Organochlorine Concentrations in Bonnethead Sharks (Sphyrna tiburo) from Four Florida Estuaries

  • J Gelsleichter
  • C. A. Manire
  • N. J. Szabo
  • E. Cortés
  • J. Carlson
  • L. Lombardi-Carlson
Article
  • 282 Downloads

Abstract

Because of their persistence in aquatic environments and ability to impair reproduction and other critical physiological processes, organochlorine (OC) contaminants pose significant health risks to marine organisms. Despite such concerns, few studies have investigated levels of OC exposure in sharks, which are fish particularly threatened by anthropogenic pollution because of their tendency to bioaccumulate and biomagnify environmental contaminants. The present study examined concentrations of 29 OC pesticides and total polychlorinated biphenyls (PCBs) in the bonnethead shark (Sphyrna tiburo), an abundant species for which evidence of reproductive impairment has been observed in certain Florida populations. Quantifiable levels of PCBs and 22 OC pesticides were detected via gas chromatography and mass spectrometry in liver of 95 S. tiburo from four estuaries on Florida’s Gulf coast: Apalachicola Bay, Tampa Bay, Florida Bay, and Charlotte Harbor. In general, OC concentrations were significantly higher in Apalachicola Bay, Tampa Bay, and Charlotte Harbor S. tiburo in relation to the Florida Bay population. Because the rate of infertility has been shown to be dramatically higher in Tampa Bay versus Florida Bay S. tiburo, the present findings allude to a possible relationship between OC exposure and reproductive health that requires further investigation. Pesticide and PCB concentrations did not appear to significantly increase with growth or age in S. tiburo, suggesting limited potential for OC bioaccumulation in this species compared with other sharks for which contaminant data are available. Concentrations of OCs in serum and muscle were not correlated with those in liver, indicating that these tissues are poor surrogates for measuring internal OC burden in this species via nonlethal sampling procedures.

