Changes in Phytoplankton and Water Quality During Sustainable Restoration of an Urban Lake Used for Recreation and Water Supply

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Article Changes in Phytoplankton and Water Quality during Sustainable Restoration of an Urban Lake Used for Recreation and Water Supply

Anna Kozak 1,*, Ryszard Gołdyn 1 ID , Renata Dondajewska 1, Katarzyna Kowalczewska-Madura 1 and Tomasz Holona 2

1 Department of Water Protection, Faculty of Biology, Adam Mickiewicz University in Poznań, Umultowska 89, Poznań61-614, Poland; [email protected] (R.G.); [email protected] (R.D.); [email protected] (K.K.-M.) 2 Szczecin City Office, ZDiTM, Armii Krajowej 1, Szczecin 70-456, Poland; [email protected] * Correspondence: [email protected]; Tel.: +48-061-829-5878

Received: 19 May 2017; Accepted: 11 September 2017; Published: 18 September 2017

Abstract: Groundwater intake near Lake Gł˛ebokie,situated in the city of Szczecin in Northwestern Poland, resulted in a distinct decrease in the lake water level. Water intake from a river and a neighboring urban area led to eutrophication and a strong cyanobacterial water bloom. Both the water intake and recreation were threatened due to the possible inﬂuence of cyanobacterial toxins. The lake was subjected to three sustainable restoration methods: aeration of sediment-water; iron addition to precipitate P, and; biomanipulation. The goal of our study was to determine the changes in the taxonomic composition of phytoplankton and chemical water variables during restoration measures. A comparison of the data obtained during this research with the pre-restoration data showed that, as a result of the treatments orthophosphates decreased, rarely exceeding 0.06 mg P·L−1, and cyanobacterial water blooms disappeared. Cyanobacteria were found in the lake but they were not abundant. Chrysophytes and diatoms were the most abundant in springtime of each year. Green algae, desmids and chrysophytes were particularly abundant in summer, while cryptophytes predominated in autumn. Algae from all these groups do not pose a threat to either recreation or water intake. The deep chlorophyll maximum occurring in summer at a depth of 5 m as a result of restoration conﬁrms the lower trophic status of the lake, alluding to mesotrophic conditions.

Keywords: biomanipulation; deep water aeration; iron addition; phytoplankton composition; water supply

1. Introduction Artificial aeration of degraded lakes is a restoration method aiming at the improvement of oxygen conditions in the near-bottom water layer [1]. Usually this method involves supplying the hypolimnion with compressed air or oxygenated water from the surface, leading to thermal destratification of the water column [2]. The effectiveness of water aeration is well documented due to numerous applications of these methods in eutrophied lake ecosystems [3–8]. However, the negative result of such water mixing is moving the nutrient-rich hypolimnetic waters up to the surface, which stimulates primary production [1]. This disadvantage can be avoided by the use of hypolimnetic aeration as performed by McQueen and Lean [9], who stated that well-designed aerators should not cause significant destratification or warming of hypolimnetic waters. An increase of oxygen concentration at the sediment-water interface and a simultaneous decrease of hydrogen sulfide, methane and ammonia content, together with a decrease of internal phosphorus loading, were the main results. Therefore, hypolimnetic aeration leads to an improvement in water quality and is one of the basic

Water 2017, 9, 713; doi:10.3390/w9090713 www.mdpi.com/journal/water Water 2017, 9, 713 2 of 16 methods of lake restoration [10]. The most economically advantageous is the use of wind-driven pulverizing aerators [11]. The most commonly used chemical treatment for decreasing phosphorus content in the water column is to use a solution of iron or aluminum compounds. Typically, high doses of chemicals (ca. 1 ton ha−1) are applied, which lead to coagulation of the total suspension, and phosphorus removal by adsorption [12,13]. Such strong interference by chemicals in the lake ecosystem is often unacceptable to lake users, so recently a new, sustainable method of iron addition has been used in which only small doses of chemicals are introduced (4–15 kg ha−1) for precipitation of phosphorus. This method does not have a direct influence on the biota, including phytoplankton. However, a reduction in the concentration of phosphates in the water column leads to a limitation of phytoplankton growth [11]. Biomanipulation involves stocking the lake with predatory species or removing zooplanktivorous and benthivorous fish [14,15]. However, as a result of a number of feedback mechanisms, this method fails when used separately [16–18]. Therefore, it is often used as a complementary method, together with physical and chemical methods [11,19]. In each case, it is important to apply the protection methods of the lake to be restored, by sewage diversion and limiting spatial sources of pollution, including, inter alia, the sewage entering the lake from leaky septic tanks [13]. Phytoplankton in restored lakes is dependent on many factors, related both to the type of restoration method used, as well as natural factors specific to a particular waterbody [20,21]. This is especially true for shallow lakes, which are very sensitive to external factors [22,23]. Thus, it is difficult to construct a universal model to describe phytoplankton depending on the method of lake restoration. This is especially so because there is still not enough long-term data on the variability of phytoplankton in such lakes [19,24]. Restoration efforts can have effects on physico-chemical variables of water quality. Such effects lead to changes in phytoplankton production and community composition. Biomanipulation, for example, the removal of benthi- and planktivorous fish or stocking of piscivorous fish, could change the zooplankton community and increase the density of herbivorous zooplankton (mainly Daphnia). Increase of grazing pressure can cause changes in phytoplankton abundance and share of taxonomic groups. The increase of chlorophytes, diatoms and cryptophytes were noted in Danish biomanipulated lakes [25]. As was reported by Schriver and others [26], cryptophytes tend to dominate in systems characterized by high zooplankton grazing. Some phytoplankton groups may be favored by additions of iron complexes used in the precipitation of P. As an example, heterocytous cyanobacterial species are promoted by iron in restored lakes [27]. Iron addition experiments with freshwater green algae showed lower growth rates after additions of Fe compared to control conditions without iron addition [28]. Also, the water aeration system has been noticed as changing phytoplankton dynamics, causing a decrease in cyanobacteria proportion and abundance, and an increase in other phytoplankton groups, for example, chlorophytes, diatoms, cryptophytes and chrysophytes, in small waterbodies [29]. The aim of our study was to analyze the response of phytoplankton composition and abundance in the light of three sustainable restoration methods, applied simultaneously in the shallow, partly stratified Lake Gł˛ebokie.

