Skip to main content
SpringerLink
Log in

Mercury and Organochlorine Pesticides in Tissues of Loggerhead Sea Turtles (Caretta caretta) Stranded Along the Southwestern Mediterranean Coastline (Andalusia, Spain)

  • Published:
Bulletin of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

Nineteen loggerhead sea turtles (Caretta caretta) stranded along the southwestern Mediterranean coastline (Andalusia) were used in this study. A total of 68 samples of fat (n = 18), liver (n = 15), kidney (n = 13), pectoral muscle (n = 19), and brain (n = 3) were analysed for total mercury (Hg) and organochlorine pesticides [OC: ∑Dichlorodiphenyltrichloroethanes (∑DDT), ∑Hexachlorocyclohexane (∑HCH), ∑Heptachlor, ∑Drins and ∑Endosulfan]. These loggerhead sea turtles showed tissue Hg and OC concentrations similar to or lower than those reported in other studies. Few growth-related variations in Hg or OC levels in relation to straight carapace length were found, probably because the specimens were mostly juveniles. This study will help to fill the gap on spatio-temporal exposure data and ascertain the real world-wide picture of the contamination levels in loggerhead sea turtles.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aguilar A (1984) Relationships of DDE/DDT in marine mammals to the chronology of DDT input into ecosystems. Can J Fish Aquat Sci 41:840–844

    CAS  Google Scholar 

  • Bjorndal KA, Bolten A, Bennet R, Jacobson ER, Wronski TJ, Valeski JJ, Eleazar PJ (1998) Age and growth in sea turtles: limitations of skeletochronology for demographic studies. Copeia 1:23–30

    Google Scholar 

  • Blus LJ, Henny CJ, Krynitsky AJ (1985) The effects of heptachlor and lindane on birds, Columbia Basin, Oregon and Washington DC, 1976–1981. Sci Total Environ 46:73–81

    CAS  Google Scholar 

  • Bucchia M, Camacho M, Santos MRD et al (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

    CAS  Google Scholar 

  • Call DJ, Shave HJ, Binger HC, Bergeland ME, Ammann BD, Worman JJ (1976) DDE poisoning in wild great blue heron. Bull Environ Contam Toxicol 16:310–313

    CAS  Google Scholar 

  • Camacho M, Oros J, Boada LD, Zaccaroni A, Silvi M, Formigaro C et al (2013a) 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

    CAS  Google Scholar 

  • Camacho M, Luzardo OP, Boada LD, López Jurado LF, Medina M, Zumbado M, Orósa J (2013b) 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

    Google Scholar 

  • Casale P, Freggi D, Basso R, Argano R (2005) Size at male maturity, sexing methods and adult sex ratio in loggerhead turtles (Caretta caretta) from Italian waters investigated through tail measurements. Herpetol J 15:145–148

    Google Scholar 

  • Casale P, Tucker AD (2017) Caretta caretta (amended version of 2015 assessment). The IUCN Red List of Threatened Species 2017: e.T3897A119333622. Downloaded on 20 January 2020.

  • Commission Decision of 30 September 2008 concerning the non-inclusion of dicofol in Annex I to Council Directive 91/414/EEC and the withdrawal of authorisations for plant protection products containing that substance

  • Cortés-Gómez AA, Romero D, Girondot M (2017) The current situation of inorganic elements in marine turtles: A general review and meta-analysis. Environ Pollut 229:567–585

    Google Scholar 

  • D’Ilio S, Mattei D, Blasi MF, Alimonti A, Bogialli S (2011) The occurrence of chemical elements and POPs in loggerhead turtles (Caretta caretta): an overview. Mar Pollut Bull 62(8):1606–1615

    Google Scholar 

  • 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 Perspect 115(10):1421–1428

    CAS  Google Scholar 

  • Day RD, Christopher SJ, Becker PR, Whitaker DW (2005) Monitoring mercury in the loggerhead sea turtle. Caretta caretta Environ Sci Technol 39(2):437–446

    CAS  Google Scholar 

  • Dodd CK Jr (1988) Synopsis of the biological data on the loggerhead sea turtle Caretta caretta (Linnaeus 1758). US Fish and Wildlife Service Biological Report 88(14): 110.

