Download Primary production dynamics of dominant hydrophytes

Cent. Eur. J. Biol. • 4(2) • 2009 • 250–257
DOI: 10.2478/s11535-009-0013-5
Central European Journal of Biology
Primary production dynamics of dominant
hydrophytes in Lake Provala (Serbia)
Research Article
Ljiljana Nikolić1*, Slobodanka Pajević2, Branka Ljevnaić1
University of Novi Sad, Faculty of Agriculture,
21 000 Novi Sad, Serbia
1
University of Novi Sad, Faculty of Sciences and Mathematics,
21000 Novi Sad, Serbia
2
Received 12 November 2008; Accepted 11 February 2009
Abstract: The objective of this investigation was to analyze the primary production of the dominant hydrophytes by monitoring levels of organic
matter and organic carbon and estimating photosynthetic potential via the total chlorophyll content. The survey was conducted in
Lake Provala (Serbia) throughout the peak vegetation period of the year 2000. The contents of organic matter and organic carbon
for Myriophyllum spicatum L. were 105.11 g m-2 and 73.66 g m-2, Nymphoides peltata (Gmel.) Kunt. were 95.51 g m-2 and
45.26 g m-2 and Ceratophyllum demersum L. were 52.17 g m-2 and 29.75 g m-2. Chlorophyll A (Chl a) and chlorophyll A+B (Chl a+b)
pigments ranged from 1.54 mg g-1(Chl a) and 2.1 mg g-1(Chl a+b) in M. spicatum to 5.27 mg g-1(Chl a) and 7.53 mg g-1(Chl a+b) in
C. demersum. At full leaf out, the latter aquatic plants exceeded 50% cover of the open water surface. All species achieved maximum
growth in June, but significant differences in growth dynamics were observed. At the end of the vegetation period, these plants sink
to the bottom and decompose
Keywords: Aquatic macrophytes • Organic matter • Organic C • Chlorophyll
© Versita Warsaw and Springer-Verlag Berlin Heidelberg. 1. Introduction
Macrophytic type aquatic ecosystems are dominated
by various aquatic vascular plant species which play
an important role in the structure and function of
these ecosystems [1]. Aquatic vascular macrophytes
are adapted to living under certain aquatic conditions
and their occurrence and distribution depend on an
array of factors. These factors include water depth,
transparency, regime, chemical composition, pH and
salinity [2-11]. Sediment composition and properties are
also important for the presence of certain macrophytic
species in aquatic ecosystems [12-15].
The presence of macrophytes in aquatic biotopes
have multiple impacts not only on the local biota but
also on the properties of water and the underlying
sediments [16,17]. In shallow lakes, environmental
disturbances can change the distribution and abundance
250
of macrophytes [18]. Release of nutrients from
decomposing macrophytes, their incorporation into lake
sediments and their subsequent uptake by the growing
macrophytes presents a considerable portion of nutrient
cycling in a lake system [19]. Aquatic macrophytes have
a high capacity for nutrient uptake from water, which
affects the eutrophication process [20-24].
On the other hand, high productivity of aquatic
macrophytes may create large problems, particularly
at the time of decomposition of their biomass, which
may accelerate the eutrophication process [25-27]. It
is therefore important to monitor aquatic ecosystems
for growth and development of macrophytes with high
biomass production [28] thus protecting the ecological
balance in these ecosystems.
Shallow freshwater ecosystems are characterized
by high productivity. Phytoplankton and emergent,
floating and submerged macrophytes are principal
* E-mail:[email protected]
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L. Nikolić, S. Pajević, B. Ljevnaić
primary producers [11,29]. Individual primary producers
differ in productivity because they utilize different
sources of carbon dioxide and nutrients and they
differ in light energy utilization [29]. For example, the
emergent species take up carbon dioxide from the air
and are superior competitors for light. The position of
the floating macrophytes is intermediate with respect to
the terrestrial and emergent species. On the other side,
the submerged species are similar to phytoplankton
in that they use inorganic carbon and nutrients from
water and they compete for light. On that account,
phytoplankton and submerged macrophytes hold key
positions regarding their contributions to the productivity
of the water column. Their relationship is specific and
related to their spatial distribution along water depth
[30,31]. In general, it can be stated that macrophytes
are dominant and principal primary producers in small,
shallow and transparent aquatic ecosystems [11], while
phytoplankton is the main link of the bioproduction
chain in large, deep and poorly transparent aquatic
ecosystems [32-34].
