Skip to main content

Advertisement

SpringerLink
Log in

Analysis of Trace Element Concentrations and Antioxidant Enzyme Activity in Muscle Tissue of the Atlantic Sharpnose Shark, Rhizoprionodon terraenovae

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

Metals occur naturally in the environment; however, anthropogenic practices have greatly increased metal concentrations in waterways, sediments, and biota. Metals pose health risks to marine organisms and have been associated with oxidative stress, which can lead to protein denaturation, DNA mutations, and cellular apoptosis. Sharks are important species ecologically, recreationally, and commercially. Because they occupy a high trophic level, assessing muscle tissue metal concentrations in sharks may reflect metal transfer in marine food webs. In this study, concentrations of cadmium, copper, lead, nickel, selenium, silver, and zinc were measured in the muscle of Rhizoprionodon terraenovae (Atlantic sharpnose shark) from 12 sites along the coast of the southeastern United States. Activities of antioxidant enzymes (superoxide dismutase, catalase, glutathione peroxidase, and glutathione reductase) also were examined in the muscle tissue of R. terraenovae. A total of 165 samples were analyzed, and differences in trace element bioaccumulation and enzyme activity were observed across sites. R. terraenovae samples collected from South Florida and South Carolina had the highest cumulative trace element concentrations whereas those collected from North Carolina and Alabama had the lowest cumulative concentrations. Trace element concentrations in shark muscle tissue were significantly correlated to antioxidant enzyme activity, particularly with glutathione peroxidase, suggesting that this enzyme may serve as a non-lethal, biomarker of metal exposure in R. terraenovae. This is one of the most extensive studies providing reference levels of trace elements and oxidative stress enzymes in a single elasmobranch species within the U.S.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adams DH, McMichael RH Jr (1999) Mercury levels in four species of sharks from the Atlantic coast of Florida. Fish Bull 97(2):372–379

    Google Scholar 

  • Adel M, Copat C, Asl MRS, Conti GO, Babazadeh M, Ferrante M (2018) Bioaccumulation of trace metals in banded Persian bamboo shark (Chiloscyllium arabicum) from the Persian Gulf: a food safety issue. Food Chem Toxicol 113:198–203

    CAS  Google Scholar 

  • Alves LM, Nunes M, Marchand P, Le Bizec B, Mendes S, Correia JP, Lemos MF, Novais SC (2016) Blue sharks (Prionace glauca) as bioindicators of pollution and health in the Atlantic Ocean: contamination levels and biochemical stress responses. Sci Total Environ 563:282–292

    Google Scholar 

  • Amiard-Triquet C, Cossu-Leguille C, Mouneyrac C (2012) Biomarkers of defense, tolerance, and ecological consequences. Ecological biomarkers. CRC Press, Boca Raton, p 450. https://doi.org/10.1201/b13036-4

    Book  Google Scholar 

  • Bethea DM, Grace MA (2013) Tag and recapture data for Atlantic Sharpnose, Rhizoprionodon terraenovae, and Bonnethead Shark, Sphyrna tiburo, in the Gulf of Mexico and US South Atlantic: 1998–2011. SEDAR34-WP-04. SEDAR North Charleston, SC

  • Bethea DM, Carlson JK, Buckel JA, Satterwhite M (2006) Ontogenetic and site-related trends in the diet of the Atlantic sharpnose shark Rhizoprionodon terraenovae from the northeast Gulf of Mexico. Bull Mar Sci 78(2):287–307

    Google Scholar 

  • Bielmyer GK, Gatlin D, Isely JJ, Tomasso J, Klaine SJ (2005) Responses of hybrid striped bass to waterborne and dietary copper in freshwater and saltwater. Comp Biochem Physiol C: Toxicol Pharmacol 140(1):131–137

    Google Scholar 

  • Bielmyer GK, Tomasso J, Klaine SJ (2006) Physiological responses of hybrid striped bass to aqueous copper in freshwater and saltwater. Arch Environ Contam Toxicol 50(4):531–538

    CAS  Google Scholar 

  • Bielmyer-Fraser GK, Patel P, Grosell M (2018) Sublethal effects of seawater acidification and copper exposure in two coral species. Mar Pollut Bull 133:781–790

