their Relatives II: Biodiversity, Adaptive Physiology, and Conservation. CRC Press, p. 491-537.). Despite that, elasmobranchs are widely consumed in Brazil (Bornatowski et al. 2018BORNATOWSKI H, BRAGA RR & BARRETO RP. 2018. Elasmobranchs consumption in Brazil: impacts and consequences. In: Advances in Marine Vertebrate Research in Latin America, Coastal Research Library 22: 251-262., Marques et al. 2019MARQUES RA, JULIO TG, SOLE-CAVA AM & VIANNA M. 2019. A new strategy proposal to monitor ray fins landings in south-east Brazil. Aquat Conser Mar Freshwat Ecosyst 30: 68-85.), which contribute to increasing human exposure to Hg, since diet is the main source of Hg contamination (Castro-González & Méndez-Armenta 2008CASTRO-GONZÁLEZ MI & MÉNDEZ-ARMENTA M. 2008. Heavy metals: Implications associated to fish consumption. Environ Toxicol Pharmacol 26: 263-271.). Therefore, this study investigated the occurrence and variability Hg concentrations in two coastal elasmobranchs (the ray H. guttatus and the shark R. porosus) with different life strategies, caught off the coast of Recife, State of Pernambuco, NE Brazil, where these species are the most caught elasmobranchs by local fishermen. The observed Hg contents are interpreted taking into consideration biological and geographical parameters.

The state of Pernambuco has a human population of about 4.2 million inhabitants living in the coastal zone, with a high density of 1,017 inhabitants/km2 (IBGE 2018IBGE. 2018. Estimativas da população para Estados e Municípios com data de referência em 1º de julho de 2018. Instituto Brasileiro de Geografia e Estatística, Resolução Nº 2, de 28 de agosto de 2018. Diário Oficial da União (Seção 1), Nº 167 (29/08/2018), p. 55-78.), such an anthropogenic pressure led to a high degree of urbanization, mostly in the metropolitan area of the state capital, Recife. Several changes in the past decades due to unplanned development have led to decreased environmental quality (Sant’Anna et al. 2001). Above all, an unusual, elevated population growth rate as well as accelerated harbor and industrial facilities occurred in the past two decades (Lima & Quinamo 1998LIMA T & QUINAMO T. 1998. Características sócio-econômicas. In: Gerenciamento ambiental participativo. PADCT-CIAMB FINEP/ FUNDAJ/UFPE/UFRPE, Recife, p. 115-132.). Notwithstanding, many estuaries, like the Santa Cruz Channel, are biological diverse and highly productive and support abundant fisheries of both finfish and shellfish. Taking this into consideration, we hypothesized that Hg concentrations in and the respective human exposure from local sharks and rays, shall be higher in the region compared to other sites along the Brazilian coast and, therefore, that elasmobranchs do reflect environmental Hg levels. We size-adjusted Hg concentrations to consider differences associated with fish age/length and to allow comparisons with previous studies.

MATERIALS AND METHODS

From 2014 to 2018, specimens of H. guttatus (n = 24) and of R. porosus (n = 24) were collected from fishers (stations 1 to 5) or acquired in fishing landings in Ponta das Pedras, Itamaraca and Brasília Teimosa, in the metropolitan area of Recife (Figure 1). Biometric data were recorded for all individuals and included total length (TL, cm) for the shark and disk width (DW, cm) for the ray, weight (g) and sex. Duplicate samples of muscle tissues were also taken from each individual. Fish age (in years) was estimated using the inverted von Bertalanffy growth model (Sparre & Venema 1997SPARRE P & VENEMA SC. 1997. Introducción a la evaluación de recursos pesqueros tropicales (No. 04; SH327. 5, S63). Food and Agriculture Organization – FAO, Roma.) with the equation proposed by Santos (2017)SANTOS AMA. 2017. Idade e crescimento da raia Dasyatis guttata (Bloch & Schneider, 1801) capturada em Pernambuco. Monografia - Universidade Federal Rural de Pernambuco, Recife. for H. guttatus and by Lessa et al. (2009)LESSA RP, SANTANA FM & ALMEIDA ZS. 2009. Age and growth of the Brazilian sharpnose shark, Rhizoprionodon lalandii and Caribbean sharpnose shark, R. porosus (Elasmobranchii, Carcharhinidae) on the northern coast of Brazil (Maranhão). Pan-Am J Aquat Sci 4: 532-544. for R. porosus.

Figure 1
The Pernambuco coast where rays (H. guttatus) and sharks (R. porosus) were obtained from local fishers (stations 1 to 5) and fish landings (Villages I, II, III).

All samples were freeze-dried (Terroni, model Enterprise II), weighed (~0.5 g) in Teflon vessels adding 10 mL of HNO3 (65%). Prior to digestion, samples were left at room temperature for 1 h. Then, digestion was carried out in a microwave accelerated reaction system (MARS, CEM Corporation) at 200 °C for 30 min. Following digestion, 1 mL of H2O2 was added to each vessel, transferred to 100-mL volumetric flask. Total Hg concentrations were quantified by cold vapor atomic absorption spectrometer (CV-AAS) (model NIC RA-3, NIPPON).

