Long-Term Trends for Blue Mussels from the German Environmental Specimen Bank Show First Evidence of Munition Contaminants Uptake
Abstract
:1. Introduction
2. Materials and Methods
2.1. Sample Locations
2.2. Sampling and Sample Processing for Blue Mussels (Mytilus edulis Complex)
2.3. Materials and Chemicals
2.4. Extraction and GC-MS/MS Analyses
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Beck, A.J.; Gledhill, M.; Schlosser, C.; Stamer, B.; Böttcher, C.; Sternheim, J.; Greinert, J.; Achterberg, E.P. Spread, Behavior, and Ecosystem Consequences of Conventional Munitions Compounds in Coastal Marine Waters. Front. Mar. Sci. 2018, 5, 141. [Google Scholar] [CrossRef] [Green Version]
- Beddington, J.; Kinloch, A.J. Munitions Dumped at Sea: A Literature Review; Imperial College Consultants: London, UK, 2005. [Google Scholar]
- Lotufo, G.R.; Chappell, M.A.; Price, C.L.; Ballentine, M.L.; Fuentes, A.A.; Bridges, T.S.; George, R.D.; Glisch, E.J.; Carton, G. Review and Synthesis of Evidence Regarding Environmental Risks Posed by Munitions Constituents (MC) in Aquatic Systems; Engineer Research and Development Center: Vicksburg, MS, USA, 2017; 254p. [Google Scholar]
- Böttcher, C.; Knobloch, T.; Rühl, N.-P.; Sternheim, J.; Wichert, U.; Wöhler, J. Munitionsbelastung der Deutschen Meeresgewässer- Bestandsaufnahme und Empfehlungen (Stand 2011). 2011. Available online: https://www.meeresschutz.info/sonstige-berichte.html?file=files/meeresschutz/berichte/sonstige/munition/2011_Munitionsbelastung_DE_Meeresgewaesser.pdf (accessed on 27 September 2022).
- Rodacy, P.; Reber, S.; Walker, P.; Andre, J. Chemical Sensing of Explosive Targets in the Bedford Basin, Halifax, Nova Scotia; SAND2001–3569; Sandia National Laboratories: Albuquerque, NM, USA; Livermore, CA, USA, 2001; p. 789594. [Google Scholar]
- Knobloch, T.; Bełdowski, J.; Böttcher, C.; Söderström, M.; Rühl, N.-P.; Sternheim, J. Chemical Munitions Dumped in the Baltic Sea. Report. of the ad hoc Expert Group. to Update and Review the Existing Information on Dumped Chemical Munitions in the Baltic Sea (HELCOM MUNI); Baltic Marine Environment Protection Commission: Helsinki, Finland, 2013; Volume 142. [Google Scholar]
- Maser, E.; Bünning, T.H.; Brenner, M.; Van Haelst, S.; De Rijcke, M.; Müller, P.; Wichert, U.; Strehse, J.S. Warship wrecks and their munition cargos as a threat to the marine environment and humans: The V 1302 “JOHN MAHN” from World War II. Sci. Total Environ. 2023, 857, 159324. [Google Scholar] [CrossRef] [PubMed]
- Monfils, R. The Global Risk of Marine Pollution from WWII Shipwrecks: Examples from the Seven Seas. Int. Oil Spill Conf. Proc. 2005, 2005, 1049–1054. [Google Scholar] [CrossRef] [Green Version]
- Jurczak, W.; Fabisiak, J. Corrosion of ammunition dumped in the Baltic Sea. J. KONBiN 2017, 41, 227–246. [Google Scholar] [CrossRef] [Green Version]
- Silva, J.A.K.; Chock, T. Munitions integrity and corrosion features observed during the HUMMA deep-sea munitions disposal site investigations. Deep Sea Res. Part II Top. Stud. Oceanogr. 2016, 128, 14–24. [Google Scholar] [CrossRef]
- den Otter, J.H.; Pröfrock, D.; Bünning, T.H.; Strehse, J.S.; van der Heijden, A.E.D.M.; Maser, E. Release of Ammunition-Related Compounds from a Dutch Marine Dump Site. Toxics 2023, 11, 238. [Google Scholar] [CrossRef]
- MacLeod, I.D. In-situ Corrosion Measurements of WWII Shipwrecks in Chuuk Lagoon, Quantification of Decay Mechanisms and Rates of Deterioration. Front. Mar. Sci. 2016, 3, 38. [Google Scholar] [CrossRef] [Green Version]
- Juhasz, A.L.; Naidu, R. Explosives: Fate, Dynamics, and Ecological Impact in Terrestrial and Marine Environments. In Reviews of Environmental Contamination and Toxicology; Springer: New York, NY, USA, 2007; Volume 191, pp. 163–215. ISBN 978-0-387-69162-6. [Google Scholar]