  • Espín S, García-Fernández AJ, Herzke D et al (2016) Tracking pan-continental trends in environmental contamination using sentinel raptors – what types of samples should we use? Ecotoxicology 25(4):777–801

    Google Scholar 

  • Espín S, Martínez-López E, Gómez-Ramírez P, María-Mojica P, García-Fernández AJ (2010) Assessment of organochlorine pesticide exposure in a wintering population of razorbills (Alca torda) from the Southwestern Mediterranean. Chemosphere 80:1190–1198

    Google Scholar 

  • Espín S, Martínez-López E, Gómez-Ramírez P, María-Mojica P, García-Fernández AJ (2012a) Razorbills (Alca torda) as bioindicators of mercury pollution in the southwestern Mediterranean. Mar Pollut Bull 64(11):2461–2470

    Google Scholar 

  • Espín S, Martínez-López E, María-Mojica P, García-Fernández AJ (2012b) Razorbill (Alca torda) feathers as an alternative tool for evaluating exposure to organochlorine pesticides. Ecotoxicology 21(1):183–190

    Google Scholar 

  • Finlayson KA, Leusch FDL, van de Merwe JP (2019) Cytotoxicity of organic and inorganic compounds to primary cell cultures established from internal tissues of Chelonia mydas. Sci Total Environ 664:958–967

    CAS  Google Scholar 

  • García-Fernández AJ, Espín S, Gómez-Ramírez P, Martínez-López E, Navas I (2020) Wildlife Sentinels for Human and Environmental Health Hazards in Ecotoxicological Risk Assessment. In: Roy K (ed) Ecotoxicological QSARs. Methods in Pharmacology and Toxicology, Springer, LLC, pp 77–94

    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(2):557–563

    Google Scholar 

  • Godley BJ, Smith SM, Clark PF, Taylor JD (1997) Molluscan and crustacean items in the diet of the loggerhead turtle, Caretta caretta (Linnaeus, 1758) Testudines: Chelonidae in the eastern Mediterranean. J Molluscan Stud 63:474–476

    Google Scholar 

  • Hopkins BC, Willson JD, Hopkins WA (2013) Mercury exposure is associated with negative effects on turtle reproduction. Environ Sci Technol 47(5):2416–2422

    CAS  Google Scholar 

  • Jæger I, Hop H, Gabrielsen GW (2009) Biomagnification of mercury in selected species from an Arctic marine food web in Svalbard. Sci Total Environ 407:4744–4751

    Google Scholar 

  • Kampalath R, Gardner SC, Mendez-Rodriguez L, Jay JA (2006) Total and methylmercury in three species of sea turtles of Baja California Sur. Mar Pollut Bull 52:1784–1832

    Google Scholar 

  • Kawai S, Fukushima M, Miyazaki N, Tatsukawa R (1988) Relationship between lipid composition and organochlorine levels in tissues of Striped Dolphin. Mar Pollut Bull 19:129–133

    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

    CAS  Google Scholar 

  • 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(10):1074–1079

    CAS  Google Scholar 

  • Law RJ, Fileman CF, Hopkins AD, Baker JR, Harwood J, Jackson DB, Kennedy S, Martin AR, Morris RJ (1991) Concentrations of trace metals in the livers of marine mammals (seals, porpoises and dolphins) from waters around the British Isles. Mar Pollut Bull 22:183–191

    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(1):121–129

    CAS  Google Scholar 

  • Li YF, Cai DJ, Singh A (1998) Technical hexachlorocyclohexane use trends in China and their impact on the environment. Arch Environ Contam Toxicol 35:688–697

    CAS  Google Scholar 

  • Lutcavage ME, Plotkin P, Witherington B, Lutz PL (1997) Human impacts on sea turtle survival. In: Lutz PL, Musick JA (eds) The Biology of Sea Turtles. CRC, Boca Raton, FL, pp 387–409

    Google Scholar 

  • Maffucci F, Caurant F, Bustamante P, Bentivegna F (2005) Trace element (Cd, Cu, Hg, Se, Zn) accumulation and tissue distribution in loggerhead turtles (Caretta caretta) from the Western Mediterranean Sea (southern Italy). Chemosphere 58(5):535–542

    CAS  Google Scholar 

  • Malarvannan G, Takahashi S, Isobe T, Kunisue T, Sudaryanto A, Miyagi T, Nakamura M, Yasumura S, Tanabe S (2011) Levels and distribution of polybrominated diphenyl ethers and organochlorine compounds in sea turtles from Japan. Mar Pollut Bull 63(5–12):172–178

