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Heavy Metal Contamination in Phrynops geoffroanus (Schweigger, 1812) (Testudines: Chelidae) in a River Basin, São Paulo, Brazil

Abstract

The Piracicaba River basin is considered the most disturbed river basin in the state of São Paulo. Considerable amounts of agricultural residues are seasonally drained into the river, and the region is also highly urbanized and industrialized with an incipient sewage treatment system. The presence of heavy metals has been previously reported for the water and riverbed in Piracicaba river basin. In this study we evaluated 13 heavy metals in the blood of 37 Geoffroy’s side-necked turtles, Phrynops geoffroanus, from Piracicaba River and Piracicamirim Creek, one of its tributaries. Blood levels of As, Co, Cr, Se and Pb varied among sites, whereas Sn varied between males and females. However, no obvious pathology was detected. Serum level of Cu (2,194 ng g−1) and Pb (1,150 ng g−1) found in this study are the highest ever described for any reptile; however, no clinical symptoms have been detected in the present study. There is no information about the time scale of such contamination, which could be currently subclinical and yet lead to a breakdown in the population reproductive success in a few years. Based on the present study, legal enforcement is urged in order to locate and extirpate heavy metal sources in the Piracicaba River basin. In addition, monitoring should include humans and commercial fish consumed in local markets.

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References

  1. Belskii EA, Lugas’kova NV, Karfidova AA (2005) Reproductive parameters of adult birds and morphophysiological characteristics of chicks in the Pied Flycatcher (Ficedula hypoleuca Pall.) in technogenically polluted habitats. Russian J Ecol 36:362–369

    Google Scholar 

  2. Burger J, Campbell KR, Campbell TS, Shukla T, Jeitner C, Gochfeld M (2005) Use of skin and blood as nonlethal indicators of heavy metals contamination in Northern water snakes (Nerodia sipedon). Arch Environ Contam Toxicol 49:232–238

    Article  CAS  Google Scholar 

  3. Burger J, Murray S, Gaines KF, Novak JM, Punshon T, Dixon C, Gochfeld M (2006) Element levels in snakes in South Carolina: differences between a control site and exposed site on the Savannah river site. Environ Monit Asses 112:35–52

    Article  CAS  Google Scholar 

  4. Burger J, Campbell KR, Murria S, Campbell TS, Gaines KF, Jeitner C, Shukla T, Burke S, Gochfeld M (2007) Metal in blood, muscle and liver of water snakes (Nerodia spp.) from New Jersey, Tennessee and South Carolina. Scien Total Environ 373:556–563

    Article  CAS  Google Scholar 

  5. Campbell KR, Campbell TS, Burger J (2005) Heavy metals concentrations in Northen water snakes (Nerodia sipedon) from East Fork Poplar Creek, and the Little river, east Tennessee, USA. Arch Environ Contam Toxicol 49:239–248

    Article  CAS  Google Scholar 

  6. Clark DR, Bickham JW, Baker DL, Cowman DF (2000) Environmental contaminants in Texas, USA, wetland reptiles: evaluation using blood simples. Environ Toxicol Chem 19:2259–2265

    Article  CAS  Google Scholar 

  7. Day RD, Segars AL, Arendt MD, Lee AM, Peden-Adams MM (2007) Relationship of blood Mercury levels to health parameters in the Loggerhead Sea Turtle (Caretta caretta). Environ Health Persp 115:1421–1428

    CAS  Google Scholar 

  8. Falótico MHB (2001) Distribuição das concentrações de metais em agua, matéria em suspensão e sedimento de fundo na bacia do rio Piracicaba/SP. Ph.D. Universidad de São Paulo, Piracicaba, Brazil

  9. Favaro PC, Fernandes EAN, Ferraz ESB, Falótico MHB (2004) Time still to restore the polluted Piracicaba river basin. J Radioanal Nucl Chem 259:217–221

    Article  CAS  Google Scholar 

  10. Ferraz ESB, Fernandes EAN, Favaro PC, Ferraz FFB, Lopes CH, Martins FSA, Kronka EM (1996) Contaminação por metais e elementos traço em sedimentos de fundo do Ribeirao Piracicamirim. In: Anais do II Workshop do Projeto Piracena. São Paulo, Brazil, pp. 114–118

