Exposure to a mixture of organic pollutants in a threatened freshwater turtle Emys orbicularis: effects of age, sex, and temporal variation

Leslie-Anne Merleau; Olivier Lourdais; Anthony Olivier; Marion Vittecoq; Fabrice Alliot; Sira Traore; Carole Leray; Aurélie Goutte

doi:10.24072/pcjournal.684

journal article Mar 09, 2026

Exposure to a mixture of organic pollutants in a threatened freshwater turtle Emys orbicularis: effects of age, sex, and temporal variation

Leslie-Anne Merleau

Sira Traore Carole Leray Aurélie Goutte

Peer Community Journal Vol. 6 · Peer Community In

View at Publisher Save 10.24072/pcjournal.684

Abstract

Freshwater ecosystems constitute major sinks for organic contaminants, increasing anthropogenic pressures and threatening the unique biodiversity they harbour. In addition to persistent legacy compounds, such as polychlorinated biphenyls (PCBs) and organochlorine pesticides (OCPs), various pollutants are less persistent but are chronically released, including polycyclic aromatic hydrocarbons (PAHs), phthalate diesters (PAEs), pyrethroid pesticides, and insect repellent. Heretofore, these pollutants have received insufficient attention in freshwater reptiles, considering their potential to trigger detrimental effects on organisms. During two years (2019 and 2020), we quantified plasma levels of 46 compounds from 7 chemical families in two monitored populations of the protected European pond turtle (
Emys orbicularis
) in the Camargue wetland, France. PAHs and PAEs were found predominantly and concomitantly, with similar occurrences and levels in the two populations. We observed similar inter-annual variations in PAHs and PAEs with differences between males and females, highlighting the need for a better assessment of the role of sex in the exposure pathway and the toxicokinetics of contaminants, especially in turtles. The negative relationship between PAH levels and age, as well as the high intra-individual variation in levels of both contaminant families, provides further evidence of limited bioaccumulation of these pollutants in the blood of
E. orbicularis
. This could be explained by the metabolic biotransformation of parent compounds, highlighting the need to quantify the levels of PAH metabolites and phthalate monoesters. Finally, our work underscores the importance of long-term monitoring to better determine the vulnerability of turtle populations already exposed to a wide range of contaminants.

Topics

No keywords indexed for this article. Browse by subject →

References

95

[1]

[1] Alam, Mohammad Shah; Maowa, Zannatul; Hasan, Mohammad Nazmol Phthalates toxicity in vivo to rats, mice, birds, and fish: A thematic scoping review, Heliyon, Volume 11 (2025) no. 1, p. e41277 10.1016/j.heliyon.2024.e41277

[2]

[2] Aulsebrook, Lucinda C; Bertram, Michael G; Martin, Jake M; Aulsebrook, Anne E; Brodin, Tomas; Evans, Jonathan P; Hall, Matthew D; O’Bryan, Moira K; Pask, Andrew J; Tyler, Charles R; Wong, Bob B M Reproduction in a polluted world: implications for wildlife, Reproduction, Volume 160 (2020) no. 2, p. R13-R23 10.1530/rep-20-0154

[3]

[3] Bakola, Maria; Hernandez Carballo, Ireri; Jelastopulu, Eleni; Stuckler, David The impact of COVID-19 lockdown on air pollution in Europe and North America: a systematic review, European Journal of Public Health, Volume 32 (2022) no. 6, pp. 962-968 10.1093/eurpub/ckac118

[4]

Fitting Linear Mixed-Effects Models Using lme4

Douglas Bates, Martin Mächler, Ben Bolker et al.

