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Article

The Decreased Incidence of Raphidiopsis raciborskii Bloom in a Temperate Floodplain Lake in the Middle Danube Affected by Extreme Hydrological Events

by
Filip Stević
,
Melita Mihaljević
*,
Dubravka Špoljarić Maronić
,
Tanja Žuna Pfeiffer
and
Vanda Zahirović
Department of Biology, Josip Juraj Strossmayer University of Osijek, Ulica cara Hadrijana 8/A, 31000 Osijek, Croatia
*
Author to whom correspondence should be addressed.
Water 2025, 17(3), 309; https://doi.org/10.3390/w17030309
Submission received: 20 December 2024 / Revised: 17 January 2025 / Accepted: 20 January 2025 / Published: 23 January 2025
(This article belongs to the Special Issue Protection and Restoration of Freshwater Ecosystems)
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Abstract

:
Extreme hydrological events have become more frequent in the Danube River Basin in recent decades. In this research, we focus on the consequences of such events on the dynamic of invasive cyanobacteria Raphidiopsis raciborskii (Wołoszyńska) Aguilera et al. (formerly known as Cylindrospermopsis raciborskii (Wołoszyńska) Seenayya et Subba Raju). In the Danube floodplain lake used as a case study, the investigated period from 2003 to 2016 was characterized by the cyclical occurrence of extreme floods (2006 and 2013) and extreme droughts (2003 and 2015). As a result, the lake changed several times from a phytoplankton turbid state to a clear state characterized by a very low phytoplankton biomass. R. raciborskii was abundant in the phytoplankton and bloomed in summer 2003 (June–September) and then in summer 2007 (June–August) and in August 2013. Extreme summer drought triggered the bloom, and water temperature was the most significant environmental variable during the bloom. The observed declining trend in total cyanobacterial biomass, including the less frequent occurrence of the R. raciborskii bloom, can be linked to the ecological disturbances in the stable state of the lake caused by extreme hydrological events. This suggests that the effects of climate change may be less detrimental in preserved natural river–floodplain systems.

1. Introduction

Extreme climatic events such as heat waves, droughts, heavy rainfall, and floods are natural occurrences affecting river and stream ecosystems globally [1]. The analysis of historical flood events and projections for central and eastern Europe shows that the intensity and frequency of floods will likely increase [2]. At the same time, a trend towards more intense heatwaves and more extended periods of little or no precipitation has already been observed [3]. According to the ICPDR report [4], extreme hydrological events during the last decades affected significant parts of the Danube River Basin. Moreover, extreme floods alternated with dry periods. Thus, widespread droughts in 2003 affected a third of the EU territory and were followed by events that affected portions of northern, southern, and western Europe in 2007, 2011, and 2012. In 2015, parts of Europe were marked by extraordinarily high temperatures in the summer, and the conditions, particularly in central and eastern Europe, were very dry, perhaps the driest in decades [4]. In the same decade, more precisely in 2002, extreme floods for the Danube occurred due to the heavy rains in central and eastern Europe and later on in the spring and summer of 2006 due to the large amounts of melted snow, a very warm spring, and heavy precipitation. The Danube water levels at a particular river stretch exceeded the maxima observed during the previous 130 years [5]. Again, in the summer of 2013, extreme floods occurred along the middle Danube; in some sections, the water levels were even higher than the previous record in 2006 [6]. Relevant research highlights a statistically significant trend in increased extreme events in the Danube Basin for both the winter and summer [7].
Extreme events may have even more profound consequences on freshwater environments rather than incremental changes in average conditions, with many systems being exposed to conditions with no recent historical precedent [8]. Generally, the impacts of single extreme events such as floods, droughts, etc., depend on the context and can ultimately be deleterious but also beneficial; the factors that need to be considered are the magnitude, extent, and timing of the event in relation to the life cycles of the constituent species [1]. Nowadays, there is a consensus that an increase in freshwater cyanobacterial blooms occur as a consequence of the cumulative effect of water eutrophication by nutrient enrichment and global warming, including other concomitant environmental changes, such as more frequent extreme rainfall events [9]. Future climatic change scenarios predict increasingly higher temperatures, an even more intense vertical stratification of aquatic eco-systems, and alterations in seasonal and interannual weather patterns (including droughts, storms, and floods); these changes all favor harmful cyanobacterial blooms in eutrophic waters [10].
Various species of harmful cyanobacteria may benefit from regional and global climatic change, and one of them is undoubtedly the invasive cyanobacterium Raphidiopsis raciborskii (Wołoszyńska) Aguilera et al. (formerly known as Cylindrospermopsis raciborskii (Wołoszyńska) Seenayya et Subba Raju) [11]. Recent studies using molecular methods (reviewed by [12]) have demonstrated the genetical likeness between the Cylindrospermopsis and Raphidiopsis genera.
The bloom-forming potential of R. raciborskii is the focus of current research due to its toxicity and its consequences on public and environmental health [13]. R. raciborskii is a planktonic species with a primary origin in tropical lakes and rapid invasion throughout various freshwater biotopes worldwide [14]. It seems to prefer highly eutrophic waters when water temperature is high and light conditions are poor, but lower trophic status does not affect it significantly, and it can also be dominant under varied abiotic conditions, such as high concentrations of dissolved minerals or variable salinity [15]. The success of R. raciborskii in the world’s lakes can be attributed to multiple reasons, as summarized by Padisák [14], especially the good floating ability that allows diurnal migration, superior shade tolerance, high-affinity ammonia uptake, the possibility to fix atmospheric N, relatively high-affinity P-uptake, and high P-storage capacity, as well as resistance to grazing.
In the context of the historical records of the spreading of R. raciborskii along the European freshwaters, according to Padisák [14], there is only one certain record of R. raciborskii in Europe before the 1970s, in Lake Castoria (Greece), whereas it has been successful in spreading along the various lentic and lotic habitats. The first finding of R. raciborskii in the Danube River Basin was in 1958, at four localities (arms and bays) near Ismail and Reni (Moldavia), then in a Dunaszegi dead-arm of river Danube between 1975 and 1980, and finally in the Danube River during the 1980–1990s ([16,17,18,19] reference cited in [14]). Until the beginning of this century, the bloom of R. raciborskii was registered in the floodplain areas from the Lower Danube [20] to the Upper Danube [21]. For example, in the shallow urban lake Alte Donau (Wienna), a switch of the ecosystem to the complete dominance of the R. raciborskii occurred in 1992, and this compositional change was accompanied by a six-fold increase in annual average biovolume and a dramatic loss of macrophytes [22].
Many contemporary studies focused on the climate impact on the blooming of R. raciborskii, as summarized by Sinha et al. [23] and Briand et al. [24], who indicated that an increase in temperature will very likely contribute to the more frequent formation of water blooms and the further spread of R. raciborskii in temperate regions. However, little is known about how other consequences of climate change, such as the more frequent occurrence of extreme events, especially extreme floods, affect the bloom formation of R. raciborskii. Of particular interest in this context are aquatic biotopes in floodplains where the dynamics of flooding are the main ecological factor that can have a dual impact on the development of algal and cyanobacterial planktonic communities [25]. For this reason, we chose Lake Sakadaš, a small shallow lake in the floodplain of the Middle Danube, as the case studied herein. The aim of this study was to observe the progress of the development of the R. raciborskii population in Lake Sakadaš in the period from 2003, when the first bloom of R. raciborskii was recorded [26], to 2016. Since the aforementioned period was marked by extreme hydrological events, especially floods in that part of the Danube Basin, it was to be expected that this would be reflected in the dynamics of R. raciborskii occurrence on the annual scale but not in the long-term spread of R. raciborskii in this floodplain lake.

