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Relationship between organochlorine pesticides and stress indicators in hawksbill sea turtle (Eretmochelys imbricata) nesting at Punta Xen (Campeche), Southern Gulf of Mexico

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Abstract

Data on the impact of environmental pollution on the homeostasis of sea turtles remains scarce, particularly in the Southern Gulf of Mexico. As many municipalities along the coastline of the Yucatan Peninsula do not rely on a waste treatment plant, these organisms could be particularly vulnerable. We searched for relationships between the presence of organochlorine pesticides (OCP) and the level of several oxidative and pollutant stress indicators of the hawksbill sea turtle (Eretmochelys imbricata) during the 2010 nesting season at Punta Xen (Campeche, Mexico). Of the 30 sampled sea turtles, endosulfans, aldrin related (aldrin, endrin, dieldrin, endrin ketone, endrin aldehyde) and dichlorodiphenyldichloroethylene (DDT) families were detected in 17, 21 and 26, respectively. Significant correlation existed between the size of sea turtles with the concentration of methoxychlor, cholinesterase activity in plasma and heptachlors family, and catalase activity and hexachlorohexane family. Cholinesterase activity in washed erythrocytes and lipid peroxidation were positively correlated with glutathione reductase activity. Antioxidant enzyme actions seem adequate as no lipids damages were correlated with any OCPs. Future studies are necessary to evaluate the effect of OCPs on males of the area due to the significant detection of methoxychlor, which target endocrine functioning and increases its concentration with sea turtles size.

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References

  • Aebi H (1984) Catalase in vitro. In: Packer L (ed) Methods in enzymology, vol. 105: Oxygen radicals in biological systems. Academic Press, London, pp 121–125

    Chapter  Google Scholar 

  • Agnihotri NP, Pandey SY, Jain HK, Srivastava KP (1977) Persistence of aldrin, dieldrin, lindane, heptachlor and p,p’-DDT in soil. J Ent Res 1:89–91

    CAS  Google Scholar 

  • Alava JJ, Keller JM, Wyneken J, Crowder L, Scott G, Kucklick JR (2011) Geographical variation of persistent organic pollutants in eggs of threatened loggerhead sea turtles (Caretta caretta) from southeastern United States. Environ Toxicol Chem 30:1677–1688

    Article  CAS  Google Scholar 

  • Becker RA, Wilks AR (2016) R version by Brownrigg R, enhancements Minka TP, Deckmyn A (2016) maps: draw geographical maps. R package version 3.1.1. https://CRAN.R-project.org/package=maps

  • Beckmen KB, Lowenstine LJ, Newman J, Hill J, Hanni K, Gerber J (1997) Clinical and pathological characterization of northern elephant seal skin disease. J Wildlife Dis 33:438–449. doi:10.7589/0090-3558-33.3.438

    Article  CAS  Google Scholar 

  • Blum JL, James MO, Stuchal LD, Denslow ND (2008) Stimulation of transactivation of the largemouth bass estrogen receptors alpha, beta-a, and beta-b by methoxychlor and its mono- and bis-demethylated metabolites in HepG2 cells. J Steroid Biochem 108:55–63. doi:10.1016/j.jsbmb.2007.06.004

    Article  CAS  Google Scholar 

  • Bucchia M, Camacho M, Santos MRD, Boada LD, Roncada P, Mateo R, Ortiz-Santaliestra ME, Rodríguez-Estival J, Zumbado M, Orós J, Henríquez-Hernández LA, García-Álvarez N, Luzardo OP (2015) Plasma levels of pollutants are much higher in loggerhead turtle populations from the Adriatic Sea than in those from open waters (Eastern Atlantic Ocean). Sci Total Environ 523:161–169. doi:10.1016/j.scitotenv.2015.03.047

    Article  CAS  Google Scholar 

  • Camacho M, Boada LD, Orós J, López P, Zumbado M, Almeida-González M, Luzardo OP (2014) Monitoring organic and inorganic pollutants in juvenile live sea turtles: results from a study of Chelonia mydas and Eretmochelys imbricata in Cape Verde. Sci Total Environ 481:303–310. doi:10.1016/j.scitotenv.2014.02.051

    Article  CAS  Google Scholar 

  • Camacho M, Luzardo OP, Boada LD, Jurado LFL, Medina M, Zumbado M, Orós J (2013) 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. doi:10.1016/j.scitotenv.2013.04.043

    Article  CAS  Google Scholar 

  • Cribb AE, Leeder JS, Spielberg SP (1989) Use of microplate reader in an assay of gluthatione reductase using 5, 5/dithiobis(2-nitrobenzoic acid). Anal Biochem 183:195–196. doi:10.1016/0003-2697(89)90188-7