  11. Fostier AH, Falótico MHB, Ferraz ESB, Tomazelli AC, Salomão MSMB, Martinelli LA, Victoria RL (2005) Impact of anthropogenic activity on the Hg concentrations in the Piracicaba river basin (São Paulo state, Brazil). Water Air Soil Poll 381:381–402

    Article  Google Scholar 

  12. Gagneten AM, Imhof A, Gervasio S (2008) Accumulation and elimination of Cr in gills and eggs by the freshwater crab Zilchiopsis collastinensis after experimental exposure. Fresenius Environ Bull 17:182–187

    CAS  Google Scholar 

  13. Golden NH, Rattner BA, McGowan PC, Parsons KC, Ottinger MA (2003) Concentration of metals in feathers and blood of nestling Black-crowned night-herons (Nyctiocorax nyctiocorax) in Chesapeake and Delaware Bays. Bull Environ Contam Toxicol 70:385–393

    Article  CAS  Google Scholar 

  14. Guirlet E, Das K, Girondot M (2008) Maternal transfer of trace elements in leatherback turtles (Dermochelys coriacea) of French Guiana. Aquatic Toxicol 88:267–276

    Article  CAS  Google Scholar 

  15. Hopkins WA, Rowe CL, Congdon JD (1999) Elevated trace element concentrations and standard metabolic rate in Banded water snakes (Nerodia fasciata) exposed to coal combustion wastes. Environ Toxicol Chem 18:1258–1263

    Article  CAS  Google Scholar 

  16. Hopkins WA, Roe JH, Snodgrass JW, Jackson BP, Kling DE, Rowe CL, Congdon JD (2001) Nondestructive indices of trace element exposure in squamate reptiles. Environ Pollut 115:1–7

    Article  CAS  Google Scholar 

  17. Hopkins WA, Staub BP, Baionno JA, Jackson BP, Roe JH, Ford NB (2004) Trophic and maternal transfer of selenium in brown house snakes (Lamprophis fuliginosus). Ecotoxicol Environ Saf 58:285–293

    Article  CAS  Google Scholar 

  18. Kitana N, Callard IP (2008) Effect of cadmium on gonadal development in freshwater turtle (Trachemys scripta, Chrysemys picta) embryos. J Environ Sci Health A 43:262–271

    Article  CAS  Google Scholar 

  19. Lance VA, Horn TR, Elsey RM, de Peyster A (2006) Chronic incidental lead ingestion in a group of captive-reared alligators (Alligator mississippiensis): possible contribution to reproductive failure. Comp Biochem Physiol C Toxicol Pharmacol 142:30–35

    Article  Google Scholar 

  20. Lara LBLS, Artaxo P, Martinelli LA, Victoria RL, Camargo PB, Krusche AV, Ayers GP, Ferraz ESB, Ballester MV (2001) Chemical composition of rainwater and anthropogenic influences in the Piracicaba river basin, Southeast Brazil. Atmosph Environ 35:4937–4945

    Article  CAS  Google Scholar 

  21. Márquez-Ferrando R, Santos X, Pleguezuelos JM, Ontiveros D (2009) Bioaccumulation of heavy metals in the lizard Psammodromus algirus after a tailing-dam collapse in Aznalcóllar (Southwest Spain). Arch Environ Contam Toxicol 56:276–285

    Article  Google Scholar 

  22. Martinelli LA, da Silva AM, Camargo PB, Moretti LR, da Silva DML, Fischer EG, Sonoda KC, Salomão MSMB (2002) Levantamento das cargas orgânicas lançadas nos rios do Estado de São Paulo. Biota Neotropica 2:1–18

    Google Scholar 

  23. Mendoza JA, Ulriksen P, Picado F, Dahlin T (2008) Aquifer interactions with a polluted mountain river of Nicaragua. Hydrol Process 22:2264–2273

    Article  CAS  Google Scholar 

  24. Nagle RD, Rowe CL, Congdon JD (2001) Accumulation and selective maternal transfer of contaminants in the turtle Trachemys scripta associated with coal ash deposition. Arch Environ Contam Toxicol 40:531–536