- Nipper, M.; Carr, R.S.; Biedenbach, J.M.; Hooten, R.L.; Miller, K.; Saepoff, S. Development of Marine Toxicity Data for Ordnance Compounds. Arch. Environ. Contam. Toxicol. 2001, 41, 308–318. [Google Scholar] [CrossRef]
- Rosen, G.; Lotufo, G.R. Toxicity of explosive compounds to the marine mussel, Mytilus galloprovincialis, in aqueous exposures. Ecotoxicol. Environ. Saf. 2007, 68, 228–236. [Google Scholar] [CrossRef]
- Liu, D.H.W.; Spanggord, R.J.; Bailey, H.C.; Javitz, H.S.; Jones, D.C.L. Toxicity of TNT Wastewaters to Aquatic Organisms. Final Report, Volume 1. Acute Toxicity of LAP Wastewater and 2,4,6-Trinitrotoluene; Report No AD-A142 144; US Army Medical Research and Development Command: Frederick, MD, USA, 1983; p. 21701. [Google Scholar]
- Koske, D.; Goldenstein, N.I.; Kammann, U. Nitroaromatic compounds damage the DNA of zebrafish embryos (Danio rerio). Aquat. Toxicol. 2019, 217, 105345. [Google Scholar] [CrossRef]
- Strehse, J.S.; Appel, D.; Geist, C.; Martin, H.-J.; Maser, E. Biomonitoring of 2,4,6-trinitrotoluene and degradation products in the marine environment with transplanted blue mussels (M. edulis). Toxicology 2017, 390, 117–123. [Google Scholar] [CrossRef] [PubMed]
- Schuster, R.; Strehse, J.S.; Ahvo, A.; Turja, R.; Maser, E.; Bickmeyer, U.; Lehtonen, K.K.; Brenner, M. Exposure to dissolved TNT causes multilevel biological effects in Baltic mussels (Mytilus spp.). Mar. Environ. Res. 2021, 167, 105264. [Google Scholar] [CrossRef] [PubMed]
- Bolt, H.M.; Degen, G.H.; Dorn, S.B.; Plöttner, S.; Harth, V. Genotoxicity and Potential Carcinogenicity of 2,4,6-Trinitrotoluene: Structural and Toxicological Considerations. Rev. Environ. Health 2006, 21, 217–228. [Google Scholar] [CrossRef] [PubMed]
- Shinkai, Y.; Nishihara, Y.; Amamiya, M.; Wakayama, T.; Li, S.; Kikuchi, T.; Nakai, Y.; Shimojo, N.; Kumagai, Y. NADPH-cytochrome P450 reductase-mediated denitration reaction of 2,4,6-trinitrotoluene to yield nitrite in mammals. Free Radic. Biol. Med. 2016, 91, 178–187. [Google Scholar] [CrossRef]
- Homma-Takeda, S.; Hiraku, Y.; Ohkuma, Y.; Oikawa, S.; Murata, M.; Ogawa, K.; Iwamuro, T.; Li, S.; Sun, G.F.; Kumagai, Y.; et al. 2,4,6-Trinitrotoluene-induced Reproductive Toxicity via Oxidative DNA Damage by its Metabolite. Free Radic. Res. 2002, 36, 555–566. [Google Scholar] [CrossRef] [PubMed]
- Beck, A.J.; Gledhill, M.; Kampmeier, M.; Feng, C.; Schlosser, C.; Greinert, J.; Achterberg, E.P. Explosives compounds from sea-dumped relic munitions accumulate in marine biota. Sci. Total Environ. 2022, 806, 151266. [Google Scholar] [CrossRef]
- Koske, D.; Straumer, K.; Goldenstein, N.I.; Hanel, R.; Lang, T.; Kammann, U. First evidence of explosives and their degradation products in dab (Limanda limanda L.) from a munition dumpsite in the Baltic Sea. Mar. Pollut. Bull. 2020, 155, 111131. [Google Scholar] [CrossRef]
- Beck, A.J.; van der Lee, E.M.; Eggert, A.; Stamer, B.; Gledhill, M.; Schlosser, C.; Achterberg, E.P. In Situ Measurements of Explosive Compound Dissolution Fluxes from Exposed Munition Material in the Baltic Sea. Environ. Sci. Technol. 2019, 53, 5652–5660. [Google Scholar] [CrossRef]
- Porter, J.W.; Barton, J.V.; Torres, C. Ecological, Radiological, and Toxicological Effects of Naval Bombardment on the Coral Reefs of Isla de Vieques, Puerto Rico. In Warfare Ecology; Machlis, G.E., Hanson, T., Špirić, Z., McKendry, J.E., Eds.; Springer: Dordrecht, The Netherlands, 2011; pp. 65–122. [Google Scholar]
- Rosen, G.; Lotufo, G.R.; Belden, J.B.; George, R.D. Environmental Characterization of Underwater Munitions Constituents at a Former Military Training Range. Environ. Toxic. Chem. 2022, 41, 275–286. [Google Scholar] [CrossRef]
- Appel, D.; Strehse, J.S.; Martin, H.-J.; Maser, E. Bioaccumulation of 2,4,6-trinitrotoluene (TNT) and its metabolites leaking from corroded munition in transplanted blue mussels (M. edulis). Mar. Pollut. Bull. 2018, 135, 1072–1078. [Google Scholar] [CrossRef]