    Article  CAS  Google Scholar 

  • Cuevas E, Abreu-Grobois FA, Guzman-Hernandez V, Liceaga-Correa MA, Van Dam RP (2008) Post-nesting migratory movements of hawksbill turtles Eretmochelys imbricata in waters adjacent to the Yucatan Peninsula, Mexico. Endang Species Res 10:123–133. doi:10.3354/esr00128

    Article  Google Scholar 

  • Díaz-Barriga F, Borja-Aburto V, Waliszewski S, Yáñez L (2003) DDT in Mexico. In: Fiedler H (ed) Persistent organic pollutants. Springer, Berlin and Heidelberg, pp 371–388

    Chapter  Google Scholar 

  • Doherty JD, Matsumura F (1975) DDT effects on certain ATP related systems in the peripheral nervous system of the lobster Homarus americanus. Pestic Biochem Phys 5:242–252. doi:10.1016/0048-3575(75)90006-1

    Article  CAS  Google Scholar 

  • Elgar KE (1975) The dissipation and accumulation of aldrin and dieldrin residues in soil. Environ Qual Safety 3:250–257

    CAS  Google Scholar 

  • Ellman GL, Courtney D, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95. doi:10.1016/0006-2952(61)90145-9

    Article  CAS  Google Scholar 

  • Finlayson KA, Leusch FDL, van de Merwe JP (2016) The current state and future directions of marine turtle toxicology research. Environ Int 94:113–123. doi:10.1016/j.envint.2016.05.013

    Article  CAS  Google Scholar 

  • Folmar LC, Hemmer MJ, Denslow ND, Kroll K, Chen J, Cheek A, Richman H, Meredith H, Grau EG (2002) A comparison of the estrogenic potencies of estradiol, ethynylestradiol, diethylstilbestrol, nonylphenol and methoxychlor in vivo and in vitro. Aquat Toxicol 60:101–110. doi:10.1016/S0166-445X(01)00276-4

    Article  CAS  Google Scholar 

  • Fossi MC, Marsili L, Neri G, Natoli A, Politi E, Panigada S (2003) The use of a non-lethal tool for evaluating toxicological hazard of organochlorine contaminants in Mediterranean cetaceans: new data 10 years after the first paper published in MPB. Mar Pollut Bull 46:972–982. doi:10.1016/S0025-326X(03)00113-9

    Article  Google Scholar 

  • Fossi MC, Minutoli R, Guglielmo L (2001) Preliminary results of biomarker responses in zooplankton of brackish environments. Mar Pollut Bull 42:745–748. doi:10.1016/S0025-326X(00)00214-9

    Article  CAS  Google Scholar 

  • Fulton MH, Key PB (2001) Acetylcholinesterase inhibition in estuarine fish and invertebrates as an indicator of organophosphorus insecticide exposure and effects. Environ Toxicol Chem 20:37–45. doi:10.1002/etc.5620200104

    Article  CAS  Google Scholar 

  • García-Besné G, Valdespino C, Rendón von Osten J (2015) Comparison of organochlorine pesticides and PCB residues among hawksbill (Eretmochelys imbricata) and green (Chelonia mydas) turtles in the Yucatan Peninsula and their maternal transfer. Mar Pollut Bull 91:139–148. doi:10.1016/j.marpolbul.2014.12.015

    Article  Google Scholar 

  • Gardner SC, Pier MD, Wesselman R, Juárez JA (2003) Organochlorine contaminants in sea turtles from the Eastern Pacific. Mar Pollut Bull 46:1082–1089. doi:10.1016/S0025-326X(03)00254-6

    Article  CAS  Google Scholar 

  • Garduño-Andrade M, Guzmán V, Miranda E, Briseño-Dueñas R, Abreu-Grobois FA (1999) Increases in hawksbill turtle (Eretmochelys imbricata) nestings in the Yucatan Peninsula, Mexico, 1977-1996: data in support of successful conservation? Chelonian Conserv Bi 3:286–295

    Google Scholar 

  • González-Farias F, Cisneros Estrada X, Fuentes Ruíz C, Díaz González G, Botello AV (2002) Pesticides distribution in sediments of a tropical coastal lagoon adjacent to an irrigation district in northwest Mexico. Environ Technol 23:1247–1256. doi:10.1080/09593332308618323

    Article  Google Scholar 

  • Guilhermino L, Lopes MC, Carvalho AP, Soares AMVM (1996) Inhibition of acetylcholinesterase activity as effect criterion in acute tests with juvenile Daphnia magna. Chemosphere 32:727–738. doi:10.1016/0045-6535(95)00360-6

