Chemical mixtures; Freshwater ecosystem; Marine ecosystem; Network analysis visualization; Top predators; Fresh Water; Freshwater environments; Marine environment; Marine mammals; Network analyse visualization; Predator-Prey; Prey-predator; Top predator; Environmental Engineering; Environmental Chemistry; Waste Management and Disposal; Pollution
Abstract :
[en] Marine and freshwater mammalian predators and fish samples, retrieved from environmental specimen banks (ESBs), natural history museum (NHMs) and other scientific collections, were analysed by LIFE APEX partners for a wide range of legacy and emerging contaminants (2545 in total). Network analysis was used to visualize the chemical occurrence data and reveal the predominant chemical mixtures for the freshwater and marine environments. For this purpose, a web tool was created to explore these chemical mixtures in predator-prey pairs. Predominant chemicals, defined as the most prevalent substances detected in prey-predator pairs were identified through this innovative approach. The analysis established the most frequently co-occurring substances in chemical mixtures from AP&P in the marine and freshwater environments. Freshwater and marine environments shared 23 chemicals among their top 25 predominant chemicals. Legacy chemical, including perfluorooctanesulfonic acid (PFOS), brominated diphenyl ethers (BDEs), polychlorinated biphenyls (PCBs), hexachlorobenzene and mercury were dominant chemicals in both environments. Furthermore, N-acetylaminoantipyrine was a predominant pharmaceutical in both environments. The LIFE APEX chemical mixture application (https://norman-data.eu/LIFE_APEX_Mixtures) was proven to be useful to establish most prevalent compounds in terms of number of detected counts in prey-predator pairs. Nonetheless, further research is needed to establish food chain associations of the predominant chemicals.
Disciplines :
Aquatic sciences & oceanology
Author, co-author :
Alygizakis, Nikiforos; Environmental Institute, Okružná 784/42, 97241 Koš, Slovak Republic, National and Kapodistrian University of Athens, Panepistimiopolis Zografou, 15771 Athens, Greece. Electronic address: alygizakis@ei.sk
Kostopoulou, Niki; National and Kapodistrian University of Athens, Panepistimiopolis Zografou, 15771 Athens, Greece
Gkotsis, Georgios; National and Kapodistrian University of Athens, Panepistimiopolis Zografou, 15771 Athens, Greece
Nika, Maria-Christina; National and Kapodistrian University of Athens, Panepistimiopolis Zografou, 15771 Athens, Greece
Orfanioti, Anastasia; National and Kapodistrian University of Athens, Panepistimiopolis Zografou, 15771 Athens, Greece
Ng, Kelsey; Environmental Institute, Okružná 784/42, 97241 Koš, Slovak Republic
Bizani, Erasmia; National and Kapodistrian University of Athens, Panepistimiopolis Zografou, 15771 Athens, Greece
Nikolopoulou, Varvara; National and Kapodistrian University of Athens, Panepistimiopolis Zografou, 15771 Athens, Greece
Badry, Alexander; German Environment Agency, 06844 Dessau, Germany
Brownlow, Andrew; Scottish Marine Animal Stranding Scheme, School of Biodiversity, One Health and Veterinary Medicine, College of Medical, Veterinary and Life Science, University of Glasgow, Glasgow, UK
Centelleghe, Cinzia; Department of Comparative Biomedicine and Food Science, University of Padua, 35020 Legnaro, Italy
Chadwick, Elizabeth A; Cardiff University, Biomedical Science Building, Museum Avenue, Cardiff CF10 3AX, UK
Ciesielski, Tomasz M; Department of Biology, Norwegian University of Science and Technology, Norway, Department of Arctic Technology, The University Centre in Svalbard (UNIS), P.O. Box 156, 9171 Longyearbyen, Norway
Cincinelli, Alessandra; Department of Chemistry "Ugo Schiff", University of Florence, 50019 Sesto Fiorentino, Italy
Claßen, Daniela; German Environment Agency, 06844 Dessau, Germany
Danielsson, Sara; Naturhistoriska riksmuseet, Box 50007, 104 05 Stockholm, Sweden
Dekker, Rene W R J; Naturalis Biodiversity Center, 2333 RA Leiden, the Netherlands
Duke, Guy; Environmental Change Institute, University of Oxford, 3 South Parks Rd, Oxford OX1 3QY, United Kingdom
Glowacka, Natalia; Environmental Institute, Okružná 784/42, 97241 Koš, Slovak Republic
Gol'din, Pavel; Schmalhausen Institute of Zoology, National Academy of Sciences of Ukraine, Kyiv, Ukraine
Jansman, Hugh A H; Wageningen University & Research, Wageningen Environmental Research, Droevendaalsesteeg 3-3 A, 6708 PB Wageningen, the Netherlands
Jauniaux, Thierry ; Université de Liège - ULiège > Département de morphologie et pathologie (DMP)
