Unpredicted ecosystem response to compound human impacts in a European river.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
16 Jul 2024
Historique:
received: 22 12 2023
accepted: 05 07 2024
medline: 17 7 2024
pubmed: 17 7 2024
entrez: 16 7 2024
Statut: epublish

Résumé

Climate change elevates the threat of compound heat and drought events, with their ecological and socioeconomic impacts exacerbated by human ecosystem alterations such as eutrophication, salinization, and river engineering. Here, we study how multiple stressors produced an environmental disaster in a large European river, the Oder River, where a toxic bloom of the brackish-water planktonic haptophyte Prymnesium parvum (the "golden algae") killed approximately 1000 metric tons of fish and most mussels and snails. We uncovered the complexity of this event using hydroclimatic data, remote sensing, cell counts, hydrochemical and toxin analyses, and genetics. After incubation in impounded upstream channels with drastically elevated concentrations of salts and nutrients, only a critical combination of chronic salt and nutrient pollution, acute high water temperatures, and low river discharge during a heatwave enabled the riverine mass proliferation of B-type P. parvum along a 500 km river section. The dramatic losses of large filter feeders and the spreading of vegetative cells and resting stages make the system more susceptible to new harmful algal blooms. Our findings show that global warming, water use intensification, and chronic ecosystem pollution could increase likelihood and severity of such compound ecoclimatic events, necessitating consideration in future impact models.

Identifiants

pubmed: 39014022
doi: 10.1038/s41598-024-66943-9
pii: 10.1038/s41598-024-66943-9
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

16445

Informations de copyright

© 2024. The Author(s).