    Article  CAS  Google Scholar 

  25. Ometo JPHB, Martinelli LA, Ballester MV, Gessner A, Krusche AV, Victoria RL, Williams M (2000) Effects of land use on water chemistry and macroinvertebrates in two streams of the Piracicaba river basin, south–east Brazil. Freshw Biol 44:327–337

    Article  CAS  Google Scholar 

  26. Pain DJ (1996) Lead in waterfowl. In: Beyer WN, Heinz GH, Redmond-Norwood AW (eds) Environmental contaminants in wildlife: interpreting tissue concentrations. Lewis, New York, pp 251–264

    Google Scholar 

  27. Rogers KD, Booth DT (2004) A method of sampling blood from Australian freshwater turtles. Wildl Res 31:93–95

    Article  Google Scholar 

  28. Rowe CL, Kinney OM, Nagle RD, Congdon JD (1998) Elevated maintenance costs in an anuran (Rana catesbeiana) exposed to a mixture of trace elements during embryonic and early larval periods. Physiol Zool 71:27–35

    Article  CAS  Google Scholar 

  29. Sileo L, Creekmore LH, Audet DJ, Snyder MR, Meteyer CU, Franson JC, Locke LN, Smith MR, Finley DL (2001) Lead poisoning of waterfowl by contaminated sediment in the Coeur d’Alene River. Arch Environ Contam Toxicol 41:364–368

    Article  CAS  Google Scholar 

  30. Silvano RAM, Begossi A (2001) Seasonal dynamics of fishery at the Piracicaba river (Brazil). Fish Res 51:69–86

    Article  Google Scholar 

  31. Souza FL, Abe AS (2000) Feeding ecology, density and biomass of the freshwater turtle, Phrynops geoffroanus, inhabiting a polluted urban river in south-eastern Brazil. J Zool Lond 252:437–466

    Article  Google Scholar 

  32. Spears BL, Hansen JA, Audet DJ (2007) Blood lead concentration in waterfowl utilizing lake Coeur d’Alene, Idaho. Arch Environ Contam Toxicol 52:121–128

    Article  CAS  Google Scholar 

  33. Toledo AMA, Ballester MVR (2001) Variabilidade espaço-temporal do uso e cobertura do solo e a qualidade da água em duas microbacias hidrográficas do Estado de São Paulo. In: Simpósio Brasileiro de Sensoriamento Remoto. Anais, Paraná, Brazil. Instituto Nacional de Pesquisas Espaciais (INPE), São José dos Campos, SP, Brazil, pp 543–545

  34. Tomazelli AC, Martinelli LA, Avelar WEP, Camargo PB, Fostier AH, Ferraz ESB, Krug FJ, Santos Júnior D (2003) Biomonitoring of Pb and Cd in two impacted watersheds in Southeast Brazil, using the freshwater mussel Anodontites trapesialis (Lamarck, 1819) (Bivalvia: Mycetopodidae) as a biological monitor. Braz Arch Biol Technol 46:673–684

    Article  CAS  Google Scholar 

  35. Xu Q, Fang S, Wang Z (2006) Heavy metal distribution in tissues and eggs of Chinese Alligator (Alligator sinensis). Arch Environ Contam Toxicol 50:580–586

    Article  CAS  Google Scholar 

  36. Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice-Hall, New Jersey

    Google Scholar 

Download references

Acknowledgments

The Phrynops geoffroanus ecology project was sponsored by FAPESP Research Grant. (n. 2005/00210-9). The animals were captured under IBAMA license (proc. 02010.000005/05-61).

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Correspondence to C. I. Piña.

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Piña, C.I., Lance, V.A., Ferronato, B.O. et al. Heavy Metal Contamination in Phrynops geoffroanus (Schweigger, 1812) (Testudines: Chelidae) in a River Basin, São Paulo, Brazil. Bull Environ Contam Toxicol 83, 771 (2009). https://doi.org/10.1007/s00128-009-9866-6

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Keywords

  • Geoffroy’s side-necked turtle
  • Piracicaba river
  • Piracicamirim creek