Limnologica 52 (2015) 5966

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Limnologica
journal homepage: www.elsevier.com/locate/limno

Climate driven changes in the submerged macrophyte and

phytoplankton community in a hard water lake
Wojciech Ejankowski , Tomasz Lenard
The John Paul II Catholic University of Lublin, Institute of Environment Protection, Department of Botany and Hydrobiology, Konstantynw 1H,
20-708 Lublin, Poland

a r t i c l e i n f o a b s t r a c t

Article history: We studied the changes in the submerged aquatic vegetation (SAV) and phytoplankton community in a
Received 6 June 2014 hard water lake during different meteorological conditions. We hypothesized that variations in climatic
Received in revised form 6 February 2015 conditions (precipitation and temperature) can inuence the physicochemical parameters of water and,
Accepted 3 March 2015
in turn, affect SAV and phytoplankton development. The investigations were performed in Lake Rogzno
Available online 3 April 2015
(the West Polesie region, Eastern Poland) over 10 years from 2003 to 2013. The physicochemical param-
eters, the structure of macrophytes and the phytoplankton community in the dry (20032006, DP) and
Keywords:
wet periods (20072013, WP) were analyzed. Between the dry and wet periods, the water color and
Charophytes
Bryophytes
the concentration of dissolved organic carbon (DOC) increased considerably, whereas water conduc-
Flagellated algae tivity decreased. Other parameters (concentration of nutrients, water reaction and transparency) were
Cyanobacteria comparable during both periods. When the precipitation and water level were low (DP), charophytes
Water color dominated the SAV and cyanobacteria dominated the phytoplankton community. After the precipita-
Precipitation tion and water level increased (WP), the charophyte population declined and the vascular plants and
Long term monitoring bryophytes dominated. Furthermore, agellated algae belonging to the dinophytes and cryptophytes
were the most numerous in the phytoplankton community. These changes in the SAV and phytoplank-
ton were linked with the variations of physicochemical parameters determined by the total precipitation
and mean air temperature in March.
2015 Elsevier GmbH. All rights reserved.

Introduction
Water level uctuations induced by natural processes or human
activity are considered to be one of the major factors affect-
ing environmental conditions in lakes. The decrease in the water
level, especially in shallow lakes, improves the light climate for
submerged aquatic vegetation and also affects the abundance of
phytoplankton (Blindow, 1992; Bucak et al., 2012; Haldna et al.,
2008). Therefore, the controlled regulation of the water level can
be a useful tool in lake management, e.g., the restoration of dis-
turbed lakes, revegetation or the removal of nuisance macrophytes
(Coops and Hosper, 2002; Rrslett and Johansen, 1996).
Changes in the water level have a variety of effects on the lakes
ecological state. For example, rising of water levels in a humic
lake can increase the hydration of the surrounding wetlands and
forests, thereby intensifying the transport of dissolved organic car-
bon (DOC), including humic substances, from the catchment area
Corresponding author. Tel.: +48 814454590.
E-mail address: wejan@kul.pl (W. Ejankowski).
into the water (Boyer et al., 1997; Klimaszyk and Rzymski, 2011).
The humic substances are a heterogeneous mix of yellow- and
brown colored compounds. Their concentration in natural waters
is a very important factor affecting the functioning of the lake
(Steinberg et al., 2006; Wetzel, 2001). Water runoff enriched with
DOC from the upper soil layers can modify the trophic state of a lake
and its phytoplankton community. An increase in the concentration
of DOC increases water color and reduces water visibility, elec-
trolytic conductivity, calcium and nutrient concentrations (Peczua
and Szczurowska, 2013). The concentration of DOC in the water can
vary considerably over the years, potentially stimulating changes
in the lake ecosystems (Pace and Cole, 2002).
The concentration of humic substances in a lake can be
correlated with the meteorological variability (Hongve et al.,
2004), as precipitation often causes uctuations in the water
levels of lakes (Michalczyk et al., 2011). Therefore, the current
climate changes can indirectly inuence the physicochemical
parameters of the water, including the DOC concentration. Sig-
nicant positive trends in precipitation extremes over Europe
since the middle of the 20th century (van den Besselaar et al.,
2012; Zolina et al., 2009) and increasing trends of annual

