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Influence of a Former Mining Area in the Heavy Metals Concentrations in Blood of Free-Living Mediterranean Pond Turtles (Mauremys leprosa)

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Abstract

The objective of this study was to assess metal exposure in the Mediterranean Pond Turtle (Mauremys leprosa) inhabiting a watercourse in an ancient mining district polluted by different metals (“Rambla de Las Moreras”, southeastern Spain) and included in the Ramsar Convention. For this purpose, mercury (Hg), lead (Pb), copper (Cu), zinc (Zn) and cadmium (Cd) were analysed in blood samples from 42 M. leprosa healthy adults (27 males and 13 females). The highest median concentrations were found for Zn, followed by Cu, Pb, Hg and Cd (366, 33, 9, 0.83 and 0.14 µg/dL, respectively). Although the literature regarding toxic metals in freshwater turtles is relatively scarce, Pb may cause deleterious effects in our population. In general, males presented higher levels than females, which could be due to maternal transfer during egg formation. The significant correlations between Cu–Cd and Cu–Hg suggest the implication of an efficient mechanism of detoxification involving metallothioneins.

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References

  • Anan Y, Kunito T, Sakai H, Tanabe S (2002) Subcellular distribution of trace elements in the liver of sea turtles. Mar Pollut Bull 45:224–229

    Article  CAS  Google Scholar 

  • Andreu AC, López-Jurado LF (1998) Género Mauremys (Gray 1869). In: Reptiles Fauna Ibérica, 2nd edn. Museo Nacional de Ciencias Naturales, Ramos MA et al (eds). CSIC, Madrid, 102–108

  • Auer M, Taskavak E (2004) Population structure of syntopic Emys orbicularis and Mauremys rivulata in western Turkey. Biologia 59:81–84

    Google Scholar 

  • Cortés-Gómez AA, Fuentes-Mascorro G, Romero D (2014) Metals and metalloids in whole blood and tissues of Olive Ridley turtles (Lepidochelys olivacea) from La Escobilla Beach (Oaxaca, Mexico). Mar Pollut Bull 89(1):367–375

    Article  Google Scholar 

  • Council of the European Commision (1992) Council Directive 92/43/EEC of 21 May 1992 on the conservation of natural habitats and of wild fauna and flora. Off J L 206:0007–0050

    Google Scholar 

  • Cox N, Chanson J, Stuart S (2006). The status and distribution of reptiles and amphibians of the Mediterranean basis. IUCN, Gland, Switzerland, and Cambridge, UK

  • Day RD, Christopher SJ, Becker PR, Whitaker DW (2005). Monitoring mercury in the loggerhead sea turtle, Caretta caretta. Environ Sci Technol 39:437–446

    Article  CAS  Google Scholar 

  • Díaz-Paniagua C, Andreu AC, Keller C (2015). Galápago leproso – Mauremys leprosa. En: Enciclopedia Virtual de los Vertebrados Españoles. Salvador A, Marco A. (eds). Museo Nacional de Ciencias Naturales, Madrid. http://www.vertebradosibericos.org/

  • García-Fernández AJ, Sánchez-García JA, Jiménez-Montalbán P, Luna A (1995) Lead and cadmium in wild birds in southeastern Spain. Environ Toxicol Chem 14(12):2049–2058

    Article  Google Scholar 

  • García-Fernández AJ, Gómez-Ramírez P, Martínez-López E, Hernández-García A, María-Mojica P, Romero D, Jiménez P, Castillo JJ, Bellido JJ (2009). Heavy metals in tissues from loggerhead turtles (Caretta caretta) from the southwestern Mediterranean (Spain). Ecotoxicol Environ Saf 72:557–563

    Article  Google Scholar 

  • Gasith A, Resh VH (1999) Streams in Mediterranean climate regions: abiotic influences and biotic responses to predictable seasonal events. Annu Rev Ecol Syst 30:51–81