Knopf, Burkhard; Fraunhofer Institute for Molecular Biology and Applied Ecology, 57392 Schmallenberg, Germany
Koschorreck, Jan; German Environment Agency, 06844 Dessau, Germany
Krone, Oliver; Department of Wildlife Diseases, Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany
Lekube, Xabier; Biscay Bay Environmental Biospecimen Bank (BBEBB), Research Centre for Experimental Marine Biology and Biotechnology (PiE-UPV/EHU), University of the Basque Country (UPV/EHU), Areatza 47, 48620 Plentzia, Basque Country, Spain, CBET+ Research Group, Department of Zoology and Animal Cell Biology, Faculty of Science and Technology, Research Centre for Experimental Marine Biology and Biotechnology PIE, University of the Basque Country UPV/EHU, Sarriena z/g, Leioa, Basque Country, Spain
Martellini, Tania; Department of Chemistry "Ugo Schiff", University of Florence, 50019 Sesto Fiorentino, Italy
Movalli, Paola; Naturalis Biodiversity Center, 2333 RA Leiden, the Netherlands
O'Rourke, Emily; Cardiff University, Biomedical Science Building, Museum Avenue, Cardiff CF10 3AX, UK
Oswald, Peter; Environmental Institute, Okružná 784/42, 97241 Koš, Slovak Republic
Oswaldova, Martina; Environmental Institute, Okružná 784/42, 97241 Koš, Slovak Republic
Saavedra, Camilo; Instituto Español de Oceanografía, IEO-CSIC, Centro Oceanográfico de Vigo, Vigo, Spain
Persson, Sara; Naturhistoriska riksmuseet, Box 50007, 104 05 Stockholm, Sweden
Rohner, Simon; Institute for Terrestrial and Aquatic Wildlife Research, University of Veterinary Medicine Hannover, 25761 Buesum, Germany
Roos, Anna; Naturhistoriska riksmuseet, Box 50007, 104 05 Stockholm, Sweden
Routti, Heli; Norwegian Polar Institute, Fram Centre, Tromsø, Norway
Schmidt, Britta; Institute for Terrestrial and Aquatic Wildlife Research, University of Veterinary Medicine Hannover, 25761 Buesum, Germany
Sciancalepore, Giuseppe; Department of Comparative Biomedicine and Food Science, University of Padua, 35020 Legnaro, Italy
Siebert, Ursula; Institute for Terrestrial and Aquatic Wildlife Research, University of Veterinary Medicine Hannover, 25761 Buesum, Germany, Department of Ecoscience, Marine Mammal Research, Aarhus University, Denmark
Treu, Gabriele; German Environment Agency, 06844 Dessau, Germany
van den Brink, Nico W; Division of Toxicology, Wageningen University, Wageningen, the Netherlands
Vishnyakova, Karina; Ukrainian Scientific Center of Ecology of the Sea, 89 Frantsuzsky Blvd., 65062 Odesa, Ukraine
Walker, Lee Anthony; UK Centre for Ecology and Hydrology, Lancaster LA1 4AP, United Kingdom
Thomaidis, Nikolaos S; National and Kapodistrian University of Athens, Panepistimiopolis Zografou, 15771 Athens, Greece. Electronic address: ntho@chem.uoa.gr
Slobodnik, Jaroslav; Environmental Institute, Okružná 784/42, 97241 Koš, Slovak Republic
This study was financed by the European Union through the project LIFE17 ENV/SK/000355 \u2018Systematic use of contaminant data from apex predators and their prey in chemicals management\u2019. Naturalis Biodiversity Center wishes to thank M. Geut (A Seal, Seal Recovery Centre, Stellendam) and A. Oosterbaan (Ecomare, Texel) for the Dutch seal samples. Ringed seal and bearded seal sampling was supported by the Environmental Specimen Bank, Norway and the Norwegian Polar Institute. The samples of cetaceans from northwestern Spain were provided by the regional stranding network \"Coordinadora para o Estudo dos Mam\u00EDferos Mari\u00F1os (CEMMA). The authors would like to thank Dr. Iwona Pawliczka for provision of samples. All samples were shipped following the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) lists. The content of this article reflects only the authors' views and the Research Executive Agency is not responsible for any use that may be made of the information it contains.This study was financed by the European Union through the project LIFE17 ENV/SK/000355 \u2018Systematic use of contaminant data from apex predators and their prey in chemicals management\u2019. Naturalis Biodiversity Center wishes to thank M. Geut (A Seal, Seal Recovery Centre, Stellendam) and A. Oosterbaan (Ecomare, Texel) for the Dutch seal samples. Ringed seal and bearded seal sampling was supported by the Environmental Specimen Bank, Norway and the Norwegian Polar Institute. The samples of cetaceans from northwestern Spain were provided by the regional stranding network \"Coordinadora para o Estudo dos Mam\u00EDferos Mari\u00F1os (CEMMA). The authors would like to thank Dr. Iwona Pawliczka for provision of samples.
