Insights into Toxic Prymnesium parvum Blooms as a Cause of the Ecological Disaster on the Odra River

Abstract

In 2022, Poland and Germany experienced a prolonged and extensive mass fish kill in the Odra River. During the period from the end of July to the beginning of September 2022, a high level of incidental disease and mortality was observed in various fish species (dozens of different species were found dead). The fish mortality affected five Polish provinces (Silesia, Opole, Lower Silesia, Lubuskie, and Western Pomerania) and involved reservoir systems covering most of the river (the Odra River is 854 km long, of which 742 km are in Poland). Fatal cases were investigated using toxicological, anatomopathological, and histopathological tests. Water samples were collected to determine nutrient status in the water column, phytoplankton biomass, and community composition. High nutrient concentrations indicated high phytoplankton productivity, with favorable conditions for golden algal blooms. The harmful toxins (prymnesins secreted by Prymnesium parvum habitats) had not been found in Poland before, but it was only a matter of time, especially in the Odra River, whose waters are permanently saline and still used for navigation. The observed fish mortality resulted in a 50% decrease in the fish population in the river and affected mainly cold-blooded species. Histopathological examinations of fish showed acute damage to the most perfused organs (gills, spleen, kidneys). The disruption to hematopoietic processes and damage to the gills were due to the action of hemolytic toxins (prymnesins). An evaluation of the collected hydrological, meteorological, biological, and physico-chemical data on the observed spatio-temporal course of the catastrophe, as well as the detection of three compounds from the group of B-type prymnesins in the analyzed material (the presence of prymnesins was confirmed using an analysis of the fragmentation spectrum and the accurate tandem mass spectrometry (MS/MS) measurement, in combination with high-performance liquid chromatography-tandem mass spectrometry (LC-MS/MS), allowed the formulation and subsequent testing of the hypothesis for a direct link between the observed fish mortality and the presence of prymnesins in the Odra River. This article systematizes what is known about the causes of the fish kill in the Odra River in 2022, based on official government reports (one Polish and one German) and the EU technical report by the Joint Research Centre. A review and critical analysis of government findings (Polish and German) on this disaster were conducted in the context of what is known to date about similar cases of mass fish kills.

Keywords: aquatic toxicity; ecological catastrophe; environmental monitoring; eutrophication; fish kill; harmful algal blooms; microalgal ecology; prymnesins; river ecosystem; water pollution.

Figure 1

P. parvum (N. Carter 1937) [85].

Figure 2

River Odra—geographical position with indication of measuring and control stations. Note: Different colors indicate 5 different Polish voivodeships (provinces) through which the Odra River flows (order from the top): West Pomeranian Voivodeship, Lubuskie Voivodeship, Lower Silesian Voivodeship, Opole Voivodeship, and Silesian Voivodeship. (source: own elaboration).

Figure 3

Locations along the Odra River where fish kills were reported (source: own elaboration).

Figure 4

MS/MS spectrum of PRM prymnesin B (Cl + 1 hexose) and PRM B1 (Cl + 2 hexose) compounds in a sample from the Odra River. The analysis was performed using a QTRAP5500 spectrometer. The apparent loss of the Δ 81 fragment indicates the presence of hexose (source: own elaboration based on IOŚ-PIB official government report [16]).

Figure 5

Chromatograms from the analysis of prymnesins content in water samples (source: based on [110]). The successive panels in the chromatogram show (from top): (1) UV at 280 nm; (2) chromatogram of extracted B-type prymnesin ions containing a chlorine unit and a hexose unit; (3) chromatogram of extracted B-type prymnesin ions containing a chlorine unit and two hexose units; and (4) chromatogram of extracted B-type prymnesin ions containing chlorine to which no sugar is bound (also called skeleton) (source: own elaboration based on IOŚ-PIB official government report [16,110]).

Figure 6

Distribution of group B prymnesins in selected water samples from the Odra River, reservoirs, and Gliwice Canal (source: own elaboration based on IOŚ-PIB official government report [16,110]).

Figure 7

Estimated prymnesin content, expressed in nmol/L (C), in selected water samples from the Odra River, reservoirs, and Gliwice Canal (source: own elaboration based on IOŚ-PIB official government report [16,110]).

Figure 8

Relationship between cell abundance of P. parvum (cells/L) and the relative number of prymnesins (left panel) and the relative number of prymnesins in log-transformed values (right panel) (source: own elaboration based on IOŚ-PIB official government report [16,110]).

Figure 9

Diagram showing the “golden algae” hypothesis testing (source: own elaboration).

Figure 10

Changes in water pH at General Inspectorate of Environmental Protection (GIOS) monitoring and control points between 28 July and 20 September 2022 (source: own elaboration). Subsequent bars indicate measured data (unclassified indicator). The toxicity of P. parvum appears to be increased at a pH above 7.0 [16,95,146], as indicated with the red line.

Figure 11

Values for electrolytic conductivity at measuring and control points of the General Inspectorate of Environmental Protection (GIOŚ) between 28 July and 20 September 2022 (source: own elaboration). NOTE: The red line shows the limit of good status for large lowland rivers (850 µS/cm).

Figure 12

Chlorophyll concentration in the Odra River from 19 July to 26 August 2022 (source: own elaboration based on the IOŚ-PIB official report).

Figure 12

Chlorophyll concentration in the Odra River from 19 July to 26 August 2022 (source: own elaboration based on the IOŚ-PIB official report).

Figure 13

Summary showing the “golden algae” hypothesis testing (source: own elaboration).