2. Materials and Methods

2.1. Study Area Lake Gł˛ebokie (53◦28’N, 14◦29’E) is a natural lake localized in Szczecin (NW Poland, Figure1). It has no natural inflows or outflows. Since 1997, the lake has been artificially supplied with water from the River Gunica (from October to April), using a pipe located in its northwest part. This prevents the lowering of the water level due to intake of groundwater for water supply from wells nearby. The lake covers an area of 31 ha. It has an average depth 2.4 m, and its maximum depth reaches 6 m [30]. The lake was polluted by sewage leakage from septic tanks in a residential area located in the vicinity and by intensive recreational use. The increase of nutrient concentrations led to the intensive Water 2017, 9, 713 3 of 16 growth of phytoplankton and the appearance of water cyanobacterial blooms [31]. Both the water intake from the wells situated near the shoreline and recreation were threatened due to the possible influence ofWater cyanobacterial 2017, 9, 713 toxins. Eighty percent of the catchment area of Lake Gł˛ebokieis3 of 17 covered by Water 2017, 9, 713 3 of 17 forest, however,Głębokie and is covered almost by 19% forest, is occupiedhowever, and by almost a residential 19% is occupied area [32 by]. a Itresidential is a popular area [32]. local It is attraction a as a place for leisure and recreation, therefore proper water quality is vital. The average air temperature popularGłębokie local is covered attraction by forest, as a place however, for leisure and almost and recreation, 19% is occupied therefore by proper a residential water areaquality [32]. is Itvital. is a ◦ (April–October)Thepopular average in local subsequent air attraction temperature as years a place(April–October) was for leisure the highest inand subsequent recreation, in 2011 years therefore (14.97 was the properC), highest but water thein 2011quality maximum (14.97 is vital. °C), value was but the maximum value was found in 2010. Precipitation was the highest in 2011 and the lowest in found in 2010.The average Precipitation air temperature was the (April–October) highest in in 2011 subsequent and the years lowest was the in highest 2012 [ 33in ],2011 (Figure (14.97 2°C),). 2012but the [33], maximum (Figure 2). value was found in 2010. Precipitation was the highest in 2011 and the lowest in 2012 [33], (Figure 2).

Figure 1. The location of sampling stations at Lake Głębokie in Szczecin (city is marked in the map of Figure 1. ThePoland). location of sampling stations at Lake Gł˛ebokiein Szczecin (city is marked in the map Figure 1. The location of sampling stations at Lake Głębokie in Szczecin (city is marked in the map of of Poland).Poland).

Figure 2. Monthly values of mean air temperature and sum of precipitation (according to [33]). Figure 2. Monthly values of mean air temperature and sum of precipitation (according to [33]). Figure2.2. Restoration 2. Monthly Treatments values of mean air temperature and sum of precipitation (according to [33]). 2.2. RestorationThe restoration Treatments of the Lake Głębokie began in 2008, when a wind‐driven pulverizing aerator was installed. A Savonius wind turbine is used to drive the paddle wheel, which pulverizes water taken 2.2. RestorationThe Treatments restoration of the Lake Głębokie began in 2008, when a wind‐driven pulverizing aerator was frominstalled. the nearA Savonius bottom wind area. turbine Hydrogen is used sulphide to drive and the other paddle gases wheel, are whichreleased pulverizes in this processwater taken and The restoration of the Lake Gł˛ebokiebegan in 2008, when a wind-driven pulverizing aerator replacedfrom the bynear oxygen bottom from area. the Hydrogen air. The aeratedsulphide water and othersinks gasesto the arebottom released through in this a specialprocess pipe, and was installed.withoutreplaced A any Savoniusby mixingoxygen of windfrom the surfacethe turbine air. water The is aerated [34]. used towater drive sinks the to paddlethe bottom wheel, through which a special pulverizes pipe, water taken fromwithout theThe near anysecond mixing bottom method of the area. of surface restoration Hydrogen water was [34]. iron sulphide addition. and Periodically, other gasessmall doses are of released coagulant in PIX this‐ process 112 (ironThe secondsulphate method III) were of restoration used for the was precipitation iron addition. of phosphorusPeriodically, from small the doses water of coagulantcolumn to PIX the‐ and replacedbottom by sediments oxygen from[35]. These the air.applications The aerated were performed water sinks with the to use the of bottom a mobile through vessel in doses a special pipe, 112 (iron sulphate III) were used for the precipitation of phosphorus from the water column to the without any mixing of the surface water [34]. adjustedbottom sediments to the phosphorus [35]. These contentapplications in lake were water, performed which withwas themonitored use of a duringmobile thevessel restoration in doses

The secondadjusted methodto the phosphorus of restoration content in was lake iron water, addition. which was Periodically, monitored during small the doses restoration of coagulant PIX-112 (iron sulphate III) were used for the precipitation of phosphorus from the water column to the bottom sediments [35]. These applications were performed with the use of a mobile vessel in doses adjusted to the phosphorus content in lake water, which was monitored during the restoration [35,36]. This chemical was used twice in 2008 (300 and 450 kg), four times in 2009 (300, 350 and 250 kg twice), Water 2017, 9, 713 4 of 16 once in 2010 (450 kg) and six times in 2011 (mean 350 kg). Additionally, biomanipulation was used as a third method of restoration to obtain top-down effects of predatory fish on phytoplankton and water transparency. The lake was stocked in 2009 with 50,000 hatching pike (Esox lucius), 9000 summer fry of pikeperch (Sander lucioperca) and 3000 autumn fry of catfish (Silurus glanis). In 2010 it was stocked with 9000 summer pikeperch and 2210 autumn catfish fry, in 2011 31 kg of summer pikeperch fry, 3000 autumn catfish and 71 kg of autumn pike fry were introduced, while in 2012 a total of 5000 catfish summer fry, 60,000 pike summer fry and 800 autumn pike fry were brought into the lake. The leakage of the largest loads of nitrogen and phosphorus from the direct catchment area to Lake Gł˛ebokie were stopped in the meantime due to the construction of a sewer and discharge of effluent to a wastewater treatment plant [36].