    CAS  Google Scholar 

  • Margaritoulis D, Argano R, Baran I, Bentivegna F, Bradai MN, Camiñas JA, Casale P, De Metrio G, Demetropoulos A, Gerosa G, Godley BJ, Haddoud DA, Houghton J, Laurent L, Lazar B (2003) Loggerhead turtles in the Mediterranean Sea: present knowledge and conservation perspectives. In: Bolten AB, Witherington BE (eds) Loggerhead Sea Turtles. Smithsonian Books, Washington, pp 175–198

    Google Scholar 

  • María-Mojica P, Jiménez P, Barba A, Navas I, García-Fernández AJ (2000) Residuos de insecticidas organoclorados en Cernícalo común (Falco tinnunculus) de la Región de Murcia. An Vet (Murcia) 16:55–66

    Google Scholar 

  • Martínez-López E, Gómez-Ramírez P, Espín S, Aldeguer MP, García-Fernández AJ (2017) 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(2):167–172

    Google Scholar 

  • Martínez-López E, Peñalver J, Escriña A, Lara L, Gens MJ, María-Dolores E, Alcaraz A, García-Fernández AJ (2019a) Trace metals in striped dolphins (Stenella coeruleoalba) stranded along the Murcia coastline, Mediterranean Sea, during the period 2009–2015. Chemosphere 229:580–588

    Google Scholar 

  • Martínez-López E, Peñalver J, Lara L, García-Fernández AJ (2019b) Hg and Se in organs of three cetacean species from the Murcia Coastline (Mediterranean Sea). Bull Environ Contam Toxicol 103(4):521–527

    Google Scholar 

  • McKenzie C, Godley BJ, Furness RW, Wells DE (1999) Concentrations and patterns of organochlorine contaminants in marine turtles from Mediterranean and Atlantic waters. Mar Environ Res 47:117–135

    CAS  Google Scholar 

  • Merhaby D, Rabodonirina S, Net S, Ouddane B, Halwani J (2019) Overview of sediments pollution by PAHs and PCBs in mediterranean basin: transport, fate, occurrence, and distribution. Mar Poll Bull 149:110646

    CAS  Google Scholar 

  • Muñoz-Arnanz J, Jiménez B (2011) New DDT inputs after 30 years of prohibition in Spain. A case study in agricultural soils from south-western Spain. Environ Pollut 159:3640–3646

    Google Scholar 

  • Novillo O, Pertusa JF, Tomas J (2017) Exploring the presence of pollutants at sea: monitoring heavy metals and pesticides in loggerhead turtles (Caretta caretta) from the western Mediterranean. Sci Total Environ 598:1130–1139

    CAS  Google Scholar 

  • Perugini M, Giammarino A, Olivieri V, Guccione S, Lai OR, Amorena M (2006) Polychlorinated biphenyls and organochlorine pesticide levels in tissues of Caretta caretta from the Adriatic Sea. Dis Aquat Organ 71:155–161

    CAS  Google Scholar 

  • Pratt HM (1972) Nesting success of common egrets and great blue herons in the San Francisco bay region. Condor 74:447–453

    Google Scholar 

  • Regulation (EC) (2004) No 850/2004 of the european parliament and of the council of 29 April 2004 on persistent organic pollutants and amending directive 79/117/EEC. Official Journal L 158:7–49

  • Rybitski MJ, Hale RC, Musick JA (1995) Distribution of Organochlorine Pollutants in Atlantic Sea Turtles. Copeia 2:379–390

    Google Scholar 

  • Sakai H, Saeki K, Ichihashi H, Suganuma H, Tanabe S, Tatsukawa R (2000a) Species-specific distribution of heavy metals in tissues and organs of loggerhead turtle (Caretta caretta) and green turtle (Chelonia mydas) from Japanese coastal waters. Mar Pollut Bull 40:701–709

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Scheuhammer AM (1987) The chronic toxicity of aluminium, cadmium, mercury, and lead in birds: a review. Environ Pollut 46:263–295

    CAS  Google Scholar 

  • Schneider L, Maher W, Green A, Vogt RC (2013) Mercury contamination in reptiles: an emerging problem with consequences for wild life and human health. In: Kim KH, Richard JCB (eds) Mercury: sources, applications and health impacts. Nova Science Publishers Inc, New York, pp 173–232

    Google Scholar 

  • Schuyler Q, Hardesty BD, Wilcox C, Townsend K (2012) To eat or not to eat? Debris selectivity by marine turtles. PLoS ONE 7(7):e40884