2. Materials and Methods

Lake Sakadaš is a shallow floodplain lake (an average depth of about 5 m, with a surface water area of about 0.15 km2) located in the natural floodplain along the River Danube (river 1383–1410 km) (Figure 1) and is a part of the Kopački rit Nature Park (Croatia). The lake is in direct hydrological connection with the Danube through a system of natural channels. Flooding of the floodplain begins when the Danube water level (DWL) at the gauge station near Apatin (river 1401.4 km) rises above 3 m [27]. Floods may occur at any time during the year, but, usually, floods occur in the first half of the year (in mid-spring) [28]. Firstly, flooding occurs in the nethermost terrain and spreads through the floodplain area in extension, which depends on the increase in the river discharge. According to Schwarz [29], minor floods (3–3.5 m DWL) inundate less than 10% of the floodplain area, while extremely high floods (more than 5 m DWL) inundate almost the entire floodplain.
Sampling was carried out monthly from 2003 to 2016. In situ data of water temperature (WT), dissolved oxygen concentration (DO), and pH were measured with the portable measuring device WTW Multi 340i (Wissenschaftlich-Technische Werkstätten, Germany); water depth (WD) was estimated with a calibrated rope and transparency (SD) with a Secchi disc. The nutrient analysis included the determination of ammonium (NO4-N; [30]), nitrates (NO3-N; [31]), nitrites (NO2-N; [32]), total nitrogen (TN; [33]), and total phosphorus (TP; [34]).
Integrated water samples for phytoplankton analysis were collected by filtering 10 L of water through a phytoplankton net and determining the species under a microscope (Carl Zeiss Jena) using phytoplankton identification manuals [35,36,37,38,39]. A quantitative phytoplankton assessment was carried out according to [40] using an inverted microscope (Axiovert 25, Carl Zeiss, Inc., Göttingen, Germany) by counting and measuring the individuals (unicell, colony, coenobium, or filament) in the sedimentation chambers. The biovolumes were estimated using the recommended geometric shapes [41] and converted into biomass according to [42,43].
The relationship between the environmental variables and the biomass of phytoplankton groups and the relationship between the environmental variables and the biomass of cyanobacterial species in the bloom years were evaluated by redundancy analysis (RDA). RDA was selected as the best constrained ordination method according to the detrended correspondence analysis (DCA) [44]. Forward selection based on the permutation test (Monte Carlo, 499 permutations) identified a significant set of environmental variables (p < 0.05) explaining the species data. A total of 12 environmental variables were included in the analysis: DWL (mean water level of the Danube 10 days prior to sampling), SD, WT, WD, DO, pH, NH4-N, NO2-N, NO3-N, TN, TP, and the ratio of total nitrogen and total phosphorus (TN/TP), with only the significant environmental variables shown in the ordination diagrams. The analyses were carried out using CANOCO 4.5 software (Biometrics-Plant Research International, Wageningen, the Netherlands). Correlations (Pearson’s coefficient, r) were performed to analyze the relationship between DWL in different years and cyanobacterial biomass. Z-score standardization was used for data standardization (x = (original data-mean)/standard deviation).

3. Results

3.1. Flooding Patterns and Environmental Parameters

The flooding patterns can be defined on the basis of the fluctuations in the DWL measured at the gauge at river kilometer 1401.4 (Figure 2). During the observation period, the DWL fluctuated significantly, from extremely low values (−0.46 m in 2003, −0.30 m in 2011, and −0.07 m in 2016) to extremely high water levels, with values up to 8.17 m in 2013, 8.08 m in 2006, 7.80 m in 2010, and 7.28 m in 2009.
Based on the changes in physical and chemical parameters on an annual level (Table 1, Figure 3), the trends of their changes in the observed period of 14 years can be defined. Mean annual values of WT were in the range of 14.7–19.9 °C, showing a decreasing trend. Large oscillations were recorded in the mean values of lake WD (4.31–7.93 m), with an increasing trend influenced by frequent occurrences of high floods. The mean annual values of water transparency (SD, 0.86–1.47 m) were highly variable. Moreover, there were very significant changes in the values of nutrients. The mean annual values of NO2-N (0.01–0.11 mg L−1), NO3-N (0.14–1.24 mg L−1), and HN4-N (0.03–0.61 mg L−1) showed a decreasing trend, while mean annual values of TN (0.83–3.91 mg L−1), TP (0.13–0.81 mg L−1), and TN/TP (4.76–28.74) showed an increasing trend.

3.2. Phytoplankton Biomass Dynamic

During the research period (2003–2016), the total phytoplankton biomass fluctuated on a monthly basis from only 0.01 mg L−1 (August 2014) to 274.96 mg L−1 (July 2003). The highest values of mean annual phytoplankton biomass were reached in years when cyanobacterial bloom developed, namely, 2003, 2004, 2007, 2008, 2011, and 2013 (Figure 4). This can be characterized as a phytoplankton turbid state. In other years, the water bloom of cyanobacteria was not developed, and the highest achieved biomass was more or less below 50 mg L−1, so the mean annual value of the total phytoplankton biomass was also low. Such a condition can be characterized as a phytoplankton clear state. This indicates that the cyclic change between phytoplankton turbid and clear state occurred in very short intervals of only one year to a maximum of three years (Figure 5).