Androulakakis, A., Alygizakis, N., Gkotsis, G., Nika, M.C., Nikolopoulou, V., Bizani, E., et al. Determination of 56 per- and polyfluoroalkyl substances in top predators and their prey from Northern Europe by LC-MS/MS. Chemosphere, 287, 2022, 131775.
Badry, A., Rudel, H., Gockener, B., Nika, M.C., Alygizakis, N., Gkotsis, G., et al. Making use of apex predator sample collections: an integrated workflow for quality assured sample processing, analysis and digital sample freezing of archived samples. Chemosphere, 309, 2022, 136603.
Badry, A., Slobodnik, J., Alygizakis, N., Bunke, D., Cincinelli, A., Claßen, D., et al. Using environmental monitoring data from apex predators for chemicals management: towards harmonised sampling and processing of archived wildlife samples to increase the regulatory uptake of monitoring data in chemicals management. Environ. Sci. Eur., 2022, 34.
Basu, N., Scheuhammer, A.M., O'Brien, M., Polychlorinated biphenyls, organochlorinated pesticides, and polybrominated diphenyl ethers in the cerebral cortex of wild river otters (Lontra canadensis). Environ. Pollut. 149 (2007), 25–30.
Beckers, L.M., Altenburger, R., Brack, W., Escher, B.I., Hackermuller, J., Hassold, E., et al. A data-derived reference mixture representative of European wastewater treatment plant effluents to complement mixture assessment. Environ. Int., 179, 2023, 108155.
Bignert, A., Helander, B.O., Monitoring of contaminants and their effects on the common Guillemot and the White-tailed sea eagle. J. Ornithol. 156 (2015), 173–185.
Bopp, S.K., Barouki, R., Brack, W., Dalla Costa, S., Dorne, J.C.M., Drakvik, P.E., et al. Current EU research activities on combined exposure to multiple chemicals. Environ. Int. 120 (2018), 544–562.
Cooke, R., Whiteley, P., Jin, Y., Death, C., Weston, M.A., Carter, N., et al. Widespread exposure of powerful owls to second-generation anticoagulant rodenticides in Australia spans an urban to agricultural and forest landscape. Sci. Total Environ., 819, 2022, 153024.
Diamanti, K.S., Alygizakis, N.A., Nika, M.C., Oswaldova, M., Oswald, P., Thomaidis, N.S., et al. Assessment of the chemical pollution status of the Dniester River Basin by wide-scope target and suspect screening using mass spectrometric techniques. Anal. Bioanal. Chem. 412 (2020), 4893–4907.
Dibbern, M., Elmeros, M., Dietz, R., Søndergaard, J., Michelsen, A., Sonne, C., Mercury exposure and risk assessment for Eurasian otters (Lutra lutra) in Denmark. Chemosphere, 272, 2021, 129608.
Du, B., Haddad, S.P., Luek, A., Scott, W.C., Saari, G.N., Kristofco, L.A., et al. Bioaccumulation and trophic dilution of human pharmaceuticals across trophic positions of an effluent-dependent wadeable stream. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci., 369, 2014.
European Commission, Commission Directive 2009/90/EC of 31 July 2009 Laying Down, Pursuant to Directive 2000/60/EC of the European Parliament and of the Council, Technical Specifications for Chemical Analysis and Monitoring of Water Status. 2009.
Finckh, S., Carmona, E., Borchardt, D., Buttner, O., Krauss, M., Schulze, T., et al. Mapping chemical footprints of organic micropollutants in European streams. Environ. Int., 183, 2024, 108371.
Fuentes, E., Gaffard, A., Rodrigues, A., Millet, M., Bretagnolle, V., Moreau, J., et al. Neonicotinoids: still present in farmland birds despite their ban. Chemosphere, 321, 2023, 138091.