Under the operational conditions described, the analytical detection limit of the method (DL) was 0.1 ng g−1, based on the ratio between three standard deviation estimated by Sy/x (Sy/x ¼ = {∑(y1 – y)2 (n – 2)-1}1/2) and the slope of the regression line of the calibration curve (Miller & Miller, 1993MILLER JC & MILLER JN. 1993. Statistics for analytical chemistry. New York: Ellis Horwood and Prentice Hall, 115 p.). Quality control was performed by the analysis of certified reference materials (TORT–2 - lobster hepatopancreas, 0.27 ± 0.06 ng.g-1 and DOLT-3 – dogfish liver, 3.37 ± 0.14 ng.g-1) average recovery of standards was 89.1% (77.5% - 101.2%). We only accepted a minimum of 85% recovery; thus we have discarded the sample batch that gave 77.5%.

Bioaccumulation curves were built to compare biometric data and Hg concentration in each species. Concentrations on a wet weight basis, for estimation of exposure risk and literature comparisons, were obtained using the specific water content for each species: 76% in H. guttatus and 75% in R. porosus which were similar to published values for these species (Rabelo 2017RABELO JN. 2017. Concentração de mercúrio total nas raias Hypanus americanus e Hypanus guttatus e avaliação de risco pelo seu consumo. Dissertação de Mestrado, Universidade Federal do Ceará, Fortaleza. (Unpublished)., Magalhães et al. 2007MAGALHÃES MC, COSTA V, MENEZES GM, PINHO MR, SANTOS RS & MONTEIRO LR. 2007. Intra- and inter-specific variability in total and methylmercury bioaccumulation by eight marine fish species from the Azores. Mar Pollut Bull 54: 1654-1662., Escobar-Sánchez et al. 2016ESCOBAR-SÁNCHEZ O, RUELAS-INZUNZA J, MORENO-SÁNCHEZ XG, ROMO-PIÑERA AK & FRÍAS-ESPERICUETA MG. 2016. Mercury concentrations in Pacific angel sharks (Squatina californica) and prey fishes from southern Gulf of California, Mexico. Bull Environ Contam Toxicol 96: 15-19.).

Health risk associated with the ingestion of fish from the studied area was assessed by equation (1), reported by Newman & Unger (2002)NEWMAN MC & UNGER MA. 2002. Fundamentals of ecotoxicology. Lewis Publishers, Boca Raton, 376 p..

HQ = E / RfD Eq. 1.

Where, HQ is the risk coefficient, E is the level of exposure or Hg intake and RfD is the reference dose for Hg (Hg = 0.47 µg.kg-1 body weight/day (BCS 2007BCS. 2007. Human health risk assessment of mercury in fish and health benefits of fish consumption. Bureau of Chemical Safety, Food Directorate, Health Products and Food Branch, 76 p. Ontario. http://hc-sc.gc.ca/fn-an/pubs/mercur/merc_fish_ poisson_e.html. Assessed on 21 November 2019.
http://hc-sc.gc.ca/fn-an/pubs/mercur/mer...
). Exposure level (E) was calculated using the equation (2).

E = C I / W Eq. 2.

Where, C is the concentration of Hg (µg.g-1 wet weight); I is the ingestion rate per capita (35.6 g day-1; Sartori & Amancio 2012SARTORI AGO & AMANCIO RD. 2012. Pescado: importância nutricional e consumo no Brasil. Segur Alimen Nutr 19: 83-93.) and W is the average weight of an adult (70 kg). At HQ < 1.0 exposure level is smaller than the reference dose; meaning that daily exposure to this level is unlikely to cause adverse effects to consumers.

The normality of the data was evaluated by the Shapiro–Wilk test and the homoscedasticity by the Levene test. Spearman correlation was used for non-normal data, while Pearson correlation was used for normal and homocedastic data. ANOVA followed by the post-hoc Tukey test was used for comparing Hg concentrations and biometric data in H. guttatus from different sampling sites and a Mann-Whitney test in the case of R. porosus. The level of significance for all tests was 95%. Statistical tests and graphs were done with IBM SPSS v.20 and Microsoft® Office Excel 2010.

RESULTS

Table I summarizes the biometric and Hg concentration averages obtained for the two elasmobranch species studied, whereas Supplementary Material - Table SI and Table SII shows the figures for every individual analyzed. A sample of 24 individuals of R. porosus were collected (14 females and 10 males) with total length varying from 33.3 and 79.5 cm (mean = 42 ± 3 cm) and weight from 125 to 1,900 g (mean = 272 ± 114 g). The youngest shark was 0.3 years-old and the oldest 5.4 years (mean age = 1.0 ± 0.3 years). Muscle tissues Hg concentrations ranged from 40 to 1,020 ng.g-1 w.w. (median = 125; mean = 124 ± 48 ng.g-1 w.w.). The risk coefficient (HQ) varied from 0.043 to 1.104 in R. porosus (mean HQ = 0.220) and did not surpass the reference level of exposure. Nonetheless, the largest and oldest individual showed an HQ above the reference level (Supplementary Material - Figure S1). There was no significant difference between Hg concentrations found in male and female sharks (U = 47; p > 0.05). Also, no significant differences in Hg concentrations were detected between sampling sites (U = 46; p > 0.05) (Figure S1). The highest Hg concentrations were found in the Itamaracá site, where the oldest individuals were found. The lack of significant differences in Hg concentrations among sampling sites suggests that sharks respond to a regional “coastal-wide” geographical area, rather than local sampling sites.