Journal of Statistical Software 2015 10.18637/jss.v067.i01

[5]

[5] Beau, Frédéric; Bustamante, Paco; Michaud, Bruno; Brischoux, François Environmental causes and reproductive correlates of mercury contamination in European pond turtles (Emys orbicularis), Environmental Research, Volume 172 (2019), pp. 338-344 10.1016/j.envres.2019.01.043

[6]

[6] Bergé, Alexandre; Cladière, Mathieu; Gasperi, Johnny; Coursimault, Annie; Tassin, Bruno; Moilleron, Régis Meta-analysis of environmental contamination by phthalates, Environmental Science and Pollution Research, Volume 20 (2013) no. 11, pp. 8057-8076 10.1007/s11356-013-1982-5

[7]

[7] Berny, Philippe; Sadoul, Nicolas; Dol, Sophie; Videman, Bernadette; Kayser, Yves; Hafner, Heinz Impact of local agricultural and industrial practices on organic contamination of little egret (Egretta garzetta) eggs in the rhône Delta, Southern France, Environmental Toxicology and Chemistry, Volume 21 (2002) no. 3, pp. 520-526 10.1002/etc.5620210308

[8]

[8] Blasi, Monica Francesca; Avino, Pasquale; Notardonato, Ivan; Di Fiore, Cristina; Mattei, Daniela; Gauger, Marco Friedrich Walter; Gelippi, Michelle; Cicala, Davide; Hochscheid, Sandra; Camedda, Andrea; De Lucia, Giuseppe Andrea; Favero, Gabriele Phthalate esters (PAEs) concentration pattern reflects dietary habitats (δ13C) in blood of Mediterranean loggerhead turtles (Caretta caretta), Ecotoxicology and Environmental Safety, Volume 239 (2022), p. 113619 10.1016/j.ecoenv.2022.113619

[9]

[9] Burkart, Louisiane; Olivier, Anthony; Lourdais, Olivier; Vittecoq, Marion; Blouin‐Demers, Gabriel; Alliot, Fabrice; Le Gac, Clément; Martin, Nicolas; Goutte, Aurélie Determinants of Legacy Persistent Organic Pollutant Levels in the European Pond Turtle (Emys orbicularis) in the Camargue Wetland, France, Environmental Toxicology and Chemistry, Volume 40 (2021) no. 8, pp. 2261-2268 10.1002/etc.5077

[10]

[10] Camacho, María; Boada, Luis D.; Orós, Jorge; Calabuig, Pascual; Zumbado, Manuel; Luzardo, Octavio P. Comparative study of polycyclic aromatic hydrocarbons (PAHs) in plasma of Eastern Atlantic juvenile and adult nesting loggerhead sea turtles (Caretta caretta), Marine Pollution Bulletin, Volume 64 (2012) no. 9, pp. 1974-1980 10.1016/j.marpolbul.2012.06.002

[11]

[11] Camacho, María; Luzardo, Octavio P.; Boada, Luis D.; López Jurado, Luis F.; Medina, María; Zumbado, Manuel; Orós, Jorge Potential adverse health effects of persistent organic pollutants on sea turtles: Evidences from a cross-sectional study on Cape Verde loggerhead sea turtles, Science of The Total Environment, Volume 458-460 (2013), pp. 283-289 10.1016/j.scitotenv.2013.04.043

[12]

[12] Campioni, Letizia; Oró-Nolla, Bernat; Granadeiro, José P.; Silva, Mónica C.; Madeiros, Jeremy; Gjerdrum, Carina; Lacorte, Silvia Exposure of an endangered seabird species to persistent organic pollutants: Assessing levels in blood and link with reproductive parameters, Science of The Total Environment, Volume 930 (2024), p. 172814 10.1016/j.scitotenv.2024.172814

[13]

[13] Castanet, Jacques Les méthodes d’estimation de l’âge chez les chéloniens, Mésogée, Volume 48 (1988), pp. 21-28

[14]

[14] Cocci, Paolo; Mosconi, Gilberto; Bracchetti, Luca; Nalocca, John Mark; Frapiccini, Emanuela; Marini, Mauro; Caprioli, Giovanni; Sagratini, Gianni; Palermo, Francesco Alessandro Investigating the potential impact of polycyclic aromatic hydrocarbons (PAHs) and polychlorinated biphenyls (PCBs) on gene biomarker expression and global DNA methylation in loggerhead sea turtles (Caretta caretta) from the Adriatic Sea, Science of The Total Environment, Volume 619-620 (2018), pp. 49-57 10.1016/j.scitotenv.2017.11.118