Références

IPCC. Climate Change 2022: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change (Cambridge University Press, 2022).
Ridder, N. N. et al. Global hotspots for the occurrence of compound events. Nat. Commun. 11, 5956 (2020).
pubmed: 33235203 pmcid: 7687898 doi: 10.1038/s41467-020-19639-3
Zscheischler, J. et al. A typology of compound weather and climate events. Nat. Rev. Earth Environ. 1, 333–347 (2020).
doi: 10.1038/s43017-020-0060-z
Bastos, A. et al. A joint framework for studying compound ecoclimatic events. Nat. Rev. Earth Environ. 4, 333–350 (2023).
doi: 10.1038/s43017-023-00410-3
Woolway, R. I., Kraemer, B. M., Zscheischler, J. & Albergel, C. Compound hot temperature and high chlorophyll extreme events in global lakes. Environ. Res. Lett. 16, 124066 (2021).
doi: 10.1088/1748-9326/ac3d5a
Tye, S. P. et al. Climate warming amplifies the frequency of fish mass mortality events across north temperate lakes. Limnol. Oceanogr. Lett. 7, 510–519 (2022).
doi: 10.1002/lol2.10274
Hartman, K. J. et al. A case study of a Prymnesium parvum harmful algae bloom in the Ohio River drainage: Impact, recovery and potential for future invasions/range expansion. Water 13, 3233 (2021).
doi: 10.3390/w13223233
Brown, A. R. et al. Assessing risks and mitigating impacts of harmful algal blooms on mariculture and marine fisheries. Rev. Aquacult. 12, 1663–1688 (2020).
doi: 10.1111/raq.12403
Southard, G. M., Fries, L. T. & Barkoh, A. Prymnesium parvum: The Texas experience 1. JAWRA J. Am. Water Resour. Assoc. 46, 14–23 (2010).
doi: 10.1111/j.1752-1688.2009.00387.x
Burford, M. A., Hamilton, D. P. & Wood, S. A. Emerging HAB research issues in freshwater environments. In Global Ecology and Oceanography of Harmful Algal Blooms. 391–402 (2018).
Carmichael, W. W. & Boyer, G. L. Health impacts from cyanobacteria harmful algae blooms: Implications for the North American Great Lakes. Harmful Algae 54, 194–212 (2016).
pubmed: 28073476 doi: 10.1016/j.hal.2016.02.002
Glibert, P. M., Berdalet, E., Burford, M. A., Pitcher, G. C. & Zhou, M. Harmful algal blooms and the importance of understanding their ecology and oceanography. In Global Ecology and Oceanography of Harmful Algal Blooms (eds. Glibert, P. M. et al.). 9–25 (Springer, 2018).
Reynolds, C. S. & Descy, J.-P. The production, biomass and structure of phytoplankton in large rivers. Large Rivers 3, 161–187 (1996).
Fischer, E. M., Sippel, S. & Knutti, R. Increasing probability of record-shattering climate extremes. Nat. Clim. Change 11, 689–695 (2021).
doi: 10.1038/s41558-021-01092-9
Søballe, D. M. & Kimmel, B. L. A large-scale comparison of factors influencing phytoplankton abundance in rivers, lakes, and impoundments. Ecology 68, 1943–1954 (1987).
pubmed: 29357178 doi: 10.2307/1939885
Bruns, N. E., Heffernan, J. B., Ross, M. R. V. & Doyle, M. A simple metric for predicting the timing of river phytoplankton blooms. Ecosphere 13, 4 (2022).
doi: 10.1002/ecs2.4348
Cañedo-Argüelles, M. et al. Saving freshwater from salts. Science 351, 914–916 (2016).
pubmed: 26917752 doi: 10.1126/science.aad3488
Olli, K., Ptacnik, R., Klais, R. & Tamminen, T. Phytoplankton species richness along coastal and estuarine salinity continua. Am. Nat. 194, E41–E51 (2019).
pubmed: 31318279 doi: 10.1086/703657
Havens, K. E. & Paerl, H. W. Climate change at a crossroad for control of harmful algal blooms. Environ. Sci. Technol. 49, 12605–12606 (2015).
pubmed: 26465060 doi: 10.1021/acs.est.5b03990
Krodkiewska, M., Spyra, A. & Cieplok, A. Assessment of pollution, and ecological status in rivers located in the Vistula and Oder river basins impacted by the mining industry in Central Europe (Poland). Ecol. Indic. 144, 109505 (2022).
doi: 10.1016/j.ecolind.2022.109505
Free, G. et al. An EU Analysis of the Ecological Disaster in the Oder River of 2022 (2023).
Kolada, A. E. A. Wstępny Raport Zespołu ds. Sytuacji na Rzece Odrze (2022).
Schulte, C. et al. Fischsterben in der Oder, August 2022, Statusbericht Stand 30.09.2022 (Umweltbundesamt, 2022).
Lu, R. et al. Heat waves in summer 2022 and increasing concern regarding heat waves in general. Atmos. Ocean. Sci. Lett. 16, 100290 (2023).
doi: 10.1016/j.aosl.2022.100290
Schumacher, D. L. et al. Detecting the human fingerprint in the summer 2022 West-Central European soil drought. EGUsphere 2023, 1–41 (2023).
Brandenburg State Office for the Environment. https://lfu.brandenburg.de/lfu/de/aufgaben/wasser/fliessgewaesser-und-seen/gewaesserueberwachung/wasserguetemessnetz/frankfurt-oder/ (2022).
Binzer, S. B. et al. A-, B- and C-type prymnesins are clade specific compounds and chemotaxonomic markers in Prymnesium parvum. Harmful Algae 81, 10–17 (2019).
pubmed: 30638493 doi: 10.1016/j.hal.2018.11.010
Svenssen, D. K. et al. Development of an indirect quantitation method to assess ichthyotoxic B-type prymnesins from Prymnesium parvum. Toxins 11, 251 (2019).
pubmed: 31060245 pmcid: 6563205 doi: 10.3390/toxins11050251
Zscheischler, J. et al. Future climate risk from compound events. Nat. Clim. Change 8, 469–477 (2018).
doi: 10.1038/s41558-018-0156-3
Olson, J. R. Predicting combined effects of land use and climate change on river and stream salinity. Philos. Trans. R Soc. Lond. B Biol. Sci. 374, 20180005 (2018).