    CAS  Google Scholar 

  • Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O (2012) Oxidative stress and antioxidant defense. World Allergy Org J 5(1):9

    CAS  Google Scholar 

  • Blewett TA, Wood CM (2014) Salinity-dependent nickel accumulation and oxidative stress responses in the euryhaline killifish (Fundulus heteroclitus). Arch Environ Contam Toxicol 68(2):382–394

    Google Scholar 

  • Bosch AC, O’Neill B, Sigge GO, Kerwath SE, Hoffman LC (2015a) Heavy metal accumulation and toxicity in smoothhound (Mustelus mustelus) shark from Langebaan Lagoon, South Africa. Food Chem 190:871–878

    Google Scholar 

  • Bosch AC, O’Neill B, Sigge GO, Kerwath SE, Hoffman LC (2015b) Heavy metals in marine fish meat and consumer health: a review. J Sci Food Agric 96(1):32–48

    Google Scholar 

  • Bradl H (ed) (2005) Heavy metals in the environment: origin, interaction and remediation, vol 6. Elsevier, Amsterdam

    Google Scholar 

  • Branco V, Vale C, Canário J, dos 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. Environ Pollut 150(3):373–380

    CAS  Google Scholar 

  • Brock J, Bielmyer GK (2013) Metal accumulation and sublethal responses in the sea anemone, Aiptasia pallida after waterborne exposure to metal mixtures. Comp Biochem Physiol C 158:150–158

    CAS  Google Scholar 

  • Bury NR, Walker PA, Glover CN (2003) Nutritive metal uptake in teleost fish. J Exp Biol 206(1):11–23

    CAS  Google Scholar 

  • Carlson JK, Baremore IE (2003) Changes in biological parameters of Atlantic sharpnose shark Rhizoprionodon terraenovae in the Gulf of Mexico: evidence for density-dependent growth and maturity? Mar Freshw Res 54(3):227–234

    Google Scholar 

  • Carlson JK, Heupel MR, Bethea DM, Hollensead LD (2008) Coastal habitat use and residency of juvenile Atlantic sharpnose sharks (Rhizoprionodon terraenovae). Estuaries Coasts 31(5):931–940

    Google Scholar 

  • Close DC, Hagerman, AE (2006) What are reactive oxygen species? In Alessio HM & Hagerman AE (ed) Oxidative stress, exercise, and aging. Imperial College Press, London, pp 1–8

  • Compagno LJV (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 Fish Synop 125(4/2):251–655. FAO, Rome

  • Converse RR, Piehler MF, Noble RT (2011) Contrasts in concentrations and loads of conventional and alternative indicators of fecal contamination in coastal stormwater. Water Res 45(16):5229–5240

  • Cornish AS, Ng WC, Ho VC, Wong HL, Lam JC, Lam PK, Leung KM (2007) Trace metals and organochlorines in the bamboo shark Chiloscyllium plagiosum from the southern waters of Hong Kong, China. Sci Total Environ 376(1–3):335–345

    CAS  Google Scholar 

  • Davis MM, Suárez-Moo PDJ, Daly-Engel TS (2018) Genetic structure and congeneric range overlap among sharpnose sharks (genus Rhizoprionodon) in the Northwest Atlantic Ocean. Can J Fish Aquat Sci 76(7):1203–1211

    Google Scholar 

  • De Boeck G, Grosell M, Wood C (2000) Sensitivity of the spiny dogfish (Squalus acanthias) to waterborne silver exposure. Aquat Toxicol 54(3–4):261–275

    Google Scholar 

  • De Boeck G, Hattink J, Franklin NM, Bucking CP, Wood S, Walsh PJ, Wood CM (2007) Copper toxicity in the spiny dogfish (Squalus acanthias): urea loss contributes to the osmoregulatory disturbance. Aquat Toxicol 84(2):133–141

    Google Scholar 

  • De Boeck G, Eyckmans M, Lardon I, Bobbaers R, Sinha AK, Blust R (2010) Metal accumulation and metallothionein induction in the spotted dogfish Scyliorhinus canicula. Comp Biochem Physiol A: Mol Integr Physiol 155(4):503–508