References

  1. Alam, SK, Brim, MS 2000Organochlorine, PCB, PAH, and metal concentrations in eggs of loggerhead sea turtles (Caretta caretta) from northwest Florida, USAJ Environ Sci Health B35705724PubMedGoogle Scholar
  2. Blanch, GP, Serrano, R, Glausch, A, Schurig, V, Gonzalez, MJ 1996Quantification and determination of enantiomeric ratios of chiral PCB 95, PCB 132, PCB 149 in shark liver samples (C. coelolepis) from the Atlantic oceanJ High Resol Chromatogr19390396CrossRefGoogle Scholar
  3. Braune, BM, Donaldson, GM, Hobson, KA 2002Contaminant residues in seabird eggs from the Canadian Arctic. II. Spatial trends and evidence from stable isotopes for intercolony differencesEnviron Pollut117133145PubMedGoogle Scholar
  4. Brim, MS, Alam, SK, Jenkins, LG 2001Organochlorine pesticides and heavy metals in muscle and ovaries of Gulf coast striped bass (Morone saxatilis) from the Apalachicola River, Florida, USAJ Environ Sci Health B361527PubMedGoogle Scholar
  5. Camhi M, Fowler S, Musick J, Brautigam A, Fordham S (1998) Sharks and their relatives: ecology and conservation. IUCN/SSC Shark Specialist Group. IUCN, Gland, Switzerland and Cambridge, UKGoogle Scholar
  6. Cantillo AY, Lauenstein GG, O’Connor TP, Johnson WE (1999) Status and trends of contaminant levels in biota and sediments of south Florida. Regional report series 2. National Status and Trends Program for Marine Environmental Quality. Center for Coastal Monitoring and Assessment, National Centers for Coastal Ocean Science, Silver Spring, MDGoogle Scholar
  7. Carlson, JK, Parsons, GR 1997Age and growth of the bonnethead shark, Sphyrna tiburo, from northwest Florida, with comments on clinal variationEnviron BioI Fish50331341CrossRefGoogle Scholar
  8. Carr, RS, Long, ER, Windom, HL, Chapman, DC, Thursby, G, Sloane, GM, Wolfie, DA 1996Sediment quality assessment studies of Tampa Bay, FloridaEnviron Toxicol Chern1512181231Google Scholar
  9. Castro, JC 1993The shark nursery of Bulls Bay, South Carolina, with a review of the shark nurseries of the southeastern coast of the United StatesEnviron BioI Fish383748CrossRefGoogle Scholar
  10. Chapman, DD, Prodöhl, PA, Gelsleichter, J, Manire, CA, Shivji, MS 2004Molecular insights into shark mating systems: predominance of genetic monogamy by females in the hammerhead Sphyrna tiburo (Carcharhiniformes, Sphyrnidae)Mol EcoI1319651974Google Scholar
  11. Corsolini, C, Focardi, S, Kannan, K, Tanabe, S, Borrell, A, Tatsukawa, R 1995Congener profile and toxicity assessment of polychlorinated biphenyls in dolphins, sharks and tuna collected from Italian watersMar Environ Res403353Google Scholar
  12. Cortés, E, Manire, CA, Hueter, RE 1996Diet, feeding habits, and diel feeding chronology of the bonnethead shark, Sphyrna tiburo in southwest FloridaBull Mar Sci58353367Google Scholar
  13. Cortés, E, Parsons, GR 1996Comparative demography of two populations of the bonnethead shark (Sphyra tiburo)Can J Fish Aquat Sci53709718CrossRefGoogle Scholar
  14. Crain, DA, Guillette, LJ,Jr, Rooney, AA, Pickford, DB 1997Alterations in steroidogenesis in alligators (Alligator mississippiensis) exposed naturally and experimentally to environmental contaminantsEnviron Health Perspect105528533PubMedGoogle Scholar
  15. Davis, JA, May, MD, Greenfield, BK, Fairey, R, Roberts, C, Ichikawa, G, Stoelting, MS, Becker, JS, Tjeerdema, RS 2002Contaminant concentrations in sport fish from San Francisco Bay, 1997Mar Pollut Bull4411171129PubMedGoogle Scholar
  16. Derocher, AE Wolkers, H Colborn, T Schlabach, M Larsen, TS Wiig2003Contaminants in Svalbard polar bear samples archived since 1967 and possible population level effectsSci Total Environ301163174PubMedGoogle Scholar