http://dx.doi.org/10.1016/j.limno.2015.03.003
0075-9511/ 2015 Elsevier GmbH. All rights reserved.
60 W. Ejankowski, T. Lenard / Limnologica 52 (2015) 5966
precipitation in Europe have been observed (European Environ-
ment Agency: http://www.eea.europa.eu). Conversely, snow cover
duration, which can also affect the hydrologic regime, decreased in
recent decades across Europe (Livingstone et al., 2010; Peng et al.,
2013). In fact, in recent years, the concentration of DOC increased
in the northern temperate lakes of Europe (Hongve et al., 2004;
Vuorenmaa et al., 2006).
The inuence of the water level on the water reservoirs and shal-
low aquatic ecosystems is well documented (Bucak et al., 2012;
Wantzen et al., 2008); however, no data describing the effects of
the uctuating water level on deep, hard water lakes is available.
This type of lake is usually nutrient poor and has relatively high
concentrations of calcium, high water reaction, low phytoplankton
biomass and high water transparency. In hard water lakes, charo-
phytes occupy large portions of the bottom, and their development
is related to light availability. They interfere with phytoplankton by
enhanced sedimentation, reduced resuspension, nutrient immobi-
lization and allelopathic effects (Berger and Schagerl, 2004; Kufel
and Kufel, 2002; van den Berg et al., 1998). Nevertheless, charo-
phytes are very susceptible to lake eutrophication, and they tend
to disappear due to increased water turbidity (Blindow, 1992;
Blindow et al., 2002).
The colonization or disappearance of charophytes in lakes,
which can indicate environmental changes, has been observed
many folds in long time perspective (Kosowski et al., 2006;
Sinkeviciene and Urbaite-Mazevic, 2012). The occurrence of charo-
phytes in lakes is mostly affected by nutrient enrichment; however,
many changes in this macrophyte group are not clearly correlated
with increased lake trophy (Bociag et al., 2011; Kosowski et al.,
2006). Due to the high sensitivity of charophytes to humic sub-
stances in water (Szmeja and Bociag, 2004), we predicted that many
transformations of the charophyte vegetation are governed by vari-
ations of the DOC concentration caused by natural, climatic factors.
In this study, we aimed to nd a link between meteorological
variability and changes in the submerged macrophyte and phy-
toplankton communities in a hard water, charophyte dominated
lake. We hypothesized that variations in climatic conditions can
inuence macrophyte and phytoplankton development indirectly
through the changes in the physicochemical parameters of water.
Materials and methods
This study was carried out in Lake Rogzno (51 22 36 N,
22 58 21 E) in the Western Polesie region of eastern Poland. The
lake is small (0.57 km2 ), deep (mean depth of 7.4 m, max. depth of
25.4 m), dimictic and devoid of inow and outow. The catchment
area (7.75 km2 ) is mostly at and its relative height is 9.2 m. Most of
the catchment is occupied by arable areas (38%), forests (37%) and
meadows (11%). The vegetation surrounding the lake is composed
mainly of swampy alder forest (by the western lakeside) and conif-
erous forests with Scots pine (by the north eastern lakeside). From
the 1950s until the beginning of the 21st century, Lake Rogzno was
characterized as a mesotrophic, hard water lake, with extensive
charophyte vegetation (Ciecierska and Radwan, 2000; Fijakowski,
1959; Sugier, 2008). The average water stage in the lake from 1991
to 2010 was 167.05 m a.s.l. with an amplitude of 0.64 m. The strong
positive trend of increasing water levels in Lake Rogzno, with an
amplitude of approximately 0.6 m, was observed during the last
10 years (20032013) due to high precipitation totals during this
period (Michalczyk et al., 2011). Since 2007, the water level in
Lake Rogzno has risen, and the large area of the lake catchment
(approximately 0.05 km2 ) has become more hydrated.
Data on air temperature and precipitation from a meteoro-
logical station in the town of Wodawa located in the Polesie
region were accessed through an online climatological service
(http://www.tutiempo.net). Because the water state in the lakes
of the Polesie region is correlated with meteorological conditions
(Michalczyk et al., 2011), the effects of the total precipitation dur-
ing particular periods on the lake functioning were analyzed. The
considered periods were as follows: three months before data
sampling (from March to May), one hydrologic year (12 months
from November to October before data sampling), one and a half
hydrologic year (18 months from November to April before data
sampling), two hydrologic years (24 months from November to
October before data sampling) and three hydrologic years (36
months from November to October before data sampling). Addi-
tionally, the mean temperature of March was included in the
analysis as a predictor of ice cover melting.
The studies of the phytoplankton biomass, chlorophyll-a con-
centration and physicochemical parameters of the water in Lake
Rogzno were carried out during the dry (20032006, DP) and
wet periods (20072013, WP). The water samples were col-
lected monthly (JuneAugust) in 2003, 20052007, 2010 and 2013,
excluding water hardness, which was determined in 2003, 2008
and 2013. Water samples for analyses were obtained using the Rut-
tner type water sampler (2.0 L capacity) from the water surface to
the end of the euphotic zone at 1 m intervals and split into two col-
lective samples: the rst from 0.5, 1, 2 and 3 m (upper water layer)
and the second from 5, 6 and 7 m (lower water layer). During the
course of the eld studies, selected physicochemical properties of
the water, i.e., electrolytic conductivity (EC), water reaction (pH)
and transparency by Secchi Disk visibility (SD), were measured.
In the laboratory, spectrophotometric analyses were used to
determine the concentration of chlorophyll-a (Nush, 1980), total
phosphorus (TP), total nitrogen (TN, Hermanowicz et al., 1999) and
dissolved organic carbon (DOC) expressed as values of absorbance
at 254 nm (Brandstetter et al., 1996). Water color was measured
colourimetrically at 440 nm (converted to mg Pt L1 ; Lean, 1998),
and water hardness was determined using the titrimetric method
with disodium EDTA in mval L1 (converted to mg CaCO3 L1 ),
according to Hermanowicz et al. (1999).
The samples for phytoplankton analysis were xed with Lugols
iodine solution and a formalin glycerine mixture. The abundance
of phytoplankton was determined according to Utermhls (1958)
method and algal biovolume was calculated using the formula
described by Hillebrand et al. (1999). The water samples were
transferred to a settling chamber with a 5 ml capacity; after sed-
imentation, the algal abundance was evaluated using an inverted
microscope (Zeiss Axiovert 135). In each chamber, small phyto-
plankton species were counted on the belts at 400 magnication
(at least 200 individuals); larger forms (lamentous or coccal
colonies) were counted on the entire bottom of the chamber at
a magnication of 200. The unit length of 100 m and a surface
of 300 m2 were considered to be one individual for lamentous
and coccal colonies, respectively. Additionally, the samples for tax-
onomic analysis of phytoplankton were collected using a plankton
net (20 m mesh size) and were left without xation in order to
observe live specimens under a light microscope (Nikon Eclipse
80i).
The analysis of submerged aquatic vegetation (SAV) in Lake
Rogzno included the structure and distribution of the macro-
phytes in 2013 (during WP) and in the years 19992006 (including
DP). In July 2013, 30 transects were staked out throughout the
lake, each one situated from the lake margins to the maximum
depth occupied by vegetation. The plant associations were deter-
mined according to the nomenclature of Matuszkiewicz (2001).
The locations of particular plant communities in the lake were
marked with a GPS receiver (Garmin 60Cx) and the plant commu-
nity areas were calculated using the MapSource Trip & Waypoint
Manager program and the bathymetric plan of the lake (Wilgat
et al., 1991). Data on vegetation from 1999 to 2006 were taken
 W. Ejankowski, T. Lenard / Limnologica 52 (2015) 5966 61

