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Environmental Science and Pollution Research

, Volume 25, Issue 36, pp 36671–36679 | Cite as

Relationship between plasma biochemistry values and metal concentrations in nesting olive ridley sea turtles

  • Adriana A. Cortés-Gómez
  • Asta Tvarijonaviciute
  • Marc Girondot
  • Fernando Tecles
  • Diego Romero
Research Article
  • 23 Downloads

Abstract

A hundred nesting olive ridley turtles were sampled to determine biochemical parameters (ALP, AST, ALT, creatinine, albumin, cholesterol, glucose, proteins, triglycerides, urea, and P-nitrophenyl acetate esterase activity). Esterase activity (EA) is a new biomarker very sensitive to metals. Most of the samples showed detectable levels. We also analyzed the concentration of 11 inorganic elements (As, Cd, Cr, Cu, Mn, Ni, Pb, Sr, Ti, Se, and Zn), some of them previously reported with very high concentrations in this population (especially cadmium with 82 and 150 μg g−1 ww in liver and kidney, respectively). Cadmium presented two negative relationships with creatinine and glucose. Some other understudied elements, Sr and Ti, for instance, presented five and four significant relationships with some biochemical parameters, respectively (most of them positive). EA was the parameter with most negative relationships (with Pb, Ti, As, Cr, and Se), reinforcing the results of other researchers in humans regarding the possible inhibition of EA by metals.

Keywords

Biochemistry Stress proteins Inorganic elements Cadmium Marine turtles Cortisol 

Notes

Acknowledgments

The authors would like to thank A. Caballol, I. Aquino, and A. Juárez for the sampling collection. To the Centro Mexicano de la Tortuga for permits and use of facilities, especially to M. Rodriguez, E. Peralta, and T. Luna, without their support, this work would not have been possible. Thanks too are due to S. Ros for the assistance in the biochemical sample analysis. And to the editor and anonymous reviewers who have contributed their time and expertise to improve this manuscript.