- Maser, E.; Strehse, J.S. “Don’t Blast”: Blast-in-place (BiP) operations of dumped World War munitions in the oceans significantly increase hazards to the environment and the human seafood consumer. Arch. Toxicol. 2020, 94, 1941–1953. [Google Scholar] [CrossRef] [PubMed]
- Maser, E.; Strehse, J.S. Can seafood from marine sites of dumped World War relicts be eaten? Arch. Toxicol. 2021, 95, 2255–2261. [Google Scholar] [CrossRef] [PubMed]
- den Otter, J.H.; Olde, M.; van der Heijden, A.; Koolloos, M. Monitoring Munitiestort Oosterschelde 2020; TNO 2020 R12211; TNO Publiek: Hague, The Netherlands, 2021. [Google Scholar]
- Estoppey, N.; Mathieu, J.; Gascon Diez, E.; Sapin, E.; Delémont, O.; Esseiva, P.; de Alencastro, L.F.; Coudret, S.; Folly, P. Monitoring of explosive residues in lake-bottom water using Polar Organic Chemical Integrative Sampler (POCIS) and chemcatcher: Determination of transfer kinetics through Polyethersulfone (PES) membrane is crucial. Environ. Pollut. 2019, 252, 767–776. [Google Scholar] [CrossRef] [PubMed]
- Lotufo, G.R.; George, R.D.; Belden, J.B.; Woodley, C.M.; Smith, D.L.; Rosen, G. Investigation of polar organic chemical integrative sampler (POCIS) flow rate dependence for munition constituents in underwater environments. Environ. Monit. Assess. 2018, 190, 171. [Google Scholar] [CrossRef] [PubMed]
- Rosen, G.; Lotufo, G.R.; George, R.D.; Wild, B.; Rabalais, L.K.; Morrison, S.; Belden, J.B. Field validation of POCIS for monitoring at underwater munitions sites: Field validation of POCIS for underwater munitions sites. Environ. Toxicol. Chem. 2018, 37, 2257–2267. [Google Scholar] [CrossRef]
- Lotufo, G.R.; George, R.D.; Belden, J.B.; Woodley, C.; Smith, D.L.; Rosen, G. Release of Munitions Constituents in Aquatic Environments Under Realistic Scenarios and Validation of Polar Organic Chemical Integrative Samplers for Monitoring. Environ. Toxicol. Chem. 2019, 38, 2383–2391. [Google Scholar] [CrossRef]
- Farrington, J.W.; Tripp, B.W.; Tanabe, S.; Subramanian, A.; Sericano, J.L.; Wade, T.L.; Knap, A.H.; Edward, D. Goldberg’s proposal of “the Mussel Watch”: Reflections after 40 years. Mar. Pollut. Bull. 2016, 110, 501–510. [Google Scholar] [CrossRef]
- Strehse, J.S.; Maser, E. Marine bivalves as bioindicators for environmental pollutants with focus on dumped munitions in the sea: A review. Mar. Environ. Res. 2020, 158, 105006. [Google Scholar] [CrossRef]
- Fliedner, A.; Rüdel, H.; Göckener, B.; Krehenwinkel, H.; Paulus, M.; Koschorreck, J. Environmental specimen banks and the European Green Deal. Sci. Total Environ. 2022, 852, 158430. [Google Scholar] [CrossRef]
- Knopf, B.; Fliedner, A.; Radermacher, G.; Rüdel, H.; Paulus, M.; Pirntke, U.; Koschorreck, J. Seasonal variability in metal and metalloid burdens of mussels: Using data from the German Environmental Specimen Bank to evaluate implications for long-term mussel monitoring programs. Environ. Sci. Eur. 2020, 32, 7. [Google Scholar] [CrossRef] [Green Version]
- Yuan, B.; Rüdel, H.; de Wit, C.A.; Koschorreck, J. Identifying emerging environmental concerns from long-chain chlorinated paraffins towards German ecosystems. J. Hazard. Mater. 2022, 424, 127607. [Google Scholar] [CrossRef] [PubMed]
- Halbach, M.; Vogel, M.; Tammen, J.K.; Rüdel, H.; Koschorreck, J.; Scholz-Böttcher, B.M. 30 years trends of microplastic pollution: Mass-quantitative analysis of archived mussel samples from the North and Baltic Seas. Sci. Total Environ. 2022, 826, 154179. [Google Scholar] [CrossRef] [PubMed]
- Fliedner, A.; Rüdel, H.; Knopf, B.; Lohmann, N.; Paulus, M.; Jud, M.; Pirntke, U.; Koschorreck, J. Assessment of seafood contamination under the marine strategy framework directive: Contributions of the German environmental specimen bank. Environ. Sci. Pollut. Res. 2018, 25, 26939–26956. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wichert, U.; Kiel, Germany. Personal Communication, 2022.