[15]

[15] Couture, Patrice Plasma levels of organic pollutants in the protected European pond turtle *Emys orbicularis* from the Camargue wetland reflect past and present urban, industrial and agricultural activities in its watershed, Peer Community in Ecotoxicology and Environmental Chemistry, Volume 1 (2026), p. 100252 10.24072/pci.ecotoxenvchem.100252

[16]

[16] Dendievel, André-Marie; Mourier, Brice; Dabrin, Aymeric; Delile, Hugo; Coynel, Alexandra; Gosset, Antoine; Liber, Yohan; Berger, Jean-François; Bedell, Jean-Philippe Metal pollution trajectories and mixture risk assessed by combining dated cores and subsurface sediments along a major European river (Rhône River, France), Environment International, Volume 144 (2020), p. 106032 10.1016/j.envint.2020.106032

[17]

[17] Dron, Julien; Ratier, Aude; Austruy, Annabelle; Revenko, Gautier; Chaspoul, Florence; Wafo, Emmanuel Effects of meteorological conditions and topography on the bioaccumulation of PAHs and metal elements by native lichen (Xanthoria parietina), Journal of Environmental Sciences, Volume 109 (2021), pp. 193-205 10.1016/j.jes.2021.03.045

[18]

[18] Dudgeon, David Multiple threats imperil freshwater biodiversity in the Anthropocene, Current Biology, Volume 29 (2019) no. 19, p. R960-R967 10.1016/j.cub.2019.08.002

[19]

[19] Fay, Rémi; Ficheux, Sébastien; Béchet, Arnaud; Besnard, Aurélien; Crochet, Pierre‐André; Leblois, Raphaël; Crivelli, Alain; Wattier, Rémi; Olivier, Anthony Direct and indirect estimates of dispersal support strong juvenile philopatry and male‐biased dispersal in a freshwater turtle species (Emys orbicularis), Freshwater Biology, Volume 68 (2023) no. 12, pp. 2042-2053 10.1111/fwb.14171

[20]

[20] Ficheux, Sébastien; Olivier, Anthony; Fay, Rémi; Crivelli, Alain; Besnard, Aurélien; Béchet, Arnaud Rapid response of a long-lived species to improved water and grazing management: The case of the European pond turtle (Emys orbicularis) in the Camargue, France, Journal for Nature Conservation, Volume 22 (2014) no. 4, pp. 342-348 10.1016/j.jnc.2014.03.001

[21]

[21] Fourgous, C.; Chevreuil, M.; Alliot, F.; Amilhat, E.; Faliex, E.; Paris-Palacios, S.; Teil, M.J.; Goutte, A. Phthalate metabolites in the European eel (Anguilla anguilla) from Mediterranean coastal lagoons, Science of The Total Environment, Volume 569-570 (2016), pp. 1053-1059 10.1016/j.scitotenv.2016.06.159

[22]

[22] Frapiccini, E.; Panfili, M.; Guicciardi, S.; Santojanni, A.; Marini, M.; Truzzi, C.; Annibaldi, A. Effects of biological factors and seasonality on the level of polycyclic aromatic hydrocarbons in red mullet (Mullus barbatus), Environmental Pollution, Volume 258 (2020), p. 113742 10.1016/j.envpol.2019.113742

[23]

Reproducibility of the Blood and Urine Exposome: A Systematic Literature Review and Meta-Analysis

Jantje Goerdten, Li Yuan, Inge Huybrechts et al.