    Google Scholar 

  • Delius B, Morgan A (2018) Rhizoprionodon Terraenovae. Retrieved from Florida Museum of Natural History.https://www.floridamuseum.ufl.edu/fish/discover/species-profiles/rhizoprionodon-terraenovae

  • de Pinho AP, Guimarães JRD, Martins AS, Costa PAS, Olavo G, Valentin J (2002) Total mercury in muscle tissue of five shark species from Brazilian offshore waters: effects of feeding habit, sex, and length. Environ Res 89(3):250–258

    Google Scholar 

  • Delorenzo DM, Bethea DM, Carlson JK (2015) An assessment of the diet and trophic level of Atlantic Sharpnose Shark Rhizoprionodon terraenovae. J Fish Biol 86(1):385–391

    CAS  Google Scholar 

  • Di Toro DM, Allen HE, Bergman HL, Meyer G, Paquin PR, Santore RC (2001) Abiotic ligand model of the acute toxicity of metals. 1. Technical basis. Environ Toxicol Chem 20:2383–2396

    Google Scholar 

  • Domi N, Bouquegneau JM, Das K (2005) Feeding ecology of five commercial shark species of the Celtic Sea through stable isotope and trace metal analysis. Mar Environ Res 60(5):551–569

    CAS  Google Scholar 

  • Drymon JM, Powers SP, Carmichael RH (2012) Trophic plasticity in the Atlantic sharpnose shark (Rhizoprionodon terraenovae) from the north central Gulf of Mexico. Environ Biol Fishes 95(1):21–35

    Google Scholar 

  • Duce RA, Hoffman GL, Zoller WH (1975) Atmospheric trace metals at remote northern and southern hemisphere sites: pollution or natural? Science 187(4171):59–61

    CAS  Google Scholar 

  • Duckworth CG, Picariello CR, Thomason RK, Patel KS, Bielmyer-Fraser GK (2017) Responses of the sea anemone, Exaiptasia pallida, to ocean acidification conditions and zinc or nickel exposure. Aquat Toxicol 182:120–128

    CAS  Google Scholar 

  • Ehnert-Russo SL, Gelsleichter J (2019) Mercury accumulation and effects in the brain of the Atlantic Sharpnose Shark (Rhizoprionodon terraenovae). Arch Environ Contam Toxicol 78:267–283

    Google Scholar 

  • 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. Mar Pollut Bull 56(10):1774–1780

    CAS  Google Scholar 

  • Ercal N, Gurer-Orhan H, Aykin-Burns N (2001) Toxic metals and oxidative stress part I: mechanisms involved in metal-induced oxidative damage. Curr Top Med Chem 1(6):529–539

    CAS  Google Scholar 

  • Escobar-Sánchez O, Galván-Magaña F, Rosíles-Martínez R (2011) Biomagnification of mercury and selenium in blue shark Prionace glauca from the Pacific Ocean off Mexico. Biol Trace Elem Res 144(1–3):550–559

    Google Scholar 

  • Espinosa-Diez C, Miguel V, Mennerich D, Kietzmann T, Sánchez-Pérez P, Cadenas S, Lamas S (2015) Antioxidant responses and cellular adjustments to oxidative stress. Redox Biol 6:183–197

  • Eyckmans M, Lardon I, Wood CM, De Boeck G (2013) Physiological effects of waterborne lead exposure in spiny dogfish (Squalus acanthias). Aquat Toxicol 126:373–381

    CAS  Google Scholar 

  • Fenton HJH (1876) On a new reaction of tartaric acid. Chem News 33:190

    Google Scholar 

  • Fenton HJH (1894) Oxidation of tartaric acid in presence of iron. J Chem Soc Trans 65:899–910

    CAS  Google Scholar 

  • Frazier BS, Driggers III WB, Ulrich GF (2015) Longevity of Atlantic Sharpnose Sharks Rhizoprionodon terraenovae and Blacknose Sharks Carcharhinus acronotus in the western North Atlantic Ocean based on tag-recapture data and direct age estimates. F1000Research 3 pp 1–9