2.3. Sampling and Analysis The phytoplankton composition and selected water variables were analyzed in the years 2009–2012. Water for chemical and phycological analyses was usually sampled between February and November with differing frequency: four times in 2009 and 2012; six times in 2011, and; eight times in 2010. Winter samples were impossible to collect due to the thin ice. Two sampling stations were located along the longitudinal axis of the lake (A and B-near aerator) in the deepest part of the lake (Figure1). Water samples were collected in depth profile from 1 m to a depth of 5 m in 1 m intervals. Nutrient concentrations: ammonium, nitrite and nitrate nitrogen, orthophosphates and total phosphorus (TP) were analyzed in preserved samples according to the ISO Standard Methods [37]. Dissolved reactive phosphorus (DRP) and total phosphorus (TP) were analyzed spectrophotometrically using the molybdate method with ascorbic acid as a reducer (TP after the persulfate digestion procedure), ammonium nitrogen—using the Nessler method, nitrate N—the salicylate method, nitrite N—the diazotization method with sulfanilic acid. In the years 2011–2012 the concentration of total nitrogen (TN) was also analyzed, due to organic nitrogen analyzing using the Kjeldahl digestion method. Throughout the research period the amount of total suspended solids (TSS) and chlorophyll-a (Chl-a) concentrations were measured after water filtration, using GF/C Whatman filters. TSS was calculated as the weight difference of the dry mass of the filter before and after filtration, and chlorophyll a concentration was analyzed using the Lorenzen method after acetone extraction [37,38].

2.4. Statistical Analyses Phytoplankton composition and abundance was analyzed in 0.67 mL Sedgwick-Rafter chambers with an Olympus microscope in samples preserved with Lugol’ solution, using 400× magnification. Phytoplankton abundance was expressed as number of specimens (cell/colony/filament/coenobium) per milliliter. Phytoplankton diversity was calculated according to the Shannon-Weaver formula using the software for scientific analysis Past software 3.16 [39]. Data concerning the phytoplankton and nutrient concentration from one station in the year 2011 had already been taken for comparisons with other lakes [24]. Differences between phytoplankton abundance and its biodiversity in the individual studied years were tested by the non-parametric ANOVA Kruskal-Wallis Rank test, while differences between phytoplankton abundance at stations A and B were tested with the Mann-Witney test (Past software) [39]. To ascertain the environmental variables in determining the abundance of phytoplankton the Canonical Correspondence Analysis (CCA) was applied [40]. CCA was used to create models explaining relationships between phytoplankton taxonomical groups vs physico-chemical variables and meteorological (air temperature and precipitation) parameters. The nine taxonomic phytoplankton groups and individual taxa appearing in high density (mean > 30% in the total phytoplankton abundance) were correlated with the physico-chemical variables. The results obtained from two sampling stations were tested. The Monte Carlo permutation was used to assess statistical significance in the regression. Water 2017, 9, 713 5 of 16 Water 2017, 9, 713 5 of 17

3. Results Results DuringDuring the the period period of of research research the the water water temperature temperature and and oxygen oxygen concentration concentration did didnot have not have any visibleany visible long long-term‐term trends trends (Figure (Figure 3).3 Oxygen). Oxygen depletion depletion was was noted noted during during summer, summer, influencing inﬂuencing thethe concentrationsconcentrations of nutrients, for example, ammonium nitrogen. Its content content in in the the water water column column varied varied · −1 fromfrom 0.51 to 6.18 mgmg N-NHN‐NH44∙L−1. .Higher Higher values values were were noted noted in in 2009 2009 at at the the beginning beginning of of restoration, restoration, −1 −1 exceeding 3 mg N-NH ·−L1 at a depth of 5 m at station B and reached almost 2 mg N-NH−1 ·L at exceeding Water3 mg 2017 N, ‐9NH, 713 4∙4L at a depth of 5 m at station B and reached almost 2 mg N‐NH54 ∙ofL 17 at4 station Astation (Figure A (Figure4, Figure4, Figure5A). It 5wasA). Itlower was in lower the following in the following years and years the and mean the vales mean were vales similar were similar at both 3. Results · −1 researchat both research stations. stations. Ammonium Ammonium nitrogen nitrogen content was content usually was lower usually than lower 1 mg than N‐NH 1 mg4∙L N-NH−1 in the4 Ldepthin ofthe 1 depthm. Higher of 1During m.values Higher the were period values occasionally of research were occasionallythe noted water temperaturein 2009 noted and and in 2012. 2009oxygen There and concentration 2012. were There no did statistically not were have no any statistically important importantvisible differences long‐term between trends (Figure stations 3). AOxygen and Bdepletion (p > 0.05, was Kruskal-Wallis noted during summer, test). influencing the differencesconcentrations between stations of nutrients, A and for example,B (p > 0.05, ammonium Kruskal nitrogen.‐Wallis Its test).content in the water column varied from 0.51 to 6.18 mg N‐NH4∙L−1. Higher values were noted in 2009 at the beginning of restoration, exceeding 3 mg N‐NH4∙L−1 at a depth of 5 m at station B and reached almost 2 mg N‐NH4∙L−1 at station A (Figure 4, Figure 5A). It was lower in the following years and the mean vales were similar at both research stations. Ammonium nitrogen content was usually lower than 1 mg N‐NH4∙L−1 in the depth of 1 m. Higher values were occasionally noted in 2009 and 2012. There were no statistically important differences between stations A and B (p > 0.05, Kruskal‐Wallis test).

Figure 3. Changes of water temperature and oxygen concentration in vertical profile (1–5 m) of Figure 3. Changes of water temperature and oxygen concentration in vertical proﬁle (1–5 m) of Głębokie Lake. Gł˛ebokieLake.Figure 3. Changes of water temperature and oxygen concentration in vertical profile (1–5 m) of Głębokie Lake.

Figure 4. Concentration of ammonium, nitrite, nitrate nitrogen and orthophosphates in vertical profile Figure 4. Concentrationat station A. of ammonium, nitrite, nitrate nitrogen and orthophosphates in vertical proﬁle at station A. Figure 4. Concentration of ammonium, nitrite, nitrate nitrogen and orthophosphates in vertical profile at station A.

Water 2017, 9, 713 6 of 16 Water 2017, 9, 713 6 of 17

FigureFigure 5. Mean 5. Mean concentration, concentration, standard standard deviationdeviation and and max max-min‐min values values of ofanalyzed analyzed water water quality quality variables:variables: (A) ( ammoniumA) ammonium nitrogen; nitrogen; ( B)) total total nitrogen; nitrogen; (C) ( orthophosphates;C) orthophosphates; (D) total (D phosphorus;) total phosphorus; (E) (E) chlorophyll-a;chlorophyll‐a; ((F) total suspended suspended solids. solids.

Nitrite nitrogen concentration was below 0.01 mg N‐NO2∙L−1 in all− the1 analyzed years. Slightly Nitrite nitrogen concentration was below 0.01 mg N-NO2·L in all the analyzed years. higher values were occasionally noted at a depth of 5 m (Figure 4). In the case of nitrate nitrogen, Slightly higher values were occasionally noted at a depth of 5 m (Figure4). In the case of noted values were usually below the sensitivity of the applied analytical method. Only in March 2010 nitrate nitrogen, noted values were usually below the sensitivity of the applied analytical method. and February 2011 was an increase of content noted, respectively, up to 1.9 and 1.200 mg N‐NO3∙L−1. Only in MarchTN content 2010 was and visibly February higher 2011 in 2011,was anboth increase in the case of of content maximum noted, values respectively, exceeding 4 up mg to N∙L 1.9−1 and −1 1.200and mg N-NOmean annual3·L . values (ca. 3 mg N∙L−1). In 2012 mean TN content was scarcely 1.740 mg N∙L−1 at − TNstation content A and was 1.700 visibly mg N higher∙L−1 at station in 2011, B (Figure both in 5B). the case of maximum values exceeding 4 mg N·L 1 and meanA annual slight variability values (ca. in 3 the mg mean N·L− annual1). In 2012 concentrations mean TN of content orthophosphates was scarcely was 1.740 noted mg in N the·L −1 at stationanalyzed A and period—from 1.700 mg N·L a− minimum1 at station of B0.023 (Figure mg P5 B).O4∙L−1 in 2009 to a maximum of 0.035 mg PO4∙L−1

A slight variability in the mean annual concentrations of orthophosphates was noted in the −1 −1 analyzed period—from a minimum of 0.023 mg P O4·L in 2009 to a maximum of 0.035 mg PO4·L −1 in 2010 (Figure5C). The highest value in all the analyzed samples, reaching 0.150 mg P O4·L , Water 20172017,, 99,, 713713 7 of 1617 in 2010 (Figure 5C). The highest value in all the analyzed samples, reaching 0.150 mg P O4∙L−1, was wasobserved observed in 2012 in 2012at station at station A, although A, although this appeared this appeared to be to an be individual an individual phenomenon. phenomenon. The −1 Theorthophosphate orthophosphate concentration concentration in most in samples most was samples lower was than lower0.050 mg than P O 0.0504∙L−1. Orthophosphate mg P O4·L . −1 Orthophosphateconcentration in the concentration water column in the varied water from column zero varied to 0.074 from mg zeroP O4∙ toL− 0.0741, and mg from P O0.0104·L to, and0.150 from mg −1 0.010P O4∙L to−1 0.150in the mg water P O4 ·layerL in at the the water depth layer of 5 at m, the reflecting depth of 5changes m, reflecting in oxygen changes and in temperature oxygen and temperatureconditions in conditions vertical profile in vertical throughout profile the throughout year. the year. −1 TP content content was was lower lower in in 2009 2009 in in the the case case of mean of mean annual annual value, value, reaching reaching 0.055 0.055 mg P mg∙L−1. PMean·L . −1 Meanconcentrations concentrations increased increased in the infollowing the following years, years, reaching reaching 0.072 0.072 mg P mg∙L−1 P in·L 2012in 2012(Figure (Figure 5D). 5TheD). −1 Themaximum maximum value value of phosphorus of phosphorus content content was reached was reached in 2012, in exceeding 2012, exceeding 0.200 mg 0.200 P∙L−1 mg at station P·L A.at −1 stationMean annual A. Mean values annual in the values water in column the water ranged column from rangedbelow 0.055 from mg below P∙L− 0.0551 in 2009 mg up P· Lto 0.065in 2009 mg −1 upP∙L− to1 in0.065 successive mg P·L years.in successiveMean annual years. values Mean at a annual depth of values 5 m showed at a depth the same of 5 m variation, showed changing the same −1 variation,from 0.082 changing to 0.100 mg from P∙L 0.082−1. N:P to (mineral 0.100 mg forms) P·L ratio. N:P showed (mineral the forms) downward ratio showed trend from the 30.6 downward in 2009 trendto 11.1 from in 2012. 30.6 in 2009 to 11.1 in 2012. Chlorophyll-aChlorophyll‐a (Chl (Chl-a)‐a) concentrations concentrations were were similar similar at both at both stations stations in 2009, in 2009, varying varying from 4.0 from to −1 −1 4.039.6 to μ 39.6g∙L−1µ. Meang·L .annual Mean annualvalues reached values reached ca 21 μg ca∙L− 211. Inµ g2010·L mean. In 2010 content mean decreased content decreased below 15 μ belowg∙L−1, −1 15althoughµg·L ,the although range of the values range ofincreased values increased (Figure 5E). (Figure The5 highestE). The highestmaximum maximum Chl‐a content Chl-a content was noted was −1 notedin 2011, in exceeding 2011, exceeding 64 μg 64∙L−µ1 gat·L bothat stations. both stations. A visible A visible decrease decrease in the in range the range of values of values was was noted noted in −1 in2012, 2012, while while the the mean mean values values remained remained at atthe the same same level level of of ca ca 16 16 μgµ∙gL·−L1. . −1 TSS content was higher higher in in 2009 2009 (mean (mean values values over over 8 8 mg mg∙L·L−1 at atboth both stations) stations) and and decreased decreased in −1 inthe the following following years years (Figure (Figure 5F).5F). In In 2010–2012 2010–2012 mean mean annual values variedvaried fromfrom 5.35.3 to to 7.0 7.0 mg mg·L∙L−1.. Slightly higher values were usually noted at station A. TSS values in the 1 1-m‐m water layer ranged from −1 1.2 to 11.311.3 mgmg·∙L −1, ,while while in in the the case case of of the the water water layer layer at at a a depth depth of of 5 5 m m TSS TSS content content was was significantly signiﬁcantly −1 higher in 2009, especially at station A, reachingreaching aa maximummaximum ofof 36.536.5 mgmg·∙LL−1. . Phytoplankton was represented by 165 taxa of prokaryotic and eukaryotic algae (Figure 66)) belonging to nine systematicsystematic groups. The The dominant group group was green algae (mainly members of Chlorococcales), whichwhich accountedaccounted forfor 44%44% of the total number of taxa, diatoms 14% and cyanobacteria 13%. Other groups were infrequent and represented byby aa smaller number of taxa (1–9%). The richness of phytoplanktonphytoplankton speciesspecies showed showed an an upward upward trend trend in in the the analyzed analyzed period, period, from from 84 taxa84 taxa in 2009 in 2009 to 133 to in133 2012. in 2012.

180 Conjugatophyceae 160 140 Xantophyceae taxa 120 Dinophyceae of 100 Chlorophyceae 80 Bacillariophyceae

Number 60 Chrysophyceae 40 Cryptophyceae 20 Euglenophyceae 0 2009 2010 2011 2012 2009-2012 Cyanobacteria

Figure 6. Number of identified taxa in Głębokie Lake. Figure 6. Number of identified taxa in Gł˛ebokieLake. The Shannon‐Weaver diversity index varied from 0.25 to 3.00 (Figure 7). There were no significant differencesThe Shannon-Weaver in diversity between diversity station index A and varied B (p from > 0.05, 0.25 Mann to 3.00‐Witney (Figure test).7). There Mean were values no of significant the index differencesincreased in in subsequent diversity between years and station reached A and 1.22 B (p in> 0.05,2009, Mann-Witney 2.00 in 2010, test).2.03 in Mean 2011 values and 2.32 of the in index2012, increasedhowever, the in subsequentdifferences were years significant and reached only 1.22 in 2011 in 2009, and 2012 2.00 in(p < 2010, 0.05, 2.03 Kruskal in 2011‐Wallis and test). 2.32 in 2012, however, the differences were significant only in 2011 and 2012 (p < 0.05, Kruskal-Wallis test).

Water 2017, 9, 713 8 of 16 Water 2017, 9, 713 8 of 17

Water 2017, 9, 713 8 of 17

Figure 7. The diversity index of the phytoplankton in the studied period. Figure 7. The diversity index of the phytoplankton in the studied period. PhytoplanktonFigure abundance 7. The diversity decreased index from of the a phytoplanktonmean annual valuein the studiedof ca 20.4 period. × 10 3 specimens mL−1 − in Phytoplankton2009 to ca. 5.7 × 10 abundance3 spec. mL− decreased1 in 2010. An from increase a mean in annualphytoplankton value of abundance ca 20.4 × 10was3 specimens noted in 2011, mL 1 3 −1 inas 2009 thePhytoplankton to mean ca. 5.7value× 10reached abundance3 spec. 10.3 mL ×decreased− 101 in3 spec. 2010. mLfrom An−1, and increasea mean slightly annual in phytoplanktondecreased value of in ca 2012 20.4 abundance when × 10 specimensthe mean was noted value mL in 3 −1 2011,reachedin 2009 as the to 8.6 meanca. ×5.7 10 value ×3 10 spec. spec. reached mL mL−1 10.3(Figure in 2010.× 10 8). An3 spec. Differences increase mL− in1, phytoplankton andbetween slightly phytoplankton decreased abundance in 2012abundancewas noted when in theof 2011, the mean 3 −1 valueindividualas the reached mean studied value 8.6 × reached 10years3 spec. were 10.3 mL ×significant 10−1 spec.(Figure mL (p8 ).<, 0.05,and Differences slightly Kruskal decreased between‐Wallis test). phytoplanktonin 2012 The when differences the abundance mean between value of reached 8.6 × 103 spec. mL−1 (Figure 8). Differences between phytoplankton abundance of the thestations individual A and studied B were years not statistically were signiﬁcant significant (p < ( 0.05,p > 0.05, Kruskal-Wallis Mann‐Witney test). test). The differences between individual studied years were significant (p < 0.05, Kruskal‐Wallis test). The differences between stations A and B were not statistically signiﬁcant (p > 0.05, Mann-Witney test). stations A and B were not statistically significant (p > 0.05, Mann‐Witney test).

Figure 8. Mean values of phytoplankton abundance, standard deviation and min‐max at both stations.

TheFigure highest 8. Mean abundance values of phytoplankton of phytoplankton abundance, organisms standard wasdeviation found and in min February‐max at both 2011. stations. The most Figure 8. Mean values of phytoplankton abundance, standard deviation and min-max at both stations. abundant were centric diatoms then, mainly small‐sized taxa such as Cyclotella minutula, Cyclotella sp. and StephanodiscusThe highest abundance sp. Centric of diatoms phytoplankton were more organisms abundant was in coldfound months, in February that is, 2011.in March The 2009,most AprilabundantThe 2010 highest were and centric abundanceJanuary diatoms 2012. of There then, phytoplankton mainlywere also small representatives organisms‐sized taxa was such of found asthe Cyclotella pennate in February minutula group, 2011.,but Cyclotella stated The sp. mostin abundantotherand Stephanodiscus periods, were centric for example, sp. diatoms Centric Ulnaria then,diatoms acus mainly ,were Fragilaria small-sized more crotonensis abundant taxa, Asterionellain such cold as months,Cyclotella formosa that minutula, especially is, in March, Cyclotella noted 2009, in sp. andAprilStephanodiscus 2009,2010 Octoberand Januarysp. 2010, Centric 2012. and diatomsJuneThere 2011 were were and also 2012. more representatives abundant in of cold the months,pennate thatgroup, is, but in March stated 2009,in Aprilother 2010Green periods, and algae Januaryfor were example, the 2012. most Ulnaria There numerous acus were, Fragilaria also in 2009 representatives crotonensis (Figure 9),, Asterionella achieving of the pennate aformosa maximum, group,especially value but ofnoted stated 37.4 in × in other10April3 spec. periods, 2009, mL October− for1. The example, most 2010, numerous andUlnaria June acus species2011, Fragilariaand were 2012. Tetraedron crotonensis minimum, Asterionella, Scenedesmus formosa ecornis, especially, S. raciborski noted, in April 2009,Green October algae were 2010, the and most June numerous 2011 and in 2012. 2009 (Figure 9), achieving a maximum value of 37.4 × 103 spec. mL−1. The most numerous species were Tetraedron minimum, Scenedesmus ecornis, S. raciborski,

Water 2017, 9, 713 9 of 16

Green algae were the most numerous in 2009 (Figure9), achieving a maximum value of Water 2017, 9, 713 9 of 17 37.4 × 103 spec. mL−1. The most numerous species were Tetraedron minimum, Scenedesmus ecornis, S. raciborskiarmatus, ,S.S. acuminatus armatus, S. and acuminatus Didimocystisand Didimocystis sp. The abundancesp. The abundanceof green algae of green in the algae years in 2010–2012 the years 2010–2012was significantly was signiﬁcantly lower (p < 0.05, lower Kruskal (p < 0.05,‐Wallis Kruskal-Wallis test). test).

Figure 9. Contribution of taxonomical groups in the phytoplankton abundance, an example from the Figure 9. Contribution of taxonomical groups in the phytoplankton abundance, an example from the depth of 1 m at station A. depth of 1 m at station A. Besides chlorophytes small conjugatophytes also increased their participation in October 2009, especiallyBesides Cosmarium chlorophytes bioculatum small var. conjugatophytes depressum. This also group increased was also their abundant participation in August in October 2010 and 2009, in especiallyJune 2012. Cosmarium bioculatum var. depressum. This group was also abundant in August 2010 and in JuneCyanobacteria 2012. were found only at the beginning and the end of the studied period, achieving 6.3 × Cyanobacteria103 spec. mL−1 in were April found 2009 and only 1.8 at × 10 the3 spec. beginning mL−1 in and September the end 2012, of although the studied at that period, time 3 −1 3 −1 achievingthey were 6.3not× the10 dominantspec. mL groupin April(Figure 2009 8). andThe 1.8most× numerous10 spec. mL speciesin Septemberwere Aphanizomenon 2012, although gracile at, thatLimnothrix time they redekei were and not thePlanktolyngbya dominant group limnetica (Figure. Less8). The abundant most numerous were Cuspidothrix species were issatschenkoiAphanizomenon and gracileMerismopedia, Limnothrix tenuissima redekei, especiallyand Planktolyngbya in deeper limneticawater layers.. Less abundant were Cuspidothrix issatschenkoi and MerismopediaThe participation tenuissima of cryptophytes, especially and in deeper chrysophytes water layers. such as Erkenia subaequiciliata, Cryptomonas marssoniiThe, C. participation reflexa, Rhodomonas of cryptophytes lacustris and Rh. and lens chrysophytes was observed in such cold as months,Erkenia especially subaequiciliata in April, Cryptomonasand October of marssonii 2010–2012., C. reflexa, Rhodomonas lacustris and Rh. lens was observed in cold months, especiallyThe CCA in April diagram and October showed of that 2010–2012. the abundance of phytoplankton taxonomic groups such as chrysophytes,The CCA diatoms diagram and showed cryptophytes that the were abundance negatively of phytoplankton correlated with taxonomic temperature groups (Figure such 10A). as chrysophytes,Chlorophytes, diatomsconjugatophytes and cryptophytes and Dinophytes were negatively were positively correlated correlated with temperature with water temperature, (Figure 10A). Chlorophytes, conjugatophytes and Dinophytes were positively correlated with water temperature, while negatively with pH and NO3‐N. The ordination diagram of CCA explained 29.9% of variance whileof phytoplankton negatively with groups. pH and Environmental NO3-N. The ordination and meteorological diagram of CCA variables explained such 29.9% as oftemperature, variance of phytoplankton groups. Environmental and meteorological variables such as temperature, dissolved dissolved oxygen, NO3‐N, NO2‐N, N:P ratio, pH, precipitation and air temperature had a significant oxygen,effect on NO phytoplankton3-N, NO2-N, distribution N:P ratio, pH, (Monte precipitation Carlo test, and p < air 0.01). temperature The environmental had a significant variable effect such onas p phytoplanktonNH4‐N and PO4 distribution‐P had no significant (Monte Carlo effect test, (p > 0.05)< 0.01). on phytoplankton The environmental group variable abundance such (Table as NH 1).4-N and POA few4-P taxa, had no for significant example, Aphanizomenon effect (p > 0.05) gracile on phytoplankton and Rhodomonas group lacustris abundance, negatively (Table correlated1). with air andA fewwater taxa, temperature for example, andAphanizomenon precipitation (Figure gracile 10B).and RhodomonasThe Cyclotella lacustris species, negativelynegatively correlatedcorrelated Cyclotella with airNH and4‐N and water positively temperature with andNO3 precipitation‐N. Tetraedron (Figure minimum 10B)., present The in all thespecies studied negatively months, Tetraedron minimum correlatedpositively correlated with NH4 -Nwith and PO positively4‐P. The ordination with NO3 -N.diagram of CCA explained, present 51.9% in allof thevariance studied of months,phytoplankton positively taxa. correlated The Monte with Carlo PO4 -P.permutation The ordination test diagramselected environmental of CCA explained variables 51.9% ofthat variance had a ofsignificant phytoplankton effect on taxa. distribution The Monte of Carlodominant permutation taxa of phytoplankton test selected environmental (p < 0.05) such variables as air and that water had temperature, N:P ratio, NH4‐N, NO3‐N and pH and insignificant (p > 0.05) PO4‐P, NO2‐N and dissolved oxygen (Table 1).

Water 2017, 9, 713 10 of 16 a signiﬁcant effect on distribution of dominant taxa of phytoplankton (p < 0.05) such as air and water temperature, N:P ratio, NH4-N, NO3-N and pH and insigniﬁcant (p > 0.05) PO4-P, NO2-N and Waterdissolved 2017, 9 oxygen, 713 (Table1). 10 of 17

(A) (B)

Figure 10. Canonical Correspondence Analysis (CCA) (CCA) diagrams diagrams showing showing the the relationships relationships between: between: (A) environmental variables variables and and abundance abundance of of phytoplankton phytoplankton groups; groups; (B) ( environmentalB) environmental variables variables and andphytoplankton phytoplankton dominating dominating taxa. Abbreviations: taxa. Abbreviations:Aph.gra —AphAphanizomenon.gra—Aphanizomenon gracile; Coel gracile.ret—; CoelastrumCoel.ret— Coelastrumreticulatum ;reticulatumCos.bio—; CosmariumCos.bio—Cosmarium bioculatum bioculatum; Cos.sp—; CosCosmarium.sp—Cosmariumsp.; Cycsp.;.spp— Cyc.spp—CyclotellaCyclotellasp.; sp.;Did .sp.—Did.sp.—DidymocystisDidymocystissp.; Din sp.;.soc Din—.Dinobryonsoc—Dinobryon sociale ;socialeErk.sub; Erk—Erkenia.sub—Erkenia subaequiciliata subaequiciliata; Glo.pel;— GloGloeotila.pel— Gloeotilapelagica; Kerpelagica.sue—; KerKeratococcus.sue—Keratococcus suecicus; Limsuecicus.red—; LimLimnothrix.red—Limnothrix redekei; Plb redekei.lim—; PlanktolyngbyaPlb.lim—Planktolyngbya limnetica; limneticaRho.lac—; RhodomonasRho.lac—Rhodomonas lacustris; Sce lacustris.eco—;Scenedesmus Sce.eco—Scenedesmus ecornis; Tet ecornis.min—; TetraëdronTet.min—Tetraëdron minimum. minimum.

TableTable 1. Results of the Monte Carlo permutation test. Relationships between Environmental Relationships between Relationships between Environmental Relationships between Environmental VariableVariable VariablesVariables and and Abundance Abundance of of VariablesEnvironmental and Phytoplankton Variables and PhytoplanktonPhytoplankton Groups Groups PhytoplanktonDominating Dominating Taxa Taxa pp‐-valuevalue F-ratioF‐ratio p-valuep‐value F-ratioF‐ratio PrecipitationPrecipitation 0.002 0.002 13.4213.42 0.0020.002 3.433.43 Air temperature 0.002 9.09 0.002 3.97 Air temperature 0.002 9.09 0.002 3.97 Water temperature 0.004 5.27 0.030 2.05 WaterDissolved temperature oxygen 0.004 0.004 4.975.27 0.3960.030 1.062.05 N:PDissolved (mineral forms) oxygen ratio 0.0040.002 9.584.97 0.0060.396 3.091.06 N:P (mineralNH4 forms)-N ratio 0.002 0.230 1.349.58 0.0040.006 2.723.09 NO2-N 0.004 4.38 0.196 1.42 NH4‐N 0.230 1.34 0.004 2.72 NO3-N 0.002 16.01 0.002 2.97 NOpH2‐N 0.004 0.004 4.504.38 0.0380.196 2.061.42 NOPO43‐-PN 0.002 0.204 1.3216.01 0.0940.002 1.752.97 pH 0.004 4.50 0.038 2.06 4. DiscussionPO4‐P 0.204 1.32 0.094 1.75 Lake Gł˛ebokie as a shallow lake has partial thermal stratification (epi- and metalimnion) observed 4. Discussion only in summer. This phenomenon affected the changes of oxygen and nutrient concentrations in the depthLake profileGłębokie [32 ].as In a summer shallow months lake has the partial lake suffers thermal from stratification oxygen depletion (epi‐ and in the metalimnion) near bottom observedwater layer, only which in alsosummer. influences This nutrient phenomenon content. Theaffected amount the of changes ammonia of nitrogen oxygen and and phosphorus nutrient concentrationsincrease at the depth in the of depth 5 m, profile indicating [32]. the In sediments summer months as the main the lake source suffers of these from nutrients oxygen fordepletion the water in thecolumn. near bottom Water circulationwater layer, in which the entire also influences vertical profile nutrient during content. autumn The resultsamount in of increasing ammonia nitrogen and phosphorus increase at the depth of 5 m, indicating the sediments as the main source of these nutrients for the water column. Water circulation in the entire vertical profile during autumn results in increasing nitrogen and phosphorus concentrations in the surface water layer. Such seasonal changes point to the role of sediments in nutrient cycling in the lake and the phenomenon of internal loading [41]. In shallow lakes such as Lake Głębokie, two‐way phosphorus exchange on the interphase water‐sediment is much more significant due to the great area of sediments in relation to