3.3. Raphidiopsis raciborskii Blooming

Cyanobacteria were present in the investigated lake with 44 species, among which particular species were periodically well-developed and characterized turbid conditions with a contribution to the total phytoplankton biomass of up to 95.8%, as was found in June 2003 (Figure 6a). However, there has been a visible trend of the decreasing biomass of cyanobacteria and total phytoplankton biomass over the years (Figure 4).
The species R. raciborskii was present in at least one sample in nine observed years (35 samples out of a total of 135) with its proportion of the total biomass ranging from 0.2% (August 2012) to 69.4% (August 2013) (Figure 6b). The blooming of R. raciborskii was detected in 2003, 2007, and 2013, while the low abundant population was found in 2008, 2011, 2015, and 2016. In 2012, R. raciborskii accounted for no more than 0.2% of the total phytoplankton biomass, while in 2005–2006, 2009–2010, and 2013, R. raciborskii was not found.
Among other cyanobacterial species, P. agardhii was continuously present during the entire research period. This species was found in almost all years (in a total of 88 months) with a contribution to the total phytoplankton biomass from 0.3% (August 2013) to 69.6% (October 2008) (Figure 6c). In the observed period, R. raciborskii and P. agardhii often appeared together, showing a statistically significant positive correlation in 2007 (r = 0.9828, p < 0.01), 2008 (r = 0.9806, p = 0.019), and 2011 (r = 0.9052, p < 0.01).
In 2003, R. raciborskii dominated the phytoplankton community throughout the summer, from June to September. The highest contribution of R. raciborskii to the phytoplankton biomass (48.5%, 87.6 mg L−1) was found in September 2003, while the highest biomass (91.41 mg L−1, 40.1%) was found in August. P. agardhii was also well developed in August and September, with 77.94 mg L−1 (34.2%) and 36.57 mg L−1 (20.3%), respectively. In 2007, from June to August, R. raciborskii (28.31–71.12 mg L−1, 27.7–38.4%) together with P. agardhii (26.60–99.92 mg L−1, 36.1–50.5%) were the best-developed species. In September, there was a high flood, and the lake volume rapidly increased with a disruption of thermal stratification and a sudden drop in water temperature, which led to a significant decrease in R. raciborskii biomass (up to 5.6%). In 2013, the development of R. raciborskii started in July (3.30 mg L−1, 6.5%), reaching a biomass of 71.24 mg L−1 in August (69.4% of phytoplankton biomass). During that period, the contribution of P. agardhii was under 5% of phytoplankton biomass.

3.4. Ordinations

The RDA was used to determine the relationships between environmental parameters and the biomass of phytoplankton groups in the years with cyanobacterial blooms (2003–2004, 2007–2008, 2011, and 2013). In addition, another RDA was conducted to determine the relationships between environmental parameters and cyanobacterial species during the period R. raciborskii development (May to October of the mentioned years). The species–environment correlations for RDA axes 1 and 2 (Table 2) show a significant relationship between six environmental variables and the biomass of phytoplankton groups and a significant relationship between five environmental parameters and the biomass of cyanobacteria species (Figure 7). The cyanobacteria group was characterized by higher WT and NH4-N concentration and lower WD, DWL, SD, and TN/TP values (Figure 7a). WT, NH4-N, and NO3-N concentrations were significant variables for R. raciborskii and P. agardhii, along with lower WD and DWL (Figure 7b).