Table I
Biometrics, Hg concentrations (mean ± standard deviation) and exposure risk (HQ) from of sharks (R. porosus) and stingrays (H. guttatus) from the Pernambuco coast in Northeastern Brazil. TL= total length and DW= Disk width.

A significant (p < 0.01) exponential relationship was obtained between age and Hg concentrations in R. porosus from the Pernambuco coast (Figure 2). Mercury concentrations were particularly high in large individuals older than 3.5 years. An exception was 52.7 cm individual, aged 2.5 years, that presented 485 ng.g-1 of Hg.

Figure 2
Relationship between total length and Hg concentrations in R. porosus from different sampling sites along the Pernambuco coast in NE Brazil.

Biometry of the 24 individuals (13 females and 11 males) of H. guttatus varied between 34 and 67 cm DW (50 ± 2 cm), whereas age varied between 2.1 to 9.1 years (4.9 ± 0.4 years). The Hg concentrations in H. guttatus varied between 129 to 2,130 ng.g-1 w.w. (919 ± 139 ng.g-1 w.w.); up to seven times higher than those measured in the shark R. porosus. No significant differences were found between sex (U = 49; p > 0.05). However, different from sharks, stingrays sampled in Ponta de Pedras and Barra de Catuama, located in the northern part of the Santa Cruz Channel, showed significantly higher Hg concentrations (H = 16; p < 0.05). Stingrays from Ponta de Pedras presented the highest Hg levels (1,792 ± 180 ng.g-1), similar (P > 0.05) to Barra Catuama (1,580 ± 215 ng.g-1) (Figure S1). In fact the majority of the sampled individuals of H. guttatus from these two sites presented Hg concentrations above the legal limits for human consumption of 1,000 ng.g-1 w.w.

Unlike R. porosus, H. guttatus did not show significant correlations (p > 0.05) between Hg concentrations with size or age (Figure 3). The extremely high Hg concentrations found in rays from the inner reaches of the Santa Cruz Canal, where Ponta de Pedras and Barra de Catuama are located, would mask any relationship between Hg concentrations and animal size. This suggests that stingrays respond to local, rather than regional, Hg concentrations.

Figure 3
Relationship between disk width and Hg concentrations in H. guttatus sampled from the Pernambuco coast, NE Brazil.

The risk coefficient (HQ) varied from 0.14 to 2.30 in rays (average 1.07). In contrast to R. porosus, H. guttatus presented a higher HQ average, exceeding the reference level of exposure. About 50% of individuals presented HQ that can cause adverse effects to consumers (HQ > 1), whereas 16% exhibited HQ two times higher than the reference dose.

DISCUSSION

The small inshore shark Rhizoprionodon porosus is distributed over the western continental shelf of the Atlantic Ocean from Florida to South America (Gomes et al. 2010GOMES UL, SIGNORI C, GADIG OBF & SANTOS HRS. 2010. Guia para identificação de tubarões e raias do Rio de Janeiro. Rio de Janeiro, Technical Books, 234 p.). It inhabits sandy bottoms from inshore and offshore waters down to about 90 m deep (Montealegre-Quijano 2002MONTEALEGRE-QUIJANO S. 2002. Idade, crescimento e análise demográfica do cação Rhizoprionodon porosus (Poey, 1861) (Elasmobranchii: Carcharhinidae) na plataforma continental do estado de Pernambuco, Brasil. Dissertação de Mestrado, Universidade Federal de Pernambuco, Recife. (Unpublished).) and is considered an opportunistic predator feeding on fish, mostly from the Stromateidae, Trichiuridae, Sciaenidae, Engraulidae, Tetraodontidae, Clupeidae and Batracoididae, squids, crabs and shrimps. Males and females do not differ in feeding habits (Silva & Almeida 2001SILVA CML & ALMEIDA ZF. 2001. Alimentação de Rhizoprionodon porosus (Elasmobranchii: Carcharhinidae) da costa do Maranhão, Brasil. Bol Inst Pesca 27: 201-207.), which may explain the non-significant difference of Hg concentrations between sexes since the main source of Hg is through diet (Hall et al. 1997HALL BD, BODALY RA, FUDGE RJP, RUDD JWM & ROSENBERG DM. 1997. Food as the dominant pathway of methylmercury uptake by Fish. Water Air Soil Pollut 100: 13-24.). Biometric data (total length and total weight) of R. porosus from Pernambuco characterize a typically mature population of females and subadult males (Mattos et al. 2001MATTOS SMG, BROADHURST MK, HAZIN FHV & JONNES DM. 2001. Reproductive biology of the Caribbean sharpnose shark, Rhizoprionodon porosus, from northern Brazil. Mar Freshwat Res 52: 745-752., Mattos & Pereira 2002MATTOS SMG & PEREIRA JA. 2002. Parâmatros de crescimento do tubarão Rabo-Seco, Rhizoprionodon porosus (POEY, 1861), no litoral do Estado de Pernambuco, Brasil. Arq Ciênc Mar 35: 57-66.).