    Article  Google Scholar 

  • Gibbons JW, Scott DE, Avis TR, Ryan J, Buhlmann KA, Tuberville TD, Metts S, Greene SL, Mills T, Leiden Y, Poppy S, Winne CT (2000) The global decline of reptiles, déjá vu amphibians. Bioscience 50:653–666

    Article  Google Scholar 

  • Gómez-Ramírez P, Martínez-López E, María-Mojica P, León-Ortega M, García-Fernández AJ (2011). Blood lead levels and δ-ALAD inhibition in nestlings of Eurasian Eagle Owl (Bubo bubo) to assess lead exposure associated to an abandoned mining area. Ecotoxicology 20:131–138

    Article  Google Scholar 

  • Guirlet E, Das K (2012). Cadmium toxicokinetics and bioaccumulation in turtles: trophic exposure of Trachemys scripta elegans. Ecotoxicology 21:18–26

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hays KA, McBee K (2007). Flow cytometric analysis of red-eared slider turtles (Trachemys scripta) from Tar Creek Superfund Site. Ecotoxicology 16:353–361.

    Article  Google Scholar 

  • Henny CJ, Blus LJ, Hoffman DJ, Grove RA (1994) Lead in hawks, falcons and owls downstream from a mining site on the Coeur d’Alene River, Idaho. Environ Monit Assess 29:267–288

    Article  CAS  Google Scholar 

  • Herbst LH, Klein PA (1995) Green turtle fibropapillomatosis: challenges to assessing the role of environmental cofactors. Environ Health Perspect 103:27–30

    Article  Google Scholar 

  • Jiménez J, Lacomba I, Sancho V, Risueño P (2002). Peces continentales, anfibios y reptiles de la Comunidad Valenciana. Generalitat valenciana. Colección Biodiversidad, 10. Generalitat Valenciana, Conselleria de Medi Ambient. Valencia. 271 pp

  • Keller C. (1997). Ecología de las poblaciones de Mauremys leprosa y Emys orbicularis del Parque Nacional de Doñana. Tesis Doctoral. Univ. Sevilla. 217pp

  • Keller C. (1999). Estrategias adaptativas de los quelonios acuáticos Mauremys leprosa y Emys orbicularis en el Parque Nacional de Doñana. Fundación Caja Madrid.&nbsp

  • 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(3):262–271

    Article  CAS  Google Scholar 

  • Lovich JE, Znari M, Ait Baamrane MA, Naimi M, Mostalih A (2010). Biphasic geographic variation in sexual size dimorphism of turtle (Mauremys leprosa) populations along an environmental gradient in Morocco. Chelonian Conservat Biol 9:45–53

    Article  Google Scholar 

  • Manteca Martínez JI, de Perceval Pérez Verde MA, López-Morel MA (2005). La industria minera en Murcia durante la época contemporánea. In: Bocamina AAVV (ed) Patrimonio Geológico y Minero de la Región de Murcia. Museode la Ciencia y el Agua, Murcia, pp. 123–134

    Google Scholar 

  • Martínez-López E, Martínez JE, María-Mojica P, Peñalver J, Pulido M, Calvo JF, García-Fernández AJ (2004) Lead in feathers and δ-aminolevulinic acid dehydratase activity in three raptor species from an unpolluted mediterranean forest (southeastern Spain). Arch Environ Contam Toxicol 47:270–275

    Article  Google Scholar 

  • Martínez-López E, Sousa AR, María-Mojica P, Gómez-Ramírez P, Guilhermino L, García-Fernández AJ (2010) Blood δ-ALAD, lead and cadmium concentrations in spur-tighed tortoises (Testudo graeca) from Southeastern Spain and Northern Africa. Ecotoxicol 19:670–677