- Paulus, M.; Klein, R.; Teubner, D. Environmental Specimen Bank: Guideline for Sampling and Sample Treatment Blue Mussel (Mytilus edulis-Complex); Standard Operating Procedure (SOP); Umweltbundesamt: Dessau-Roßlau, Germany, 2018. [Google Scholar]
- Rüdel, H.; Uhlig, S.; Weingärtner, M. German Environment Specimen Bank: Guidelines for Sampling and Sample Processing. Pulverisation and Homogenisation of Environmental Samples by Cryomilling. Standard Operating Procedure (SOP); Umweltbundesamt: Dessau-Roßlau, Germany, 2009. [Google Scholar]
- Rüdel, H.; Weingärtner, M. Guidelines for Sampling and Sample Processing Storage of Environmental Samples under Cryogenic Conditions; Fraunhofer Institute for Molecular Biology and Applied Ecology: Schmallenberg, Germany, 2008. [Google Scholar]
- Bünning, T.; Strehse, J.; Hollmann, A.; Bötticher, T.; Maser, E. A Toolbox for the Determination of Nitroaromatic Explosives in Marine Water, Sediment, and Biota Samples on Femtogram Levels by GC-MS/MS. Toxics 2021, 9, 60. [Google Scholar] [CrossRef]
- Armbruster, D.A.; Pry, T. Limit of blank, limit of detection and limit of quantitation. Clin. Biochem. Rev. 2008, 29 (Suppl. S1), S49–S52. [Google Scholar]
- Strehse, J.S.; Brenner, M.; Kisiela, M.; Maser, E. The explosive trinitrotoluene (TNT) induces gene expression of carbonyl reductase in the blue mussel (Mytilus spp.): A new promising biomarker for sea dumped war relicts? Arch. Toxicol. 2020, 94, 4043–4054. [Google Scholar] [CrossRef]
- Mariussen, E.; Stornes, S.M.; Bøifot, K.O.; Rosseland, B.O.; Salbu, B.; Heier, L.S. Uptake and effects of 2, 4, 6-trinitrotoluene (TNT) in juvenile Atlantic salmon (Salmo salar). Aquat. Toxicol. 2018, 194, 176–184. [Google Scholar] [CrossRef]
- Ek, H.; Dave, G.; Sturve, J.; Almroth, B.C.; Stephensen, E.; Förlin, L.; Birgersson, G. Tentative biomarkers for 2,4,6-trinitrotoluene (TNT) in fish (Oncorhynchus mykiss). Aquat. Toxicol. 2005, 72, 221–230. [Google Scholar] [CrossRef]
- Appel, D.; Beck, A.J.; Eggert, A.; Gräwe, U.; Kampmeier, M.; Martin, H.-J.; Maser, E.; Schlosser, C.; Song, Y.; Strehse, J.S.; et al. Practical Guide for Environmental Monitoring of Conventional Munitions in the Seas—Results from the BMBF funded project UDEMM “Umweltmonitoring für die Delaboration von Munition im Meer” Version 1.1; Greinert, J., Ed.; GEOMAR: Kiel, Germany, 2019. [Google Scholar] [CrossRef]
- Kampmeier, M.; van der Lee, E.M.; Wichert, U.; Greinert, J. Exploration of the munition dumpsite Kolberger Heide in Kiel Bay, Germany: Example for a standardised hydroacoustic and optic monitoring approach. Cont. Shelf Res. 2020, 198, 104108. [Google Scholar] [CrossRef]
- Böttcher, C.; Knobloch, T.; Sternheim, J.; Weinberg, I.; Wichert, U.; Wöhler, J. Munitionsbelastung der Deutschen Meeresgewässer—Entwicklung und Fortschritt (Jahr 2017); Für den Bund/Länder-Ausschuss Nord- und Ostsee (BLANO)—Ministerium für Energiewende, Landwirtschaft, Umwelt und ländliche Räume des Landes Schleswig-Holstein: Kiel, Germany, 2017. [Google Scholar]
- Warmke, J.; GeoInfo Division, German Navy Headquarters, Rostock, Germany. Personal Communication, 2022.