There was no difference in Hg concentrations between sampling locations, which is expected since this species forages along the entire coast, on the continental shelf (Montealegre-Quijano 2002MONTEALEGRE-QUIJANO S. 2002. Idade, crescimento e análise demográfica do cação Rhizoprionodon porosus (Poey, 1861) (Elasmobranchii: Carcharhinidae) na plataforma continental do estado de Pernambuco, Brasil. Dissertação de Mestrado, Universidade Federal de Pernambuco, Recife. (Unpublished).). According to Gadig (2001)GADIG OBF. 2001.Tubarões da Costa Brasileira. Tese de doutorado, Unesp, campus de Rio Claro, São Paulo, 343 p., this shark exhibits a predominantly coastal pattern, presenting continuous distribution throughout the continental shelf, apparently without a zoogeographic barrier that interrupts its distribution. It may migrate to deeper waters during summer, coming back to shallow areas for reproduction (Menni & Lessa 1998MENNI RC & LESSA RP. 1998. The Chondrichthyan community off Maranhão (northeastern Brazil). II Biology of species. Acta Zool Lilloana 44: 69-89., Mattos et al. 2001MATTOS SMG, BROADHURST MK, HAZIN FHV & JONNES DM. 2001. Reproductive biology of the Caribbean sharpnose shark, Rhizoprionodon porosus, from northern Brazil. Mar Freshwat Res 52: 745-752.).

These ecological characteristics suggest that any eventual differences in Hg concentrations among individuals are related to biological variables, particularly size and age, as clearly shown in Figures 2 and 3. This in agreement with other studies on this species which also observed significant positive correlations between size and Hg content, as well as on shark species with similar ecology as R. porosus from other coastal areas worldwide (Fisk et al. 2002FISK AT, TITTLEMIER SA, PRANSCHKE JL & NORSTROM RJ. 2002. Using anthropogenic contaminants and stable isotopes to assess the feeding ecology of Greenland shark. Ecology 83: 2162-2172., Frías-Espericueta et al. 2019FRÍAS-ESPERICUETA MG, RUELAS-INZUNZA J, BENÍTEZ-LIZÁRRAGA R, ESCOBAR-SÁNCHEZ O, OSUNA-MARTÍNEZ CC, DELGADO-ALVAREZ CG & VOLTOLINA D. 2019. Risk assessment of mercury in sharks (Rhizoprionodon longurio) caught in the coastal zone of Northwest Mexico. J Cons Protec Food Saf 14: 349-354., Hurtado-Banda et al. 2012HURTADO-BANDA R, GOMEZ-ALVAREZ A, MARQUEZ-FARIAS JF, CORDOBA-FIGUEROA M, NAVARRO-GARCIA G & MEDINA-JUAREZ LA. 2012. Total mercury in liver and muscle tissue of two coastal sharks from the Northwest of Mexico. Bull Environ Contam Toxicol 88: 971-975., Lacerda et al. 2000LACERDA LD, PARAQUETTI HHM, MARINS RV, REZENDE CE, ZALMON IR, GOMES MP & FARIAS V. 2000. Mercury content in shark species from the south-eastern Brazilian coast. Rev Brasil Biol 60: 571-576., Rumbold et al. 2014RUMBOLD D, WASNO R, HAMMERSCHLAG N & VOLETY A. 2014. Mercury accumulation in sharks from the coastal waters of southwest Florida. Arch Environ Contam Toxicol 67: 402-412.). As a result, R. porosus Hg contents reflect the regional, coastal-wide, scale environmental Hg levels of the eastern coast of NE Brazil, and thus allows interregional comparisons (Table II).

Table II
Reported Hg concentrations, size and location of American and Caribbean sharpnose in sharks Rhizoprionodon spp. and stingrays Hypanus spp. * rounded to unit.

In Rio de Janeiro, SE Brazil (lat. 21º27’S; long. 41º00’W), Lacerda et al. (2000)LACERDA LD, PARAQUETTI HHM, MARINS RV, REZENDE CE, ZALMON IR, GOMES MP & FARIAS V. 2000. Mercury content in shark species from the south-eastern Brazilian coast. Rev Brasil Biol 60: 571-576., reported total Hg concentrations in R. porosus varying from 1.8 to 21.3 ng.g-1 w.w. (Average 9.9 ng.g-1 w.w.), but individual’s size varied from 26 to 50 cm, characterizing that population as juveniles. More recently, Amorim-Lopes et al. (2020)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. Elem Sci Anthr 8: 22. https://doi.org/10.1525/elementa.022.
https://doi.org/10.1525/elementa.022...
reported much higher Hg concentrations for this species in the same region (80 to 370 ng.g-1 w.w.). Individuals, however, were much larger, but yet juveniles (43 – 52 cm). In Ceará State, in the western coast of NE, Brazil, one large individual (85 cm) of the species showed Hg concentrations of about 509 ng.g-1 w.w. (Lacerda et al. 2016LACERDA LD, BEZERRA MF, COSTA BGB, BRAGA TM & GOYANNA FA. 2016. Mercury distribution in fish commercialized at the mucuripe market, Fortaleza, Ceará state, Brazil. Arq Ciênc Mar 49: 50-54.). These results suggest the Pernambuco population, considering their size range, presents higher Hg concentrations that those previously reported in SE Brazil, and similar to other NE coastal areas.