4. Discussion

The first important finding from this study is that the investigated lake shifted from a clear to a turbid state several times over a period of 14 years. A phytoplankton turbid state with high phytoplankton biomass occurred in 2003–2004 and 2007–2008, and then again in 2011 and 2013, while a phytoplankton clear state with very low total biomass occurred in 2005–2006 and 2009–2010 and then in 2012 and again in 2014–2016. The change from the turbid to clear state of the lake did not surprise us as we had already observed it in previous short-term studies [45], but what did surprise us were the cyclically repeated changes between clear and turbid state in very short periods of two to three years.
It is known that some shallow lakes can repeatedly alternate between a vegetation-dominated clear-water state and a contrasting phytoplankton turbid state, as shown by examples presented by [46,47,48,49] and many others. In general, such changes occur quite irregularly, but, in some cases, the changes between states are remarkably regular [50], and lakes can be shifted several times within a few decades, as has been observed, for example, in two shallow eutrophic lakes in southern Sweden [51]. Determining the causes of such changes is difficult, mainly because the shift is usually not caused by a single factor or process but by several pressures [52,53]. However, nutrients are always the first in focus. Our results show that the alternative states exist across a wide range of nutrient concentrations, particularly phosphorus concentration, as can be seen from the conventional biomass–phosphorus diagram.
Significantly, the frequent alternations between clear-water and phytoplankton turbid states coincided with the extreme hydrological events in the Danube region described above. Similarly, extreme hydrological phenomena such as flash floods or prolonged droughts caused a change in regime from clear water to turbid or vice versa in six floodplain lakes of the Lower Vistula in the period 2007–2015 [54]. In general, floodplains and oxbow lakes are excellent examples of stable states, and they can switch from one dominance to another due to changes in natural factors such as changes in water level or reductions in flow [22]. For example, cyclic shifts in the lakes of the Paraná floodplain have been associated with extreme drought and flood events related to the El Niño Southern Oscillation, which is associated with discharge anomalies in the river [55]. Another example is 70 lakes in the Lower Rhine floodplains in the Netherlands, where episodes of low water levels caused by a dry period, particularly the extremely dry summer of 2003, appear to be an important external factor in the alternation between the two contrasting states [56]. While some lakes quickly became turbid again, others, such as the lake in our study, took several years to transition to the turbid state.
The blooming of cyanobacteria was the main feature of the turbid state. The abundant population of R. raciborskii, which can be characterized as a bloom (biomass above 50 mg L−1 [14]), occurred irregularly and developed in the summer of 2003 (June–September) and then in the summer of 2007 (June–August) and in August 2013. Contrary to predictions, the duration of the bloom became shorter over time, and the biomass of R. raciborskii reached became lower, which fits into the general downward trend of the total biomass of cyanobacteria and the total biomass of phytoplankton. The monodominant bloom of R. raciborskii occurred only in 2013, while the co-dominant species during the bloom in 2003 and 2007 was P. agardhii, a filamentous cyanobacteria that bloomed more frequently and contributed more to the total biomass than R. raciborskii. Depending on local environmental conditions, R. raciborskii was found in association with other cyanobacterial species, for example, with Limnothrix redekei in a highly eutrophic urban lake [21], with L. redekei and Microcystis aeruginosa in a shallow Mediterranean lake [57], or with Aphanizomenon gracile and M. aeruginosa in hypertrophic shallow wetlands [20]. As in our lake, R. raciborskii was in association with P. agardhii in two lakes in western Poland [58], and the results of this study suggested that light was an important factor of phytoplankton community structure, leading to a shift from a community dominated by P. agardhii in very turbid waters to communities that were more diverse, including the invasive R. raciborskii, in clearer waters. However, our results show a positive correlation between the biomass dynamics of R. raciborskii and P. agardhii, and, during the bloom, these two species contributed complementary to the establishment of equilibrium. According to Sommer et al. [59], this means that R. raciborskii and P. agardhii, together or with only one other species, account for more than 80% of the total biomass and that such conditions endure for more than 1–2 weeks but also that the total biomass does not increase significantly during this time.
Another specificity established in our research is that the biomass of P. agardhii was changed gradually. At the same time, R. raciborskii shifted sharply from being a highly dominated population to a solitary filament that appeared in the phytoplankton. This finding is the opposite of the established responses of these two species to environmental gradients in many lakes in different climatic regions [60]. Thus, in many respects, the dynamic of R. raciborskii in this floodplain lake indicates certain environmental specificities that could significantly impact its bloom.
Extremely long-lasting dry conditions in 2003 were incidental in this part of Central and East Europe and that seems to have triggered the heavy bloom of R. raciborskii in this lake. Padisák [14] pointed out that incidental warm conditions, with a water temperature of 22–24 °C as optimal for the germination of R. raciborskii, can explain the irregularity of its bloom in Lake Balaton, which consistently occurred in the third to the fourth week of the continuously warm period. Similarly, water temperature was the most significant environmental variable, as was shown by the RDA analysis, that influenced the dynamic of R. raciborskii in the investigated lake. The water temperature was in the range of 24–26 °C during its blooming, which is near the temperature of around 30 °C at which the maximum growth rates of various strains of R. raciborskii from different geographic regions were established [24]. Conversely, the significant effect of lower temperature on R. raciborskii development in this lake was evident from the rapid disappearance of the bloom in September 2007, when the water temperature suddenly dropped to only 16 °C in conditions of long-lasting rainy weather and huge income of colder floodwaters from the Danube.
The blooming of R. raciborskii in temperate regions almost obligatory occurs in the late season when the temperatures are the warmest and nutrient concentrations are low because most of the nutrients have been used by other cyanobacteria [61]. Our results indicate that the significant variables for the cyanobacterial bloom were the concentration of the NH4-N and TN/TP ratio among nutrients. The concentration of ammonia was very low in summer, which can be an advantage for R. raciborskii because, having heterocysts, it can fixate N when growth is directly limited by ammonium. Besides that, ammonium is the preferred nitrogen form for R. raciborskii [62], and it also has a high affinity for phosphorus and can accumulate phosphorus at relatively low ambient concentrations [63]. These physiological advantages may act in isolation or synchronously to contribute to its capacity to form dense water blooms [64]. Our results show an increasing trend of TN/TP values in the observed period, which may have negative consequences for cyanobacterial blooms and can contribute to the decreasing trend of phytoplankton biomass [65,66]. However, Chislock et al. [67] have proven that R. raciborskii can dominate under very low and high nitrogen-to-phosphorus ratios. Therefore, we could not find a strong relation between the decreasing trend of R. raciborskii blooming and nutrient levels, maybe because, unlike many bloom-forming species, the dominance of this species is not simply linked to higher nutrient loads [68].
Variables indicating the income of floodwaters into the investigated lake, such as the DWL and WD, were significant for cyanobacteria during the vegetation period, as indicated by the RDA analysis. Our previous results by Mihaljević and Stević [45] show that flooding dynamics and intensity can be qualified as the most important factors controlling cyanobacterial blooms in this floodplain lake, as well as in most floodplain lakes both in temperate regions, as well as in tropical and subtropical areas [69]. The results indicate that the inflow of floodwaters was a disturbing factor for the population dynamics of R. raciborskii, and it is evident that the biomass of R. raciborskii rapidly fell to extremely low values during high-intensity flooding. It is known that hydraulic flushing can cause a greater loss of phytoplankton and can directly affect the shift of phytoplankton composition between cyanobacteria dominance/non-dominance in eutrophic waters [9]. In addition to the effect of flushing, floods also cause the mixing of water, to which many cyanobacterial species are sensitive [70], but R. raciborskii has a wide tolerance for mixing and is commonly reported in mixed conditions [60]. A study on extensive data sets covering different climatic regions and laboratory experiments by Bonilla et al. [60] indicates that R. raciborskii, like P. agardhii, has a wide tolerance for mixing. Moreover, Figueredo and Giani [71] showed that the constant mixed water column may have been an essential factor driving the long-term dominance of R. raciborskii. Contrary to this, water mixing caused by floods, especially during extreme floods when the speed of water entering the lake is high, seems to have had a long-term negative consequence on the development of R. raciborskii bloom in the investigated floodplain lake.

5. Conclusions

Our research has shown that extreme hydrological events, which are becoming more frequent due to climate change, can significantly affect the ecological stability of floodplain lakes. According to the dynamics of the occurrence of extreme floods and droughts, the studied lake cyclically alternated between clear and turbid states in short periods of time. Such disturbances had unpredictable effects on the occurrence of the R. raciborskii bloom—instead of the expected increasingly massive development, the duration of the bloom shortened over time and the biomass achieved became lower. In addition, our results suggest that the decreasing trend of total cyanobacterial biomass as well as total phytoplankton biomass in the studied floodplain shallow lake with a clear trend of nutrient increase is related to the increasing frequency of extreme hydrological events. Therefore, the effects of climate change on the progressive development of invasive cyanobacterial species, including R. raciborskii, may be less detrimental in dynamic ecosystems as they are floodplain lakes with a preserved natural connection to the parent river.

Author Contributions

Conceptualization, M.M. and F.S.; methodology, M.M., F.S. and D.Š.M.; validation, M.M., F.S., D.Š.M. and T.Ž.P.; formal analysis, F.S.; investigation, M.M., F.S., D.Š.M. and V.Z.; data curation, F.S., D.Š.M., T.Ž.P. and V.Z.; writing—original draft preparation, M.M. and F.S.; writing—review and editing, M.M., F.S., D.Š.M. and T.Ž.P.; visualization, F.S.; funding acquisition, M.M. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded partly by the Ministry of Science, Education and Sports of the Republic of Croatia (project No. 285-0000000-2674) and the Josip Juraj Strossmayer University of Osijek, Department of Biology (Institutional project No. 3105-1).

Data Availability Statement

Raw data that support the outcomes of this study are available from the corresponding author upon reasonable request.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Ledger, M.; Milner, A. Extreme Events in Running Waters. Freshw. Biol. 2015, 60, 2455–2652. [Google Scholar] [CrossRef]
  2. Hattermann, F.; Wortmann, M.; Liersch, S.; Toumi, R.; Sparks, N.; Genillard, C.; Schröter, K.; Steinhausen, M.; Gyalai-Korpos, M.; Máté, K.; et al. Simulation of Flood Hazard and Risk in the Danube Basin with the Future Danube Model. Clim. Serv. 2018, 12, 14–26. [Google Scholar] [CrossRef]
  3. Hoy, A.; Haensel, S.; Skalák, P.; Ustrnul, Z.; Bochnicek, O. The Extreme European Summer of 2015 in a Long-Term Perspective. Int. J. Climatol. 2017, 37, 943–962. [Google Scholar] [CrossRef]
  4. The 2015 Droughts in the Danube River Basin|ICPDR—International Commission for the Protection of the Danube River. Available online: https://www.icpdr.org/resources/2015-droughts-danube-river-basin (accessed on 3 December 2024).
  5. Mikhailov, V.; Morozov, V.; Cheroy, N.; Mikhailova, M.; Zav’yalova, Y. Extreme Flood on the Danube River in 2006. Russ. Meteorol. Hydrol. 2008, 33, 48–54. [Google Scholar] [CrossRef]
  6. Home|ICPDR—International Commission for the Protection of the Danube River. Available online: https://www.icpdr.org/ (accessed on 16 July 2024).
  7. Leščešen, I.; Basarin, B.; Pavic, D.; Mudelsee, M.; Pekarova, P.; Mészáros, M. Are Extreme Floods in the Danube River Getting More Frequent?: A Case Study of the Bratislava Station. J. Water Clim. Chang. 2024, 15, 1300–1312. [Google Scholar] [CrossRef]
  8. Woodward, G.; Bonada, N.; Brown, L.E.; Death, R.G.; Durance, I.; Gray, C.; Hladyz, S.; Ledger, M.E.; Milner, A.M.; Ormerod, S.J.; et al. The Effects of Climatic Fluctuations and Extreme Events on Running Water Ecosystems. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2016, 371, 20150274. [Google Scholar] [CrossRef] [PubMed]
  9. Richardson, J.; Feuchtmayr, H.; Miller, C.; Hunter, P.D.; Maberly, S.C.; Carvalho, L. Response of Cyanobacteria and Phytoplankton Abundance to Warming, Extreme Rainfall Events and Nutrient Enrichment. Glob. Change Biol. 2019, 25, 3365–3380. [Google Scholar] [CrossRef] [PubMed]
  10. Paerl, H.W.; Huisman, J. Climate Change: A Catalyst for Global Expansion of Harmful Cyanobacterial Blooms. Environ. Microbiol. Rep. 2009, 1, 27–37. [Google Scholar] [CrossRef]
  11. Aguilera, A.; Berrendero, E.; Kaštovský, J.; Echenique, R.; Salerno, G. The Polyphasic Analysis of Two Native Raphidiopsis Isolates Supports the Unification of the Genera Raphidiopsis and Cylindrospermopsis (Nostocales, Cyanobacteria). Phycologia 2018, 57, 130–146. [Google Scholar] [CrossRef]
  12. Liberato Pagni, R.; de Falco, P.; Dos Santos, A. Autecology of Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju. Acta Limnol. Bras. 2020, 32, e24. [Google Scholar] [CrossRef]
  13. Antunes, J.; Leao, P.; Vasconcelos, V. Cylindrospermopsis raciborskii: Review of the Distribution, Phylogeography, and Ecophysiology of a Global Invasive Species. Front. Microbiol. 2015, 6, 473. [Google Scholar] [CrossRef] [PubMed]
  14. Padisak, J. Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju, an Expanding, Highly Adaptive Cyanobacterium: Worldwide Distribution and Review of Its Ecology. Arch. Hydrobiol. 1997, 107, 563–593. [Google Scholar]
  15. Maileht, K.; Nõges, T.; Nõges, P.; Ott, I.; Mischke, U.; Carvalho, L.; Dudley, B. Water Colour, Phosphorus and Alkalinity Are the Major Determinants of the Dominant Phytoplankton Species in European Lakes. Hydrobiologia 2013, 704, 115–126. [Google Scholar] [CrossRef]
  16. Roll, Y.V. Fitoplankton Sovetskogo Ychastka Dynaya, Ego Rukavov Zalivov (Phytoplankton of the Soviet section of the Danube, its branches of the bays). Tr. Instituta Gidrobiol. AN USSR 1961, 36, 70–93. (In Russian) [Google Scholar]
  17. Bartalis, É.T. A Duna Szigetközi Szakaszának és Hullámaetéri Vizeinek Biológiai Vízminosége (Biological Water Quality of the Szigetköz Section of River Danube). Kisalföldi Dunaszakasz Ökológiája 1987, 42–77. (In Hungarian) [Google Scholar]
  18. Schmidt, A. Contribution to the Knowledge about the Algae of Water of Southern Hungary I. Bot. Közlemények 1987, 183–195. [Google Scholar]
  19. Schmidt, A. Main Characteristics of the Phytoplankton of the Southern Hungarian Section of the River Danube. Hydrobiologia 1994, 289, 97–108. [Google Scholar] [CrossRef]
  20. Stoyneva, M.P. Steady-State Phytoplankton Assemblages in Shallow Bulgarian Wetlands. Hydrobiologia 2003, 502, 169–176. [Google Scholar] [CrossRef]
  21. Dokulil, M.T.; Mayer, J. Population Dynamics and Photosynthetic Rates of a Cylindrospermopsis—Limnothrix Association in a Highly Eutrophic Urban Lake, Alte Donau, Vienna, Austria. Arch. Für Hydrobiol. Suppl. Algol. Stud. 1996, 83, 179–195. [Google Scholar] [CrossRef]
  22. Dokulil, M.T.; Donabaum, K.; Pall, K. Alternative Stable States in Floodplain Ecosystems. Ecohydrol. Hydrobiol. 2006, 6, 37–42. [Google Scholar] [CrossRef]
  23. Sinha, R.; Pearson, L.; Davis, T.W.; Burford, M.A.; Orr, P.T.; Neilan, B.A. Increased Incidence of Cylindrospermopsis raciborskii in Temperate Zones - Is Climate Change Responsible? Wat. Res. 2012, 46, 1408–1419. [Google Scholar] [CrossRef]
  24. Briand, J.; Leboulanger, C.; Humbert, J.; Bernard, C.; Dufour, P. Cylindrospermopsis raciborskii (Cyanobacteria) Invasion at Mid-Latitudes: Selection, Wide Physiological Tolerance, or Global Warming? J. Phycol. 2004, 40, 231–238. [Google Scholar] [CrossRef]
  25. Mihaljević, M.; Stević, F.; Horvatić, J.; Hackenberger Kutuzović, B. Dual Impact of the Flood Pulses on the Phytoplankton Assemblages in a Danubian Floodplain Lake (Kopački Rit Nature Park, Croatia). Hydrobiologia 2009, 618, 77–88. [Google Scholar] [CrossRef]
  26. Stević, F. Složenost Utjecaja Poplava na Strukturu i Dinamiku Fitoplanktona Poplavnog Područja; Poslijediplomski sveučilišni interdisciplinarni znanstveni studij Zaštita prirode i okoliša: Osijek, Zagreb, 2011. [Google Scholar]
  27. Mihaljević, M.; Getz, D.; Tadić, Z.; Živanović, B.; Gucunski, D.; Topić, J.; Kalinović, I.; Mikuska, J. Kopački Rit-Research Survey and Bibliography; Croatian Academy of Arts and Sciences: Zagreb, Croatia, 1999. [Google Scholar]
  28. Buijse, A.D.; Coops, H.; Staras, M.; Jans, L.; Van Geest, G.J.; Grift, R.; Ibelings, B.; Oosterberg, W.; Roozen, F. Restoration Strategies for River Floodplain Along Large Lowland Rivers in Europe. Freshw. Biol. 2002, 47, 889–907. [Google Scholar] [CrossRef]
  29. Schwarz, U. Landschaftsökologische Charakterisierung Des Kopački Rit Unter Besonderer Berücksichtigung von Flusslandschaftsformen Sowie Deren Genese Und Typologie; University of Wien: Vienna, Austria, 2005. [Google Scholar]
  30. HRN ISO 7150-1:1998 ISO; Water Quality—Determination of Ammonium—Part 1: Manual Spectrometric Method. ISO: Geneva, Switzerland, 1998.
  31. HRN ISO 7890-3:1998 ISO; Water Quality—Determination of Nitrate—Part 3: Spectrometric Method Using Sulfosalicylic Acid. ISO: Geneva, Switzerland, 1998.
  32. HRN EN 26777:1998 ISO; Water Quality—Determination of Nitrite—Molecular Absorption Spectrometric Method. ISO: Geneva, Switzerland, 1998.
  33. HRN ISO 5663:2001 ISO; Water Quality—Determination of Total Nitrogen—Method after Mineralization with Selenium. ISO: Geneva, Switzerland, 2001.
  34. HRN ISO 6878:2008 ISO; Water Quality—Determination of Phosphorus—Ammonium Molybdate Spectrometric Method. ISO: Geneva, Switzerland, 2008.
  35. Hustedt, F. Bacillariophyta (Diatomeae), 2nd ed.; Koeltz: Königstein, Germany, 1976. [Google Scholar]
  36. Hindák, F.; Cyrus, Z.; Marvan, P.; Javornicky, P.; Komarek, J.; Etll, H.; Rosa, K.; Sladečkova, A.; Popovsky, J.; Punčocharova, M.; et al. Slatkovodne Riasy; Hindák, F., Ed.; Slovenske Pedagogicke Nakladelstvo: Bratislava, Slovakia, 1978. [Google Scholar]
  37. Meffert, M.-E.; Oberhäuser, R.; Overbeck, J. Morphology and Taxonomy of Oscillatoria Redekei (Cyanophyta). Br. Phycol. J. 1981, 16, 107–114. [Google Scholar] [CrossRef]
  38. Komárek, J.; Anagnostidis, K. Süßwasserflora von Mitteleuropa, Bd. 19/2: Cyanoprokaryota, Bd. 2/Part 2: Oscillatoriales; Spektrum Akademischer Verlag Heidelberg: Heidelberg, Germany, 2005. [Google Scholar]
  39. Komárek, J. Süßwasserflora von Mitteleuropa, Bd. 19/3: Cyanoprokaryota, 3. Teil/3rd Part: Heterocytous Genera; Springer Spektrum: Berlin/Heidelberg, Germany, 2013. [Google Scholar]
  40. Utermöhl, H. Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Int.Ver. Theor. Angew. Limnol. 1958, 9, 1–38. [Google Scholar] [CrossRef]
  41. Rott, E. Some Results from Phytoplankton Counting Intercalibrations. Schweiz. Z. Hydrol. 1981, 43, 34–62. [Google Scholar] [CrossRef]
  42. Javornický, P.; Komárková, J. The Changes in Several Parameters of Plankton Primary Productivity in Slapy Reservoir 1960–1967, Their Mutual Correlations and Correlations with the Main Ecological Factors. In Hydrobiological studies; Academia: Prague, Czech Republic, 1973; pp. 155–211. [Google Scholar]
  43. Sakshaug, E. Phytoplankton Manual—Monographs on Oceanographic Methodology, 6A. Sournia (Editor) UNESCO, Paris, 1978, 337 Pp. Ocean Manag. 1981, 6, 247–248. [Google Scholar] [CrossRef]
  44. Leps, J.; Smilauer, P. Multivariate Analysis of Ecological Data Using CANOCO; Cambridge University Press: Cambridge, UK, 2003; Volume 3, ISBN 978-0-521-89108-0. [Google Scholar]
  45. Mihaljević, M.; Stević, F. Cyanobacterial Blooms in a Temperate River-Floodplain Ecosystem: The Importance of Hydrological Extremes. Aquat. Ecol. 2011, 45, 335–349. [Google Scholar] [CrossRef]
  46. Scheffer, M. Multiplicity of Stable States in Freshwater Systems. Hydrobiologia 1990, 200, 475–486. [Google Scholar] [CrossRef]
  47. Scheffer, M.; Jeppesen, E. Regime Shifts in Shallow Lakes. Ecosystems 2007, 10, 1–3. [Google Scholar] [CrossRef]
  48. Loverde-Oliveira, S.; Huszar, V.; Mazzeo, N.; Scheffer, M. Hydrology-Driven Regime Shifts in a Shallow Tropical Lake. Ecosystems 2009, 12, 807–819. [Google Scholar] [CrossRef]
  49. Scheffer, M. Ecology of Shallow Lakes; Chapman & Hall: New York, NY, USA, 1998; ISBN 978-0-412-74920-9. [Google Scholar]
  50. van Nes, E.H.; Rip, W.J.; Scheffer, M. A Theory for Cyclic Shifts between Alternative States in Shallow Lakes. Ecosystems 2007, 10, 17–28. [Google Scholar] [CrossRef]
  51. Blindow, I.; Andersson, G.; Hargeby, A.; Johansson, S. Long-Term Pattern of Alternative Stable States in Two Shallow Eutrophic Lakes. Freshw. Biol. 1993, 30, 159–167. [Google Scholar] [CrossRef]
  52. Scheffer, M.; Carpenter, S.; Foley, J.A.; Folke, C.; Walker, B. Catastrophic Shifts in Ecosystems. Nature 2001, 413, 591–596. [Google Scholar] [CrossRef]
  53. Hargeby, A.; Blindow, I.; Hansson, L.-A. Shifts between Clear and Turbid States in a Shallow Lake: Multi-Causal Stress from Climate, Nutrients and Biotic Interactions. Arch. Hydrobiol. 2005, 161, 433–454. [Google Scholar] [CrossRef]
  54. Dembowska, E.A. Impacts of Different Hydrological Conditions on Phytoplankton Communities in Floodplain Lakes of a Regulated River (Lower Vistula, Poland). Hydrobiologia 2022, 849, 2549–2567. [Google Scholar] [CrossRef]