    Article  Google Scholar 

  • 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 

  • Oyarzun R, Lillo J, López-García JA, Esbrí JM, Cubas P, Llanos W, Higueras P (2011) The Mazarrón Pb–(Ag)–Zn mining district (SE Spain) as a source of heavy metal contamination in a semiarid realm: geochemical data from mine wastes, soils, and stream sediments. J Geochem Explor 109(1):113–124

    Article  CAS  Google Scholar 

  • Páez-Osuna F, Calderón-Campuzano MF, Soto-Jiménez MF, Ruelas-Inzunza JR (2010). Trace metals (Cd, Cu, Ni, and Zn) in blood and eggs of the Sea Turtle (Lepidochelys olivacea) from a nesting colony of Oaxaca, Mexico. Arch Environ Contam Toxico 59: 632–641.

    Article  Google Scholar 

  • Páez-Osuna F, Calderón-Campuzano MF, Soto-Jiménez MF, Ruelas-Inzunza JR (2011) Mercury in blood and eggs of the sea turtle Lepidochelys olivacea from a nesting colony in Oaxaca, Mexico. Mar Pollut Bull 62:1320–1323

    Article  Google Scholar 

  • Perrault JR, Debra L, Millerb DL, Garnerc J, Wyneken J (2013) Mercury and selenium concentrations in leatherback sea turtles (Dermochelys coriacea): population comparisons, implications for reproductive success, hazard quotients and directions for future research. Sci Total Environ 463–464:61–71

    Article  Google Scholar 

  • Rie MT, Lendas KA, Callard IP (2001) Cadmium: tissue distribution and binding induction in the painted turtle, Chrysemys picta. Comp Biochem Physiol C 130:41–51

    CAS  Google Scholar 

  • Sakai H, Saeki K, Ichihashi H, Kamezaki N, Tanabe S, Tasukawa R (2000) Growth-related changes in heavy metal accumulation in green turtles (Chelonia mydas) from Yaeyama Islands, Okinawa, Japan. Arch Environ Contam Toxicol 39(3):378–385

    Article  CAS  Google Scholar 

  • Salvador, A., Pleguezuelos, J. M. (2002). Reptiles españoles: Identificación, historia natural y distribución. Canseco Ed., Talavera de la Reina

  • Storelli MM, Storelli A, D’Addabbo R, Marano C, Bruno R, Marcotrigiano GO (2005). Trace elements in loggerhead turtles (Caretta caretta) from the eastern Mediterranean Sea: overview and evaluation. Environ Pollut 135:163–170

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study has been supported by NOVEDAR-Consolider Project CSD00C-07-22204, Confederación Hidrográfica del Segura, and Fundación SENECA (MASCA’2014 Project 19481/pi/14). Silvia Espín was in part funded by the Academy of Finland (Project Number 265859) and by Fundación SENECA (Project 20031/SF/16). We are especially grateful to ANSE for the inestimable collaboration in the collection of samples, especially to J. Sánchez, M. Ferrández, P.López and JF Martínez. Thanks to M.Yelo and S. Fernández for the support in metal analyses.

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Authors and Affiliations

  1. Department of Toxicology, Faculty of Veterinary Medicine, University of Murcia, Campus de Espinardo, 30100, Murcia, Spain

    E. Martínez-López, P. Gómez-Ramírez, S. Espín, M. P. Aldeguer & A. J. García-Fernández

  2. Section of Ecology, Department of Biology, University of Turku, 20014, Turku, Finland

    S. Espín

Authors
  1. E. Martínez-López
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  2. P. Gómez-Ramírez
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  3. S. Espín
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  4. M. P. Aldeguer
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  5. A. J. García-Fernández
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Correspondence to E. Martínez-López.

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Martínez-López, E., Gómez-Ramírez, P., Espín, S. et al. Influence of a Former Mining Area in the Heavy Metals Concentrations in Blood of Free-Living Mediterranean Pond Turtles (Mauremys leprosa). Bull Environ Contam Toxicol 99, 167–172 (2017). https://doi.org/10.1007/s00128-017-2122-6

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