    CAS  Google Scholar 

  • Stickel WH, Stickel LF, Spann JW (1969) Tissue residues of dieldrin in relation to mortality in birds and mammals. In: Miller MW, Berg GG (eds) Chemical Fallout: Current Research on Persistent Pesticides. Charles C Thomas, Springfield, Illinois, p 174

    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(2–3):456–463

    CAS  Google Scholar 

  • Storelli MM, Ceci E, Marcotrigiano GO (1998a) Distribution of heavy metal residues in some tissues of Caretta caretta (Linnaeus) specimen beached along the Adriatic Sea (Italy). Bull Environ Contam Toxicol 60(4):546–552

    CAS  Google Scholar 

  • Storelli MM, Ceci E, Marcotrigiano GO (1998b) Comparison of total mercury, methylmercury, and selenium in muscle tissues and in the liver of Stenella coeruleoalba (Meyen) and Caretta caretta (Linnaeus). Bull Environ Contam Toxicol 61(4):541–547

    CAS  Google Scholar 

  • Storelli MM, Marcotrigiano GO (2000) Chlorobiphenyls, HCB, and organochlorine pesticides in some tissues of Caretta caretta (Linnaeus) specimens beached along the Adriatic Sea. Italy Bull Environ Contam Toxicol 64(4):481–488

    CAS  Google Scholar 

  • 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(1):163–170

    CAS  Google Scholar 

  • Teas WG (1993) Species composition and size class distribution of marine turtle strandings on the Gulf of Mexico and southeast United States coasts, 1985–1991. U.S. Dep. Commer., NOAA Tech. Memo. NMFS-SEFSC-315, pp 43.

  • Tong J, Wang Y, Lu Y (2016) In vitro evaluation of inorganic and methyl mercury mediated cytotoxic effect on neural cells derived from different animal species. J Environ Sci 41:138–145

    CAS  Google Scholar 

  • Torrent A, González-Díaz OM, Monagas P, Orós J (2004) Tissue distribution of metals in loggerhead turtles (Caretta caretta) stranded in the Canary Islands, Spain. Mar Poll Bull 49:854–860

    CAS  Google Scholar 

  • Van der Gon HD, Van het Bolscher M, Visschedijk A, Zandveld P (2007) Emissions of persistent organic pollutants and eight candidate POPs from UNECE-Europe in 2000, 2010 and 2020 and the emission reduction resulting from the implementation of the UNECE POP Protocol. Atmos Environ 41:9245–9261

    Google Scholar 

  • Zillioux EJ, Porcella DB, Benoit JM (1993) Mercury cycling and effects in freshwater wetland ecosystems. Environ Toxicol Chem 12:2245–2264

    CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by the Aula del Mar (Málaga), and projects from the Spanish Government (MASCA’2008 CGL-2008-4318/BOS-and NOVEDAR-CONSOLIDER - CSD00C-07-22204). Silvia Espín was funded by Ministerio de Ciencia, Innovación y Universidades (Juan de la Cierva-Incorporación contract, IJCI-2017-34653). Thanks to Juan J. Castillo and Juan J. Bellido from CREMA (Threatened Marine Species Rehabilitation Centre- Aula del Mar, Málaga) for their inestimable help with sampling and necropsies, and C. Bolumar for collaborating with the analysis of mercury.

Author information

Author notes

  1. Pilar Gómez-Ramírez and Silvia Espín have contributed equally and should be considered co-first authors.

Authors and Affiliations

  1. Toxicology and Risk Assessment Research Group, IMIB-Arrixaca, Faculty of Veterinary, University of Murcia, Campus de Espinardo, 30100, Murcia, Spain

    Pilar Gómez-Ramírez, Silvia Espín, Isabel Navas, Emma Martínez-López, Pedro Jiménez, Pedro María-Mojica, José Peñalver & Antonio J. García-Fernández

Authors
  1. Pilar Gómez-Ramírez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Silvia Espín
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Isabel Navas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Emma Martínez-López
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pedro Jiménez
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Pedro María-Mojica
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. José Peñalver
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Antonio J. García-Fernández
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Silvia Espín or Antonio J. García-Fernández.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOC 129 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gómez-Ramírez, P., Espín, S., Navas, I. et al. Mercury and Organochlorine Pesticides in Tissues of Loggerhead Sea Turtles (Caretta caretta) Stranded Along the Southwestern Mediterranean Coastline (Andalusia, Spain). Bull Environ Contam Toxicol 104, 559–567 (2020). https://doi.org/10.1007/s00128-020-02822-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00128-020-02822-z

Keywords

Search

Navigation