  17. Fisher, WS, Oliver, LM, Winstead, JT, Long, ER 2000A survey of oysters Crassostrea virginica from Tampa Bay, Florida: associations of internal defense measurements with contaminant burdensAquat Toxicol51115138PubMedGoogle Scholar
  18. Fisk, AT, Tittlemier, SA, Pranschke, JL, Norstrom, RJ 2002Using anthropogenic contaminants and stable isotopes to assess the feeding ecology of greenland sharksEcology8321622172Google Scholar
  19. Gelsleichter, J, Steinetz, BG, Manire, CA, Ange, C 2003Serum relaxin concentrations and reproduction in male bonnethead sharks, Sphyrna tiburoGen Comp Endocrinol1322734PubMedGoogle Scholar
  20. Gelsleichter, J, Rasmussen, LEL, Manire, CA, Tyminski, J, Chang, B, Lombardi-Carlson, L 2002Serum steroid concentrations and development of the reproductive system during puberty in male bonnethead sharks, Sphyrna tiburoFish Physiol Biochem26389401Google Scholar
  21. Guillette, LJ,Jr, Brock, JW, Rooney, AA, Woodward, AR 1999Serum concentrations of various environmental contaminants and their relationship to sex steroid concentrations and phallus size in juvenile American alligatorsArch Environ Contam Toxicol36447455PubMedGoogle Scholar
  22. Guruge, KS, Watanabe, M, Tanaka, H, Tanabe, S 2001Accumulation status of persistent organochlorines in albatrosses from the North Pacific and the Southern OceanEnviron Pollut114389398PubMedGoogle Scholar
  23. Hanchet, S 1988Reproductive biology of Squalus acanthias from the east coast, South Island, New ZealandJ Mar Freshwat Res22537549Google Scholar
  24. Helander, B, Olsson, A, Bignert, A, Asplund, L, Litzen, K 2002The role of DDE, PCB, coplanar PCB and eggshell parameters for reproduction in the white-tailed sea eagle (Haliaeetus albicilla) in SwedenAmbio31386403PubMedGoogle Scholar
  25. Henriksen, EO, Wiig, O, Skaare, JU, Gabrielsen, GW, Derocher, AE 2001Monitoring PCBs in polar bears: lessons learned from SvalbardJ Environ Monit3493498PubMedGoogle Scholar
  26. Hutchinson, JD, Simmonds, MP 1994Organochlorine contamination in pinnipedsRev Environ Contam Toxicol136123167PubMedGoogle Scholar
  27. Kajiwara, N, Kannan, K, Muraoka, M, Watanabe, M, Takahashi, S, Gulland, F, Olsen, H, Blankenship, AL, Jones, PD, Tanabe, S, Giesy, JP 2001Organochlorine pesticides, polychlorinated biphenyls, and butyltin compounds in blubber and livers of stranded California sea lions, elephant seals, and harbor seals from coastal California, USAArch Environ Contam Toxicol419099PubMedGoogle Scholar
  28. Kumari, A, Sinha, RK, Gopal, K, Lata, S 2002Concentration of organochlorines in Ganges River dolphins from Patna, BiharJ Environ Biol23279281PubMedGoogle Scholar
  29. Le Boeuf, BJ, Giesy, JP, Kannan, K, Kajiwara, N, Tanabe, S, Debier, C 2002Organochloride pesticides in California sea lions revisitedBMC Ecol211PubMedGoogle Scholar
  30. Lie, E, Bernhoft, A, Riget, F, Belikov, SE, Boltunov, AN, Derocher, AE, Garner, GW, Wiig, O, Skaare, JU 2003Geographical distribution of organochlorine pesticides (OCPs) in polar bears (Ursus maritimus) in the Norwegian and Russian ArcticSci Total Environ306159170PubMedGoogle Scholar
  31. Lombardi-Carlson, LA, Cortés, E, Parsons, GR, Manire, CA 2004Latitudinal variation in life-history traits of bonnet head sharks, Sphyrna tiburo (Carcharhiniformes: Sphyrnidae) from the eastern Gulf of MexicoMar Freshwat Res54875883CrossRefGoogle Scholar
  32. Macauley, JM, Summers, JK, Engle, VD, Harwell, LC 2002The ecological condition of south Florida estuariesEnviron Monit Assess75253269PubMedGoogle Scholar