  • Frías-Espericueta MG, Cardenas-Nava NG, Márquez-Farías JF, Osuna-López JI, Muy-Rangel MD, Rubio-Carrasco W, Voltolina D (2014) Cadmium, copper, lead and zinc concentrations in female and embryonic pacific sharpnose shark (Rhizoprionodon longurio) tissues. Bull Environ Contam Toxicol 93(5):532–535

    Google Scholar 

  • Gaion A, Scuderi A, Sartori D, Pellegrini D, Ligas A (2016) Trace metals in tissues of Galeus melastomus (Rafinesque, 1810) from the northern Tyrrhenian Sea (NW Mediterranean). Acta Adriat Int J Mar Sci 57(1):165–172

    Google Scholar 

  • Garrett RG (2000) Natural sources of metals to the environment. Hum Ecol Risk Assess 6(6):945–963

    CAS  Google Scholar 

  • Gelsleichter 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, Boca Raton, pp 491–540

    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. Environ Biol Fishes 54(2):205–217

    Google Scholar 

  • Georgia Ports Authority (2015) Economic Development Brochure. Retrieved from Georgia Ports: https://www.gaports.com/Portals/2/Documents/Brochures/GPA3852016EconDevBrochure-WEB.pdf?ver=2016-05-18-130432-000

  • Grosell M (2012) Copper. In: Wood CM, Farrell AP, Brauner CJ (eds) Homeostasis and toxicology of essential metals. Fish Physiology 31A. Academic Press, USA, pp 53–112

  • Haman KH, Norton TM, Thomas AC, Dove AD, 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 Wildl Dis 48(2):295–306

    CAS  Google Scholar 

  • Harrington T, Plumlee J, Drymon JM, Wells D (2016) Diets of Atlantic sharpnose shark (Rhizoprionodon terraenovae) and bonnethead (Sphyrna tiburo) in the northern Gulf of Mexico. Gulf Caribb Res 27(1):42–51

    Google Scholar 

  • Hendon JM, Hoffmayer ER, Parsons GR (2013) Tag and recapture data for Atlantic sharpnose, Rhizoprionodon terraenovae, and bonnethead, Sphyrna tiburo, sharks caught in the northern Gulf of Mexico from 1998–2011. SEDAR34-WP-33. SEDAR, North Charleston, SC, 6 pp

  • Hogstrand C (2012) Zinc. In: Wood CM, Farrell AP, Brauner CJ (eds) Homeostasis and toxicology of essential metals. Fish Physiology 31A. Academic Press, USA, pp 135–186

  • Hutton M (1983) Sources of cadmium in the environment. Ecotoxicol Environ Saf 7(1):9–24

    CAS  Google Scholar 

  • Imlay JA, Chin SM, Linn S (1988) Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science 240(4852):640–642

    CAS  Google Scholar 

  • Janz D (2012) Selenium. In: Wood CM, Farrell AP, Brauner CJ (eds) Homeostasis and toxicology of essential metals. Fish Physiology 31A. Academic Press, USA, pp 327–365

  • Jarvis TA, Lockhart JM, Loughry WJ, Bielmyer GK (2013) Metal accumulation in wild nine-banded armadillos. Ecotoxicology 22(6):1053–1062

    CAS  Google Scholar 

  • Kirby J, Maher W, Krikowa F (2001) Selenium, cadmium, copper, and zinc concentrations in sediments and mullet (Mugil cephalus) from the southern basin of Lake Macquarie, NSW, Australia. Arch Environ Contam Toxicol 40(2):246–256

    CAS  Google Scholar 

  • Klaassen CD (2008) Casarett and Doull’s toxicology: the basic science of poisons, 7th edn. McGraw-Hill, New York

    Google Scholar 

  • Kohler NE, Turner PA (2019) Distributions and movements of atlantic shark species: a 52-year retrospective atlas of mark and recapture data. Accessed 10 Jan 2020. https://spo.nmfs.noaa.gov/sites/default/files/pdf-content/mfr8121_0.pdf

  • Kohler NE, Bailey D, Turner PA, McCandless C (2013) Mark/Recapture Data for the Atlantic Sharpnose Shark (Rhizoprionodon terraenovae), in the Western North Atlantic from the NEFSC Cooperative Shark Tagging Program. SEDAR, North Charleston