167.6 750 Table 1

The results of ANOVA (F-test) of differences between mean values of physicochem-
ical parameters in the dry (20032006, DP) and wet periods (20072013, WP) in
167.35 650 Lake Rogzno.
water level [m a.s.l.]

precipitatiom [mm]
Parameters DP WP df F-Test
167.1 550
EC (S cm1 ) 372.1 251.7 1 52.22b
Water color (mg Pt L1 ) 12.9 27.8 1 6.55a
166.85 450 SD (m) 2.9 2.5 1 0.37
pH 8.2 8.3 1 0.49
TN (mg L1 ) 2.58 2.17 1 3.18
n.d.
166.6 350 TP (mg L1 ) 0.14 0.08 1 2.71
2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013
a
p < 0.05.
b
precipitation max water level min water level n.d. - not determined p < 0.001.

Fig. 1. Minimum and maximum water levels and total yearly precipitation in Lake
Rogzno from 2003 to 2013. 0
1
2

SD [m]
3
4
from published (Ciecierska and Radwan, 2000; Sugier, 2008) and
5
unpublished sources (Dept. of Botany and Hydrobiology, The John 500
Paul II Catholic University of Lublin).

conductivity [ S cm- 1]
Factor analysis (FA) with Pearsons correlation coefcient was 400
used in order to reduce the number of highly correlated variables
measured in the lake. In the FA, data were standardized prior to
300
the analysis, the model was veried by the Bartlett test, and the
selection of signicant factors was performed using Kaisers crite-
200
rion. The factors with eigenvalues () higher than 1 were taken into
75
account until they explained 70% of the total variance.
In other statistical analyses, data were logarithmically trans- 60
water colour [mgPt L-1]

formed prior to the calculations, and a non-parametric test was 45

used if the data did not t the assumptions of parametric tests. 30
The normality of the data was veried with Levenes test, and 15
homogeneity was veried using a KolmogorovSmirnov test. The 0
differences in the physicochemical parameters of water between J J A J J A J J A J J A J J A J J A
the DP and the WP were veried using Fishers test (ANOVA), 2003 2005 2006 2007 2010 2013
and its relationships with climatic data by analysis of covariance
u.w.l. l.w.l. SD
(ANCOVA). The signicance of correlations was assessed using a
nonparametric Spearmans test. All calculations were performed Fig. 2. Secchi depths (SD), conductivity and water color in Lake Rogzno from 2003
according to Sokal and Rohlf (1995) with Statistica 10 software. to 2013. Explanations: u.w.l. upper water layer (0.53 m), l.w.l. lower water layer
(57 m).