Funding information

The first author received grants from CONACyT, Mexico (No 216671). A. Tvarijonaviciute was supported by the postdoctoral program (Juan de la Cierva Incorporacion) of the Ministerio de Economía y Competitividad, Spain.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723CrossRefGoogle Scholar
  2. Anderson ET, Minter LJ, Clarke EO 3rd, Mroch RM 3rd, Beasley JF, Harms CA (2011) The effects of feeding on hematological and plasma biochemical profiles in green (Chelonia mydas) and Kemp's Ridley (Lepidochelys kempii) sea turtles. Vet Med Int 2011:890829–890827.  https://doi.org/10.4061/2011/890829 CrossRefGoogle Scholar
  3. Bolten AB, Jacobson ER, Bjorndal KA (1992) Effects of anticoagulant and autoanalyzer on blood biochemical values of loggerhead sea turtles (Caretta caretta). Am J Verterinary Res 53:2224–2227Google Scholar
  4. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer-Verlag, New YorkGoogle Scholar
  5. Camacho M, Luzardo OP, Boada LD, Lopez Jurado LF, Medina M, Zumbado M, Oros J (2013a) Potential adverse health effects of persistent organic pollutants on sea turtles: evidences from a cross-sectional study on Cape Verde loggerhead sea turtles. Sci Total Environ 458-460:283–289.  https://doi.org/10.1016/j.scitotenv.2013.04.043 CrossRefGoogle Scholar
  6. Camacho M, Oros J, Boada LD, Zaccaroni A, Silvi M, Formigaro C, Lopez P, Zumbado M, Luzardo OP (2013b) Potential adverse effects of inorganic pollutants on clinical parameters of Loggerhead Sea turtles (Caretta caretta): results from a nesting colony from Cape Verde, West Africa. Mar Environ Res 92:15–22.  https://doi.org/10.1016/j.marenvres.2013.08.002 CrossRefGoogle Scholar
  7. Casal AB, Camacho M, Lopez-Jurado LF, Juste C, Oros J (2009) Comparative study of hematologic and plasma biochemical variables in eastern Atlantic juvenile and adult nesting loggerhead sea turtles (Caretta caretta). Vet Clin Pathol 38:213–218.  https://doi.org/10.1111/j.1939-165X.2008.00106.x CrossRefGoogle Scholar
  8. Çay M, Naziroğlu M (1999) Effects of intraperitoneally-administered vitamin E and selenium on the blood biochemical and haematological parameters in rats. Cell Biochem Funct 17:143–148.  https://doi.org/10.1002/(SICI)1099-0844(199906)17:2<143::AID-CBF802>3.0.CO;2-H CrossRefGoogle Scholar
  9. 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 89:367–375.  https://doi.org/10.1016/j.marpolbul.2014.09.035 CrossRefGoogle Scholar
  10. Cortés-Gómez AA, Romero D, Girondot M (2017a) The current situation of inorganic elements in marine turtles: a general review and meta-analysis. Environ Pollut 229:567–585.  https://doi.org/10.1016/j.envpol.2017.06.077 CrossRefGoogle Scholar
  11. Cortés-Gómez AA, Tvarijonaviciute A, Teles M, Cuenca R, Fuentes-Mascorro G, Romero D (2017b): P-Nitrophenyl acetate esterase activity and cortisol as biomarkers of metal pollution in blood of olive Ridley turtles (Lepidochelys olivacea). Arch environ Contam Toxicol doi: https://doi.org/10.1007/s00244-017-0464-z
  12. Cortés-Gómez AA, Morcillo P, Guardiola FA, Espinosa C, Esteban MA, Cuesta A, Girondot M, Romero D (2018) Molecular oxidative stress markers in olive ridley turtles (Lepidochelys olivacea) and their relation to metal concentrations in wild populations. Environ Pollut 233:156–167.  https://doi.org/10.1016/j.envpol.2017.10.046 CrossRefGoogle Scholar
  13. Costa LG, Vitalone A, Cole TB, Furlong CE (2005) Modulation of paraoxonase (PON1) activity. Biochem Pharmacol 69:541–550.  https://doi.org/10.1016/j.bcp.2004.08.027 CrossRefGoogle Scholar
  14. Fazio E, Liotta A, Medica P, Bruschetta G, Ferlazzo A (2011) Serum and plasma biochemical values of health loggerhead sea turtles (Caretta caretta). Comp Clin Pathol 21:905–909.  https://doi.org/10.1007/s00580-011-1197-4 CrossRefGoogle Scholar
  15. Finlayson KA, Leusch FD, van de Merwe JP (2016) The current state and future directions of marine turtle toxicology research. Environ Int 94:113–123.  https://doi.org/10.1016/j.envint.2016.05.013 CrossRefGoogle Scholar