The objective of this investigation was to analyze
the primary production dynamics of the dominant
hydrophytes by monitoring their levels of organic matter
and organic carbon and estimating their photosynthetic
potential via the total chlorophyll content. These factors
tend to accelerate the eutrophication process in a
Danube floodplain lake.
1.1 Study area
A man-made levee and a natural fluvial process had
been essential for the formation of Lake Provala (the
Vojvodina Province, Serbia). This lake was the result of
the Danube flood water spilling through a broken levee
in 1924, and the water rush formed a basin 19 m deep
[35,36]. After the flood waters withdrew, a lake remained
in the basin behind the levee. Its geographic position
is 45o29’ North latitude and 18o86’ East longitude, at
the altitude of 79 m. Presently, the Danube River flows
5.5 km west of the lake. At the average water level in the
lake, its area is about 42,000 m2, and its volume, owing
to the large depth (19 m max.), is 282,580 m3 (Figure 1).
Water transparency in the deepest part of the lake is
150 cm [35].
The Vojvodina Province, a part of the Pannonian
Plain, has a moderate continental climate. The location of
Lake Provala has a mean annual temperature of 10.7oC
and 17.5oC for the vegetation period. The amplitude
difference of the mean monthly temperatures is 21.9oC,
the temperatures ranging from -0.8oC in January to
21.1oC in July.
The floristic composition of the lake and the riparian
belt includes 65 plant species [37]. Emergent vegetation
Figure 1. Isobathic map of Lake Provala.
dominated by reed (Phragmites australis (Cav.) Trin.
ex Steud) flourishes in the riparian area along the
south banks of the lake. Lake waters are dominated
by three hydrophytes, N. peltata., M. spicatum and
C. demersum.
2. Experimental Procedures
Floristic investigations and collection of macrophytic
plant species for the analysis of primary production
were conducted in the course of the 2000 vegetation
period. Plant identification was performed according to
Flora Europaea [38]. Organic matter, organic carbon
and chlorophyll contents were measured according to
standard methods [39]. Vascular aquatic macrophytes
were collected from a boat, using a 0.5 m2 wooden frame
and a 0.25 m2 Petite-Ponard dredge. Macrophytes were
sampled in five replications, in previously labeled spots
(the deepest part, medium deep and the shallowest
part), throughout the growing season in one year.
Whole plants were taken from sample areas of 0.5 m2 or
0.25 m2. Plant material was labeled and taken to
laboratory where it was rinsed, wrung out and weighed.
Samples were dried at 105oC for 30 hours i.e., until a
constant weight was reached. Plant material was ground
and burnt for as long as it emitted gasses. The residue
was incinerated at 550oC for 6 hours. After cooling in
a desiccator, the residue was weighed to calculate the
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Primary production dynamics of dominant hydrophytes
in Lake Provala (Serbia)
Plant
Species
Date
(month/day)
Biomass *
5/13
5/31
6/14
6/28
7/17
7/31
8/16
9/4
9/26
x
S
V
I
M. spicatum
OM
OC
163
76
194
90
258
120
208
97
84
39
43
20
-
-
-
158.33
73.66
96.56
44.91
56.91
56.93
455.18
211.66
N. peltata
OM
OC
50
23
71
33
180
84
244
114
132
62
60
28
78
36
103
48
28
13
105.11
49.00
65.79
31.35
68.88
69.27
247.21
114.95
C. demersum
OM
OC
-
84
39
115
54
90
42
80
37
63
29
18
9
31
15
29
13
63.75
29.75
33.59
15.62
64.38
64.39
105.78
49.19
Table 1. Growing season changes in organic matter and organic carbon content for three aquatic plant species
* OM - organic matter (g m-²); OC - organic carbon (g C m-2); x - arithmetic mean; S - standard deviation; V - variation coefficient; I - variation
interval; N = 3
content of organic matter, which was expressed in g m-2.