Results Physicochemical parameters of water

Climatic and hydrologic conditions
Precipitation totals in the hydrologic years of 20042013
increased to a maximum in 2011 (717.8 mm) after a sharp decrease
in 2003 (369.5 mm). In 20032006 (DP), the average annual pre-
cipitation was 480.2 mm, whereas in 20072013 (WP) it was much
higher (629.9 mm, Fig. 1). The precipitation strongly affected the
water stage in the lake, e.g., during the WP, mean and minimum
values of the water level increased in comparison to the DP. The
highest water level in the lake (167.5 m a.s.l.) was observed in 2011
in the middle of the WP, whereas the lowest water level (166.7 m
a.s.l.) was noted in 2004 after the extremely dry hydrologic year
in 2003 (Fig. 1). During the decreased precipitation in 2012, the
water level slightly decreased; however, it was still much higher in
comparison to the water level during the DP.
The mean air temperature in March during 20032013 varied
considerably (from 2.4 C to 6.3 C) and was usually above zero,
excluding 2005, 2006 and 2013, when it was 0.7 C, 1.7 C and
2.4 C, respectively. During the winter of 2007, with an anoma-
lously warm March (6.3 C), Lake Rogzno was not covered with ice,
whereas in the very cold winters of 2006 and 2013, with an anoma-
lously cold March, the lake was covered with ice from January to
the second half of April.
The values of the physicochemical parameters changed con-
siderably in the studied years. Two parameters, electrolytic
conductivity (EC) and water color, were signicantly different in the
DP (20032006) than in the WP (20072013), as shown in Table 1.
The values of EC decreased during the studies from 484 S cm1
in 2003 to 217 S cm1 in 2010. Water color had an increasing
trend, rising from 0.2 mg Pt L1 in 2003 to 65.4 mg Pt L1 in 2013
(Fig. 2), and it was correlated with the concentration of dissolved
organic carbon (Spearmans test, rS = 0.72, p < 0.05). In some years,
there were large discrepancies in values of EC and water color in the
water column, e.g., in 2013, a lower EC and higher water color were
observed in the upper (0.53 m) compared to the lower (57 m)
water layers (Fig. 2).
Other parameters, including Secchi Disk visibility (SD) and
water reaction (pH), were independent of the periods (Table 1).
Water transparency in the DP was comparable to those in the
WP (Table 1); however, the variation of SD was higher in the DP
(1.44.3 m) than the WP (1.33.5 m). In the WP, water color had a
negative effect on water transparency (Spearmans test, rS = 0.55,
p < 0.05), Fig. 2. During the studies, the pH ranged from 7.5 to 8.9,
and it was not correlated with water color (rS = 0.26, p > 0.05) or
DOC (rS = 0.10, p > 0.05). Therefore, no difference was observed
between the DP and the WP (Table 1). The concentration of total
62 W. Ejankowski, T. Lenard / Limnologica 52 (2015) 5966

Table 2 35 45
The results of ANCOVA (F-test) of relationships between the two main gradients
in the factor analysis (FA 1 and FA 2) and climatic conditions (temperature and 28 36

chlorophyll-a [ g L-1]
precipitation), date of sampling (month) and water layer (depth).

biomass [mg L-1]

21 27
Effects df FA 1 FA 2
14 18
TemperatureMarch 1 18.99b 22.28b
PrecipitationMarchMay 1 6.08a 0.35 7 9
Precipitation12 months 1 7.32a 2.32
Precipitation18 months 1 60.29b 1.22 0 0
J J A J J A J J A J J A J J A J J A
Precipitation2-years 1 0.24 0.58
Precipitation3-years 1 0.009 3.02 2003 2005 2006 2007 2010 2013
Month 2 0.06 0.06 biomass u.w.l. biomass l.w.l.
Depth 1 0.74 0.25 chlorophyll-a u.w.l. chlorophyll-a l.w.l.
a
p < 0.05.
b Fig. 3. Phytoplankton biomass and chlorophyll-a concentrations in Lake Rogzno
p < 0.001.
from 2003 to 2013. Explanations: u.w.l. upper water layer (0.53 m), l.w.l. lower
water layer (57 m).
nitrogen (TN) and phosphorus (TP) varied between the years across
a broad range: 1.343.81 mg L1 and 0.010.34 mg L1 , respec-
tively. Nevertheless, no signicant differences between the DP and
the WP were found in either parameter (Table 1). Throughout the
courses of the studies, Lake Rogzno was categorized as a hard
water lake. The lake water hardness ranged from 98.5 mg CaCO3
L1 in 2003 (DP) to 101.5109.5 mg CaCO3 L1 in 2008 and from
140 to 152 mg CaCO3 L1 in 2013 (WP). In spite of the increasing
water color, the water hardness did not decrease as expected.
The relationships between the physicochemical parameters of
water were tested with Factor Analysis (FA). In the best tting
model veried positively by the Bartlett test (2 = 22.9, p < 0.001),
two main factors (eigenvalues 1 = 1.57 and 1 = 1.21) explained
69.5% of the total variance (Table 2). The factor 1 (FA 1) showed
that the main gradient of the physicochemical parameters in the
lake were positively correlated with electrolytic conductivity (Pear-
sons r = 0.87) and negatively with water color (r = 0.84). Factor 2
(FA 2) had lower signicance and was related to TN and TP (r = 0.7
and r = 0.68, respectively). Hence, FA 2 can be treated as the factor
describing lake trophy. Other physicochemical parameters, such as
SD, pH and DOC, were excluded from the model because of their
low accuracy.
The physicochemical parameters in Lake Rogzno were cor-
related with the meteorological conditions. The most important
gradient (FA 1) was affected by both the mean air temperature in
March and total precipitation (Table 2). The total precipitation in
the period of 18 months preceding data sampling was best tted in
the model. The inuence of precipitation totals in one hydrologic
year or in three months (MarchMay) before data sampling were
also signicant (Table 2); however, they had much less importance
than the total precipitation in an 18-month period. The effect of
longer periods (2 or 3 hydrologic years preceding data sampling)
on FA 1 was not noticeable. Moreover, the values of FA 1 were sim-
ilar throughout the whole summer season (Month) in particular
years and were independent of water layer (Depth), Table 2. Fig. 4. The structure of the phytoplankton community in Lake Rogzno from 2003 to
2013. Explanations: (a) upper water layer (0.53 m), (b) lower water layer (57 m).
The FA 2 describing trophic gradient was inuenced by mean air
temperature in March that indicated the positive effect of late ice
cover breakup on the concentration of nutrients in water (Table 2). 2010 (Fig. 3). It was caused by the presence of different taxo-
None of precipitation periods correlated with the FA 2. Trophic nomical groups and species. In these seasons, a high proportion
gradient (the FA 2), like the FA 1, was independent of depth and of the phytoplankton biomass had lamentous blue-green algae
month. (Fig. 4). In 2005 and 2006, two non-N2 -xing species prevailed,
affecting the chlorophyll-a concentration. In 2005, Planktothrix
Characteristic of the phytoplankton community agardhii (Gom.) Anagn. & Kom. dominated the upper water layer,
whereas in 2006, Planktothrix rubescens (DC. ex Gom.) Anagn. &
The values of phytoplankton biomass varied across a Kom. had its maximum biomass in the lower water layer. In the
broad range in the upper (0.5530.91 mg L1 ) and lower upper water layer in 2010, other lamentous blue-green alga,
(1.3426.77 mg L1 ) water layers (Fig. 3). Similarly, large including N2 -xing Aphanizomenon gracile (Lemm.) Lemm., had
differences in chlorophyll-a concentrations were observed a high share in the phytoplankton biomass (Fig. 4). The mass
(2.0243.55 g L1 and 5.6140.15 g L1 ). The highest verti- appearance of these species impinged on the Secchi Disk visibility
cal disproportion in the phytoplankton biomass and related if they occurred in the upper water layer, e.g., in 2005 and 2010,
chlorophyll-a concentration were observed in 2005, 2006 and when P. agardhii or A. gracile dominated. In contrary, the mass
 W. Ejankowski, T. Lenard / Limnologica 52 (2015) 5966 63