  16. Hamann M, Godfrey MH, Seminoff JA, Arthur K, Barata PCR, Bjorndal KA, Bolten AB, Broderick AC, Campbell LM, Carreras C, Casale P, Chaloupka M, Chan SKF, Coyne MS, Crowder LB, Diez CE, Dutton PH, Epperly SP, FitzSimmons N, Formia A, Girondot M, Hays GC, Cheng IS, Kaska Y, Lewison R, Mortimer JA, Nichols WJ, Reina RD, Shanker K, Spotila JR, Tomás J, Wallace BP, Work TM, Zbinden J, Godley BJ (2010) Global research priorities for sea turtles: informing management and conservation in the 21st century. Endanger Species Res 11:245–269CrossRefGoogle Scholar
  17. Hernandez AF, Gil F, Leno E, Lopez O, Rodrigo L, Pla A (2009) Interaction between human serum esterases and environmental metal compounds. Neurotoxicology 30:628–635.  https://doi.org/10.1016/j.neuro.2009.04.003 CrossRefGoogle Scholar
  18. Innis C, Ravich JB, Tlusty MF, Hoge MS, Wunn DS, Boerner-Neville LB, Merigo C, Weber ESI (2009) Hematologic and plasma biochemical ndings in cold-stunned Kemp’s ridley turtles: 176 cases (2001–2005). J Am Vet Med Assoc 235:426–432.  https://doi.org/10.2460/javma.235.4.426 CrossRefGoogle Scholar
  19. IUCN (2012): Red list of threatened species, version 2012.1. International Union for Conservation of nature, http://www.iucnredlist.org/
  20. Josse D, Bartels C, Lockridge D, Masson P (2002) P. PON1 structure. In: FC CLG (ed) Paraoxonase (PON1) in health and disease: basic and clinical aspects. Kluwer academic publishers, Norwell, MA, pp 27–52CrossRefGoogle Scholar
  21. Keller J, McClellan-Green P (2004) Effects of organochlorine compounds on cytochrome P450 aromatase activity in an immortal sea turtle cell line. Mar Environ Res 58:347–351.  https://doi.org/10.1016/j.marenvres.2004.03.080 CrossRefGoogle Scholar
  22. Keller JM, Kucklick JR, Stamper MA, Harms CA, McClellan-Green PD (2004) Associations between organochlorine contaminant concentrations and clinical health parameters in loggerhead sea turtles from North Carolina. USA Environ Health Perspect 112:1074–1079.  https://doi.org/10.1289/ehp.8143 CrossRefGoogle Scholar
  23. Keller JM, McClellan-Green PD, Kucklick JR, Keil DE, Peden-Adams MM (2006) Effects of organochlorine contaminants on loggerhead sea turtle immunity: comparison of a correlative field study and in vitro exposure experiments. Environ Health Perspect 114:70–76CrossRefGoogle Scholar
  24. Komoroske LM, Lewison RL, Seminoff JA, Deheyn DD, Dutton PH (2011) Pollutants and the health of green sea turtles resident to an urbanized estuary in San Diego, CA. Chemosphere 84:544–552.  https://doi.org/10.1016/j.chemosphere.2011.04.023 CrossRefGoogle Scholar
  25. Kowalczyk E, Kopff A, Fijatkowski P, Kopff M, Niedworok J, Btaszczyk J, Kêdziora J, Tyœlerowicz P (2003) Effect of anthocyanins on selected biochemical parameters in rats exposed to cadmium. Acta Biochim Pol 50:543–548Google Scholar
  26. Kuo CL, La Du BN (1998) Calcium binding by human and rabbit serum paraoxonases. Structural stability and enzymatic activity. Drug Metab Dispos 26:653–660Google Scholar
  27. Kuzmichevaa LV, Lopatnikovaa EA, Maksimov GV (2014) Biochemical changes in blood at lead intoxication and pectin correction. Mosc Univ Biol Sci Bull 69:51–56.  https://doi.org/10.3103/S0096392514020102 CrossRefGoogle Scholar
  28. Labrada-Martagon V, Rodriguez PA, Mendez-Rodriguez LC, Zenteno-Savin T (2011) Oxidative stress indicators and chemical contaminants in East Pacific green turtles (Chelonia mydas) inhabiting two foraging coastal lagoons in the Baja California peninsula. Comp Biochem Physiol C 154:65–75.  https://doi.org/10.1016/j.cbpc.2011.02.006 CrossRefGoogle Scholar
  29. Laird BD, Goncharov AB, Ayotte P, Chan HM (2014) Relationship between the esterase paraoxonase-1 (PON1) and metal concentrations in the whole blood of Inuit in Canada. Chemosphere 120C:479–485.  https://doi.org/10.1016/j.chemosphere.2014.08.073 CrossRefGoogle Scholar
  30. Li W-F, Pan M-H, Chung M-C, Ho C-K, Chuang H-Y (2006) Lead exposure is associated with decreased serum Paraoxonase 1 (PON1) activity and genotypes. Environ Health Perspect 114:1233–1236.  https://doi.org/10.1289/ehp.9163 CrossRefGoogle Scholar