As most of the higher plants contain 46-48% of carbon in
dry weight, organic carbon content was calculated using
the factor 46.5% and expressed in g C m-2. Chlorophyll
content (Chlorophyll A, Chl a and chlorophyll A+B, Chl
a+b) was determined spectrophotometrically, in acetone
extracts from fresh samples [40]. This analysis included
three replications of five individual plants per species.
Descriptive statistics were calculated for contents
of organic matter and organic carbon (Table 1) using
StatSoft Statistica 7.0 statistics software. Pigment
content were made in triplicate and data were analyzed
by Duncan’s multiple range test (P < 0.05).
3. Results
During the investigated period, the hydrophytes
N. peltata, M. spicatum and C. demersum were
dominant in Lake Provala waters. In full vegetation, the
three dominant aquatic plants flourished and overgrew
one half of the open water surface, while the surface
of the deepest part of the lake remains free of aquatic
vegetation.
M. spicatum, N. peltata and C. demersum were
analyzed for organic matter, organic carbon and
chlorophyll pigment contents, i.e., for indicators
of biomass production in the investigated aquatic
ecosystem.
While individual M. spicatum developed at the depth
of 6 m, the species grew in masses at the depth of 4 m
and in a large part of the lake. During the investigation
period, M. spicatum plants developed in late April,
flowered in late May and ended its vegetation period
already in August. The average annual contents of
organic matter and organic carbon in M. spicatum plants
were 158.33 g m-2 and 73.66 g m-2, respectively (Table 1).
N. peltata occurred in the course of May. They
reached maximum growth in summer and they persisted
until late fall, when some plants were still in flower.
N. peltata plants inhabited the shallower and narrower
(southern) of the lake, growing at the depths between 2
and 4 m. The average annual contents of organic matter
and organic carbon in N. peltata plants were 105.11 g m-2
and 49.00 g m-2, respectively (Table 1).
In the investigation period, C. demersum occurred
in late May. They occupied limited areas at the depths
between 4 and 6 m located at the beginning of the
southern elongation of the lake. The average annual
contents of organic matter and organic carbon in
C. demersum plants were 63.75 g m-2 and 29.75 g m-2,
respectively (Table 1).
The analyzed parameters (content of organic
matter and content of organic C) showed relatively
high coefficients and intervals of variation (Table 1).
The average values of organic matter was about 80%,
in agreement with the available literature [41,42]. The
values of organic carbon we obtained for the analyzed
species were slightly higher than those reported by
Westlake [41], while other authors [11,32] recorded
considerably higher average values.
The average values of chlorophyll pigment content
ranged from 1.54 mg g-1 (Chl a) and 2.15 mg g-1 (Chl
a+b) in M. spicatum in the month of June to 5.27 mg g-1
(Chl a) and 7.53 mg g-1 (Chl a+b) in C. demersum also
in June (Table 2).
Our results show species specificity in the seasonal
dynamics of pigment content (Table 2). The species
M. spicatum showed no significant difference among
the seasons, whereas N. peltata and C. demersum
exhibited significant differences in chlorophyll content
between the seasons in a single vegetation period.
Seasonal variation in chlorophyll content may provide
indirect indication of the dynamics of bioproduction by
the analyzed plant species. The species N. peltata has
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L. Nikolić, S. Pajević, B. Ljevnaić
M. spicatum
Month
Chlorophyll
A
C. demersum
Chlorophyll
A+B
Chlorophyll
A
N. peltata
Chlorophyll
A+B
Chlorophyll
A
Chlorophyll
A+B
May
1.86
a
2.49
a
4.23
b
5.76
b
3.27
b
4.28
b
June
1.54
a
2.15
a
5.27
a
7.53
a
1.96
c
2.65
c
July
1.79
a
2.40
a
1.88
d
2.58
e
3.04
b
3.81
b
August
-
-
3.29
c
4.64
c
4.48
a
5.98
a
September
-
-
2.87
c
3.71
d
4.64
a
5.84
a
Table 2. Growing season changes in chlorophyll A and A+B for three aquatic plant species in Lake Provala (mg g-1).