Gago-Ferrero, P., Bletsou, A.A., Damalas, D.E., Aalizadeh, R., Alygizakis, N.A., Singer, H.P., et al. Wide-scope target screening of >2000 emerging contaminants in wastewater samples with UPLC-Q-ToF-HRMS/MS and smart evaluation of its performance through the validation of 195 selected representative analytes. J. Hazard. Mater., 387, 2020, 121712.
Gkotsis, G., Nika, M.C., Nikolopoulou, V., Alygizakis, N., Bizani, E., Aalizadeh, R., et al. Assessment of contaminants of emerging concern in European apex predators and their prey by LC-QToF MS wide-scope target analysis. Environ. Int., 170, 2022, 107623.
Gkotsis, G., Nika, M.C., Athanasopoulou, A.I., Vasilatos, K., Alygizakis, N., Boschert, M., et al. Advanced throughput analytical strategies for the comprehensive HRMS screening of organic micropollutants in eggs of different bird species. Chemosphere, 312, 2023, 137092.
Greaves, A.K., Letcher, R.J., Sonne, C., Dietz, R., Born, E.W., Tissue-specific concentrations and patterns of perfluoroalkyl carboxylates and sulfonates in East Greenland polar bears. Environ. Sci. Technol. 46 (2012), 11575–11583.
Herzke, D., Nikiforov, V., Yeung, L.W.Y., Moe, B., Routti, H., Nygard, T., et al. Targeted PFAS analyses and extractable organofluorine - enhancing our understanding of the presence of unknown PFAS in Norwegian wildlife. Environ. Int., 171, 2023, 107640.
Hollender, J., Schymanski, E.L., Singer, H.P., Ferguson, P.L., Nontarget screening with high resolution mass spectrometry in the environment: ready to go?. Environ. Sci. Technol. 51 (2017), 11505–11512.
Kannan, K., Newsted, J., Halbrook, R.S., Giesy, J.P., Perfluorooctanesulfonate and related fluorinated hydrocarbons in mink and river otters from the United States. Environ. Sci. Technol. 36 (2002), 2566–2571.
Kean, E.F., Shore, R.F., Scholey, G., Strachan, R., Chadwick, E.A., Persistent pollutants exceed toxic thresholds in a freshwater top predator decades after legislative control. Environ. Pollut., 272, 2021, 116415.
Khairy, M., Brault, E., Dickhut, R., Harding, K.C., Harkonen, T., Karlsson, O., et al. Bioaccumulation of PCBs, OCPs and PBDEs in marine mammals from West Antarctica. Front. Mar. Sci., 2021, 8.
Lam, J.C., Lyu, J., Kwok, K.Y., Lam, P.K., Perfluoroalkyl substances (PFASs) in marine mammals from the South China Sea and their temporal changes 2002-2014: concern for alternatives of PFOS?. Environ. Sci. Technol. 50 (2016), 6728–6736.
Lerapetritou, M.G., Georgopoulos, P.G., Roth, C.M., Androulakis, L.P., Tissue-level modeling of xenobiotic metabolism in liver: an emerging tool for enabling clinical translational research. Clin. Transl. Sci. 2 (2009), 228–237.
Marshall, M.M., McCluney, K.E., Mixtures of co-occurring chemicals in freshwater systems across the continental US. Environ. Pollut., 268, 2021, 115793.
Miccoli, A., Maradonna, F., De Felice, A., Caputo Barucchi, V., Estonba, A., Genangeli, M., et al. Detection of endocrine disrupting chemicals and evidence of their effects on the HPG axis of the European anchovy Engraulis encrasicolus. Mar. Environ. Res. 127 (2017), 137–147.
Mohammed Taha, H., Aalizadeh, R., Alygizakis, N., Antignac, J.P., Arp, H.P.H., Bade, R., et al. The NORMAN Suspect List Exchange (NORMAN-SLE): facilitating European and worldwide collaboration on suspect screening in high resolution mass spectrometry. Environ. Sci. Eur., 34, 2022, 104.
Moriceau, M.A., Lefebvre, S., Fourel, I., Benoit, E., Buronfosse-Roque, F., Orabi, P., et al. Exposure of predatory and scavenging birds to anticoagulant rodenticides in France: exploration of data from French surveillance programs. Sci. Total Environ., 810, 2022, 151291.
Munschy, C., Bely, N., Heas-Moisan, K., Olivier, N., Pollono, C., Hollanda, S., et al. Tissue-specific bioaccumulation of a wide range of legacy and emerging persistent organic contaminants in swordfish (Xiphias gladius) from Seychelles, Western Indian Ocean. Mar. Pollut. Bull., 158, 2020, 111436.