Cancer Epidemiology, Biomarkers & Prevention 2022 10.1158/1055-9965.epi-22-0090

[24]

[24] González-Mille, Donaji J.; Ilizaliturri-Hernández, César A.; Espinosa-Reyes, Guillermo; Cruz-Santiago, Omar; Cuevas-Díaz, María D.C.; Martín Del Campo, Claudia C.; Flores-Ramírez, Rogelio DNA damage in different wildlife species exposed to persistent organic pollutants (POPs) from the delta of the Coatzacoalcos river, Mexico, Ecotoxicology and Environmental Safety, Volume 180 (2019), pp. 403-411 10.1016/j.ecoenv.2019.05.030

[25]

[25] Goutte, Aurélie; Alliot, Fabrice; Budzinski, Hélène; Simonnet-Laprade, Caroline; Santos, Raphaël; Lachaux, Victor; Maciejewski, Kevin; Le Menach, Karyn; Labadie, Pierre Trophic Transfer of Micropollutants and Their Metabolites in an Urban Riverine Food Web, Environmental Science & Technology, Volume 54 (2020) no. 13, pp. 8043-8050 10.1021/acs.est.0c01411

[26]

[26] Guigue, Catherine; Tedetti, Marc; Ferretto, Nicolas; Garcia, Nicole; Méjanelle, Laurence; Goutx, Madeleine Spatial and seasonal variabilities of dissolved hydrocarbons in surface waters from the Northwestern Mediterranean Sea: Results from one year intensive sampling, Science of The Total Environment, Volume 466-467 (2014), pp. 650-662 10.1016/j.scitotenv.2013.07.082

[27]

[27] Guillot, Héloïse; Bonnet, Xavier; Bustamante, Paco; Churlaud, Carine; Trotignon, Jacques; Brischoux, François Trace Element Concentrations in European Pond Turtles (Emys orbicularis) from Brenne Natural Park, France, Bulletin of Environmental Contamination and Toxicology, Volume 101 (2018) no. 3, pp. 300-304 10.1007/s00128-018-2376-7

[28]

[28] Hartig, Florian DHARMa: Residual Diagnostics for Hierarchical (Multi-Level / Mixed) Regression Models, R package, 2024 (https://CRAN.R-project.org/package=DHARMa)

[29]

[29] Holth, Tor F.; Beylich, Bjørnar A.; Skarphédinsdóttir, Halldóra; Liewenborg, Birgitta; Grung, Merete; Hylland, Ketil Genotoxicity of Environmentally Relevant Concentrations of Water-Soluble Oil Components in Cod (Gadus morhua), Environmental Science & Technology, Volume 43 (2009) no. 9, pp. 3329-3334 10.1021/es803479p

[30]

[30] Laborie, Stéphanie; Moreau-Guigon, Elodie; Alliot, Fabrice; Desportes, Annie; Oziol, Lucie; Chevreuil, Marc A new analytical protocol for the determination of 62 endocrine-disrupting compounds in indoor air, Talanta, Volume 147 (2016), pp. 132-141 10.1016/j.talanta.2015.09.028

[31]

[31] Lenth, Russell V. emmeans: Estimated Marginal Means, aka Least-Squares Means, R package, 2025 (https://CRAN.R-project.org/package=emmeans)

[32]

[32] Li, Ruifei; Luo, Yu; Zhu, Xu; Zhang, Jin; Wang, Zhenyu; Yang, Wenyu; Li, Yu; Li, Hui Anthropogenic impacts on polycyclic aromatic hydrocarbons in surface water: Evidence from the COVID-19 lockdown, Water Research, Volume 262 (2024), p. 122143 10.1016/j.watres.2024.122143

[33]

[33] Liu, Yin-E; Luo, Xiao-Jun; Guan, Ke-Lan; Huang, Chen-Chen; Zhu, Chun-You; Qi, Xue-Meng; Zeng, Yan-Hong; Mai, Bi-Xian Legacy and emerging organophosphorus flame retardants and plasticizers in frogs: Sex difference and parental transfer, Environmental Pollution, Volume 266 (2020), p. 115336 10.1016/j.envpol.2020.115336

[34]

[34] Liu, Yin-E; Tang, Bin; Liu, Yu; Luo, Xiao-Jun; Mai, Bi-Xian; Covaci, Adrian; Poma, Giulia Occurrence, biomagnification and maternal transfer of legacy and emerging organophosphorus flame retardants and plasticizers in water snake from an e-waste site, Environment International, Volume 133 (2019), p. 105240 10.1016/j.envint.2019.105240