- AmuCad Ammunition Cadastre Sea. 2022. Available online: https://www.amucad.org/ (accessed on 5 November 2022).
- Böttcher, C.; Knobloch, T.; Sternheim, J.; Weinberg, I.; Wöhler, J. Munitionsbelastung der Deutschen Meeresgewässer—Entwicklung und Fortschritt (Jahr 2014); Für den Bund/Länder-Ausschuss Nord- und Ostsee (BLANO)—Ministerium für Energiewende, Landwirtschaft, Umwelt und ländliche Räume des Landes Schleswig-Holstein: Kiel, Germany, 2014. [Google Scholar]
Compound | Rt SL (min) | Rt LVI (min) | Molecular Mass (g∗mol−1) | Transition (m/z) | CE (eV) | ||
---|---|---|---|---|---|---|---|
1,3-Dinitrobenzene CAS No. 99-65-0 | 2.43 | 3.20 | 168.11 | Q q q | 122.0 > 75.0 168.0 > 75.0 168.0 > 122.0 | 12 20 8 | |
2,4-Dinitrotoluene CAS No. 121-14-2 | 2.77 | 3.52 | 182.13 | Q q q | 165.0 > 63.1 165.0 > 90.1 165.0 > 118.1 | 22 16 8 | |
Trinitrotoluene CAS No. 118-96-7 | 3.41 | 4.09 | 227.13 | Q q q | 210.0 > 164.1 164.0 > 90.1 108.0 > 76.1 | 6 10 12 | |
13C15N-Trinitrotoluene CAS No. 202406-62-0 | 3.41 | 4.09 | 237.06 | Q q q | 220.1 > 173.1 220.1 > 203.1 189.1 > 82.1 | 6 8 10 | |
4-Amino-2,6-dinitrotoluene CAS No. 19406-51-0 | 4.22 | 4.85 | 197.15 | Q q q | 197.0 > 180.1 180.0 > 163.1 163.0 > 78.0 | 6 8 14 | |
2-Amino-4,6-dinitrotoluene CAS No. 35572-78-2 | 4.42 | 5.07 | 197.15 | Q q q | 197.0 > 180.1 180.0 > 133.0 180.0 > 67.0 | 6 6 12 |
Compound | LOD (ng/g d.w.) | LOQ (ng/g d.w.) | R2 |
---|---|---|---|
1,3-Dinitrobenzene | 0.03 | 0.10 | 0.985 |
2,4-Dinitrotoluene | 0.04 | 0.12 | 0.990 |
2,4,6-Trinitrotoluene | 0.20 | 0.68 | 0.986 |
4-Amino-2,6-dinitrotoluene | 0.05 | 0.17 | 0.973 |
2-Amino-4,6-dinitrotoluene | 0.04 | 0.14 | 0.980 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Strehse, J.S.; Bünning, T.H.; Koschorreck, J.; Künitzer, A.; Maser, E. Long-Term Trends for Blue Mussels from the German Environmental Specimen Bank Show First Evidence of Munition Contaminants Uptake. Toxics 2023, 11, 347. https://doi.org/10.3390/toxics11040347
Strehse JS, Bünning TH, Koschorreck J, Künitzer A, Maser E. Long-Term Trends for Blue Mussels from the German Environmental Specimen Bank Show First Evidence of Munition Contaminants Uptake. Toxics. 2023; 11(4):347. https://doi.org/10.3390/toxics11040347
Chicago/Turabian StyleStrehse, Jennifer Susanne, Tobias Hartwig Bünning, Jan Koschorreck, Anita Künitzer, and Edmund Maser. 2023. "Long-Term Trends for Blue Mussels from the German Environmental Specimen Bank Show First Evidence of Munition Contaminants Uptake" Toxics 11, no. 4: 347. https://doi.org/10.3390/toxics11040347