Water 2017, 9, 713 11 of 16 and phosphorus concentrations in the surface water layer. Such seasonal changes point to the role of sediments in nutrient cycling in the lake and the phenomenon of internal loading [41]. In shallow lakes such as Lake Gł˛ebokie, two-way phosphorus exchange on the interphase water-sediment is much more significant due to the great area of sediments in relation to water volume [42,43]. The contact of sediment with the water column in the long-term circulation period brings about the influence of various environmental conditions on sediments (water temperature, pH, oxygen content or redox potential), which are highly variable in time [44]. This significant role of sediments rich in organic matter and, consequently, in nutrients, hampers lake restoration. Inadequate inactivation of phosphorus resulting from an autochthonous supply is a frequently observed “bottleneck” in lake restoration [17,45]. Sediment withdrawal should be considered as the most beneficial method but at the same time it is the most costly, therefore other restoration methods were undertaken in Lake Gł˛ebokie. Water aeration using a wind-driven aerator together with the iron addition method aimed to achieve permanent and effective precipitation of phosphorus by increasing the amount of oxygen in deep waters and the water-sediment interphase. This resulted in a marked reduction in phosphorus concentrations in comparison with 2008 before restoration, when the concentration of total phosphorus was in the range of 0.110–0.140 mg·L−1 [46]. The content of phosphorus, both in the total form and in the orthophosphates, remained generally stable in Lake Gł˛ebokiethroughout the restoration period, especially in the case of mean annual values. Periodic higher concentrations of this element were probably related to interim lower efficiency of aeration, due to lack of wind. The effectiveness of aeration might be also limited by the lake catchment characteristics, as it is surrounded by forest, which may decrease the wind speed and therefore the efficiency of aeration. Similar conditions were stated for restored Lake Góreckie in Wielkopolski National Park [47], where the location of the lake in a depression as well as the geomorphology and forest cover in its surroundings cause a reduction in wind speed. A decrease of ammonium nitrogen was noted in Lake Gł˛ebokieduring the restoration period, especially at the lower depths near the bottom. This may indicate that oxygen transported by the aerator is used in the nitrification process, leading to nitrate availability for autotrophic organisms. In some of summer months in 2010 and 2011 an increase of Chl-a content was stated at a depth of 5 m up to 72 µg·L−1, while the amount of the pigment in the subsurface water layer was several times lower. This phenomenon is known as the deep chlorophyll maximum (DCM), which is characteristic of mesotrophic lakes [48]. Phytoplankton grows intensively in the metalimnion or even in the upper part of the hypolimnion due to the higher nutrient content, more so than in the epilimnetic zone. The most numerous species to form DCM in Lake Gł˛ebokiewere Cosmarium bioculatum var. depressum, Tetraedron minimum, Scenedesmus ecornis, Coelastrum reticulatum and Didimocystis sp. Chl-a concentration in depth profile diminished comparing the data from 2009 and 2012, especially in the case of maximum values. A visible decrease was observed in relation to the content of pigment noted before restoration, which then reached 129.3 µg·L−1 [46]. This was a result of the difference in phytoplankton abundance and composition. Intensive water blooms caused by cyanobacteria were noted in Lake Gł˛ebokiein the years before restoration. The dominant species were Limnothrix redekei, Planktolyngbya limnetica and Pseudanabaena limnetica at that time, and in cold months also Planktothrix rubescens [46]. From the beginning of the restoration a set of dominant species has been reconstructed. Species of green algae most often dominated, followed by diatoms, sometimes also chrysophytes. Cyanobacteria appeared only in the spring of 2009 and autumn 2012, however, they were not dominant. Cyanobacteria are organisms that most commonly form water blooms, and due to their high plasticity for adaptation to new conditions, they are sometimes very resistant to removal. There are many examples of lakes and reservoirs in which cyanobacteria dominate the phytoplankton composition in spite of restoration measures [49–53]. Water blooms caused by cyanobacteria are unfavorable especially for lakes used for water supply and for recreational purposes. They can pose a health threat owing to the potential production of toxins, which can lead to serious health problems [54–57]. An efficient method for removing cyanotoxins from water is Water 2017, 9, 713 12 of 16 essential [58]. Aphanizomenon gracile, in particular, noted in Lake Gł˛ebokiein 2012, is known to be a cylindrospermopsin-producing cyanobacterium in Polish lakes [59]. This toxin exhibits cytotoxic influence on a variety of groups of organisms of aquatic and terrestrial ecosystems. An increase in species richness was observed during the period of lake restoration. This is a result of disturbances caused by restoration measures, which according to intermediate disturbance hypothesis [60] enhances species diversity, facilitating the gradual rebuilding of phytoplankton composition. It is in the opposition to unsustainable methods (e.g., high doses of polyaluminium precipitants), which are destructive to the ecosystem. Among the 165 phytoplankton taxa, the dominant one in this study were green algae (73 taxa), followed by diatoms (26 taxa), mostly small-cell species of r-selection strategy with a high growth rate, which are typical for unstable environments [60]. The obtained data showed the qualitative and quantitative differences in the phytoplankton community occurring in subsequent years. They were the result of organisms adapting to environmental changes. These changes were caused by many factors, such as temperature, light availability, quantity of nutrients and presence of other biota [61,62]. Within the period of spring overturn a large participation of diatoms, cryptophytes and chrysophytes occurred. Centric diatoms dominated, but also some pennate diatoms such as Ulnaria acus and Fragilaria crotonensis were observed, which are indicators of eutrophic conditions [61]. A significant increase in the abundance of centric diatoms was noted in February 2011, influencing the mean annual abundance of phytoplankton as well as the content of Chl-a. However, the highest phytoplankton abundance was in 2009, which over the following years began to decrease, thereby indicating a decrease in the trophic status of the lake. A similar increase in diversity with a concomitant decrease in the abundance of phytoplankton in subsequent years of sustainable restoration was observed in Lake Durowskie [11]. The value of the mean Shannon-Weaver diversity index in Lake Gł˛ebokieslightly increased in successive years (2009–2012) and ranged from 1.22 to 2.32. This may reflect an improvement in the environmental condition caused by restoration, as the index is frequently used to assess water quality [63–65]. The presence of some genera, for example, Cosmarium, that was quite abundant, Coenochloris and Staurodesmus that were less abundant in Gł˛ebokieLake, indicate directional changes in the trophic state, as they are reported as tolerant or indicative of oligotrophic conditions in the lakes [66]. Additionally, Monoraphidium griffithii and Oocystis species recorded in studied lake, acc. to Hutchinsson are believed as indicators of oligotrophic conditions [67]. These taxa may indicate an improvement in water quality. Besides the restoration measures, atmospheric conditions may also affect phytoplankton community structure [68]. According to CCA, both precipitation and air temperature had a statistically significant effect on abundance of phytoplankton taxonomic groups and dominating species (Figure 10A). However, high atmospheric precipitation near the examined lake in 2010 and 2011, and also high summer air temperature, did not cause an increase in the abundance of cyanobacteria, which was observed in sustainably restored Swarz˛edzkieLake [69]. The appearance of cyanobacteria in 2012 in Gł˛ebokieLake may have been caused by a low N:P ratio that is favored by this group [70–72]. The latter was confirmed by CCA in the present study (Figure 10A). Despite the yearly stocking of the lake with predatory fish species, top-down control was not very effective. This is evidenced by numerous species of r-selection strategy in the phytoplankton, which can serve as a food source for large cladocerans [73–76], especially in 2009 and 2011. The stocking with hatching of pike in 2009, though intense, was not very effective, as survival from such hatching is very limited [76]. According to Skov et al. [77] the mortality of such stocked small fry is noticeably high (62–89%). In 2011 numerous small phytoplankton specimens appeared in spring, when large crustaceans in the zooplankton had not yet developed. This was the response of phytoplankton to the external nutrient load supplied with water pumped from the River Gunica. Water 2017, 9, 713 13 of 16

5. Conclusions The sustainable restoration of the lake led to the gradual phytoplankton reconstruction. Compared to pre-restoration data, it results in the decreasing of trophic status, which was evidenced by decreasing of nutrient concentrations and presence of deep chlorophyll maximum occurring in summer, and especially by the disappearance of cyanobacterial water blooms. The differences observed in each year of restoration were minor, caused mainly by natural ﬂuctuations, which are the result of annual variation of meteorological conditions.

Acknowledgments: The research was partly financed by the grant No. NN305 372838 from the Ministry of Science and Higher Education (Poland). The open access costs were covered by the statutory founds of the Faculty of Biology. Author Contributions: A.K. made the algological analyses; ran the statistical analyses, elaborated the data and wrote the manuscript; R.D., K.K.-M. made the chemical analyses; T.H. collected the samples and made the field measurements; A.K., R.G. contributed its revisions. Conflicts of Interest: The authors declare no conflict of interest.

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