Published studies on Hg concentrations in R. porosus and other sharpnose sharks (Rhizoprionodon spp.), from other regions in the Americas (Table II), shows that sharks of similar size range of the Pernambuco population, fall into a similar range of concentrations, with a few exceptions, generally including larger individual. Mercury concentrations in Americas sharpnose sharks, however, are relatively higher than other Rhizoprionodon species studied in other regions. For example, Tarassoli et al. (2012)TARASSOLI A, ESMAILI SA & VALINASSAB T. 2012. An investigation of mercury bioaccumulation and its relation with selenium in the muscle and liver tissues of milk shark (Rhizoprionodon acutus). J Envrion Stud 38: 37-46. analyzed twenty-two individuals of R. acutus with an average body length of 73.38 cm (similar to those from this present study) from the Persian Gulf (Bandar Abbas coastal), and reported much lower Hg concentrations with an average of 70 ng.g-1 w.w..

Hypanus guttatus is a demersal coastal marine ray, widely distributed in shallow tropical and subtropical waters down to ~35 m deep, found in estuarine sandy and muddy bottoms. Juveniles of H. guttatus live in higher salinity environments while adults prefer lower salinity environments, including intertidal zones (Bigelow & Schroeder 1953BIGELOW HB & SCHROEDER WC. 1953. Fishes of the Gulf of Maine. v. 53. Washington, DC: US Government Printing Office, 588 p., Figueiredo 1977FIGUEIREDO JL. 1977. Manual de peixes marinhos do sudeste do Brasil. I. Introdução. Cações, Raias e Quimeras. São Paulo, SP, Museu de Zoologia, Universidade de São Paulo, 104 p., Menni & Lessa 1998MENNI RC & LESSA RP. 1998. The Chondrichthyan community off Maranhão (northeastern Brazil). II Biology of species. Acta Zool Lilloana 44: 69-89., Yokota & Lessa 2007YOKOTA L & LESSA RP. 2007. Reproductive biology of three ray species: Gymnura micrura (Bloch & Schneider, 1801), Dasyatis guttata (Bloch & Schneider, 1801) and Dasyatis marianae Gomes, Rosa & Gadig, 2000, caught by artisanal fisheries in Northeastern Brazil. Cah Biol Mar 48: 249-257., Gomes et al. 2010GOMES UL, SIGNORI C, GADIG OBF & SANTOS HRS. 2010. Guia para identificação de tubarões e raias do Rio de Janeiro. Rio de Janeiro, Technical Books, 234 p., Gianeti 2011GIANETI MD. 2011. Reprodução, alimentação, idade e crescimento de Dasyatis guttata (Block & Schneider, 1801) (Elasmobranchii; Dasyatidae) na região de Caiçara do Norte – RN. Tese de Doutorado, Universidade de São Paulo, São Paulo., Melo 2016MELO ACM. 2016. Biologia reprodutiva e pesca da raia Dasyatis guttata (Block & Schneider, 1801) (Elasmobranchii: Dasyatidae) na plataforma continental de Pernambuco, Brasil. Dissertação de Mestrado, Universidade Federal Rural de Pernambuco, Recife. (Unpublished).). In Pernambuco there is a bottom gillnet fishing directed to the rays displaying an average height of 10 to 20 meshes, called “raieira” (Lira et al. 2010LIRA L, MESQUITA B, SOUZA MMC, LEITE CA, LEITE APA, FARIA AM & GALVÃO C. 2010. Diagnóstico da pesca artesanal do litoral de Pernambuco. Recife, Instituto Oceanário de Pernambuco: Departamento de Pesca e Aquicultura, 116 p., Vieira 2013VIEIRA RS. 2013. Estrutura Populacional (idade e tamanhos) e Crescimento da raia-lixa Dasyatis guttata (Bloch & Schneider, 1801), capturada no Nordeste do Brasil. Dissertação de Mestrado, Universidade Federal Rural de Pernambuco – PE, 76 p. (Unpublished).). Biometric data of disk width and total weight of H. guttatus also characterize a typical population with age range previously reported for the region, mostly constituted by adults and sub-adults (Melo 2016MELO ACM. 2016. Biologia reprodutiva e pesca da raia Dasyatis guttata (Block & Schneider, 1801) (Elasmobranchii: Dasyatidae) na plataforma continental de Pernambuco, Brasil. Dissertação de Mestrado, Universidade Federal Rural de Pernambuco, Recife. (Unpublished)., Santos 2017SANTOS AMA. 2017. Idade e crescimento da raia Dasyatis guttata (Bloch & Schneider, 1801) capturada em Pernambuco. Monografia - Universidade Federal Rural de Pernambuco, Recife., Queiroz 2017QUEIROZ APN. 2017. Ecologia alimentar de Dasyatis guttata (Bloch & Schneider, 1801) (Dasyatidae: Myliobatoidei) capturada pela pesca artesanal no litoral de Pernambuco, Brasil. Dissertação - Universidade Federal de Pernambuco. Recife. (Unpublished).). It is believed that the shallower areas are visited by adult individuals for feeding and/or reproduction (Vieira 2013VIEIRA RS. 2013. Estrutura Populacional (idade e tamanhos) e Crescimento da raia-lixa Dasyatis guttata (Bloch & Schneider, 1801), capturada no Nordeste do Brasil. Dissertação de Mestrado, Universidade Federal Rural de Pernambuco – PE, 76 p. (Unpublished).).