* Values with the same letter were not significantly different; N=5
the longest vegetation period and is distinguished for
largest and longest photosynthetic activity, which results
in the largest organic production and thus impact on the
eutrophication process. We also show that the species
differed significantly in chlorophyll content, especially
N. peltata and C. demersum (Tables 2 and 3).
The results of pigment content for the analyzed
macrophyte species were in agreement with the
available literature.
these ecological factors affected the primary production
in Lake Provala.
The submerged, rooted species M. spicatum,
thrived in the investigated aquatic ecosystem and was
characterized by a long flowering period, from spring to
fall, as reported by others [47]. At Lake Provala the peak
flowering period occurred in May through August. Gopal
and Goel describe M. spicatum as an adaptive, highly
competitive species that tolerates low light intensity
and low water temperature and possesses allelopathic
substances that inhibit the growth and development
of other aquatic species [48]. The last statement was
confirmed in Lake Provala where M. spicatum formed
predominantly pure stands. Compared with the other
two hydrophytes, M. spicatum had higher average
contents of organic matter and organic carbon, which
agrees with other studies [32], but also a relatively high
variation between the maximum and minimum values.
4. Discussion
Numerous authors [11,21,32,43-46] have emphasized
that there is a direct relationship between the primary
production dynamics of macrophytes and light regime,
temperature, water depth, sediment composition and
the amount of available nutrients. Here we show that
Plant species
M. spicatum
C. demersum
N. peltata
May
June
July
August
September
Chlorophyll A
1.86
c
1.54
b
1.79
b
-
-
Chlorophyll
A+B
2.49
c
2.15
b
2.40
b
-
-
Chlorophyll A
4.23
a
5.27
a
1.88
b
3.29
2.87
Chlorophyll
A+B
5.76
a
7.53
a
2.58
b
4.64
3.71
Chlorophyll A
3.27
b
1.96
b
3.04
a
4.48
4.68
Chlorophyll
A+B
4.28
b
2.65
b
3.81
a
5.98
5.84
Table 3. Chlorophyll A and A+B, average values of the three aquatic macrophytes (mg g.1 dry matter)
* Values with the same letter were not significantly different; N = 3
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Primary production dynamics of dominant hydrophytes
in Lake Provala (Serbia)
On the other hand, Lillie reported somewhat higher
average values, pointing out that the species produced
maximum biomass when growing at the depths between
1.5 and 3 m [49]. The high variance in our study are
undoubtedly associated with the adaptability of
M. spicatum to changes in nutrient content, light intensity
and water depth during growing period [9,50].
The floating, rooted, species N. peltata is
characterized by a long flowering period and high
biomass productivity [25,38,51]. In Lake Provala, it
achieved maximum growth in summer and persisted till
late fall, when individual plants could still be found in
flower. The contents of organic matter (around 80% in
relation to dry matter) and organic carbon (37% in relation
to dry matter) in N. peltata were somewhat lower than
those found in literature [32]. Still lower biomass values
were registered for Nymphoides [52], who pointed out
that water chemistry had an exceptionally high effect
on macrophytic species and their bioproduction. On the
other side, Brock et al. registered higher biomass values
for N. peltata at the peak of the vegetation growth [53].
In addition to numerous abiotic factors, the biomass
production dynamics is significantly affected by biotic
factors such as the rate of colonization by epiphytic
organisms [43,54], which is especially conspicuous
in the case of species with large leaf area such as
N. peltata.
The submerged, unrooted species C. demersum,
which occurs at all depths and in all regions and seasons
[47], was found in Lake Provala on a limited area, near
the bottom of this aquatic ecosystem, where it did not
form large biomass. This might be due to Ceratophyllum
and its high requirements for nitrogen and nitrogencontaining substances, which are moderately abundant
in Lake Provala [27]. Also, Phillips et al. mention the
negative allelopathic effects of Ceratophyllum on
other aquatic plants [55]. Compared with the other
two species, C. demersum had lower values of the
analyzed parameters, which were somewhat lower than
those found in literature [11]. The obtained data are a
good illustration of the primary production dynamics of
C. demersum in Lake Provala, and they also showed
lowest variations. Overall C. demersum grew and
produced biomass fairly uniformly through the vegetation
period, with an exception in June when it reached a peak
of the vegetation growth.