[35]

[35] Lohmann, Rainer; Breivik, Knut; Dachs, Jordi; Muir, Derek Global fate of POPs: Current and future research directions, Environmental Pollution, Volume 150 (2007) no. 1, pp. 150-165 10.1016/j.envpol.2007.06.051

[36]

[36] Lorrain-Soligon, Léa; Marchand, Etienne; Alliot, Fabrice; Bustamante, Paco; Petit, Fabienne; Goutte, Aurélie Starting from the bottom: Contrasted trophic transfer of antibiotics and pesticides through a riverine food web, Science of The Total Environment, Volume 1002 (2025), p. 180617 10.1016/j.scitotenv.2025.180617

[37]

[37] López-Berenguer, G.; Acosta-Dacal, A.; Luzardo, O.P.; Peñalver, J.; Martínez-López, E. Assessment of polycyclic aromatic hydrocarbons (PAHs) in mediterranean top marine predators stranded in SE Spain, Chemosphere, Volume 336 (2023), p. 139306 10.1016/j.chemosphere.2023.139306

[38]

Distribution of Phthalate Esters in a Marine Aquatic Food Web: Comparison to Polychlorinated Biphenyls

Cheryl E. Mackintosh, Javier Maldonado, Jing Hongwu et al.

Environmental Science & Technology 2004 10.1021/es034745r

[39]

[39] Malaj, Egina; von der Ohe, Peter C.; Grote, Matthias; Kühne, Ralph; Mondy, Cédric P.; Usseglio-Polatera, Philippe; Brack, Werner; Schäfer, Ralf B. Organic chemicals jeopardize the health of freshwater ecosystems on the continental scale, Proceedings of the National Academy of Sciences, Volume 111 (2014) no. 26, pp. 9549-9554 10.1073/pnas.1321082111

[40]

[40] Manzetti, Sergio Polycyclic Aromatic Hydrocarbons in the Environment: Environmental Fate and Transformation, Polycyclic Aromatic Compounds, Volume 33 (2013) no. 4, pp. 311-330 10.1080/10406638.2013.781042

[41]

[41] Marasco, Valeria; Costantini, David Signaling in a Polluted World: Oxidative Stress as an Overlooked Mechanism Linking Contaminants to Animal Communication, Frontiers in Ecology and Evolution, Volume 4 (2016) 10.3389/fevo.2016.00095

[42]

[42] Mateo, Rafael; Lacorte, Silvia; Taggart, Mark A. An Overview of Recent Trends in Wildlife Ecotoxicology, Current Trends in Wildlife Research, Volume 1, Springer International Publishing, Cham, 2016, pp. 125-150 10.1007/978-3-319-27912-1_6

[43]

[43] Matson, Cole W.; Palatnikov, Grigoriy; Islamzadeh, Arif; Mcdonald, Thomas J.; Autenrieth, Robin L.; Donnelly, K. C.; Bickham, John W. Chromosomal Damage in Two Species of Aquatic Turtles (Emys orbicularis and Mauremys caspica) Inhabiting Contaminated Sites in Azerbaijan, Ecotoxicology, Volume 14 (2005) no. 5, pp. 513-525 10.1007/s10646-005-0001-0

[44]

[44] Matthiessen, Peter; Wheeler, James R.; Weltje, Lennart A review of the evidence for endocrine disrupting effects of current-use chemicals on wildlife populations, Critical Reviews in Toxicology, Volume 48 (2018) no. 3, pp. 195-216 10.1080/10408444.2017.1397099

[45]

[45] Meador, J. P.; Stein, J. E.; Reichert, W. L.; Varanasi, U. Bioaccumulation of Polycyclic Aromatic Hydrocarbons by Marine Organisms, Reviews of Environmental Contamination and Toxicology, Volume 143, Springer New York, New York, NY, 1995, pp. 79-165 10.1007/978-1-4612-2542-3_4

[46]