pubmed: 30509907 pmcid: 6283963 doi: 10.1098/rstb.2018.0005
Baker, J. W. et al. Growth and toxicity of Prymnesium parvum (haptophyta) as a function of salinity, light, and temperature. J. Phycol. 43, 219–227 (2007).
doi: 10.1111/j.1529-8817.2007.00323.x
Baker, J. W. et al. Growth at the edge of the niche: An experimental study of the harmful alga Prymnesium parvum. Limnol. Oceanogr. 54, 1679–1687 (2009).
doi: 10.4319/lo.2009.54.5.1679
Meybeck, M. & Helmer, R. The quality of rivers: From pristine stage to global pollution. Palaeogeogr. Palaeoclimatol. Palaeoecol. 75, 283–309 (1989).
doi: 10.1016/0031-0182(89)90191-0
Granéli, E. & Salomon, P. S. Factors influencing allelopathy and toxicity in Prymnesium parvum. JAWRA J. Am. Water Resour. Assoc. 46, 108–120 (2010).
doi: 10.1111/j.1752-1688.2009.00395.x
Verzano, K. et al. Modeling variable river flow velocity on continental scale: Current situation and climate change impacts in Europe. J. Hydrol. 424–425, 238–251 (2012).
doi: 10.1016/j.jhydrol.2012.01.005
Van Looy, K. et al. The three Rs of river ecosystem resilience: Resources, recruitment, and refugia. River Res. Appl. 35, 107–120 (2019).
doi: 10.1002/rra.3396
van Treeck, R., Van Wichelen, J. & Wolter, C. Fish species sensitivity classification for environmental impact assessment, conservation and restoration planning. Sci. Total Environ. 708, 135173 (2020).
pubmed: 31796278 doi: 10.1016/j.scitotenv.2019.135173
Witt, B. A., Beyer, J. E., Hallidayschult, T. C. & Hambright, K. D. Short-term toxicity effects of Prymnesium parvum on zooplankton community composition. Aquat. Sci. 81, 4 (2019).
doi: 10.1007/s00027-019-0651-2
Dudgeon, D. Multiple threats imperil freshwater biodiversity in the Anthropocene. Curr. Biol. 29, R960–R967 (2019).
pubmed: 31593677 doi: 10.1016/j.cub.2019.08.002
Utermöhl, H. Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Int. Vereinigung Theor. Angew. Limnol. Mitteilungen 9, 1–38 (1958).
Shatwell, T., Nicklisch, A. & Köhler, J. Temperature and photoperiod effects on phytoplankton growing under simulated mixed layer light fluctuations. Limnol. Oceanogr. 57, 541–553 (2012).
doi: 10.4319/lo.2012.57.2.0541
Höhne, C. & Gessner, J. Was stört den Stör? Erste Erkenntnisse aus dem Wiedereinbürgerungsprojekt des Baltischen Störs (2022).
Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321 (2010).
pubmed: 20525638 doi: 10.1093/sysbio/syq010
Hoffmann, M., Monaghan, M. T. & Reinert, K. PriSeT: Efficient de novo primer discovery. In Proceedings of the 12th ACM Conference on Bioinformatics, Computational Biology, and Health Informatics (2021).
Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).
pubmed: 27214047 pmcid: 4927377 doi: 10.1038/nmeth.3869
Guillou, L. et al. The Protist Ribosomal Reference database (PR2): A catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Res. 41, D597-604 (2013).
pubmed: 23193267 doi: 10.1093/nar/gks1160
Medić, N., Varga, E., Waal, D. B. V. D., Larsen, T. O. & Hansen, P. J. The coupling between irradiance, growth, photosynthesis and prymnesin cell quota and production in two strains of the bloom-forming haptophyte, Prymnesium parvum. Harmful Algae 112, 102173 (2022).
pubmed: 35144820 doi: 10.1016/j.hal.2022.102173
Wevers, J. et al. IdePix for Sentinel-2 MSI algorithm theoretical basis document (version 1.0). Zenodo (2022).
Brockmann, C. et al. Evolution of the C2RCC neural network for Sentinel 2 and 3 for the retrieval of ocean colour products in normal and extreme optically complex waters. Remote Sens. Environ. Living Planet Sympos. 740, 54 (2016).
Doerffer, R. & Schiller, H. The MERIS case 2 water algorithm. Int. J. Remote Sens. 28, 517–535 (2007).
doi: 10.1080/01431160600821127
European_Commission. INSPIRE Geoportal (2023).
Team R. A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2023).
Pebesma, E. & Bivand, R. Spatial Data Science: With Applications in R (Chapman and Hall/CRC, 023).
van der Meer, L., Abad, L., Gilardi, A. & Lovelace, R. sfnetworks: Tidy Geospatial Networks (2023).
Csárdi, G. et al. igraph: Network Analysis and Visualization in R (2023).
Copernicus_Climate_Change_Service_Climate_Data_Store. River Discharge and Related Historical Data from the European Flood Awareness System. (Copernicus Climate Change Service (C3S) Climate Data Store (CDS), 2019).
Wolter, C., Hallermann, J. & Rothe, U. Erfassung und Bewertung von ausgewählten Arten und Habitaten der Fische, Rundmäuler und Großmuscheln. Endbericht im Auftrag der Nationalpark Unteres Odertal-Verwaltung, Vergabenummer: NLP-2022-01-L2 (2022).
Wolter, C. & Freyhof, J. Diel distribution patterns of fishes in a temperate large lowland river. J. Fish Biol. 64, 632–642 (2004).
doi: 10.1111/j.1095-8649.2004.00327.x
Wolter, C., Zahn, S. & Gessner, J. Entwicklung, Nutzung und Schutz der Fischfauna in der Brandenburgischen Oder: Fischfauna Brandenburgische Oder. Vol. 65 (Schriften d. Instituts f. Binnenfischerei e. V., 2023).
Rasmussen, S. A. et al. Chemodiversity of ladder-frame prymnesin polyethers in Prymnesium parvum. J. Nat. Prod. 79, 2250–2256 (2016).
pubmed: 27550620 doi: 10.1021/acs.jnatprod.6b00345