    Google Scholar 

  • Kucuksezgin F, Kayatekin BM, Uluturhan E, Uysal N, Acikgoz O, Gonenc S (2008) Preliminary investigation of sensitive biomarkers of trace metal pollution in mussel (Mytilus galloprovincialis) from Izmir Bay (Turkey). Environ Monit Assess 141(1–3):339–345

    CAS  Google Scholar 

  • Lockhart JM, Siddiqui S, Loughry WJ, Bielmyer-Fraser GK (2016) Metal accumulation in wild-caught opossums. Environ Monit Assess 188(6):110. https://doi.org/10.1007/s10661-016-5327-y

    Article  CAS  Google Scholar 

  • Loefer JK, Sedberry GR (2003) Life history of the Atlantic sharpnose shark (Rhizoprionodon terraenovae) (Richardson, 1836) off the southeastern United States. Fish Bull 101(1):75–88

    Google Scholar 

  • López-Cruz RI, Zenteno-Savín T, Galván-Magaña F (2010) Superoxide production, oxidative damage and enzymatic antioxidant defenses in shark skeletal muscle. Comp Biochem Physiol A: Mol Integr Physiol 156(1):50–56

    Google Scholar 

  • Lopez SA, Abarca NL, Meléndez RC (2013) Heavy metal concentrations of two highly migratory sharks (Prionace glauca and Isurus oxyrinchus) in the southeastern Pacific waters: comments on public health and conservation. Trop Conserv Sci 6(1):126–137

    Google Scholar 

  • Lyle JM (1986) Mercury and selenium concentrations in sharks from northern Australian waters. Mar Freshw Res 37(3):309–321

    CAS  Google Scholar 

  • Mager E (2012) Lead. In: Wood CM, Farrell AP, Brauner CJ (eds) Homeostasis and toxicology of non-essential Metals. Fish Physiology, 31A. Academic Press, USA, pp 185–225

  • Main WPL, Ross C, Bielmyer GK (2010) Copper accumulation and oxidative stress in the sea anemone, Aiptasia pallida, after waterborne copper exposure. Comp Biochem Physiol C: Toxicol Pharmacol 151(2):216–221

    CAS  Google Scholar 

  • Malek M, Haseli M, Mobedi I, Ganjali MR, MacKenzie K (2007) Parasites as heavy metal bioindicators in the shark Carcharhinus dussumieri from the Persian Gulf. Parasitology 134(7):1053–1056

    CAS  Google Scholar 

  • Marcovecchio JE, Moreno VJ, Pérez A (1991) Metal accumulation in tissues of sharks from the Bahia Blanca Estuary, Argentina. Mar Environ Res 31(4):263–274

    CAS  Google Scholar 

  • Marreiro D, Cruz K, Morais J, Beserra J, Severo J, de Oliveira A (2017) Zinc and oxidative stress: current mechanisms. Antioxidants 6(2):24

    CAS  Google Scholar 

  • Martínez-Álvarez RM, Morales AE, Sanz A (2005) Antioxidant defenses in fish: biotic and abiotic factors. Rev Fish Biol Fish 15(1–2):75–88

    Google Scholar 

  • Mathews T, Fisher NS (2009) Dominance of dietary intake of metals in marine elasmobranch and teleost fish. Sci Total Environ 407(18):5156–5161

    CAS  Google Scholar 

  • McGeer J, Niyogi S, Smith DS (2012) Cadmium. In: Wood CM, Farrell AP, Brauner CJ (eds) Homeostasis and toxicology of nonessential metals. Fish Physiology, 31A. Academic Press, USA, pp 125–169

  • Monserrat J, Letts RE, Ferreira J, Ventura-Lima J, Amado L, da Rocha A, Gorbi S, Bocchetti R, Benedetti M, Regoli F (2012) Biomarkers of oxidative stress: benefits and drawbacks for their application in biomonitoring of aquatic environments. In: Abele D, Vázquez-Medina JP, Zenteno-Savın T (eds) Oxidative stress in aquatic ecosystems. Wiley-Blackwell, Chichester, pp 317–326. https://doi.org/10.1002/9781444345988.fmatter