Compared to other areas in the Brazilian coast, concentrations found in stingrays from the Pernambuco coast, like sharpnose sharks, are in general higher than previously reported elsewhere and are also the highest ever reported for the Atlantic Ocean and the North Pacific Ocean (Table II).

Lacerda et al. (2016)LACERDA LD, BEZERRA MF, COSTA BGB, BRAGA TM & GOYANNA FA. 2016. Mercury distribution in fish commercialized at the mucuripe market, Fortaleza, Ceará state, Brazil. Arq Ciênc Mar 49: 50-54. reported average Hg concentration of 83.4 ng.g-1 w.w. in a large (84 cm) individual of H. guttatus from the Ceará coast. Similarly, Moura et al. (2020)MOURA VL ET AL. 2020. Ecological and biological factors associated to mercury accumulation in batoids (Chondrichthyes: Batoidea) from northeastern Brazil. Mar Pollut Bull 161: 111761. reported an average Hg concentration for a sample of 17 individuals, also from the Ceará coast, with mean DW of 34.3 cm, of 56 ng g-1 w.w., even considering the larger average size of the Pernambuco population (51.6 cm) the overall average Hg concentration of 993 ng g-1 w.w., from all sampling sites, is about 20 times higher than in the Ceará population.

Globally, Hg concentrations found in H. guttatus from Pernambuco is the second highest ever reported worldwide among batoid species (Bezerra et al. 2019BEZERRA MF, LACERDA LD & LAI CT. 2019. Trace metals and persistent organic pollutants contamination in batoids (Chondrichthyes: Batoidea): A systematic review. Environ Pollut 248: 684-695.), with values near the maximum found in the Mediterranean Sea, where Hg concentrations varied from 86 to 2,420 ng.g-1 w.w. among 559 specimens belonging to 10 species (Rajar et al. 2007RAJAR R, CETINA M, HORVAT M & ZAGAR D. 2007. Mass balance of mercury in the Mediterranean Sea. Mar Chem 107: 89-102.). The minimum value found in Pernambuco, however, is still 1.5 times higher than the lowest concentrations found in that study.

Figure 4 compared Hg concentrations in R. porosus and H. gutattus sampled from the Pernambuco coast. Stingrays showed significantly higher (P < 0.05) Hg concentrations than those observed in sharpnose sharks.

Figure 4
Box-and-whisker plots of Hg concentration in R. porosus and H. guttatus from the coast of Pernambuco, northeastern Brazil.