    Article  CAS  Google Scholar 

  • Gupta HCL, Kavadia VS (1979) Dissipation of aldrin residues in clay loam soil under the cover of root crops. Ind J Plant Protection 7:43–49

    CAS  Google Scholar 

  • Habig WH, Jakoby HB (1981) Glutathione S-Tranferases (rat and human). In: Jakoby WB (ed) Methods in enzymology, vol. 77: detoxication and drug metabolism: conjugation and related systems. Academic Press, London, pp 218–235

    Chapter  Google Scholar 

  • Halliwell B, Gutteridge JMC (2007) Free radicals in biology and medicine, 3rd edn. Oxford University Inc., New York, NY

    Google Scholar 

  • Harris HS, Benson SR, Gilardi KV, Poppenga RH, Work TM, Dutton PH, Mazet JA (2011) Comparative health assessment of Western Pacific leatherback turtles (Dermochelys coriacea) foraging off the coast of California, 2005-2007. J Wildlife Dis 47:321–337. doi:10.7589/0090-3558-47.2.321

    Article  CAS  Google Scholar 

  • Helsel DR (2012) Statistics for censored environmental data using minitab and R, 2nd edn. Wiley, New Jersey, NJ

    Google Scholar 

  • Herbst LH, Jacobson ER (1995) Diseases of marine turtles. In: Bjorndal KA (ed) Biology and conservation of Sea Turtles, Revised edn. Smithsonian Institution Press, Washington, DC, pp 593–596

    Google Scholar 

  • INECC or Instituto Nacional de Ecología y Cambio Climático (2015a) Lista de plaguicidas restringidos en México. Updated 26 Jun 2015. http://www2.inecc.gob.mx/sistemas/plaguicidas/lrestring.html. Accessed 4 Sep 2016

  • INECC (2015b) Lista de plaguicidas prohibidos en México. Updated 26 Jun 2015. http://www2.inecc.gob.mx/sistemas/plaguicidas/lprohibi.html. Accessed 4 Sep 2016

  • IUCN or International Union for Conservation of Nature (2016) The IUCN Red List of Threatened Species. Version 2016-2. http://www.iucnredlist.org. Accessed 4 Sep 2016

  • Keller JM, Kucklick JR, McClellan-Green PD (2004) Organochlorine contaminants in loggerhead sea turtle blood: Extraction techniques and distribution among plasma and red blood cells. Arch Environ Contam Toxicol 46:254–264. doi:10.1007/s00244-003-2262-z

    CAS  Google Scholar 

  • 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 114:70–76. doi:10.1289/ehp.8143

    Article  CAS  Google Scholar 

  • Labrada-Martagón V, Méndez-Rodríguez LC, Gardner SC, López-Castro M, Zenteno-Savín T (2010) Health indices of the green turtle (Chelonia mydas) along the Pacific coast of Baja California Sur, Mexico. I. Blood biochemistry values. Chelonian Conserv Bi 9:162–172. doi:10.2744/CCB-0806.1

    Article  Google Scholar 

  • Labrada-Martagón V, Tenorio Rodríguez PA, Méndez-Rodríguez LC, Zenteno-Savín T (2011) Oxidative stress indicators and chemical contaminants in East Pacific green turtles (Chelonia mydas) inhabiting two foraging coastal lagoons in the Baja California península. Comp Biochem Phys C 154:65–75. doi:10.1016/j.cbpc.2011.02.006

    Google Scholar 

  • Lahvis GP, Wells RS, Kuehl DW, Stewart JL, Rhinehart HL, Via CS (1995) Decreased lymphocyte responses in free-ranging bottlenose dolphins (Tursiops truncatus) are associated with increased concentrations of PCBs and DDT in peripheral blood. Environ Health Persp 103:67–72

    Article  CAS  Google Scholar 

  • Larkin P, Knoebl I, Denslow ND (2003) Differential gene expression analysis in fish exposed to endocrine disrupting compounds. Comp Biochem Phys B 136:149–161. doi:10.1016/S1096-4959(03)00228-8

    Article  CAS  Google Scholar 

  • Lazar B, Maslov L, Romanić SH, Gračan R, Krauthacker B, Holcer D, Tvrtković N (2011) Accumulation of organochlorine contaminants in loggerhead sea turtles, Caretta caretta, from the eastern Adriatic Sea. Chemosphere 82:121–129. doi:10.1016/j.chemosphere.2010.09.015