Table 3 Table 4
Spearmans rank correlation test of relationships between the phytoplankton Area of the submerged aquatic vegetation (m2 104 ) in Lake Rogzno from 1999 to
biomass, the chlorophyll-a concentration and the two main gradients in the factor 2013. Explanations: assoc. association; the names of associations originated from
analysis (FA 1 and FA 2) in Lake Rogzno. strictly dominating plant species.

Phytoplankton groups and parameters FA 1 FA 2 Association 1999a 2006b 2013

Cyanophyceae 0.06 0.1 Bryophyte vegetation

Cryptophyceae 0.41a 0.01 Fontinalis antipyretica assoc. 1.52
Euglenophyceae 0.05 0.14
Charophyte vegetation
Dinophyceae 0.39a 0.35a
Nitelletum exilis 0.24
Chrysophyceae 0.16 0.05
Charetum aculeolatae 0.48 0.03
Bacillariophyceae 0.55b 0.29
Chara delicatula assoc. 0.03 0.03
Chlorophyceae/Charophyceae 0.36a 0.47a
Charetum contrariae 0.27
Flagellated species (F) 0.49a 0.24
Lychnothamnus barbatus assoc. 9.37 10.17 0.71
Nonagellated species (NF) 0.32 0.29
Nitellopsidetum obtusae 0.20
F/NF 0.39a 0.04
Chlorophyll-a 0.29 0.12 Vascular plant vegetation
Total biomass 0.44a 0.31 Myriophylletum spicati 3.80 3.76 3.29
a Ranunculetum circinati 0.005
p < 0.05.
b Potamogeton crispus assoc. 0.01
p < 0.01.
Potamogeton praelongus assoc. 0.02
Ceratophylletum demersi 0.16
Najas marina assoc. 0.35
appearance of P. rubescens in the lower water layer (57 m) in 2006
did not affect water transparency values because its population Calculated based on:
a
Ciecierska and Radwan (2000).
occurred deeper than the maximum values of SD (ca. 4.1 m). b
Sugier (2008).
During 20032013, an increasing trend of the phytoplank-
ton biomass was observed, reaching a maximum level in August
2010 (Fig. 3). In the DP (20032006), a high proportion of the Lychnothamnus barbatus association was the most abundant plant
phytoplankton biomass had blue-green algae, e.g., coccal: Aphan- community in the lake and the area covered by other charophyte
othece clathrata West & G.S. West, Snowella lacustris (Chod.) Kom. vegetation was negligible. The vascular plant communities was pre-
& Hindk, and lamentous: P. agardhii, P. rubescens. In the WP dominated by Myriophylletum spicati and constituted 6.66.7% of
(20072013), a noticeable increase in the biomass of agellated the lake area, while no bryophytes were observed (Table 4).
species belonging to Cryptophyceae (e.g., Cryptomonas rostrata In the DP, a maximum depth of macrophyte colonization was
O.V. Troitsk., Cryptomonas marssonii Skuja) and Dinophyceae (e.g., 5 m, where Chara tomentosa L. and Chara globularis Thuillier were
Ceratium hirundinella (O.F. Mll.) Dujard., Peridinium aciculiferum present. L. barbatus (Meyen) Leonh. and Nitellopsis obtusa (Desv.) J.
Lemm.), as well as other phytoplankton groups, Bacillariophyceae Groves reached 4 m, Potamogeton praelongus Wulfen reached 3.9 m
(e.g., Asterionella formosa Hass., Cyclotella sp.), Chlorophyceae and and Myriophyllum spicatum L. reached 2.5 m, whereas the maxi-
Charophyceae (e.g., Coenococcus planctonicus Korsh., Closterium mum depth of Elodea canadensis Michx., Ceratophyllum demersum
acutum var. variabile (Lemm.) Kreiger) occurred, as shown in Fig. 4. L., Batrachium circinatum (Sibth.) Fr., Najas marina L. and Stratiotes
The changes in the phytoplankton composition during the 10- aloides L. varied from 1.4 to 2 m. Potamogeton crispus L. was found
year period from 2003 to 2013 can be explained by variations only to a depth of 0.7 m.
of the physicochemical parameters in water. The relationships In 2013 (WP), in relation to the DP, the area occupied by SAV
between phytoplankton biomass, chlorophyll-a concentration and changed considerably to 0.71 m2 104 (1.2% of the lake area) and
environmental variables were tested using the FA 1 and FA 2 4.52 m2 104 (7.9% of the lake area) for stoneworts and vascular
determined in FA. The FA 1 was correlated with Cryptophyceae, plants, respectively. The area of L. barbatus assoc. decreased con-
Dinophyceae, Bacillariophyceae and the combined group of Chloro- spicuously between the DP and the WP, whereas the area of M.
phyceae and Charophyceae (Table 3). Thus, higher water color and spicati was only slightly lower (Table 4). Charophytes, Nitellop-
lower conductivity led to a greater biomass of these species. Sim- sidetum obtusae and plant communities with Chara spp. retreated
ilarly, total phytoplankton and agellate biomass were negatively from Lake Rogzno, as did other plant associations (Ranunculetum
correlated with the FA 1. Hence, the share of agellate species (ag- circinati assoc., P. crispus assoc.). Additionally, new plant associa-
ellated/nonagellated biomass ratio, Table 3) was higher in seasons tions, i.e., Ceratophylletum demersi, N. marina assoc. and Fontinalis
with high water color and low conductivity (WP). None of the other antipyretica Hedw. assoc. expanded in the lake (Table 4). In 2013,
phytoplankton groups, i.e., Cyanophyceae, Euglenophyceae and the latter, F. antipyretica assoc., occupied a large area of the lake