These higher Hg concentrations in H. guttatus reflect the relatively low mobility of the species and benthic habits, relative to R. porosus (Machado et al. 2016MACHADO AA, SPENCER K, KLOAS W, TOFFOLON M & ZARFL C. 2016. Metal fate and effects in estuaries: A review and conceptual model for better understanding of toxicity. Sci Total Environ 541: 268-281.). In addition, H. gutattus inhabits historically Hg contaminated site of the Pernambuco coast, the Ponta de Pedras and Barra de Catuama, located in the northern part of the Santa Cruz Channel, a highly contaminated spot by past emissions Hg-rich effluents from a chlor-alkali plan, presently decommissioned. High concentrations of Hg in sediment, oysters and suspended particles were previously reported by Meyer & Medeiros (2017)MEYER U & MEDEIROS C. 2017. Mercury in the Santa Cruz Channel, NE Brazil - A potential risk.Trop Oceanogr 45: 58-75.. Also, the region harbors over 6,650 ha of mangroves (Guimarães et al. 2010GUIMARÃES AS, TRAVASSOS P, SOUZA FILHO PWME & GONCALVES FD. 2010. CostaI impact of aquaculture on mangrove areas in the northern Pernambuco Coast (Brazil) using remote sensing and geographic information system. Aquac Res 41: 828-838.) and these regions have been characterized as significant sources of organic-bound Hg, including methyl-Hg, to estuaries and coastal waters (Lacerda et al. 2020LACERDA LD, MARINS RV & DIAS FJS. 2020. An Arctic Paradox: Response of fluvial hg inputs and bioavailability to global climate change in an extreme coastal environment. Front Earth Sci 8: 93. https://doi.org/10.3389/feart.2020.00093.
https://doi.org/10.3389/feart.2020.00093...
), and this may contribute to the high Hg burdens in rays. Adult H. guttatus differently for juveniles inhabit in estuarine areas, such as the Botafogo Channel, foraging in contact with the sediment and using the snout to dig for food being more exposed to Hg present in sediments (Melo 2016MELO ACM. 2016. Biologia reprodutiva e pesca da raia Dasyatis guttata (Block & Schneider, 1801) (Elasmobranchii: Dasyatidae) na plataforma continental de Pernambuco, Brasil. Dissertação de Mestrado, Universidade Federal Rural de Pernambuco, Recife. (Unpublished)., Santos 2017SANTOS AMA. 2017. Idade e crescimento da raia Dasyatis guttata (Bloch & Schneider, 1801) capturada em Pernambuco. Monografia - Universidade Federal Rural de Pernambuco, Recife.). Also, older individuals were more frequent in the sample of H. guttatus than in R. porosus, resulting in longer Hg exposure and accumulation (Costa et al. 2009COSTA MF, BARBOSA SCT, BARLETTA M, DANTAS DV, KEHRIG HA, SEIXAS TG & MALM O. 2009. Seasonal differences in mercury accumulation in Trichiurus lepturus (Cutlassfish) in relation to length and weight in a Northeast Brazilian estuary. Environ Sci Pollut Res 16: 423-429., Lyons et al. 2017LYONS K, CARLISLE AB & LOWE CG. 2017. Influence of ontogeny and environmental exposure on mercury accumulation in muscle and liver of male Round Stingrays. Mar Environ Res 130: 30-37., Rabelo 2017RABELO JN. 2017. Concentração de mercúrio total nas raias Hypanus americanus e Hypanus guttatus e avaliação de risco pelo seu consumo. Dissertação de Mestrado, Universidade Federal do Ceará, Fortaleza. (Unpublished)., Murillo-Cisneros et al. 2018MURILLO-CISNEROS DA ET AL. 2018. Mercury concentrations in three ray species from the Pacific coast of Baja California Sur, Mexico: Variations by tissue type, sex and length. Mar Polut Bull 126: 77-85.). Trophic level may not be significant influencing the different Hg concentrations between these elasmobranchs. Trophic level of H. guttatus range from 2.6 (Froese & Pauly 2018FROESE R & PAULY D. 2018. Fish base. Disponível em: <www.fishbase.org>. Acessed on 23 jun. 2018.
www.fishbase.org...
) to 3.67 (Queiroz 2017QUEIROZ APN. 2017. Ecologia alimentar de Dasyatis guttata (Bloch & Schneider, 1801) (Dasyatidae: Myliobatoidei) capturada pela pesca artesanal no litoral de Pernambuco, Brasil. Dissertação - Universidade Federal de Pernambuco. Recife. (Unpublished).) and the trophic level of R. porosus range from 3.5 (Froese & Pauly 2018FROESE R & PAULY D. 2018. Fish base. Disponível em: <www.fishbase.org>. Acessed on 23 jun. 2018.
www.fishbase.org...
) to 4.0 (Peña 2018PEÑA LVG. 2018. Ecología trófica de cuatro especies de tiburones mediante el análisis de contenido estomacal y el uso de isotopos estables en el caribe colombiano. Monografia. Universidad De Bogotá Jorge Tadeo Lozano). Rather preference of preys closely associated with sediment, like benthic fish, are more susceptible to Hg accumulation than consumers of pelagic fish or benthic invertebrates (Storelli et al. 1998STORELLI MM, STUFFLER GR & MARCOTRIGIANO GO. 1998. Total mercury in muscle of benthic and pelagic fish from the South Adriatic Sea (Italy). Food Addit Contam 15: 876-883., 2002STORELLI MM, STUFFLER GR & MARCOTRIGIANO GO. 2002. Total and methylmercury residues in cartilaginous fish from Mediterranean Sea. Mar Pollut Bull 44: 1354-1358.).

Since the average Hg concentrations observed in the two species are higher than those reported for other regions along the Brazilian coast, anthropogenic Hg sources, might explain this result. H. gutattus reflect site-specific contamination, in particular the chlorine and caustic soda plant, which for 25 years dumped its tailings into the Botafogo River (Sant’Anna Jr et al. 2001SANT’ANNA N, COSTA M & AKAGI H. 2001. Total and methylmercury levels of a coastal human population and of fish from the Brazilian northeast. Environ Sci Pollut Res 8: 280-284., Cavalcanti 2003CAVALCANTI AD. 2003. Monitoramento da contaminação por elementos traço em ostras comercializadas em Recife, Pernambuco, Brasil. Cad Saúd Públ 19: 1545-1551.). Meyer & Medeiros (2017)MEYER U & MEDEIROS C. 2017. Mercury in the Santa Cruz Channel, NE Brazil - A potential risk.Trop Oceanogr 45: 58-75., based on total Hg content of sediments and oysters, concluded that about 10% of the total Hg load remained in sediments, equivalent to 1.2 to 2.5 tons of Hg. Most of the emitted Hg, however, would have been exported to the sea in association with suspended solids. In addition, the large harbor and urban development densely concentrated in a short and narrow stretch of coast, may raise environmental Hg levels, as suggested by the sharpnose shark Hg content. The response of elasmobranchs to regional Hg levels has been observed elsewhere (Marcovecchio et al. 1991MARCOVECCHIO JE, MORENO VJ & PEREZ A. 1991. Metal accumulation in tissues of sharks from the Bahia Blanca Estuary, Argentina. Mar Environ Res 31: 263-274., Bezerra et al. 2019BEZERRA MF, LACERDA LD & LAI CT. 2019. Trace metals and persistent organic pollutants contamination in batoids (Chondrichthyes: Batoidea): A systematic review. Environ Pollut 248: 684-695.).