    Article  CAS  Google Scholar 

  • Lopaka L (2013) NADA: Nondetects and data analysis for environmental data. R package version 1.5-6. https://CRAN.R-project.org/package=NADA

  • McKenzie C, Godley BJ, Furness RW, Wells DE (1999) Concentrations and patterns of organochlorine contaminants in marine turtles from Mediterranean and Atlantic waters. Marine Environ Res 47:117–135. doi:10.1016/S0141-1136(98)00109-3

    Article  CAS  Google Scholar 

  • Mast RB, Hutchinson BJ, Howtage ENJP (2005) IUCN/SSC marine turtle specialist group hosts the second burning issues assessment workshop. Marine Turtle Newsl 110:13–15

    Google Scholar 

  • Meylan AB, Donnelly M (1999) Status justification for listing the hawksbill turtle (Eretmochelys imbricata) as critically endangered on the 1996 IUCN Red List of threatened animals. Chelonian Conserv Bi 3:200–224

    Google Scholar 

  • Morales-Caselles C, Martín-Díaz ML, Riba I, Sarasquete C, Valls TÁD (2008) The role of biomarkers to assess oil-contaminated sediment quality using toxicity tests with clams and crabs. Environ Toxicol Chem 27:1309–1316. doi:10.1897/07-371.1

    Article  CAS  Google Scholar 

  • Oberdörster E, Cheek AO (2001) Gender benders at the beach: Endocrine disruption in marine and estuarine organisms. Environ Toxicol Chem 20:23–36. doi:10.1002/etc.5620200103

    Article  Google Scholar 

  • Oh M, Kasthuri SR, Wan Q, Bathige SDNK, Whang I, Lim B-S, Jung H-B, Oh M-J, Jung S-J, Kim SY, Lee J (2013) Characterization of MIF family proteins: MIF and DDT from rock bream, Oplegnathus fasciatus. Fish Shellfish Immun 35:458–468. doi:10.1016/j.fsi.2013.05.003

    Article  CAS  Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos, Stevens MHH, Szoecs E, Wagner H (2016) Vegan: community ecology package. R package version 2.4-0. https://CRAN.R-project.org/package=vegan

  • Owens DW, Ruiz GJ (1980) New methods of obtaining blood and cerebrospinal fluid from marine turtles. Herpetologica 36:17–20

    Google Scholar 

  • Persky AM, Green PS, Stubley L, Howell CO, Zaulyanov L, Brazeau GA, Simpkins JW (2000) Protective effect of estrogens against oxidative damage to heart and skeletal muscle in vivo and in vitro. Proc Soc Exp Biol Med 223:59–66

    Article  CAS  Google Scholar 

  • Peters CF, Weber DD (1977) DDT: Effect on the lateral line nerve of steelhead trout. In: Vernberg FJ, Calabrese J, Thurberg FP, Vernberg WB (eds) Physiological responses of marine biota to pollutants. Academic Press, New York, NY, pp 75–91

    Chapter  Google Scholar 

  • Piazza R, Ruiz-Fernández AC, Frignani M, Zangrando R, Bellucci LG, Moret I, Páez-Osuna F (2008) PCBs and PAHs in surficial sediments from aquatic environments of Mexico City and the coastal states of Sonora, Sinaloa, Oaxaca and Veracruz (Mexico). Environ Geol 54:1537–1545. doi:10.1007/s00254-007-0935-z

    Article  CAS  Google Scholar 

  • Pippenger CE, Brown RW, Armstrong D (1998) Regulatory antioxidant enzymes. In: Armstrong D (ed) Methods in molecular biology. Humana Press, Nueva Jersey, NJ, pp 299–313

    Google Scholar 

  • Presti SM, Hidalgo ARS, Seminoff JA (1999) Mercury Concentration in the Scutes of Black Sea Turtles, Chelonia mydas agassizii, in the Gulf of California. Chelonian Conserv 3:531–533

    Google Scholar 

  • R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, www.R-project.org

  • Ragland JM, Arendt MD, Kucklick JR, Keller JM (2011) Persistent organic pollutants in blood plasma of satellite-tracked adult male loggerhead sea turtles (Caretta caretta). Environ Toxicol Chem 30:1549–1556. doi:10.1002/etc.540

    Article  CAS  Google Scholar 

  • Ramírez-Elías MA, Córdova-Quiroz AV, Cerón-Bretón JG, Cerón-Bretón RM, Rendón-von Osten J, Cortés-Simón JH (2016) Dichloro-Diphenyl-Trichloroethane (DDT) and endosulfan in sediments of Sabancuy lagoon, Campeche, Mexico. OJE 6:22–31. doi:10.4236/oje.2016.61003