Auteurs

Jan Köhler (J)

Leibniz Institute of Freshwater Ecology and Inland Fisheries (IGB), Berlin, Germany. jan.koehler@igb-berlin.de.

Elisabeth Varga (E)

Department of Food Chemistry and Toxicology, University of Vienna, Vienna, Austria. elisabeth.varga@vetmeduni.ac.at.
Unit Food Hygiene and Technology, Centre for Food Science and Veterinary Public Health, Clinical Department for Farm Animals and Food System Science, University of Veterinary Medicine Vienna, Vienna, Austria. elisabeth.varga@vetmeduni.ac.at.

Stephanie Spahr (S)

Leibniz Institute of Freshwater Ecology and Inland Fisheries (IGB), Berlin, Germany.

Jörn Gessner (J)

Leibniz Institute of Freshwater Ecology and Inland Fisheries (IGB), Berlin, Germany.

Kerstin Stelzer (K)

Brockmann Consult GmbH, Hamburg, Germany.

Gunnar Brandt (G)

Brockmann Consult GmbH, Hamburg, Germany.

Miguel D Mahecha (MD)

Institute for Earth System Science and Remote Sensing, Leipzig University, Leipzig, Germany.
Remote Sensing Centre for Earth System Research, Leipzig University and Helmholtz Centre for Environmental Research, UFZ, Leipzig, Germany.
German Centre for Integrative Biodiversity Research, iDiv, Halle, Jena and Leipzig, Germany.

Guido Kraemer (G)

Institute for Earth System Science and Remote Sensing, Leipzig University, Leipzig, Germany.
Remote Sensing Centre for Earth System Research, Leipzig University and Helmholtz Centre for Environmental Research, UFZ, Leipzig, Germany.

Martin Pusch (M)

Leibniz Institute of Freshwater Ecology and Inland Fisheries (IGB), Berlin, Germany.

Christian Wolter (C)

Leibniz Institute of Freshwater Ecology and Inland Fisheries (IGB), Berlin, Germany.

Michael T Monaghan (MT)

Leibniz Institute of Freshwater Ecology and Inland Fisheries (IGB), Berlin, Germany.
Institute of Biology, Free University Berlin, Berlin, Germany.

Matthias Stöck (M)

Leibniz Institute of Freshwater Ecology and Inland Fisheries (IGB), Berlin, Germany.

Tobias Goldhammer (T)

Leibniz Institute of Freshwater Ecology and Inland Fisheries (IGB), Berlin, Germany. tobias.goldhammer@igb-berlin.de.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH