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All issues No 419 (2018) Knowl. Manag. Aquat. Ecosyst., 419 (2018) 28 Full HTML
Open Access
Issue
Knowl. Manag. Aquat. Ecosyst.
Number 419, 2018
Article Number 28
Number of page(s) 10
DOI https://doi.org/10.1051/kmae/2018017
Published online 13 June 2018

© W. Pęczuła et al., Published by EDP Sciences 2018

Licence Creative CommonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License CC-BY-ND (http://creativecommons.org/licenses/by-nd/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. If you remix, transform, or build upon the material, you may not distribute the modified material.

1 Introduction

The problem of alien, invasive and expansive species is one of the most studied topics in ecology, notably in recent decades, with the appearance of global issues of increasing importance such as climate change, loss of biodiversity, habitat fragmentation or the introduction of genetically modified organisms (Lodge, 1993; Pociecha et al., 2016). Apart from invertebrates, fish and macrophytes, invasions in aquatic habitats include planktonic cyanobacteria and algae, although the invasion of very small organisms is more cryptic than that of larger ones, and is therefore more difficult to detect (Sukenik et al., 2012; Korneva, 2014). As a good example may serve Gonyostomum semen, a planktonic flagellate from Raphidophyceae group, which mass development was firstly described in small dystrophic pond in Massachusetts (United States) already in thirties of the 20th century (Drouet and Cohen, 1935). In last decades, at the turn of the 20th and 21st centuries it became widely studied and known as a bloom-forming species in humic lakes of Sweden, Norway, Finland, Estonia and northern Russia (Cronberg et al., 1988; Hongve et al., 1988; Lepistö et al., 1994; Korneva, 2000; Laugaste and Nõges, 2005), then in Latvia, Lithuania and Poland (Hutorowicz et al., 2006; Druvietis et al., 2010; Karosiene et al., 2014) and sporadically in other European locations (Le Cohu et al., 1989; Negro et al., 2000).

Gonyostomum semen in European lakes was sometimes described as an invasive species (Hongve et al., 1988; Lepistö et al., 1994; Lebret et al., 2015), however, lack of historical records make the determination of its status very difficult. Recent studies aiming to detect resting cysts of the algae in Swedish lakes sediments with the use of PCR method, revealed that the species DNA was found in sediment depths corresponding to an age of 50 years, which suggest that the algae might be present in Swedish lakes many years before lake monitoring was started in this country (Johansson et al., 2016a). Thus, it is rather assumed that the observed expansion of G. semen consists equally of the extension of its range, the colonization of new types of ecosystems and the increase in bloom frequency within sites already colonized (Laugaste and Nõges, 2005).

The species has some features which might impede its detection in lake samples, thus making its invasion/expansion more “cryptic”. This is, among others: cell sensitivity, which effects in its deformation in fixed samples and frequent occurrence only in deeper water layers. Although several studies showed that G. semen tends to be unevenly distributed in the vertical column of water and can change its vertical location (Cowles and Brambel, 1936; Cronberg et al., 1988; Le Cohu et al., 1989, Eloranta and Räike, 1995; Pithart et al., 1997; Negro et al., 2000; Salonen and Rosenberg, 2000; Grabowska and Górniak, 2004, Pęczuła et al., 2013), there is no general agreement about the causes and mechanisms of the phenomenon. Some studies (Cronberg et al., 1988; Salonen and Rosenberg, 2000) pointed the importance of epilimnetic phosphorus depletion as a driver of the algae behavior; Eloranta and Räike (1995) stated that G. semen diel migrations are particularly related to the species light avoidance, while Pęczuła et al. (2013) suggested that the role of zooplankton grazers may be crucial as well. Trophic relations between G. semen and zooplankton species have been studied recently, mainly testing the algae as a food source, sometimes with contradictory results (Williamson et al., 1996; Lebret et al., 2012; Johansson et al., 2013; Björnerås, 2014). There are also few studies on the impact of G. semen blooms on plankton communities, benthic invertebrates or fishes in the ecosystem scale (Trigal et al., 2011; Angeler and Johnson, 2013; Karosiene et al., 2014) or in the laboratory studies (Pęczuła et al., 2017). Nevertheless, the knowledge on biotic and abiotic relations with G. semen in the context of its vertical distribution is still scarce.

Our study aimed to test the hypothesis that vertical distribution of G. semen in small humic lakes may be shaped by zooplankton structure and abundance. In addition, we wanted to check whether high biomass of this flagellate, unevenly distributed in the vertical profile has any influence on the chemical composition as well as on the planktonic bacteria abundance of the water column.

2 Material and methods

We conducted the study in four seepage, dimictic lakes (Suchar I, Suchar II, Wądołek and Widne) in the Suwałki Lakeland region (Wigierski National Park, north-eastern Poland). The lakes are situated close to each other and have small surface area (0.9–2.5 ha) but high relative depth (3.5–12.7%; Tab. 1). All of them are humic (water colour: 43.7–133.1 mg Pt dm−3, DOC: 7.4–16.5 mg dm−3; Tab. 2) with moderate or high total phosphorus content (0.052–0.368 mg dm−3) and circumneutral or slightly acidic pH (Tab. 2). Samples were collected once in mid-July 2015 in the central part of each lake, in the early afternoon during semi-cloudy weather. The water for biological and chemical analyses was sampled using a Ruttner sampler (volume of 2 dm3), from every one meter of the depth, except for zooplankton. For the latter analysis we sampled a total 10 dm3 of water from three layers: epilimnion, metalimnion and hypolimnion (Fig. 1) from one, two or three depths of each, depending on the lake and layer thickness. Then water was poured together in one sample, filtered with plankton net of 55 μm mesh and reduced to the volume of 0.1 dm3.

In biological samples, G. semen fresh biomass was determined using an inverted microscope according to Utermöhl's method (Vollenweider, 1969). As there is no generally accepted formula for Gonyostomum biovolume calculation in the published data, we have chosen an ellipsoid as a geometric model (Hillebrand et al., 1999) and then recalculated the biovolume to fresh biomass, with an assumption that the volumetric mass density of algal cells equals 1 g cm−3 (cell volume of 109 µm3 is considered as equal to 1 mg of biomass). Zooplankton was determined using light microscope (Olympus BX53, Japan). Mean values of the animal length were used to estimate the wet weight of planktonic crustaceans by applying the equations after Błędzki and Rybak (2016), while fresh biomass of rotifers was established following Ejsmont-Karabin (1998) method. Bacterial abundance in biological samples has been determined by standard epifluorescence microscopy (Olympus BX61, Japan) with Porter and Feig (1980) method. Bacterial cells were stained with fluorochrome 4′,6-diamidino-2-phenylindole (DAPI) and collected on a Nuclepore filter (pore size, 0.2 mm) and then counted. Bacterial biomass has been estimated on a base of carbon conversion factors for a single bacterial cell (Lee and Fuhrman, 1987).

Measurements of temperature, electrolytic conductivity (EC), pH and dissolved oxygen concentration were carried out in the field using a HQ40D Multi Meter (Hach-Lange GmbH) as well as water transparency with the use of standard Secchi disc. Other hydrochemical parameters were determined in the laboratory within 24 h of sampling using standard methods described by APHA (2001). Iron ion (Fe3+) concentration was measured spectrophotometrically with the 1,10-phenanthroline method. Total hardness (Ca + Mg), and calcium were measured by EDTA titration method. Magnesium concentration was calculated as the difference between total hardness and Ca concentration. Sulphate concentration was measured with turbidity spectrophotometric method. Two phosphorus (P) forms were determined: soluble reactive P (SRP) in less than 0.45 µm fraction and total P (TP) by peroxodisulphate UV digestion of unfiltered sample. Both SRP and TP fractions were analysed spectrophotometrically with the phosphormolybdenum blue method of Murphy and Riley (1962), as modified by Neal et al. (2000). Nitrogen (N) forms were analysed spectrophotometrically, using reagents by Riedel de Häen, according to the following methods: NH4+ − indofenol blue method, NO2– with sulfanilic acid by the chromotropic acid method and NO3– with N-(1-naphthyl)-ethylenediamine with the zinc catalyst method. The analyses of dissolved organic carbon (DOC), dissolved inorganic carbon (DIC) and total nitrogen (TN) concentrations were carried out using the high temperature catalytic combustion method with a Shimadzu carbon analyser (TOC-L, Japan). Water samples for DOC determinations were filtered through a 0.45 µm filter, acidified with 2 M HCl to ∼pH 2 and rinsed with synthetic air CO2 free to remove traces of inorganic carbon. Chlorophyll-a concentration was determined by the spectrophotometric method with ethanol extraction (ISO, 1992).

Relationship between G. semen biomass and chemical factors was searched with the use of Pearson correlation coefficients. Analysis was performed using Gnumeric spreadsheet ver. 1.10.13 software.

Table 1

Morphometric parameters of studied lakes (after: Górniak 2006).

Table 2

Biological, physical and chemical parameters in vertical water column of studied lakes (epi = epilimnion, meta = metalimnion, hypo = hypolimnion; chl-a = chlorophyll-a, GB = G. semen biomass, zoo = total zooplankton biomass, BA = bacterial abundance, C = water colour).

thumbnail Fig. 1

Gonyostomum semen biomass, bacterial abundance, temperature and oxygen content in the vertical column of four studied lakes.

3 Results

3.1 Gonyostomum semen biomass, chlorophyll-a and bacterial abundance

In three (Suchar I, Suchar II and Wądołek) out of four studied lakes, the mean biomass of G. semen in vertical water column was >1.0 mg dm−3, with the highest value in lake Suchar I (3.9 mg fresh weight dm−3). In lake Widne, mean biomass of the algae was much smaller and equals 0.09 mg FW dm−3. In three mentioned lakes the distribution of studied flagellate was clearly uneven with at least two various patterns which appeared in the vertical water column (Fig. 1). In lake Suchar I, the algae population was very sparse at representing thick epilimnion depth of 1 m (0.08 mg FW dm−3), increasing significantly with the increasing depth, reaching the highest biomass (7.4 mg FW dm−3) at the near-bottom, poorly oxygenated (O2 = 1.5 mg dm−3) and dark (Secchi depth = 1.2 m) layer of 4 m. The opposite pattern was found in lake Suchar II, where the highest algae biomass was noted in the epilimnetic depths of 1 and 2 m (4.7 mg FW dm−3 and 3.1 mg FW dm−3, respectively). In metalimnion (3–5 m) the biomass was several-fold lower (0.5–1.0 mg FW dm−3) as well as in the nearly anoxic (O2 = 0.6–0.8 mg dm−3) hypolimnetic layer (6–8 m) at which the population was very sparse (fresh weight: 0.1–0.3 mg dm−3). Similar (to a certain extent) pattern was observed in the deepest (12 m) lake Wądołek. We found the highest Gonyostomum biomass (1.5–2.2 mg FW dm−3) in the upper three meters, although this layers of water represented both well oxygenated and light-saturated epilimnion (1 m) and weakly oxygenated (O2 at 2 m = 2.7 mg dm−3, below 3 m < 1 mg dm−3) and dark (water transparency = 0.8 m) upper metalimnion (2–3 m). At subsequent depths (4–6 m) the biomass of the flagellate was two-fold lower (0.9–1.2 mg FW dm−3) and below 7 m had the values <0.3 mg FW dm−3 (Fig. 1).

The concentration of chlorophyll-a in the water column of studied lakes reflected the vertical distribution of G. semen only in two lakes (Fig. 1, Tab. 2). It was the most clear in Suchar I, where we noted very low concentration (6.5 µg dm−3) in epilimnetic layer and several hundred higher in meta- and hypolimnion (241.2±165 µg dm−3 and 470.9 µg dm−3, respectively). It was also visible in lake Wądołek, where the highest values of this parameter were noted in metalimnetic layer. In lake Suchar II chlorophyll-a concentrations did not reflect Gonyostomum biomass vertical distribution: we found that chlorophyll-a values increased with the increasing depth (Tab. 2). Although we had no biomass data concerning other than G. semen planktonic algae, microscopic examination (without counting) showed that in Suchar I other species was on negligible biomass level, while in Suchar II and Wądołek there were scarce populations of small cryptomonads and chlorophytes. In lake Widne at all depths, the advantage of representatives of other algae groups over raphidophytes was recorded. The highest biomass reached zygnematophytes (1 m), dinoflagellates (2 m and 3 m) and cryptomonads (4 m).

The bacterial abundance in studied lakes varied between 3.28 × 106 cells ml−1 and 6.82 × 106 cells ml−1 (mean values for the water column). In lake Suchar I bacterial number in the water column was higher with the increasing depth, reaching the highest values at 4 m (11.84 × 106 cells ml−1), which reflected the pattern of G. semen vertical distribution (Fig. 1). Increased bacterial abundance at depths where Gonyostomum formed higher biomass was also noted in two other lakes but only in upper layers (1–4 m in Suchar II and 1–5 m in Wądołek). This pattern could not be seen at deeper layers, for example in lake Suchar II, at 5 m the peak of bacterial abundance (8.37 × 106 cells ml−1) was observed, while flagellate biomass was on relatively low level. Similar case was observed in lake Wądołek at depth of 6 m (Fig. 1). In lake Widne, where Gonyostomum biomass in the water column was very low, bacterial abundance shown similar pattern to lake Suchar I, when increased values occurred with the increasing depth (Fig. 1).

3.2 Zooplankton

The total biomass of zooplankton (crustaceans and rotifers) was clearly the highest in Wądołek lake (1.74 mg FW dm−3, mean for the water column). In three other lakes the values of this parameter was more or less similar and range between 0.51 mg FW dm−3 and 0.60 mg FW dm−3 (means for the water column). Vertical distribution of zooplankton in studied lakes was analysed in the water column in three layers (epilimnion, metalimnion and hypolimnion, Fig. 2). In all lakes the highest zooplankton biomass was found in epilimnion, although in two of them (Suchar I and Wądołek) the metalimnetic zooplankton communities were likewise abundant (epi vs. meta: 0.70 vs. 0.52 mg FW dm−3; 2.61 vs. 2.44 mg FW dm−3, respectively). Interestingly, in lake Suchar I total zooplankton biomass in near-bottom, poorly oxygenated layer of 4 m was on moderate level and amounted 0.30 mg FW dm−3. In other lakes with high Gonyostomum biomass (Suchar II, Wądołek) the hypolimnetic zooplankton was scarce (0.05 mg FW dm−3 and 0.17 mg FW dm−3, respectively).

Clear differences in zooplankton structure among studied lakes was found (Fig. 2). Rotifers dominated the biomass in lake Wądołek (in epilimnion − 85%, in metalimnion − 74% of the total biomass) and Suchar II (55% and 44%, respectively) while in lake Suchar I cladocerans prevailed (49% and 79%, respectively) with small share of rotifers (10–16%). In epilimnion and metalimnion of this lake we found the highest biomass of cladocerans among all studied lakes. What is interesting, in all mentioned lakes one species dominated the rotifer community − Asplanchna priodonta, which comprised 76–99% of the group biomass. In lake Widne (where G. semen formed very small biomass) rotifers had insignificant share in the total zooplankton biomass. Cladocerans in lake Suchar I were dominated by two large-bodied Daphnia species (D. longispina, D. obtusa); the latter one being also a dominant in lake Wądołek. Clearly different cladoceran structure was found in lake Suchar II, where small-bodied Ceriodaphnia quadrangula together with Bosmina longirostris comprised 100% of the cladoceran biomass. Copepods in lakes with high Gonyostomum biomass was dominated by Eudiaptomus graciloides, while in lake Widne the most numerous species was Thermocyclops oithonoides (which did not occur in other lakes).

thumbnail Fig. 2

Biomass of total zooplankton, rotifers, cladocerans and copepods with dominant species in three thermal layers of studied lakes.

3.3 Hydrochemical parameters

All the investigated lakes have represented water quality typical for humic lakes with low pH (less than 7 pH) except the Suchar I in the epilimnion layer. The lowest pH value has been recorded in the Suchar II metalimnion layer. Investigated lakes were characterized by a small content of mineral substances in water, as shown by EC values ranging from 24 µS cm−1 (metalimnion layer in Suchar II) to 64.6 µS cm−1 (epilimnion of Widne Lake). This is confirmed with the results obtained for such parameters as Ca2+, Mg2+, SO43–and Fe2+/3+ significantly affecting EC values (Tab. 2).

An important indicator of dystrophy advance is the DIC to DOC ratio, which in any lake case is less than 1 (Tab. 2). TP concentrations in the individual water layers are on average in the range of up to 50 µg dm−3 to 110 µg dm−3 except for Suchar II, where TP values were much higher (Tab. 2). This pattern was not observed for SRP, whose concentrations in all investigated lakes were close to each other with the maximum values of soluble reactive phosphorus at the bottom water layer (Tab. 2). Total nitrogen in all tested lakes had similar values, and a gradual increase of this element along with depth was observed; however, the concentration of ammonium ions was usually two to three times higher as compared to the concentration of nitrate ions in all sampled depths. The smallest concentrations of NO3-N were recorded in Widne Lake and the highest in Suchar II. The vertical changes of this parameter in Suchar II were characterized with maximum concentration in the metalimnion (Tab. 2). Concentrations of ammonium ions ranged from about 140 µg dm−3 in the hypolimnion of Suchar I to about 350 µg dm−3 in the hypolimnion of Wądołek Lake. In case of NH4-N, the concentration changes of this parameter with the depth were described in two patterns: gradual decrease of concentration (Suchar I and Widne) and gradual increase (Suchar II and Wądołek) (Tab. 2). There was a significant negative correlation between Gonyostomum biomass and NH4-N concentration in all lakes (r2 = 0.65, p < 0.001). However, no significant correlation was found between the flagellate biomass and SRP concentration or NO3-N content (Fig. 3), as well as in the case of the other hydrochemical parameters.

thumbnail Fig. 3

Relationships between Gonyostomum semen fresh biomass (ln) and concentration of nutrient mineral forms (ln) (Pearson correlation coefficients with t-Student tests, two asterisks show statistical significance p < 0.001).

4 Discussion

The results of our study showed that G. semen daytime vertical distribution in the water column clearly varied among three small and stratified lakes with similar morphometric and chemical features. Diverse patterns of G. semen distribution was reflected in various ways in the bacterial, rotifer and crustacean vertical distribution, as well as in the taxonomic structure of zooplankton communities. Moreover, we found, that during a daytime, high G. semen biomass might influence the mineral content of the vertical water column, as can be seen in the case of ammonium ions.

Early studies on G. semen vertical distribution stated that the alga forms its density peak in the surface layer (Salonen and Rosenberg, 2000) or that its distribution is strictly dependent on the weather conditions (Eloranta and Räike, 1995). However, Cronberg et al. (1988) showed that G. semen could be vertically distributed in various ways in the same lake during summer period. This was later confirmed by Pęczuła et al. (2014), who suggested that a pattern of G. semen vertical distribution in the water column is not universal, but rather depends on particular lake conditions, including phosphate content, light climate and zooplankton. It is also well-established from a variety of studies (Cowles and Brambel, 1936; Cronberg et al., 1988; Pithart et al., 1997; Salonen and Rosenberg, 2000) that Gonyostomum migrates in the vertical water column (moves upward in the morning and downward in the afternoon); however, some studies showed that the species could stay in deep, anoxic and dark layers of the water column through most of the diurnal cycle (Pęczuła et al., 2014). Such pattern might occur in the case of lake Suchar I, where the density peak in the near-bottom layer with very sparse population in the epilimnion was found. In other studied lakes, G. semen distribution in the vertical profile was: reversed (decreased biomass with increasing depth in Suchar II), non-linear (the density peak in the metalimnion in Wądołek) or the algae population was very sparse or virtually absent (Widne). All studied lakes had common morphometric and chemical characteristics, which are known to support Gonyostomum high biomass development: small surface area with high relative depth which enables sharp thermal stratification to develop, slightly acidic or circumneutral pH, low level of calcium, moderate/high humic and phosphorus content (Rosén, 1981; Lepistö et al., 1994; Reynolds et al., 2002; Rengefors et al., 2012; Pęczuła, 2013; Pęczuła et al., 2013; Karosiene et al., 2014). The similarity of water quality parameters in studied lakes (both among them and within their water columns) taken together with diverse patterns of G. semen vertical distribution, points to a zooplankton as a potential factor influencing this diversity.

Flagellate algae can migrate at a rate of 1 m h−1 and are able to move through big temperature gradients which enables them to change their position in the vertical water column during a day (Salonen et al., 1984; Jones, 1988). It was suggested that, among others, grazing pressure by zooplankton may influence these changes (Arvola et al., 1992). Parallel to G. semen, migrations maintained by rotifers (Polyartha vulgaris, A. priodonta) and crustaceans (C. quadrangula, E. graciloides) were observed in some studies (Salonen and Rosenberg, 2000; Pęczuła et al., 2014), which suggested that zooplankton has a potential role in shaping the algae vertical distribution in lakes. However, the role of zooplankton control of G. semen by grazing is still discussed. The alga was previously considered inedible due to its large dimensions which are above the preferred size range for many filter-feeding zooplankton as well as the presence of trichocysts, which eject threads of mucilage in a mechanical stress (Cronberg et al., 1988; Havens, 1989). Nevertheless, recent studies had showed that G. semen mucilage is not harmful for Daphnia magna; moreover, disintegrated cells of the alga may serve as nutritive component enhancing daphnids body growth (Pęczuła et al., 2017). Also, many recent experimental studies revealed that Gonyostomum may be directly grazed by zooplankton, including rotifers (A. priodonta), cladocerans (Daphnia magna, Daphnia pulicaria, Holopedium gibberum) or copepods (Diaptomus oregonensis, Eudiaptomus gracilis) (Williamson et al., 1996; Lebret et al., 2012; Johansson et al., 2013; Björnerås, 2014).

In lake Suchar, where G. semen population was virtually absent in epilimnion and increased with the increasing depth, we found large bodied daphnids (D. pulicaria, D. longispina) and copepod E. graciloides as dominating in the water column, with their density peak in epilimnion and metalimnion. Rotifer A. priodonta, which dominates in other two lakes with high Gonyostomum biomass (especially in lake Wądołek) had very small abundances there. It is a well-known pattern, that communities of large-bodied zooplankton, i.e. Daphnia can graze more intensively on phytoplankton than communities dominated by rotifers or small-bodied cladocerans like Bosmina (Agasild and Nõges, 2005). It was also confirmed by a series of laboratory feeding experiments on G. semen. A. priodonta, which is a common zooplankter in Gonyostomum-dominated lakes (Cronberg et al., 1988) showed an average ingestion rate of the algae at 680 cells d−1 (Björnerås, 2014). Large-bodied crustaceans fed on G. semen with higher rate − for Daphnia magna it was 696–1922 cells d−1 (Lebret et al., 2012), for H. gibberum − 2160 cells d−1 and for E. gracilis − 1872 cells d−1 (Johansson et al., 2013). Thus, we can suppose, that in lake Suchar I the specific vertical pattern of G. semen (the most abundant population in anoxic hypolimnion) is strongly shaped by the presence of large-bodied effective feeders in the upper layer. Grazer-avoidance behaviour in G. semen was revealed experimentally by Hansson (2000), which showed that cyst recruitment of this alga is inhibited by the presence of Cladocera and hypothesised the existence of some chemical cues which might be received by Gonyostomum. Similar pattern of G. semen vertical distribution was described by Pęczuła et al. (2014) in small humic lake of 5 m depth, where dense algae population stayed most of the diurnal cycle in near-bottom layers moving at noon upwards only to the bottom of the euphotic zone, dominated by crustaceans. Different patterns of G. semen vertical distribution in lake Suchar II (with algae population as dense as in Suchar I, but concentrated in epilimnion) may be influenced by a smaller grazing pressure. It seems that small-bodied cladocerans (C. quadrangula and B. longirostris) with rotifer A. priodonta were not able to control Gonyostomum population effectively there, thus the algae may develop in high biomass in surface layers. Very poor grazing ability of Ceriodaphnia ssp. when fed on Gonyostomum was showed by Johansson et al. (2013) in experimental laboratory conditions (ingestion rate ca. 30 cells d−1). In lake Wądołek, where total zooplankton biomass was two- to three-fold higher than in the other lakes, G. semen biomass was twice lower than in lakes Suchar I and Suchar II. There was also a population of large-bodied D. obtusa there, which taken together led to the conclusion that G. semen population is effectively controlled in this lake. In lake Widne with very scarce G. semen population we observed the most different zooplankton community, with lack of A. priodonta and copepod T. oithonoides instead of E. graciloides which dominated in the other lakes. Lack of this species might suggest that they prefer only these humic lakes, which suffer with high G. semen biomass; however, we cannot deliver any evidences as our data set is too small.

The grazing pressure of zooplankton on Gonyostomum was probably decreased also by the presence of other algae as well as bacteria in the water column. The concentration of chlorophyll-a in the water column strictly followed the biomass of G. semen only in lake Suchar I. In other lakes, phytoplankton community consisted also with small flagellates − mainly cryptomonads as well as with small coccoid. As it was showed by Gladyshev et al. (1999), Cryptomonas erosa was the most preferable algal species during feeding experiments with C. quadrangula, which appeared to be a selective grazer. Cryptomonas spp. is considered as a very valuable food source also for other zooplankton species (Brett et al., 2009). This fact may decrease zooplankton grazing pressure on Gonyostomum in those of studied lakes in which there was more diverse phytoplankton community (Suchar II and Wądołek). Bacterial abundance in water column of studied lakes appeared to be diversified as well. We noted some interesting pattern in which bacterial abundance reflected (in various degree depending on the lake) the pattern of G. semen vertical distribution (in whole water column in lake Suchar I, 1–4 m in Suchar II and 1–5 m in Wądołek). We can hypothesize that extended bacterial growth may occur on the disintegrated algal biomass, which is a known phenomenon at the end of algal bloom (Van Boekel et al., 1992). Kamiyama et al. (2000) noted the increase of bacteria numbers at the end of other raphidophyte species (Heterosigma akashiwo) bloom. Moreover, Johansson et al. (2016b) found that in lakes with higher G. semen biomass, cladoceran species contained more bacterial fatty acids than those of algal origin which points to suggestion that during Gonyostomum bloom an increased utilization of bacterial resources by zooplankton take place. However, the high abundance of bacteria (increasing with depth) was noted also in lake Widne, where Gonyostomum biomass was very low, thus making the explanation of the observed patterns more complicated.

Although total nitrogen in all studied lakes had similar values, we observed the two- to three-fold higher concentration of ammonium over the nitrate form. Nitrate ions are sensitive to the low-redox conditions which occurs in humic stratified lakes experiencing high biochemical oxygen demand as a result of higher DOC concentration. Under these conditions the nitrate reduction to ammonium and gaseous nitrogen is accelerated through microbial oxidation of organic matter. The principal forms of nitrogen available to algae are nitrate, nitrite and ammonium ions (Reynolds, 2006), however natural populations of phytoplankton usually appear to exhibit preferential uptake of NH4+ over NO3– (Berman et al., 1984). Thus, high concentration of ammonium ions in studied lakes created good conditions for development of phytoplankton, especially G. semen. According to Domingues et al. (2011) preference for ammonium are group-specific and it was observed mainly in green algae and cyanobacteria. Probably G. semen may be one of the species better adapted to ammonium rather than nitrate uptake, especially that such preferences were described in other raphidophytes, like H. akashiwo (Herndon and Cochlan, 2007). Moreover, the negative and significant correlation between G. semen biomass and NH4-N concentration which was observed in our lakes suggests that during the day, the alga intense ammonium uptake may significantly change the mineral content of the water column. Such phenomenon is observed inside blooms of other species, when ambient concentrations of inorganic nutrient forms may be reduced or even depleted due to algal incorporation into its biomass (Heisler et al., 2008). Thus, our results may serve as further example of the influence of G. semen on the lake ecosystem, as it was earlier revealed or suggested in case of plankton, benthic invertebrates or fish (Trigal et al., 2011; Angeler and Johnson, 2013; Karosiene et al., 2014; Pęczuła et al., 2017). Further research including laboratory tests as well as day/night nutrient dynamics within the lake ecosystems dominated by the species may make this topic more clear.

The present study enhanced the understanding of the ecology of the expanding flagellate alga G. semen, particularly in terms of its vertical distribution and its influence on lake ecosystem. Our study confirms some previous findings but also contributes additional evidence suggesting that vertical distribution of this alga in humic lakes may be shaped by zooplankton structure and abundance. We also suppose that high G. semen biomass may modify some parameters of the water column, as it was showed in case of ammonium ions. However, with a small sample size caution must be applied in extrapolation of the results to other humic lake ecosystems; thus our study should be considered as a preliminary one and additional further research on this topic is strongly recommended.

References

  • Agasild H, Nõges T. 2005. Cladoceran and rotifer grazing on bacteria and phytoplankton in two shallow eutrophic lakes: in situ measurement with fluorescent microspheres. J Plankton Res 27: 1155–1174. [CrossRef] [Google Scholar]
  • Angeler DG, Johnson RK. 2013. Algal invasions, blooms and biodiversity in lakes: accounting for habitat-specific responses. Harmful Algae 23: 60–69. [CrossRef] [Google Scholar]
  • APHA. 2001. Standard methods for the examination of water and wastewater. American Public Health Association, 21st ed. Washington, DC, USA: APHA-AWWA-WEF. [Google Scholar]
  • Arvola L, Salonen K, Kankaala P, Lehtovaara A. 1992. Vertical distributions of bacteria and algae in a steeply stratified humic lake under high grazing pressure from Daphnia longispina. Hydrobiologia 229: 253–269. [CrossRef] [Google Scholar]
  • Berman T, Sherr BF, Sherr E, Wynne D, McCarthy JJ. 1984. The characteristics of ammonium and nitrate uptake by phytoplankton in Lake Kinneret. Limnol Oceanogr 29: 287–297. [CrossRef] [Google Scholar]
  • Björnerås C. 2014. Grazing resistance due to trichocysts may boost bloom formation in the HAB species Gonyostomum semen. MSc. Thesis, University of Lund, Lund. [Google Scholar]
  • Błędzki LA, Rybak JI. 2016. Freshwater crustacean zooplankton of Europe. Switzerland: Springer, pp. 1–918. [Google Scholar]
  • Brett MT, Kainz MJ, Taipale SJ, Seshan H. 2009. Phytoplankton, not allochthonous carbon, sustains herbivorous zooplankton production. Proc Natl Acad Sci USA 106: 21197–21201. [CrossRef] [Google Scholar]
  • Cowles RP, Brambel CE. 1936. A study of the environmental conditions in a bog pond with special reference to the diurnal vertical distribution of Gonyostomum semen. Biol Bull 71: 286–298. [CrossRef] [Google Scholar]
  • Cronberg G, Lindmark G, Björk S. 1988. Mass development of the flagellate Gonyostomum semen (Raphidophyta) in Swedish forest lakes − an effect of acidification? Hydrobiologia 161: 217–236. [CrossRef] [Google Scholar]
  • Domingues RB, Barbosa AB, Sommer U., Galvão HM. 2011. Ammonium, nitrate and phytoplankton interactions in a freshwater tidal estuarine zone: potential effects of cultural eutrophication. Aquat Sci 73: 331–343. [CrossRef] [Google Scholar]
  • Drouet F, Cohen A. 1935. The morphology of Gonyostomum semen from Woods Hole, Massachusetts. Biol Bull 68: 422–439. [CrossRef] [Google Scholar]
  • Druvietis I, Spriņģe G, Briede A, Kokorīte I., Parele E. 2010. A comparative assessment of the bog aquatic environment of the Ramsar site of Teiči Neture Reserve and North Vidzeme Biosphere Reserve, Latvia. In: Klavins M., ed. Mires and Peat. Riga: University of Latvia Press, pp. 19–40. [Google Scholar]
  • Ejsmont-Karabin J. 1998. Empirical equations for biomass calculation of planktonic rotifers. Pol Arch Hydrobiol 45: 513–522. [Google Scholar]
  • Eloranta P, Räike A. 1995. Light as a factor affecting the vertical distribution of Gonyostomum semen (Ehr.) Diesing (Raphidophyceae) in lakes. Aqua Fenn 25: 15–22. [Google Scholar]
  • Gladyshev MI, Temerova TA, Dubovskaya OP, Kolmakov VI, Ivanova EA. 1999. Selective grazing on Cryptomonas by Ceriodaphnia quadrangular fed a natural phytoplankton assemblage. Aquat Ecol 33: 347–353. [CrossRef] [Google Scholar]
  • Górniak A. 2006. Jeziora Wigierskiego Parku Narodowego. Aktualna jakość i trofia wód. Wyd. UwB, Białystok, pp. 1–176 [in Polish]. [Google Scholar]
  • Grabowska M, Górniak A. 2004. Letni fitoplankton wybranych sucharów Wigierskiego Parku Narodowego. In Fałtynowicz Z, Rant-Tanajewska M. eds. [Google Scholar]
  • Hansson LA. 2000. Synergistic effects of food web dynamics and induced behavioral responses in aquatic ecosystems. Ecology 81: 842–851. [CrossRef] [Google Scholar]
  • Havens KE. 1989. Seasonal succession in the plankton of a naturally acidic, highly humic lake in Northeastern Ohio, USA. J Plankton Res 11: 1321–1327. [CrossRef] [Google Scholar]
  • Heisler J, Glibert PM, Burkholder JM, et al. 2008. Eutrophication and harmful algal blooms: a scientific consensus. Harmful Algae 8: 3–13. [CrossRef] [PubMed] [Google Scholar]
  • Herndon J, Cochlan WP. 2007. Nitrogen utilization by the raphidophyte Heterosigma akashiwo: growth and uptake kinetics in laboratory cultures. Harmful Algae 6: 260–270. [CrossRef] [Google Scholar]
  • Hillebrand H, Dürselen CD, Kirschtel D, Pollingher U, Zohary T. 1999. Biovolume calculation for pelagic and benthic microalgae. J Phycol 35: 403–424. [CrossRef] [Google Scholar]
  • Hongve D, Løvstad Ø, Bjørndalen K. 1988. Gonyostomum semen − a new nuisance to bathers in Norwegian lakes. Verh Internat Verein Limnol 23: 430–434. [Google Scholar]
  • Hutorowicz A, Szeląg-Wasielewska E, Grabowska M, Owsianny PM, Pęczuła W, Luścińska M. 2006. The occurrence of Gonyostomum semen (Raphidophyceae) in Poland. Fragm Flor Geobot Pol 13: 399–407. [Google Scholar]
  • ISO 10260. 1992. Water quality − Measurement of biochemical parameters − Spectrometric determination of the chlorophyll-a concentration. Warszawa: PKN. [Google Scholar]
  • Johansson KSL, Vrede T, Lebret K, Johnson RK. 2013. Zooplankton feeding on the nuisance flagellate Gonyostomum semen. PLoS ONE 8: e62557. [CrossRef] [PubMed] [Google Scholar]
  • Johansson KS, Lührig K, Klaminder J, Rengefors K. 2016a. Development of a quantitative PCR method to explore the historical occurrence of a nuisance microalga under expansion. Harmful Algae 56: 67–76. [CrossRef] [PubMed] [Google Scholar]
  • Johansson KS, Trigal C, Vrede T, van Rijswijk P, Goedkoop W, Johnson RK. 2016b. Algal blooms increase heterotrophy at the base of boreal lake food webs − evidence from fatty acid biomarkers. Limnol Oceanogr 61: 1563–1573. [CrossRef] [Google Scholar]
  • Jones RI. 1988. Vertical distribution and diel migration of flagellated phytoplankton in a small humic lake. Hydrobiologia 161: 75–87. [CrossRef] [Google Scholar]
  • Kamiyama T, Itakura S, Nagasaki K. 2000. Changes in microbial loop components: effects of a harmful algal bloom formation and its decay. Aquat Microb Ecol 21: 21–30. [CrossRef] [Google Scholar]
  • Karosiene J, Kasperovičiene J, Koreiviene J, Vitonyte I. 2014. Assessment of the vulnerability of Lithuanian lakes to expansion of Gonyostomum semen (Raphidophyceae). Limnologica 45: 7–15. [CrossRef] [Google Scholar]
  • Korneva LG. 2000. Ecological aspects of the mass development of Gonyostomum semen (Ehr.) Dies. (Raphidophyta). Algologia 10: 265–277. [Google Scholar]
  • Korneva LG. 2014. Invasions of alien species of planktonic microalgae into the fresh waters of Holarctic (Review). Russ J Biol Inv 5: 65–81. [CrossRef] [Google Scholar]
  • Laugaste R, Nõges P. 2005. Nuisance alga Gonyostomum semen: implications for its global expansion. In Ramachandra TV, Ahalya N, Murty CR., eds. Aquatic Ecosystems, Conservation, Restoration and Management. Bangalore: Capital Publishing Company, pp. 77–87. [Google Scholar]
  • Le Cohu R, Guitard J, Comoy N, Brabet J. 1989. Gonyostomum semen (Raphidophycées), nuisance potentielle des grands réservoirs français? L'exemple du lac de Pareloup. Arch Hydrobiol 117: 225–236. [Google Scholar]
  • Lebret K, Fernandez MF, Hagman CHC, Rengefors K, Hansson L-A. 2012. Grazing resistance allows bloom formation and may explain invasion success of Gonyostomum semen. Limnol Oceanogr 57: 727–734. [CrossRef] [Google Scholar]
  • Lebret K, Tesson S, Kritzberg E, Carmelo T, Rengefors, K 2015. Phylogeography of the freshwater raphidophyte Gonyostomum semen confirms a recent expansion in northern Europe by a single haplotype. J Phycol 51: 768–781. [CrossRef] [PubMed] [Google Scholar]
  • Lee S, Fuhrman JA. 1987. Relationships between biovolume and biomass of naturally derived marine bacterioplankton. Appl Environ Microbiol 53: 1298–1303. [Google Scholar]
  • Lepistö L, Antikainen S, Kivinen J. 1994. The occurrence of Gonyostomum semen (Ehr.) Diesing in Finnish lakes. Hydrobiologia 273: 1–8. [CrossRef] [Google Scholar]
  • Lodge DM. 1993. Biological invasions: lessons for ecology. Trends Ecol Evol 8: 133–137. [CrossRef] [PubMed] [Google Scholar]
  • Murphy J, Riley JP. 1962. A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27: 31–36. [CrossRef] [Google Scholar]
  • Neal C, Neal M, Wickham H. 2000. Phosphate measurement in natural waters: two examples of analytical problems associated with silica interference using phosphomolybdic acid methodologies. Sci Total Environ 251/252: 513–542. [Google Scholar]
  • Negro AI, De Hoyos C, Vega JC. 2000. Phytoplankton structure and dynamics in Lake Sanabria and Valparaíso reservoir (NW Spain). Hydrobiologia 424: 25–37. [CrossRef] [Google Scholar]
  • Patalas K. 1960. Stosunki termiczne i tlenowe oraz przezroczystość wody w 44 jeziorach okolic Węgorzewa. Rocz Nauk Roln Ser B 77: 105–222 [in Polish]. [Google Scholar]
  • Pęczuła W. 2013. Habitat factors accompanying the mass appearances of nuisance, invasive and alien algal species Gonyostomum semen (Ehr.) Diesing in humic lakes of Eastern Poland. Pol J Ecol 61: 535–543. [Google Scholar]
  • Pęczuła W, Poniewozik M, Szczurowska A. 2013. Gonyostomum semen (Ehr.) Diesing bloom formation in nine lakes of Polesie region (Cental-Eastern Poland). Ann Limnol Int J Lim 49: 301–308. [CrossRef] [Google Scholar]
  • Pęczuła W, Mencfel R, Kowalczyk-Pecka D. 2014. Among-lake variation in vertical distribution of invasive, bloom-forming algal species Gonyostomum semen (Raphidophyceae) in stratified humic lakes of eastern Poland. Int Rev Hydrobiol 99: 317–325. [CrossRef] [Google Scholar]
  • Pęczuła W, Toporowska M, Pawlik-Skowrońska B, Koreiviene J. 2017. An experimental study on the influence of the bloom-forming alga Gonyostomum semen (Raphidophyceae) on cladoceran species Daphnia magna. Knowl Manag Aquat Ecosyst 418: 15. https://doi.org/10.1051/kmae/2017006 [Google Scholar]
  • Pithart D, Pechar L, Mattsson G. 1997. Summer blooms of raphidophyte Gonyostomum semen and its diurnal vertical migration in a floodplain pool. Algol Stud/Arch Hydrobiol Suppl 85: 119–133. [Google Scholar]
  • Pociecha A, Solarz W, Najberek K, Wilk-Woźniak E 2016. Native, alien, cosmopolitan, or cryptogenic? A framework for clarifying the origin status of rotifers. Aquat Biol 24: 141–149. [CrossRef] [Google Scholar]
  • Porter KG, Feig YS. 1980. The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25: 943–948. [Google Scholar]
  • Rengefors K, Weyhenmeyer GA, Bloch I. 2012. Temperature as a driver for the expansion of the microalga Gonyostomum semen in Swedish lakes. Harmful Algae 18: 65–73. [CrossRef] [Google Scholar]
  • Reynolds CS. 2006. The ecology of phytoplankton. Cambridge University Press, Cambridge, pp. 1–535. [Google Scholar]
  • Reynolds CS, Huszar VL, Naselli-Flores L, Melo S. 2002. Towards a functional classification of the freshwater phytoplankton. J Plankton Res 24: 417–428. [Google Scholar]
  • Rosén G. 1981. Phytoplankton indicators and their relations to certain chemical and physical factors. Limnologica 13: 2263–2290. [Google Scholar]
  • Salonen K, Rosenberg M. 2000. Advantages from diel vertical migration can explain the dominance of Gonyostomum semen (Raphidophyceae) in a small, steeply-stratified humic lake. J Plankton Res 22: 1841–1853. [CrossRef] [Google Scholar]
  • Salonen K, Jones RI, Arvola L. 1984. Hypolimnetic phosphorus retrieval by diel vertical migrations of lake phytoplankton. Freshwater Biol 14: 431–438. [CrossRef] [Google Scholar]
  • Sukenik A, Hadas O, Kaplan A, Quesada A. 2012. Invasion of Nostocales (cyanobacteria) to subtropical and temperate freshwater lakes − physiological, regional, and global driving forces. Front Microbiol 3: 86. [Google Scholar]
  • Trigal C, Goedkoop W, Johnson RK. 2011. Changes in phytoplankton, benthic invertebrate and fish assemblages of boreal lakes following invasion by Gonyostomum semen. Freshwater Biol 56: 1937–1948. [CrossRef] [Google Scholar]
  • Van Boekel WHM, Hansen FC, Riegman R, Bak RPM. 1992. Lysis-induced decline of a Phaeocystis spring bloom and coupling with the microbial foodweb. Mar Ecol Prog Ser 81: 269–276. [CrossRef] [Google Scholar]
  • Vollenweider RA. 1969. A manual on methods for measuring primary production in aquatic environments. Blackwell, Oxford: Edinburgh, pp. 1–213. [Google Scholar]
  • Williamson CE, Sanders RW, Moeller RE, Stutzman PL. 1996. Utilization of subsurface food resources for zooplankton reproduction: implications for diel vertical migration theory. Limnol Oceanogr 41: 224–233. [CrossRef] [Google Scholar]

Cite this article as: Pęczuła W, Grabowska M, Zieliński P, Karpowicz M, Danilczyk M. 2018. Vertical distribution of expansive, bloom-forming algae Gonyostomum semen vs. plankton community and water chemistry in four small humic lakes. Knowl. Manag. Aquat. Ecosyst., 419, 28.

All Tables

Table 1

Morphometric parameters of studied lakes (after: Górniak 2006).

In the text
Table 2

Biological, physical and chemical parameters in vertical water column of studied lakes (epi = epilimnion, meta = metalimnion, hypo = hypolimnion; chl-a = chlorophyll-a, GB = G. semen biomass, zoo = total zooplankton biomass, BA = bacterial abundance, C = water colour).

In the text

All Figures

thumbnail Fig. 1

Gonyostomum semen biomass, bacterial abundance, temperature and oxygen content in the vertical column of four studied lakes.
In the text
thumbnail Fig. 2

Biomass of total zooplankton, rotifers, cladocerans and copepods with dominant species in three thermal layers of studied lakes.
In the text
thumbnail Fig. 3

Relationships between Gonyostomum semen fresh biomass (ln) and concentration of nutrient mineral forms (ln) (Pearson correlation coefficients with t-Student tests, two asterisks show statistical significance p < 0.001).
In the text

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