  • Nriagu JO (1996) A history of global metal pollution. Science 272(5259):223–224

    CAS  Google Scholar 

  • Nriagu JO, Pacyna JM (1988) Quantitative assessment of worldwide contamination of air, water and soils by trace metals. Nature 333(6169):134

    CAS  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. Golfo de México Contaminación e impacto Ambiental: Diagnóstico y Tendencias. Universidad Autónoma de Campeche, Universidad Autónoma Campeche, Universidad Nacional Autónoma de México, Instituto Nacional de Ecología, pp 451–474

  • Oswalt SN, Johnson TG, Howell M, Bentley JW (2009) Fluctuations in national forest timber harvest and removals: the southern regional perspective. Resource Bulletin SRS-148, p 30. US Department of Agriculture Forest Service, Southern Research Station, Asheville, p 148

  • Ozkan A, Fiskin K, Ayhan AG (2007) Effect of vitamin E and selenium on antioxidant enzymes in brain, kidney and liver of cigarette smoke-exposed mice. Biologia 62(3):360–364

    CAS  Google Scholar 

  • Pacyna JM, Pacyna EG (2001) An assessment of global and regional emissions of trace metals to the atmosphere from anthropogenic sources worldwide. Environ Rev 9(4):269–298

    CAS  Google Scholar 

  • Parsons GR (1985) Growth and age estimation of the Atlantic sharpnose shark, Rhizoprionodon terraenovae: a comparison of techniques. Copeia 1985(1):80–85

  • Patel PP, Bielmyer-Fraser GK (2015) The influence of salinity and copper exposure on copper accumulation and physiological impairment in the sea anemone, Exaiptasia pallida. Comp Biochem Physiol C: Toxicol Pharmacol 168:39–47. https://doi.org/10.1016/j.cbpc.2014.11.004

    Article  CAS  Google Scholar 

  • Pham AN, Xing G, Miller CJ, Waite TD (2013) Fenton-like copper redox chemistry revisited: hydrogen peroxide and superoxide mediation of copper-catalyzed oxidant production. J Catal 301:54–64

    CAS  Google Scholar 

  • Plumlee JD, Wells RD (2016) Feeding ecology of three coastal shark species in the northwest Gulf of Mexico. Mar Ecol Prog Ser 550:163–174

    CAS  Google Scholar 

  • Pyle G, Couture P (2012) Nickel. In: Wood CM, Farrell AP, Brauner CJ (eds) Homeostasis and toxicology of essential metals. Fish Physiology, 31A. Academic Press, USA, pp 253–282

  • Ray PD, Huang BW, Tsuji Y (2012) Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 24(5):981–990

  • Rumbold D, Wasno R, Hammerschlag N, Volety A (2014) Mercury Accumulation in Sharks From the Coastal Waters of Southwest Florida. Arch Environ Contam Toxicol 67(3):402–412

  • Siddiqui S, Goddard RH, Bielmyer-Fraser GK (2015) Comparative effects of dissolved copper and copper oxide nanoparticle exposure to the sea anemone, Exaiptasia pallida. Aquat Toxicol 160:205–213

    CAS  Google Scholar 

  • Sigma (1994a) Enzyme assay of catalase (EC1.11.1.6). http://www.sigmaaldrich.com

  • Sigma (1994b) Enzymatic assay of glutathione peroxidase (EC 1.11.1.9). http://www.sigmaaldrich.com

  • Sigma (1994c) Enzymatic assay of glutathione reductase (EC 1.6.4.2). http://www.sigmaaldrich.com

  • Storelli MM, Ceci E, Storelli A, Marcotrigiano GO (2003) Polychlorinated biphenyl, heavy metal and methylmercury residues in hammerhead sharks: contaminant status and assessment. Mar Pollut Bull 46(8):1035–1039

    CAS  Google Scholar 

  • Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metal toxicity and the environment. In: Luch A (ed) Molecular, clinical and environmental toxicology. Springer, Basel, pp 133–164