  55. O’Farrell, I.; Izaguirre, I.; Chaparro, G.; Unrein, F.; Sinistro, R.; Pizarro, H.; Rodriguez, P.; de Tezanos Pinto, P.; Lombardo, R.; Tell, G. Water Level as the Main Driver of the Alternation between a Free-Floating Plant and a Phytoplankton Dominated State: A Long-Term Study in a Floodplain Lake. Aquat. Sci. 2011, 73, 275–287. [Google Scholar] [CrossRef]
  56. Van Geest, G.J.; Coops, H.; Scheffer, M.; Nes, E. Long Transients Near the Ghost of a Stable State in Eutrophic Shallow Lakes with Fluctuating Water Levels. Ecosystems 2007, 10, 36–46. [Google Scholar] [CrossRef]
  57. Moustaka-Gouni, M.; Vardaka, E.; Tryfon, E. Phytoplankton Species Succession in a Shallow Mediterranean Lake (L. Kastoria, Greece): Steady-State Dominance of Limnothrix redekei, Microcystis aeruginosa and Cylindrospermopsis raciborskii. Hydrobiologia 2007, 575, 129–140. [Google Scholar] [CrossRef]
  58. Kokocinski, M.; Stefaniak, K.; Mankiewicz-Boczek, J.; Izydorczyk, K.; Soininen, J. The Ecology of the Invasive Cyanobacterium Cylindrospermopsis raciborskii (Nostocales, Cyanophyta) in Two Hypereutrophic Lakes Dominated by Planktothrix agardhii (Oscillatoriales, Cyanophyta). Eur. J. Phycol. 2010, 45, 365–374. [Google Scholar] [CrossRef]
  59. Sommer, U.; Padisak, J.; Reynolds, C.; Juhász-Nagy, P. Hutchison Heritage—The Diversity Disturbance Relationship in Phytoplankton. Hydrobiologia 1993, 249, 1–7. [Google Scholar] [CrossRef]
  60. Bonilla, S.; Aubriot, L.; Soares, M.C.S.; González-Piana, M.; Fabre, A.; Huszar, V.L.M.; Lürling, M.; Antoniades, D.; Padisák, J.; Kruk, C. What Drives the Distribution of the Bloom-Forming Cyanobacteria Planktothrix agardhii and Cylindrospermopsis raciborskii? FEMS Microbiol. Ecol. 2012, 79, 594–607. [Google Scholar] [CrossRef] [PubMed]
  61. Jones, W.W.; Sauter, S. Distribution and Abundance of Cylindrospermopsis raciborskii in Indiana Lakes and Reservoirs. 2005. Available online: https://www.semanticscholar.org/paper/Distribution-and-Abundance-of-Cylindrospermopsis-in-Jones-Sauter/b9dcf7c2a440c34cc0461e0de576c86d4403c83e (accessed on 19 December 2024).
  62. Présing, M.; Herodek, S.; Vörös, L.; Kóbor, I. Nitrogen Fixation, Ammonium and Nitrate Uptake during a Bloom of Cylindrospermopsis raciborskii in Lake Balaton. Arch. Hydrobiol. 1996, 136, 553–562. [Google Scholar] [CrossRef]
  63. Isvánovics, V.; Shafik, H.; Présing, M.; Juhos, S. Growth and Phosphate Uptake Kinetics of the Cyanobacterium, Cylindrospermopsis raciborskii (Cyanophyceae) in Throughflow Cultures. Freshw. Biol. 2008, 43, 257–275. [Google Scholar] [CrossRef]
  64. Ryan, E.F.; Hamilton, D.P.; Barnes, G.E. Recent Occurrence of Cylindrospermopsis raciborskii in Waikato Lakes of New Zealand. N. Z. J. Mar. Freshw. Res. 2003, 37, 829–836. [Google Scholar] [CrossRef]
  65. Wagner, R.S.; Neudeck, M.J.; Heath, A.E.; Barker, K.B.; Brown, K.M.; Buchholz, S.; Ward, C.S.; Bullerjahn, G.S. The Recent Disappearance of a Persistent Planktothrix Bloom: Characterization of a Regime Shift in the Phytoplankton of Sandusky Bay (USA). Harmful Algae 2024, 136, 102656. [Google Scholar] [CrossRef]
  66. Frenken, T.; Brandenburg, K.; Van de Waal, D. Long-Term Nutrient Load Reductions and Increasing Lake TN: TP Stoichiometry Decrease Phytoplankton Biomass and Diversity in a Large Shallow Lake. Limnol. Oceanogr. 2023, 68, 2389–2401. [Google Scholar] [CrossRef]
  67. Chislock, M.F.; Sharp, K.L.; Wilson, A.E. Cylindrospermopsis raciborskii Dominates under Very Low and High Nitrogen-to-Phosphorus Ratios. Water Res. 2014, 49, 207–214. [Google Scholar] [CrossRef] [PubMed]
  68. Burford, M.A.; Willis, A.; Chuang, A.; Man, X.; Orr, P.T. Recent Insights into Physiological Responses to Nutrients by the Cylindrospermopsin Producing Cyanobacterium, Cylindrospermopsis raciborskii. J. Ocean. Limnol. 2018, 36, 1032–1039. [Google Scholar] [CrossRef]
  69. Ferencz, B.; Toporowska, M.; Dawidek, J. Role of Hydrology in Cyanobacterial Blooms in the Floodplain Lakes. Water 2023, 15, 1547. [Google Scholar] [CrossRef]
  70. Reynolds, C.; Huszar, V.; Kruk, C.; Naselli-Flores, L.; Melo, S. Towards a Functional Classification of the Freshwater Phytoplankton. J. Plankton Res. 2002, 24, 417–428. [Google Scholar] [CrossRef]
  71. Figueredo, C.; Giani, A. Phytoplankton Community in the Tropical Lake of Lagoa Santa (Brazil): Conditions Favoring a Persistent Bloom of Cylindrospermopsis raciborskii. Limnologica 2009, 39, 264–272. [Google Scholar] [CrossRef]
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Figure 1. Study area—Lake Sakadaš in the Kopački rit Nature Park—dry and flood conditions in the floodplain.
Figure 1. Study area—Lake Sakadaš in the Kopački rit Nature Park—dry and flood conditions in the floodplain.
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Figure 2. The daily fluctuations of the Danube water level (DWL) at river kilometer 1401.4 in the period 2003–2016. Note: flooding begins when the DWL is above 3 m. Blue circles represent the highest and orange circles represent extremely low DWL.
Figure 2. The daily fluctuations of the Danube water level (DWL) at river kilometer 1401.4 in the period 2003–2016. Note: flooding begins when the DWL is above 3 m. Blue circles represent the highest and orange circles represent extremely low DWL.
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Figure 3. Annual mean values of the physical and chemical properties of the waters of Lake Sakadaš in the period 2003–2016. The dashed line indicates the trend. Each series was standardized (z-scored). Legend: for abbreviation, see legend in Table 1.