The analysis of chlorophyll A and B in the three
hydrophytes indicated the presence of species
specificity as well as of seasonal dynamics of these
pigments. According to Schagerl and Pichler [56], the
content of chlorophyll A has a wide range of variation in
aquatic plants, which speaks in favor of plant adaptation
to different ecological conditions, in the first place light
and temperature. In Lake Provala, the submerged
species M. spicatum, which had the shortest vegetation
period, showed no significant differences among the
seasons [27], while the floating species N. peltata
and the submerged species C. demersum exhibited
significant differences in chlorophyll content among
the dates of measurement throughout the vegetation
period. The seasonal variation in pigment content
was an indication of bioproduction dynamics with
N. peltata having the longest period of bioproduction.
Consequently, this species had the highest effect on the
process of secondary pollution of the lake, due to the
decay and decomposition of its biomass after the end
of the vegetation period, which significantly bolster the
eutrophication process [25,27,37].
It may be concluded from the above that the
investigated aquatic ecosystem is dominated by
macrophytes, one floating (N. peltata) and two
submerged (M. spicatum and C. demersum). These plant
species are characterized by uneven biomass growth
during the vegetation period, which is brought about
by the ambient climatic conditions and the trophic state
of the investigated aquatic ecosystem. The enormous
biomass which they form by the end of the vegetation
period causes secondary pollution of the lake, which
directly affects the trophic level of the ecosystem by
accelerating the eutrophication process in this Danube
floodplain lake. Additionally, the existent macrophytes
achieve their maximum growth in June, during full tourist
season, which is a further detriment for this small and
relatively shallow lake.
In spite of an important feature of macrophytes, that
they take up large amounts of nutrients from lake water
and benthic zone [22,23,25], it is necessary to monitor and
control their growth and development [28,57] because
their enormous bioproduction may negatively affect the
ecological balance of small aquatic ecosystems and
may accelerate the process of eutrophication in them.
Because of the negative effects of the accelerated
eutrophication process, certain measures are needed
[25,28,57] to improve water quality and thus remediate
the investigated aquatic ecosystem. Since Lake Provala
is intended for tourism, sports and recreation, caution
should be exercised when selecting methods for
decelerating the eutrophication process.
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L. Nikolić, S. Pajević, B. Ljevnaić
References
[1] Chambers P.A., Lacoul P., Murphy K.J., Thomaz
S.M., Global diversity of aquatic macrophytes in
freshwater, Hydrobiologia, 2008, 595, 9-26
[2] Madsen D.J., Adams S.M., The distribution of
submerged aquatic macrophyte biomass in a
eutrophic stream, Badfish Creek: the effect of
environment, Hydrobiologia, 1989, 171, 111-119
[3] Manny B.A., Nichols S.J., Schlosser D.W., Heavy
metals in aquatic macrophytes drifting in a large
river, Hydrobiologia, 1991, 219, 333-344
[4] Squires L., van der Valk A.G., Water-depth tolerances
of the dominant emergent macrophytes of the Delta
Marsh, Manitoba, Can. J. Bot., 1992, 70, 1860-1867
[5] Vadineanu A., Sergiu C., Ignat G., Phytoplankton and
submerged macrophytes in the aquatic ecosystems
of the Danube Delta during the last decade,
Hydrobiologia, 1992, 243/244, 141-146
[6] Brink F.W.B., Velde G., Bosman W.W., Coops H.,
Effects of substrate parameters on growth responses
of eight helophyte species in relation to flooding,
Aquat. Bot., 1995, 50, 79-97
[7] Weisner E.B.S., Long-term competitive displacement
of Typha latifolia by Typha angustifolia in an eutrophic
lake, Oecologia, 1993, 94, 451-456
[8] Rea N., Ganf G.G., The influence of water regime
on the performance of aquatic plants, Water Sci.