    Google Scholar 

  • Thomason RK, Loughry WJ, Lockhart JM, Bielmyer-Fraser GK (2016) Metal accumulation in bobcats in the Southeastern United States. Environ Monitor Assess 188:565–574. https://doi.org/10.1007/s10661-016-5587-6

    Article  CAS  Google Scholar 

  • Tinggi U (2008) Selenium: its role as antioxidant in human health. Environ Health Prevent Med 13(2):102

    CAS  Google Scholar 

  • Tyminski JP, Hueter RE, Morris J (2013) Tag-recapture results of bonnethead (Sphyrna tiburo) and Atlantic sharpnose (Rhizoprionodon terraenovae) sharks in the Gulf of Mexico and Florida Coastal Waters. SEDAR34-WP-31. SEDAR, North Charleston, SC, 12 pp

  • Uhrin AV, Matthews TR, Lewis C (2014) Lobster trap debris in the Florida Keys National Marine Sanctuary: distribution, abundance, density, and patterns of accumulation. Mar Coast Fish 6(1):20–32

    Google Scholar 

  • Valko M, Morris H, Cronin MTD (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12(10):1161–1208

    CAS  Google Scholar 

  • Van der Oost R, Beyer J, Vermeulen NP (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13(2):57–149. https://doi.org/10.1016/S1382-6689(02)00126-6

    Article  Google Scholar 

  • Vas P (1991) Trace metal levels in sharks from British and Atlantic waters. Mar Pollut Bull 22(2):67–72

    CAS  Google Scholar 

  • 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 (Isurus oxyrinchus). Comp Biochem Physiol A: Mol Integr Physiol 165(4):508–514

    Google Scholar 

  • Watanabe T, Kiron V, Satoh S (1997) Trace minerals in fish nutrition. Aquaculture 151(1–4):185–207

    CAS  Google Scholar 

  • Webb NA, Wood CM (2000) Bioaccumulation and distribution of silver in four marine teleosts and two marine elasmobranchs: influence of exposure duration, concentration, and salinity. Aquat Toxicol 49(1–2):111–129

    CAS  Google Scholar 

  • Wood C (2012) Silver. In: Wood CM, Farrell AP, Brauner CJ (eds) Homeostasis and toxicology of essential metals. Fish Physiology, 31A. Academic Press, USA, pp 1–55

Download references

Acknowledgements

Funding for this project was provided by Jacksonville University, via an EPIC grant to G.K. Bielmyer-Fraser and A. Kent-Willette and a Marine Science Research Institute Advisory Board grant. Additional funding for animal collections was provided through contracts to the University of North Florida from the National Oceanic and Atmospheric Association, National Marine Fisheries Service (NOAA–NMFS), Cooperative Atlantic States Shark Pupping and Nursery Survey Program. The authors acknowledge the following individuals for assistance with sample collection: C. Bangley, C. Belcher, M. Benavides, D. Bethea, C. Carpenter, J. Davis, C. Dean, T. Driggers, J.M. Drymon, B. Falterman, B. Frazier, M. Gonzalez De Acevedo, J. Gregg, R.D. Grubbs, J. Hendon, R. Latour, D. McDowell, C. Morgan, K. Mowle, C. Peterson, J. Russo, C. Shields, and J. Whalen.

Author information

Authors and Affiliations

  1. Jacksonville University, 2800 University Blvd N, Jacksonville, FL, 32211, USA

    Rachel Somerville, Maya Fisher, Louise Persson & Gretchen Bielmyer-Fraser

  2. University of North Florida, 1 UNF Dr, Jacksonville, FL, 32224, USA

    Samantha Ehnert-Russo & James Gelsleichter

Authors
  1. Rachel Somerville
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maya Fisher
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Louise Persson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Samantha Ehnert-Russo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. James Gelsleichter
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gretchen Bielmyer-Fraser
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rachel Somerville.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 243 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Somerville, R., Fisher, M., Persson, L. et al. Analysis of Trace Element Concentrations and Antioxidant Enzyme Activity in Muscle Tissue of the Atlantic Sharpnose Shark, Rhizoprionodon terraenovae. Arch Environ Contam Toxicol 79, 371–390 (2020). https://doi.org/10.1007/s00244-020-00753-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-020-00753-8

Search

Navigation