Chrysophyceae, was inuenced by the FA 1. The correlation of this (2.7%) to a maximum depth of 2.4 m and were present in some
factor with the biomass of nonagellated species and chlorophyll-a sites previously occupied by charophytes in the DP.
concentrations had lower signicance (Table 3). Negative corre- The decreasing depth of macrophyte colonization reected
lations between the FA 2 (gradient of trophy) with Dinophyceae changes in vegetation cover between the DP and the WP. It was
and the group of Chlorophyceae and Charophyceae were found highly reduced for P. praelongus from 3.9 to 2.5 m, L. barbatus from
(Table 3). However, these correlations were strongly dependent on 4 to 2.2 m and N. obtusa from 4 to 1.8 m, and decreased only slightly
data collected in 2013, when in spite of a high nutrient concentra- for M. spicatum from 2.5 to 2.2 m. Two other submerged macro-
tion, a low abundance of phytoplankton was observed (Fig. 3). No phytes observed in the DP (P. crispus and S. aloides) were not found
other effects on the phytoplankton community were revealed in in Lake Rogzno in 2013. On the other hand, two species C. demer-
our study. sum and B. circinatum, slightly expanded from 1.4 in the DP to 2.2 m
in the WP.
Vegetation
Discussion
In the period of 19992006, including the DP (20032006),
the submerged aquatic vegetation (SAV) was predominated by Changes in the submerged macrophyte populations in lakes
stoneworts (Table 4), which constituted 18.218.3% of the lake area. due to transformations between charophytes and other submerged
64 W. Ejankowski, T. Lenard / Limnologica 52 (2015) 5966
macrophytes are often linked with increasing turbidity due to
eutrophication (Kosowski et al., 2006). During this process, charo-
phytes often give way to vascular plants (Blindow, 1992; Blindow
et al., 2002) and nally disappear from highly turbid waters with
low transparency (Sinkeviciene and Urbaite-Mazevic, 2012). Favor-
able light is required for germling growth of charophytes and
thus explains their establishment in clear water (de Winton et al.,
2004). Nevertheless, the disappearance of charophytes in Lake
Rogzno was not clearly correlated with increased trophy, which
did not change between the DP and the WP. In this lake, changes
in other physicochemical parameters of the water environment,
such as decreased conductivity and increased water color cor-
related with DOC, led to the retreat of charophytes and their
replacement by vascular plants and bryophytes. Similar effects
were observed in waters with articially increased concentrations
of humic substances (Szmeja and Bociag, 2004). These parameters
also inuenced the biomass and structure of the phytoplankton
community, especially the domination of nonagellated species in
the DP and agellated species in the WP.
Water color is correlated with concentration of DOC (Pace and
Cole, 2002) that can cause the brownication of water and thus
decrease water visibility. Charophyte establishment is limited by
reduced light conditions (de Winton et al., 2004). Stoneworts can
occur in shallow humic lakes if they grow up to the water sur-
face (Gabka et al., 2007). These results show that the occurrence of
charophytes can be limited mainly by light availability affected by
DOC. Described changes in charophytes and phytoplankton com-
munity in Lake Rogzno were independent of water transparency,
despite increases in water color. This suggests that changes in SAV
and phytoplankton community can be affected by other parameters
related to DOC concentration.
Not only the light intensity but also the light spectrum changes
in water colored with humic substances (fractions of DOC). In highly
humic lakes, light with wavelengths below 600 nm, including pho-
tosynthetically active radiation (PAR), penetrates no more than 1 m
(Wetzel, 2001). It could strongly affect the decrease of charophytes
in Lake Rogzno, especially from lower depths. The other signi-
cant effect of DOC on the SAV in freshwater ecosystems is oxidative
stress (Grigutyte et al., 2009), i.e., humic substances can inuence
the photosynthesis rate in aquatic plants (Bulychev et al., 2001).
Fish activity is an additional potential cause of the poor perfor-
mance of charophytes in lakes via direct disturbance or grazing (de
Winton et al., 2002). Changes in vegetation concern mainly charo-
phytes, and this factor was observed only at lower depths, implying
a negligible effect on the sh in Lake Rogzno.
Enrichment of the lakes water with humic substances can
lead to the chemical precipitation of mineral compounds in the
water, e.g., calcium, magnesium and phosphorus (Pagenkopf and
Whitworth, 1981; Wetzel, 2001). However, in Lake Rogzno, the
increase of water color did not affect phosphorus concentration.
Water hardness, inuenced by calcium concentration, was rela-
tively high during the study period (20032013) in spite of high
concentrations of DOC in the WP (20072013). This is consis-
tent with some observations in other hard water lakes in north
western Poland where the increasing DOC did not affect water