  33. Manire, CA, Rasmussen, LE 1997Serum concentrations of steroid hormones in the mature male bonnethead shark, Sphyrna tiburoGen Comp Endocrinol107414420PubMedGoogle Scholar
  34. Manire, CA, Rasmussen, LEL, Gelsleichter, J, Hess, DL 2004Maternal serum and yolk hormone concentrations in the placental viviparous bonnethead shark, Sphyrna tiburoGen Comp Endocrinol136241247PubMedGoogle Scholar
  35. Manire, CA, Rasmussen, LE, Gross, TS 1999Serum steroid hormones including 11-ketotestosterone, 11-ketoandrostenedione, and dihydroprogesterone in juvenile and adult bonnethead sharks, Sphyrna tiburoJ Exp Zool284595603PubMedGoogle Scholar
  36. Manire, CA, Rasmussen, LE, Hess, DL, Hueter, RE 1995Serum steroid hormones and the reproductive cycle of the female bonnethead shark, Sphyrna tiburoGen Comp Endocrinol97369376CrossRefGoogle Scholar
  37. McFarlane, GA, King, 1R, Saunders, MW 2002Preliminary study on the use of neural arches in the age determination of blunt nose sixgill sharks (Hexanchus griseus)Fish Bull100861864Google Scholar
  38. Mills, PA 1959Detection and semiquantitative estimation of chlorinated organic pesticide residues in foods by paper chromatographyJ AOAC42734740Google Scholar
  39. Muir, DC, Born, EW, Koczansky, K, Stern, GA 2000Temporal and spatial trends of persistent organochlorines in Greenland walrus (Odobenus rosmarus rosmarus)Sci Total Environ2457386PubMedGoogle Scholar
  40. National Research Council1999Hormonally active agents in the environmentNational Academy PressWashington, DCGoogle Scholar
  41. Nichols, S, Gelsleichter, J, Manire, CA, Cailliet, GM 2003Calcitonin-like immunoreactivity in serum and tissues of the bonnethead shark, Sphyrna tiburoJ Exp Zool298150161CrossRefGoogle Scholar
  42. Oliver, LM, Fisher, WS, Winstead, JT, Hemmer, BL, Long, ER 2001Relationships between tissue contaminants and defense-related characteristics of oysters (Crassostrea virginica) from five Florida baysAquat Toxicol55203222PubMedGoogle Scholar
  43. Parsons, GR 1983The reproductive biology of the Atlantic sharpnose shark, Rhizoptionodon terranovae (Richardson)Fish Bull816173Google Scholar
  44. Parsons, GR 1993aGeographic variation in reproduction between two populations of the bonnethead shark, Sphyrna tiburoEnviron BioI Fish382535CrossRefGoogle Scholar
  45. Parsons, GR 1993bAge determination and growth of the bonnethead shark Sphyrna tiburo: a comparison of two populationsMar Biol1172331CrossRefGoogle Scholar
  46. Santschi, PH, Presley, BJ, Wade, TL, Garcia-Romero, B, Baskaran, M 2001Historical contamination of PAHs, PCBs, DDTs, and heavy metals in Mississippi River Delta, Galveston Bay and Tampa Bay sediment coresMar Environ Res525179PubMedGoogle Scholar
  47. Scott, GI, Fulton, MH, Wirth, EF, Chandler, GT, Key, PB, Daugomah, JW, Bearden, D, Chung, KW, Strozier, ED, DeLorenzo, M, Sivertsen, S, Dias, A, Sanders, M, Macauley, JM, Goodman, LR, LaCroix, MW, Thayer, GW, Kucklick, J 2002Toxicological studies in tropical ecosystems: an ecotoxicological risk assessment of pesticide runoff in South Florida estuarine ecosystemsJ Agric Food Chern5044004408Google Scholar
  48. Seagars, DJ, Garlich-Miller, J 2001Organochlorine compounds and aliphatic hydrocarbons in Pacific walrus blubberMar Pollut Bull43122131PubMedGoogle Scholar
  49. Seal TL, Calder FD, Sloane GM, Schropps SJ, Windom HL (1994) Florida coastal sediment contaminants atlas. Florida Department of Environmental ProtectionGoogle Scholar
  50. Serrano, R, Fernandez, MA, Hernandez, LM, Hernandez, M, Pascual, P, Rabanal, RM, Gonzalez, MJ 1997Coplanar polychlorinated biphenyl congeners in shark livers from the North-Western African Atlantic OceanBull Environ Contam Toxical58150157Google Scholar