[46] Merleau, L-A; Lourdais, O; Olivier, A; Vittecoq, M; Alliot, F; Traore, S; Leray, C; Goutte, A Dataset from Exposure to a mixture of organic pollutants in a threatened freshwater turtle Emys orbicularis: effects of age, sex, and temporal variation, Zenodo, 2025 10.5281/zenodo.17663455

[47]

[47] Merleau, L-A; Lourdais, O; Olivier, A; Vittecoq, M; Alliot, F; Traore, S; Leray, C; Goutte, A Revised Supplementary Material (R2) for "Exposure to a mixture of organic pollutants in a threatened freshwater turtle Emys orbicularis: effects of age, sex, and temporal variation", Zenodo (2026) 10.5281/zenodo.18412046

[48]

[48] Merleau, Leslie-Anne; Goutte, Aurélie; Olivier, Anthony; Vittecoq, Marion; Bustamante, Paco; Leray, Carole; Lourdais, Olivier Blood levels of metallic trace elements are influenced by sex, age and habitat in the European pond turtle (Emys orbicularis), Science of The Total Environment, Volume 957 (2024), p. 177487 10.1016/j.scitotenv.2024.177487

[49]

[49] Merleau, Leslie-Anne; Lourdais, Olivier; Olivier, Anthony; Vittecoq, Marion; Blouin-Demers, Gabriel; Alliot, Fabrice; Burkart, Louisiane; Foucault, Yvann; Leray, Carole; Migne, Emmanuelle; Goutte, Aurélie Pesticide concentrations in a threatened freshwater turtle (Emys orbicularis): Seasonal and annual variation in the Camargue wetland, France, Environmental Pollution, Volume 341 (2024), p. 122903 10.1016/j.envpol.2023.122903

[50]

[50] Meyer, Erik; Eskew, Evan A.; Chibwe, Leah; Schrlau, Jill; Massey Simonich, Staci L.; Todd, Brian D. Organic contaminants in western pond turtles in remote habitat in California, Chemosphere, Volume 154 (2016), pp. 326-334 10.1016/j.chemosphere.2016.03.128

Showing 50 of 95 references

Metrics

0

Citations

95

References

Details

Published: Mar 09, 2026
Vol/Issue: 6

Authors

L

Leslie-Anne Merleau

École Pratique des Hautes Études, PSL Research University, UMR 7619 METIS, Sorbonne University – Paris, France; Centre d’Études Biologiques de Chizé, CNRS, UMR 7372 – Villiers-en-Bois, France; La Tour du Valat, Research Institute for the Conservation of Mediterranean Wetlands – Arles, France

O

Olivier Lourdais

Centre d’Études Biologiques de Chizé, CNRS, UMR 7372 – Villiers-en-Bois, France; School of Life Sciences, Arizona State University – Tempe, Arizona, USA

A

Anthony Olivier

La Tour du Valat, Research Institute for the Conservation of Mediterranean Wetlands – Arles, France

M

Marion Vittecoq

La Tour du Valat, Research Institute for the Conservation of Mediterranean Wetlands – Arles, France

F

Fabrice Alliot

École Pratique des Hautes Études, PSL Research University, UMR 7619 METIS, Sorbonne University – Paris, France

S

Sira Traore

École Pratique des Hautes Études, PSL Research University, UMR 7619 METIS, Sorbonne University – Paris, France

C

Carole Leray

La Tour du Valat, Research Institute for the Conservation of Mediterranean Wetlands – Arles, France

A

Aurélie Goutte

École Pratique des Hautes Études, PSL Research University, UMR 7619 METIS, Sorbonne University – Paris, France

Cite This Article

Leslie-Anne Merleau, Olivier Lourdais, Anthony Olivier, et al. (2026). Exposure to a mixture of organic pollutants in a threatened freshwater turtle Emys orbicularis: effects of age, sex, and temporal variation. Peer Community Journal, 6. https://doi.org/10.24072/pcjournal.684

Exposure to a mixture of organic pollutants in a threatened freshwater turtle Emys orbicularis: effects of age, sex, and temporal variation

You May Also Like