Technol., 1994, 29, 127-132
[9] Madsen, D.J., Wersal M.R., Tyler M., Gerard P., The
Distribution and Abundance of Aquatic Macrophytes
in Swan Lake and Middle Lake, Minnesota,
J. Freshwater Ecol., 2006, 21, 421-429
[10] Coops H., Geilen N., Van der Velde G., Distribution
and growth of the helophyte species Phragmites
australis and Scirpus lacustris in water depth
gradients in relation to wave exposure, Aquat. Bot.,
1994, 48, 273-284
[11] Vis C., Hudon C., Carignan R., Gagnon P.,
Spatial Analysis of Production by Macrophytes,
Phytoplankton and Epiphyton in a Large River
System under Different Water-Level Conditions,
Ecosystems, 2007, 10, 293-310
[12] Nichols S.A., Depth, substrate, and turbidity
relationships of some Wisconsin lake plants, Trans.
Wis. Acad. Sci. Arts Lett., 1992, 80, 97-118
[13] Brink F.W.B., Velde G., Growth and morphology of
four freshwater macrophytes under the impact of
the raised salinity level of the Lower Rhine, Aquat.
Bot., 1993, 45, 285-297
[14] Lauridsen T.L., Jeppesen E., Andersen F.O.,
Colonization of submerged macrophytes in shallow
fish manipulated Lake Veng: Impact of sediment
composition and waterfowl grazing, Aquat. Bot.,
1993, 46, 1-15
[15] Jackson L.J., Kalff J., Patterns in metal content of
submerged aquatic macrophytes - The role of plant
growth form, Freshwater Biol., 1993, 29, 351-359
[16] Chambers P.A., Prepas E.E., Nutrient dynamics
in riverbeds: The impact of sewage effluent and
aquatic macrophytes, Water Resour., 1994, 28,
453-464
[17] Brix H., Functions of Macrophytes in Constructed
Wetlands, Water Sci. Technol., 1994, 29, 71-78
[18] Capers R.S., Macrophyte colonization in a
freshwater tidal wetland (Lyme, CT, USA), Aquat.
Bot., 2003, 77, 325-338
[19] Shilla D., Asaeda T., Fujino T., Sanderson
B., Decomposition of dominant submerged
macrophytes: implications for nutrient release
in Myall Lake, NSW, Australia, Wetlands Ecol.
Manage., 2006, 14, 427-433
[20] Greenway M., Wooley A., Changes in plant biomass
and nutrient removal over 3 years in a constructed
wetland in Cairns, Australia, Water Sci. Technol.,
2001, 44, 303-310
[21] Bazarova B.B., Itigilova Ts.M., Long-term Production
Dynamics of Aquatic Vegetation in the Arakhlei Lake
(Eastern Transbaikalia), Biol. Bull., 2006, 33, 68-72
[22] Greenway M., The Role of Macrophytes in
Nutrient Removal Using Constructed Wetlands,
In: Environmental Bioremediation Technologies,
Springer Berlin Heidelberg, 2007, 331-351
[23] Strivastava J., Gupta A., Chandra H., Managing
water quality with aquatic macrophytes, Rev.