hardness and calcium concentration (Bociag, 2000). Charophytes
require hard water for massive development, e.g., the minimum
calcium concentration for N. obtusa, Chara delicatula and C. glob-
ularis ranges between 15 and 25 mg Ca L1 (Kufel and Kufel,
2002). In Lake Rogzno, the concentration of calcium (3349 mg
Ca L1 ) during the WP (20072013) was also sufcient for the
growth of L. barbatus. This species also occurred in lakes with even
lower values of calcium concentration (approximately 26 mg Ca
L1 , Sinkeviciene and Urbaite-Mazevic, 2012). Hence, the disap-
pearance of charophytes in Lake Rogzno was not linked with the
chemical precipitation of humate-calcium complexes.
Despite the increasing trend in DOC concentrations during the
study period, the water hardness was only slightly higher in the
WP, although it was not statistically conrmed. Hypothetically, it
could be explained by the ability of charophytes to diminishing
the calcium concentrations in the water, which is a constructive
element of their stems (Peechaty et al., 2013). Thus, depletion of
stoneworts during the WP could be the reason that calcium levels
increase in the water.
Enrichment of water with humic substances creates favorable
conditions for the development of acidophilic and tolerant plants.
Stoneworts disappear after increased DOC, and they are often
replaced by bryophyte F. antipyretica, which is tolerant to light de-
ciency and wave action. Thus, it colonizes shallow parts of lake
bottoms if light is limited in the water due to humic substances
(Szmeja and Bociag, 2004). This species is tolerant to environmen-
tal conditions and can inhabit water with varying levels of trophy,
transparency, hardness and reaction (Karttunen and Toivonen,
1995).
An increased concentration of DOC in the water can stimulate
the invasive non-native E. canadensis by reducing the growth of
other competitors, primarily algae and native submerged macro-
phytes (Mormul et al., 2012). The present study did not support
these observations. In Lake Rogzno, reduced competition from
charophytes promoted the development of M. spicatum and F.
antipyretica, whereas E. canadensis was scarce, probably due to the
relatively high nutrient concentration and competition.
Climatic variability can be one of the main factors responsible for
changes in aquatic vegetation. In Lake Rogzno, among submerged
plants, M. spicatum and C. demersum dominated, and charophytes
were not recorded until the 1960s (Fijakowski, 1959). Because L.
barbatus appears in the lake (Karczmarz and Malicki, 1965), the
charophyte strongly increased over approximately 50 years, and at
the beginning of the 21st century, its population was considered to
be very stable in this locality (Sugier, 2008).
Charophytes can hinder the development of the phytoplankton
in water, i.e., because of competition for nutrients and allelopathic
effect (van Donk and van de Bund, 2002). The disappearance of
charophytes in Lake Rogzno could affect the development of the
phytoplankton community.
Values of the phytoplankton biomass in Lake Rogzno were usu-
ally lower in the DP (20032006) than in the WP (20072013),
which corresponded to high differences in the phytoplankton
community structure. In the DP, the phytoplankton community
was dominated by blue-green algae characteristic of stratied
mesotrophic (e.g., P. rubescens) or eutrophic lakes, e.g., P. agardhii, A.
clathrata (Reynolds, 2006), while in the WP agellated species from
the genus Ceratium or Cryptomonas were the most abundant. Flagel-
lated species are able to ingest organic particles (Lepist and Saura,
1998), their growth can be independent of nutrient concentration,
and they are often important components of the phytoplankton
community in colored lakes (Longhi and Beisner, 2009; Peczua
and Szczurowska, 2013). Furthermore, they can move through the
water column looking for the optimum conditions for their devel-
opment, avoiding high light intensity, which could account for
the photoinhibition of their photosynthetic apparatus (Whittington
et al., 2000). The growth of some agellated species, e.g., dinoagel-
late Ceratium spp., is better stimulated by humic substances than
the growth of diatoms (Granli et al., 1989). Hence, they can be
responsible for high phytoplankton productivity in colored lakes,
as observed in Lake Rogzno during the WP.
In Lake Rogzno, the changes in the SAV and the phy-
toplankton community described above were linked to the
increasing trends of precipitation totals from 2007 to the present
(http://www.tutiempo.net). In the previous period (from 1951 to
2006), decreasing trends of precipitation were noticeable, espe-
cially in the cold season from October to February (Kaszewski et al.,
 W. Ejankowski, T. Lenard / Limnologica 52 (2015) 5966
2009), which had a profound effect on the water supply in the lake.
Specically, water level in Lake Rogzno followed the precipitation
sum with a delay of approximately one hydrologic year (Michalczyk
et al., 2011).
The physicochemical parameters in lakes are highly inuenced