Hg-contaminated elasmobranch flesh can cause several deleterious effects on humans, including neurological and psychological symptoms such as tremors, personality changes, restlessness, anxiety, sleep disturbance, memory loss, dementia, attention deficit, depression, and impaired hearing and vision. (Järup 2003JÄRUP L. 2003. Hazards of heavy metal contamination. Brit Med Bull 68: 167-182., Zahir et al. 2005ZAHIR F, RIZWI SJ, HAQ SK & KHAN RH. 2005. Low dose mercury toxicity and human health. Environ Toxicol Pharmacol 20: 351-360., WHO 2017WHO. 2017. Mercury and health. World Health Organization. https://www.who.int/news-room/fact-sheets/detail/mercury-and-health. Accessed 15th December 2018.
https://www.who.int/news-room/fact-sheet...
). Although most Hg concentrations observed in this study were relatively low, some from stingrays, may threaten humans. Similar low concentrations may cause harm to the health of the consuming population. For example, Feitosa-Santana et al. (2018)FEITOSA-SANTANA C, SOUZA GS, SIRIUS EVP, RODRIGUES AR, CORTES MIT, SILVEIRA LCL & VENTURA DF. 2018. Color vision impairment with low-level methylmercury exposure of an Amazonian population, Brazil. Neurotoxicol 66: 179-184. observed an impairment of visual capability in a group of fish-eating adults living in the Brazilian Amazon exposed to low-to-intermediate concentrations.

Risk coefficients and provisionary intake are reliable safeguard indexes to evaluate population exposure to pollutants. The potential risk to humans from consumption of edible muscle of myliobatids, from the Eastern Gulf of California, Mexico (30 – 790 ng.g-1 w.w. Hg) is low (HQ < 1.0) (Escobar-Sánchez et al. 2016ESCOBAR-SÁNCHEZ O, RUELAS-INZUNZA J, MORENO-SÁNCHEZ XG, ROMO-PIÑERA AK & FRÍAS-ESPERICUETA MG. 2016. Mercury concentrations in Pacific angel sharks (Squatina californica) and prey fishes from southern Gulf of California, Mexico. Bull Environ Contam Toxicol 96: 15-19.), much lower than the HQ measured in stingrays from Pernambuco. Hg concentrations observed by Adams & McMichael (1999)ADAMS DH & MCMICHAEL RH. 1999. Mercury levels in four species of sharks from the Atlantic coast of Florida. Fish Bull 97: 372-379. in several commonly landed shark species, including sharpnose sharks, from SE USA, and varying in the same range of concentrations found in this study, often exceed state and federal regulatory levels, posing risk to local consumers. Dietary provisional tolerable weekly intake for sharpnose sharks Rhizoprionodon lalandii and R. porosus from Rio de Janeiro, SE Brazil, except for a single value obtained within the heavily polluted Guanabara Bay, where in the same range found in Pernambuco sharks. Risk coefficients for sharks (HQ = 0.220) and specially for stingrays (HQ = 1.07) from Pernambuco, results in higher exposure to consumers relative to published values elsewhere along the Brazilian coast.

CONCLUSION

Cartilaginous fishes (H. guttatus and R. porous) investigated in the coast of Pernambuco showed relatively high Hg concentrations in muscle tissues, compared to other regions in the South Atlantic Ocean. Contamination reflects anthropogenic Hg from point sources, as demonstrated by stingrays and diffuse emissions from urban and harbor-industrial sources, as demonstrated by sharks. Consequently, levels of Hg in fish from Pernambuco are in general higher than those reported for other fishes caught along the Brazilian coast, consequently resulting in higher exposure risk to consumers. Unfortunately, there is no statistics on the consumption rates of these species by the local population, which avoids a detailed risk analysis of human exposure. However, the observed individual values of Hg concentrations already surpassing the legal limits for safe consumption, makes a risk analysis urgent. While no permanent monitoring of Hg concentrations in elasmobranchs is available, it is important for the consumer population to diversify the fishery type in order to avoid high Hg ingestion.

ACKNOWLEDGMENTS

The present research was funded by Fundação de Amparo à Pesquisa de Pernambuco - FACEPE through the APq 1011- 5.06/15; which also provided a Master of Science Scholarship to T. Julio (IBPG 1180-2.05/16). The Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq supplied a Productivity Research Grant to RPT Lessa (Proc. 306672/15- Oc) and CNPq Proc. No. 405.244/2018-5 and Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico - FUNCAP Proc. No. INT 00159-00009.01.00/19 to LD Lacerda. Thanks are due to the Centro de Tecnologias Estratégicas do Nordeste - CETENE for the lyophilization of the samples.

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SUPPLEMENTARY MATERIAL

Figure S1.

Tables SI, SII.

Publication Dates

  • Publication in this collection
    26 July 2022
  • Date of issue
    2022

History

  • Received
    1 Jan 2022
  • Accepted
    17 Apr 2022
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