  51. Serrano, R, Fernandez, M, Rabanal, R, Hernandez, M, Gonzalez, MJ 2000Congener-specific determination of polychlorinated biphenyls in shark and grooper livers from the northwest African Atlantic OceanArch Environ Contam Toxicol38217224PubMedGoogle Scholar
  52. Stefanelli, P, Ausili, A, Ciuffa, G, Colasanti, A, Di Muccio, S, Morlino, R 2002Investigation of polychlorobiphenyls and organochlorine pesticides in tissues of tuna (Thunnus thunnus thynnus) from the Mediterranean Sea in 1999Bull Environ Contam Toxicol69800807PubMedGoogle Scholar
  53. Storelli, MM, Marcotrigiano, GO 2000Chlorobiphenyls, HCB, and organochlorine pesticides in some tissues of Caretta caretta (Linnaeus) specimens beached along the Adriatic Sea, ItalyBull Environ Contam Toxicol64481488PubMedGoogle Scholar
  54. Storelli, MM, Marcotrigiano, GO 2001Persistent organochlorine residues and toxic evaluation of polychlorinated biphenyls in sharks from the Mediterranean Sea (Italy)Mar Pollut Bull4213231329PubMedGoogle Scholar
  55. Storelli, MM, Ceci, E, Storelli, A, Marcotrigiano, GO 2003aPolychlorinated biphenyl, heavy metal and methylmercury residues in hammerhead sharks: contaminant status and assessmentMar Pollut Bull4610351039Google Scholar
  56. Storelli, MM, Storelli, A, Marcotrigiano, GO 2003bCoplanar polychlorinated biphenyl congeners in the liver of Galeus melastomus from different areas of the Mediterranean SeaBull Environ Contam Toxicol71276282Google Scholar
  57. Tanabe, S 2002Contamination and toxic effects of persistent endocrine disrupters in marine mammals and birdsMar Pollut Bull456977PubMedGoogle Scholar
  58. Tangredi, BP, Evans, RH 1997Organochlorine pesticides associated with ocular, nasal, or otic infection in the eastern box turtle (Terravene carolina carolina)J Zoo Wild Med2897100Google Scholar
  59. Tilbury, KL, Stein, JE, Krone, CA, Brownell, RL,Jr, Blokhin, SA, Bolton, JL, Ernest, DW 2002Chemical contaminants in juvenile gray whales (Eschrichtius robustus) from a subsistence harvest in Arctic feeding groundsChemosphere47555564PubMedGoogle Scholar
  60. Ueno, D, Deno, D, Iwata, H, Tanabe, S, Ikeda, K, Koyama, J, Yamada, H 2002Specific accumulation of persistent organochlorines in bluefin tuna collected from Japanese coastal watersMar Pollut Bull45254261PubMedGoogle Scholar
  61. Vetter, W, Scholz, E, Gaus, C, Muller, JF, Haynes, D 2001Anthropogenic and natural organohalogen compounds in blubber of dolphins and dugongs (Dugong dugon) from northeastern AustraliaArch Environ Contam Toxicol41221231PubMedGoogle Scholar
  62. Webber, JD, Cech, JJ 1998Nondestructive diet analysis of the leopard shark from two sites in Tomales Bay, CaliforniaCalif Fish Game841824Google Scholar
  63. Wu, TH, Rainwater, TR, Platt, SG, McMurry, ST, Anderson, TA 2000aDDE in eggs of two crocodile species from BelizeJ Agric Food Chem4864166420Google Scholar
  64. Wu, TH, Rainwater, TR, Platt, SG, McMurry, ST, Anderson, TA 2000bOrganochlorine contaminants in Morelet’s crocodile (Crocodylus moreletii) eggs from BelizeChemosphere40671678Google Scholar

Copyright information

© Springer Science+Business Media, Inc. 2005

Authors and Affiliations

  • J Gelsleichter
    • 1
  • C. A. Manire
    • 1
  • N. J. Szabo
    • 2
  • E. Cortés
    • 3
  • J. Carlson
    • 3
  • L. Lombardi-Carlson
    • 3
  1. 1. Elasmobranch Physiology and Environmental Biology ProgramCenter for Shark Research, Mote Marine LaboratorySarasotaUSA
  2. 2. Analytical Toxicology Core LaboratoryUniversity of FloridaGainesvilleUSA
  3. 3. National Marine Fisheries ServiceSoutheast Fisheries Science CenterPanama CityUSA

Personalised recommendations