by land use and are characteristics of the catchment area. High pro-
portions of forest and peat lands surrounding lakes can contribute
to higher concentrations of humic substances and nutrients in the
water (Irfanullah, 2009; Reinikainen and Hyvrinen, 1997). Differ-
ent effects on the water environment can be evoked by forests: pine
forest can be a source of organic matter (DOC), whereas decidu-
ous forest can supply water mainly with nutrients (Klimaszyk and
Rzymski, 2011). However, leaf litter originating from deciduous
trees can also be an important source of allochthonous DOC in lakes
(Grigutyte et al., 2009). Long periods of high precipitation affect the
hydration of upper organic soil layers in the catchment area, facil-
itating the ushing of water enriched with DOC into nearby lakes
(Boyer et al., 1997). We observed the effect of the long term increase
of precipitation totals in Lake Rogzno, which affected water log-
ging in the area surrounding the lake, a potential source of DOC.
Our results showed an indirect effect of precipitation totals in 18
months before data sampling on water color and electrolytic con-
ductivity in the lake, which is consistent with the study by Hongve
et al. (2004). Similar changes in water color, so called browni-
cation, were found in northern temperate lakes (Forsberg, 1992;
Vuorenmaa et al., 2006).
In our model, the mean air temperature of March also affected
conductivity, water color and nutrient concentrations in the lake.
Pace and Cole (2002) observed that the date of ice melting corre-
lated with the water color and the concentration of DOC, which
were higher in years with late ice cover melting compared to years
with early ice out. This nding is consistent with our results because
we presumed that the mean air temperature of March is strongly
correlated with the term of ice out. After ice cover melting, ood-
ing of the adjacent area and subsequent ushing of water from the
catchment into a lake can lead to the enrichment of water in DOC
or simply raise the water level in lake (Boyer et al., 1997; McDowell
and Likens, 1988). Pace and Cole (2002) also suggested that the low
photodegradation of humic substances under the ice cover during
winter can be another reason for high water color in years with
late ice out. Conversely, higher measurements of DOC concentra-
tion and water color in the years with late ice out could be caused
by relatively short periods between DOC loading after ice melt-
ing and the xed data of DOC sampling. Higher concentrations of
water color and DOC was observed in the spring periods directly
after ice/snow cover melting; however, it was not statistically con-
rmed (Klimaszyk and Rzymski, 2011). Similar effects of the high
nutrient concentrations in the lake directly after ice cover melting
were described by Nges et al. (2010).
The results of our study have shown that the meteorological
variability of total precipitation and mean air temperatures during
March can affect the water level in lake and, in turn, some phys-
icochemical parameters. The climate driven variability of water
color, DOC concentration and water conductivity affects consec-
utive changes in submerged macrophytes and the phytoplankton
community in lakes. During the last 60 years, hydrologic trends
in the lakes of the Polesie region could explain some changes in
the vegetation between charophytes and other macrophyte groups.
The increase of charophytes in Lake Rogzno from the 1960s to
the beginning of the 21st century (Karczmarz and Malicki, 1965;
Sugier, 2008) could be linked with negative trends in precipita-
tion (Kaszewski et al., 2009). In the last few years (20072013),
the following increase of water level in lakes was associated with
the precipitation totals (Michalczyk et al., 2011). As a conse-
quence, transformations from charophytes to vascular plants and
briophytes in submerged vegetation and from cyanobacteria to
65
cryptophytes and dinoagellates in the phytoplankton community
were observed.
Conclusions
Despite the expected high resistance of deep hard water lakes
to disturbances, considerable changes in the physicochemical and
biological parameters were observed due to natural factors. Pre-
cipitation totals in the 18 months before data sampling and air
temperatures in March explained variations in the water param-
eters, such as water color, electrolytic conductivity and nutrient
concentrations. Increased water color and low electrolytic conduc-
tivity affected some transformations in the structure of submerged
macrophytes, e.g., the depletion of charophytes and the appearance
of bryophytes, in Lake Rogzno. The disappearance of charophytes
in this hard water lake was not linked with the chemical pre-
cipitation of humate-calcium complexes. Similar ecological effects
impacted the transformations in the phytoplankton community,
especially the relative importance of the ratio of the agellated,
e.g., cryptophytes and dinoagellates, to nonagellated species.
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