  31. Massanyi P, Stawarz R, Halo M, Formicki G, Lukac N, Cupka P, Schwarcz P, Kovacik A, Tusimova E, Kovacik J (2014) Blood concentration of copper, cadmium, zinc and lead in horses and its relation to hematological and biochemical parameters. J Environ Sci Health A Tox Hazard Subst Environ Eng 49:973–979.  https://doi.org/10.1080/10934529.2014.894322 CrossRefGoogle Scholar
  32. Matovic V, Buha A, Ethukic-Cosic D, Bulat Z (2015) Insight into the oxidative stress induced by lead and/or cadmium in blood, liver and kidneys. Food Chem Toxicol 78:130–140.  https://doi.org/10.1016/j.fct.2015.02.011 CrossRefGoogle Scholar
  33. Nandi D, Patra RC, Swarup D (2006) Oxidative stress indices and plasma biochemical parameters during oral exposure to arsenic in rats. Food Chem Toxicol 44:1579–1584.  https://doi.org/10.1016/j.fct.2006.04.013 CrossRefGoogle Scholar
  34. NOM-059-SEMARNAT-2010 (2010) NORMA Oficial Mexicana NOM-059-SEMARNAT-2010, Protección ambiental-Especies nativas de México de flora y fauna silvestres-Categorías de riesgo y especificaciones para su inclusión, exclusión o cambio-Lista de especies en riesgo. SEMARNAT, MéxicoGoogle Scholar
  35. Páez-Osuna F, Calderón-Campuzano MF, Soto-Jiménez MF, Ruelas-Inzunza JR (2010) Lead in blood and eggs of the sea turtle, Lepidochelys olivacea, from the eastern Pacific: concentration, isotopic composition and maternal transfer. Mar Pollut Bull 60:433–439.  https://doi.org/10.1016/j.marpolbul.2009.10.004 CrossRefGoogle Scholar
  36. Park EJ, Yoon J, Choi K, Yi J, Park K (2009) Induction of chronic inflammation in mice treated with titanium dioxide nanoparticles by intratracheal instillation. Toxicology 260:37–46.  https://doi.org/10.1016/j.tox.2009.03.005 CrossRefGoogle Scholar
  37. Qian Y, Falahatpisheh MH, Zheng Y, Ramos KS, Tiffany-Castiglioni E (2001) Induction of 78 kD glucose-regulated protein (GRP78) expression and redox-regulated transcription factor activity by lead and mercury in C6 rat glioma cells. Neurotox Res 3:581–589.  https://doi.org/10.1007/bf03033212 CrossRefGoogle Scholar
  38. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  39. Rhen T, Cidlowski JA (2005) Antiinflammatory action of glucocorticoids—new mechanisms for old drugs. N Engl J Med 353:1711–1723CrossRefGoogle Scholar
  40. Santillana PR (2013) Valores Hematológicos y bioquímicos sanguíneos de tortugas anidantes de Golfina (Lepidochelys olivacea) en El Salvador. BIOMA, 11–17Google Scholar
  41. Santoro M, Meneses A (2007) Haematology and plasma chemistry of breeding olive ridley sea turtles (Lepidochelys olivacea). The Veterinary Record 161:818–819CrossRefGoogle Scholar
  42. Wallace BP, DiMatteo AD, Hurley BJ, Finkbeiner EM, Bolten AB, Chaloupka MY, Hutchinson BJ, Abreu-Grobois FA, Amorocho D, Bjorndal KA, Bourjea J, Bowen BW, Dueñas RB, Casale P, Choudhury BC, Costa A, Dutton PH, Fallabrino A, Girard A, Girondot M, Godfrey MH, Hamann M, López-Mendilaharsu M, Marcovaldi MA, Mortimer JA, Musick JA, Nel R, Pilcher NJ, Seminoff JA, Troëng S, Witherington B, Mast RB (2010) Regional management units for marine turtles: a novel framework for prioritizing conservation and research across multiple scales. PLoS One 5:e15465CrossRefGoogle Scholar
  43. Wolf KN, Harms CA, Beasley JF (2008) Evaluation of ve clinical chemistry analyzers for use in health assessment in sea turtles. J Am Vet Med Assoc 233:470–475CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Toxicology area. Faculty of Veterinary Medicine, Regional Campus of International Excellence ‘Campus Mare Nostrum’University of MurciaMurciaSpain
  2. 2.Laboratory of Ecology, Systematics and Evolution, AgroParisTech, National Center of Scientific Research (CNRS), Paris SaclayUniversité Paris-SudOrsay CedexFrance
  3. 3.Interdisciplinary Laboratory of Clinical Analysis Interlab-UMU, Faculty of Veterinary Medicine, Regional Campus of International Excellence ‘Campus Mare Nostrum’University of MurciaMurciaSpain

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