Figure 3. Annual mean values of the physical and chemical properties of the waters of Lake Sakadaš in the period 2003–2016. The dashed line indicates the trend. Each series was standardized (z-scored). Legend: for abbreviation, see legend in Table 1.
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Figure 4. Dynamics of total phytoplankton biomass and cyanobacteria biomass in Lake Sakadaš in the period 2003–2016. Red dots show the occurrence of R. raciborskii regardless of the abundance achieved; the shaded area shows the cyanobacteria bloom; the dashed line shows the trend.
Figure 4. Dynamics of total phytoplankton biomass and cyanobacteria biomass in Lake Sakadaš in the period 2003–2016. Red dots show the occurrence of R. raciborskii regardless of the abundance achieved; the shaded area shows the cyanobacteria bloom; the dashed line shows the trend.
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Figure 5. Shifts in states occurred in Lake Sakadaš in the period 2003–2016 based on phytoplankton total biomass and total phosphorus concentrations.
Figure 5. Shifts in states occurred in Lake Sakadaš in the period 2003–2016 based on phytoplankton total biomass and total phosphorus concentrations.
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Figure 6. Relative contribution of cyanobacteria (a), R. raciborskii (b), and P. agardhii (c) to the total phytoplankton biomass in Lake Sakadaš in the period 2003–2016.
Figure 6. Relative contribution of cyanobacteria (a), R. raciborskii (b), and P. agardhii (c) to the total phytoplankton biomass in Lake Sakadaš in the period 2003–2016.
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Figure 7. RDA biplot based on environmental parameters and phytoplankton groups (a) and RDA biplot based on environmental parameters and cyanobacterial species (b) in years with cyanobacterial bloom in Lake Sakadaš. Note: The directions and lengths of the arrows indicate the importance and correlation with the respective axes; to achieve better visibility, only phytoplankton groups, R. raciborskii (RAPRAC) and P. agardhii (PLAAGA), are shown on the plot.
Figure 7. RDA biplot based on environmental parameters and phytoplankton groups (a) and RDA biplot based on environmental parameters and cyanobacterial species (b) in years with cyanobacterial bloom in Lake Sakadaš. Note: The directions and lengths of the arrows indicate the importance and correlation with the respective axes; to achieve better visibility, only phytoplankton groups, R. raciborskii (RAPRAC) and P. agardhii (PLAAGA), are shown on the plot.
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Table 1. Mean, standard deviation, and minimum and maximum values of the environmental parameters in the floodplain lake in the period 2003–2016.
Table 1. Mean, standard deviation, and minimum and maximum values of the environmental parameters in the floodplain lake in the period 2003–2016.
Environmental ParameterSIMean ± SDMinimalMaximal
WDm6.54 ± 1.533.1010.90
SDm1.16 ± 0.550.353.49
WT°C17.3 ± 7.33.330.6
DOmg L−19.69 ± 3.390.9419.66
pH 7.94 ± 0.416.688.98
CondµS cm−1547 ± 169285960
NH4-Nmg L−10.1571 ± 0.27340.00041.3988
NO2-Nmg L−10.0300 ± 0.08970.00130.8516
NO3-Nmg L−10.5069 ± 0.62010.00103.9500
TNmg L−11.7202 ± 1.76550.140011.6642
TPmg L−10.3512 ± 0.53540.00802.8810
TN/TP 11.33 ± 15.090.0683.73
Note(s): Legend: water depth (WD), transparency (SD), water temperature (WT), dissolved oxygen (DO), nitrites (NO2-N), nitrates (NO3-N), total nitrogen (TN), total phosphorus (TP), ammonium (NH4-N), total nitrogen, and total phosphorus ratio (TN/TP).
Table 2. Summary statistics for the first two axes of the RDA performed for the environmental parameters and phytoplankton groups and for the environmental parameters and cyanobacteria species.
Table 2. Summary statistics for the first two axes of the RDA performed for the environmental parameters and phytoplankton groups and for the environmental parameters and cyanobacteria species.
Years2003–2004, 2007–2008, 2011, and 2013
RDA analysis based onenvironmental parameters and phytoplankton groupsenvironmental parameters and cyanobacteria species
RDA axes1212
Eigenvalues0.2430.0590.2920.057
Species–environment correlations0.7130.5890.8740.717
Cumulative percentage variance
- of species data24.330.129.234.9
- of species–environment relation71.188.273.087.3
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Stević, F.; Mihaljević, M.; Špoljarić Maronić, D.; Žuna Pfeiffer, T.; Zahirović, V. The Decreased Incidence of Raphidiopsis raciborskii Bloom in a Temperate Floodplain Lake in the Middle Danube Affected by Extreme Hydrological Events. Water 2025, 17, 309. https://doi.org/10.3390/w17030309

AMA Style

Stević F, Mihaljević M, Špoljarić Maronić D, Žuna Pfeiffer T, Zahirović V. The Decreased Incidence of Raphidiopsis raciborskii Bloom in a Temperate Floodplain Lake in the Middle Danube Affected by Extreme Hydrological Events. Water. 2025; 17(3):309. https://doi.org/10.3390/w17030309

Chicago/Turabian Style

Stević, Filip, Melita Mihaljević, Dubravka Špoljarić Maronić, Tanja Žuna Pfeiffer, and Vanda Zahirović. 2025. "The Decreased Incidence of Raphidiopsis raciborskii Bloom in a Temperate Floodplain Lake in the Middle Danube Affected by Extreme Hydrological Events" Water 17, no. 3: 309. https://doi.org/10.3390/w17030309

APA Style

Stević, F., Mihaljević, M., Špoljarić Maronić, D., Žuna Pfeiffer, T., & Zahirović, V. (2025). The Decreased Incidence of Raphidiopsis raciborskii Bloom in a Temperate Floodplain Lake in the Middle Danube Affected by Extreme Hydrological Events. Water, 17(3), 309. https://doi.org/10.3390/w17030309

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