    Article  Google Scholar 

  • Richardson K, Lopez Castro M, Gardner S, Schlenk D (2010) Polychlorinated biphenyls and biotransformation enzymes in three species of sea turtles from the Baja California Peninsula of Mexico. Arch Environ Contam Toxicol 58:183–193. doi:10.1007/s00244-009-9360-5

    Article  CAS  Google Scholar 

  • Sies H (1986) Biochemistry of oxidative stress. Angew Chem Int Ed Engl 25:1058–1071. doi:10.1002/anie.198610581

    Article  Google Scholar 

  • Sies H, Ketterer B (1988) Glutathione conjugation: mechanisms and biological significance‬. Academic Press, London

    Google Scholar 

  • South A (2012) rworldxtra: Country boundaries at high resolution. R package, version 1.01. https://CRAN.R-project.org/package=rworldxtra

  • Spotila JR (2004) Sea Turtles: a complete guide to their biology, behavior, and conservation. Johns Hopkins University Press, Baltimore, MD, pp 240. Oakwood Arts

    Google Scholar 

  • Storelli MM, Barone G, Marcotrigiano GO (2007) Polychlorinated biphenyls and other chlorinated organic contaminants in the tissues of Mediterranean loggerhead turtle Caretta caretta. Sci Total Environ 373:456–463. doi:10.1016/j.scitotenv.2006.11.040

    Article  CAS  Google Scholar 

  • Suzuki K (2000) Measurement of Mn-SOD and Cu, Zn-SOD. In: Taniguchi N, Gutteridge J (eds) Experimental protocols for reactive oxygen and nitrogen species. Oxford University Press, New York, NY, pp 91–95

    Google Scholar 

  • Swarthout RF, Keller JM, Peden-Adams M, Landry AM, Fair PA, Kucklick JR (2010) Organohalogen contaminants in blood of Kemp’s ridley (Lepidochelys kempii) and green sea turtles (Chelonia mydas) from the Gulf of Mexico. Chemosphere 78:731–741. doi:10.1016/j.chemosphere.2009.10.059

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Walker CH (2009) Organic pollutants: an ecotoxicological perspective, 2nd edn. CRC press Taylor & Francis Group, Boca Raton, FL

    Google Scholar 

  • Wiese IH, Basson NCJ (1966) The degradation of some persistent chlorinated hydrocarbon, insecticides applied to different soil types. S Afr J Agric Sci 9:945–970

    CAS  Google Scholar 

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Acknowledgements

The license (SGPA/DGVS/05470/10) to collect the blood samples of 30 turtles was provided by the Secretaria de Medio Ambiente y Recursos Naturales (SEMARNAT). The authors want to thank the turtle camp Grupo Ecologista Quelonios A.C. officials who aided in the fieldwork at Punta Xen. NT had a fellowship from the Programa de Becas posdoctorales en la Universidad Nacional Autónoma de México (Mexico). Special thanks to the three anonymous reviewers whose comments improved the manuscript.

Funding

This study was funded by CONACyT, FOMIX Campeche through the project “Diagnóstico y propuestas de acción de la contaminación de la zona costera del Estado de Campeche” (grant No. 071749).

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  1. Instituto EPOMEX, Universidad Autónoma de Campeche, Campeche, Campeche, Mexico

    Nelly Tremblay, Alejandro Ortíz Arana, Mauricio González Jáuregui & Jaime Rendón-von Osten

  2. Biología y Conservación de Vertebrados, Instituto de Ecología, A.C. Carretera antigua a Coatepec 351, El Haya, Xalapa, 91070, Veracruz, Mexico

    Mauricio González Jáuregui

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  1. Nelly Tremblay
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Correspondence to Jaime Rendón-von Osten.

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Nelly Tremblay’s present address: Unidad Multidisciplinaria de Docencia e Investigación, Facultad de Ciencias, Universidad Nacional Autónoma de México, Puerto de Abrigo s/n, Sisal, C.P. 97356, Yucatán, Mexico

Alejandro Ortiz Arana’s present address: El Colegio de la Frontera Sur, Avenida Centenario km 5.5, Apartado Postal 424, Chetumal 77014, Quintana Roo, Mexico

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Tremblay, N., Ortíz Arana, A., González Jáuregui, M. et al. Relationship between organochlorine pesticides and stress indicators in hawksbill sea turtle (Eretmochelys imbricata) nesting at Punta Xen (Campeche), Southern Gulf of Mexico. Ecotoxicology 26, 173–183 (2017). https://doi.org/10.1007/s10646-016-1752-5

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