Nikolopoulou, V., Alygizakis, N.A., Nika, M.C., Oswaldova, M., Oswald, P., Kostakis, M., et al. Screening of legacy and emerging substances in surface water, sediment, biota and groundwater samples collected in the Siverskyi Donets River Basin employing wide-scope target and suspect screening. Sci. Total Environ., 805, 2022, 150253.
Oliva-Vidal, P., Martinez, J.M., Sanchez-Barbudo, I.S., Camarero, P.R., Colomer, M.A., Margalida, A., et al. Second-generation anticoagulant rodenticides in the blood of obligate and facultative European avian scavengers. Environ. Pollut., 315, 2022, 120385.
O'Rourke, E., Hynes, J., Losada, S., Barber, J.L., Pereira, M.G., Kean, E.F., et al. Anthropogenic drivers of variation in concentrations of perfluoroalkyl substances in otters (Lutra lutra) from England and Wales. Environ. Sci. Technol. 56 (2022), 1675–1687.
Parli, A., Besson, A., Wehi, P., Johnson, S., Sub-lethal exposure to a mammalian pesticide bait alters behaviour in an orthopteran. J. Insect Conserv. 24 (2020), 535–546.
Ross, P.S., Marine mammals as sentinels in ecological risk assessment. Hum. Ecol. Risk Assess. Int. J. 6 (2000), 29–46.
Sanganyado, E., Bi, R., Teta, C., Buruaem Moreira, L., Yu, X., Yajing, S., et al. Toward an integrated framework for assessing micropollutants in marine mammals: challenges, progress, and opportunities. Crit. Rev. Environ. Sci. Technol. 51 (2020), 2824–2871.
Sant, K.E., Annunziato, K., Conlin, S., Teicher, G., Chen, P., Venezia, O., et al. Developmental exposures to perfluorooctanesulfonic acid (PFOS) impact embryonic nutrition, pancreatic morphology, and adiposity in the zebrafish, Danio rerio. Environ. Pollut., 275, 2021, 116644.
Smit, M.D., Leonards, P.E., de Jongh, A.W., van Hattum, B.G., Polychlorinated biphenyls in the Eurasian otter (Lutra lutra). Rev. Environ. Contam. Toxicol. 157 (1998), 95–130.
Sonne, C., Siebert, U., Gonnsen, K., Desforges, J.P., Eulaers, I., Persson, S., et al. Health effects from contaminant exposure in Baltic Sea birds and marine mammals: a review. Environ. Int., 139, 2020, 105725.
Spaan, K.M., van Noordenburg, C., Plassmann, M.M., Schultes, L., Shaw, S., Berger, M., et al. Fluorine mass balance and suspect screening in marine mammals from the northern hemisphere. Environ. Sci. Technol. 54 (2020), 4046–4058.
Stechert, C., Kolb, M., Bahadir, M., Djossa, B.A., Fahr, J., Insecticide residues in bats along a land use-gradient dominated by cotton cultivation in northern Benin, West Africa. Environ. Sci. Pollut. Res. Int. 21 (2014), 8812–8821.
Stuart-Smith, S.J., Jepson, P.D., Persistent threats need persistent counteraction: responding to PCB pollution in marine mammals. Mar. Policy 84 (2017), 69–75.
Thomaidis, N., Aalizadeh, R., Alygizakis, N., Bletsou, A., Beretsou, V., Damalas, D., et al. S21 | UATHTARGETS |. 2022, University of Athens Target List.
Treu, G., Slobodnik, J., Alygizakis, N., Badry, A., Bunke, D., Cincinelli, A., et al. Using environmental monitoring data from apex predators for chemicals management: towards better use of monitoring data from apex predators in support of prioritisation and risk assessment of chemicals in Europe. Environ. Sci. Eur., 2022, 34.
Villanger, G.D., Kovacs, K.M., Lydersen, C., Haug, L.S., Sabaredzovic, A., Jenssen, B.M., et al. Perfluoroalkyl substances (PFASs) in white whales (Delphinapterus leucas) from Svalbard - a comparison of concentrations in plasma sampled 15 years apart. Environ. Pollut., 263, 2020, 114497.
Walther, B., Geduhn, A., Schenke, D., Jacob, J., Exposure of passerine birds to brodifacoum during management of Norway rats on farms. Sci. Total Environ., 762, 2021, 144160.
Yates, D.E., Mayack, D.T., Munney, K., Evers, D.C., Major, A., Kaur, T., et al. Mercury levels in mink (Mustela vison) and river otter (Lontra canadensis) from Northeastern North America. Ecotoxicology 14 (2005), 263–274.