Environ. Sci. Biotechnol., 2008, 7, 255-266
[24] Ciurli A., Zuccarini P., Alpi A., Growth and nutrient
absorption of two submerged aquatic macrophytes
in mesocosms, for reinsertion in a eutrophicated
shallow lake, Wetlands Ecol. Manage., 2008, 17,
107-115
[25] Marion, L., Paillisson J.-M., A mass balance
assessment of the contribution of floating-leaved
macrophytes in nutrient stocks in an eutrophic
macrophyte-dominated lake, Aquat. Bot., 2003, 75,
249-260
[26] Nikolić Lj., Stojanović S., Stanković Ž., Content
of macro- (N,P,K) and micronutrients (Fe, Mn, Zn)
in four promising emergent macrophytic species,
Fundam. Appl. Limnol. (Arch. Hydrobiol.), 2003,
147, 297-306
[27] Nikolić Lj., Čobanović K., Lazić D., N. peltata
(Gmel.) Kunt., M. spicatum L. and C. demersum
L. biomass dynamics in the Lake Provala (the
255
Unauthenticated
Download Date | 6/16/17 5:09 PM
Primary production dynamics of dominant hydrophytes
in Lake Provala (Serbia)
Vojvodina Province, Serbia), Cent. Eur. J. Biol.,
2007, 2, 156-168
[28] Coops H., van Nes E.H., van den Berg M.S.,
Butijn G.D., Promoting low-canopy macrophytes
to compromise conservation and recreational
navigation in a shallow lake, Aquat. Ecol., 2002, 36,
483-492
[29] Horne A.J., Goldman C.R., Aquatic Macrophytes
and Littoral Productivity, In: Limnology, 2nd Ed.,
McGraw-Hill, New York, 1994, 1-627
[30] Asaeda T., Van Bon T., Modelling the effects of
macrophytes on algal blooming in eutrophic shallow
lakes, Ecol. Modell., 1997, 104, 261-287
[31] Case M.L., Madsen D. J., Factors limiting the
growth of Stuckenia pectinata (sago pondweed) in
Heron Lake, Minnesota, J. Freshwater Ecol., 2004,
19, 17-23
[32] Rich P. H., Wetzel R. G., Van Thuy N., Distribution,
production and role of aquatic macrophytes in a
southern Michigan marl lake, Freshwater Biol.,
1971, 1, 3-21
[33] Scheffer M., Hosper S. H., Meijer M. L., Moss B.,
Jeppesen E., Alternative equilibria in shallow lakes,
Trends Ecol. Evol., 1993, 8, 275-279
[34] Stephen D., Moss B., Phillips G., The relative
importance of top-down and bottom-up control of
phytoplankton in a shallow macrophyte-dominated
lake, Freshwater Biol., 1998, 39, 699-713
[35] Bogdanović Ž., Jezero Provala (Provala Lake),
Bull. Serb. Geog. Soc., Beograd, 1985, 53-58 (in
Serbian)
[36] Bugarčić, P., Veštačka jezera Vojvodine - Geografski
aspekti i problemi, PhD thesis, University of Novi
Sad, 1999, (in Serbian)
[37] Nikolić Lj., Biljni svet i primarna produkcija –
indikatori eutrofizacije u jezeru Provala (Plant world
and primary production - indicators of eutrophication
process in the lake Provala), Monograph, Zadužbina
Andrejević, Biblioteka Dissertatio, Beograd, 2005,
(in Serbian)
[38] Tutin T.G. (Ed.), Flora Europaea I-V, Cambridge
University Press, 1996
[39] American Public Health Association (APHA),
Standard Methods for the Examination of Water
and Wastewater, 19th Ed., Franson M.H. (Ed.),
Washington DC, 1995
[40] Lichtentaler H.K., Wellburn A.R., Determinations of
total carotenoids and chlorophylls a and b of leaf
extracts in different solvents, Bioch. Soc. Trans.,
1983, 603, 591-592
[41] Westlake D.F., Primary production of freshwater
macrophytes, In: Cooper J.P. (Ed.), Photosynthesis
and Productivity in Different Environments,
Cambridge University Press, 1975, 189-294
[42] Duarte C., Kalff J., Peters R.H., Patterns in biomass
and cover of aquatic macrophytes in lakes, Can. J.
Fish. Aquat. Sci., 1986, 43, 1900-1908
[43] Hopson S.M., Zimba V.P., Temporal Variation in
the Biomass of Submersed Macrophytes in Lake
Okeechobee, Florida, J. Aquat. Plant Manage.,
1993, 31, 76-81
[44] Camargo A.F.M., Florentino E.R., Population
dynamics and net primary production of the aquatic
macrophyte Nymphaea rudgeana C.F. Mey in a
lotic environment of the Itanhaem River basin (SP,
Brazil), Rev. Brasil. Biol., 2000, 60, 1-10
[45] Hansel-Welch N., Butler G.M., Carlson J.T., Hanson
A.M., Changes in macrophyte community structure
in Lake Christina (Minnesota), a large shallow lake,
following biomanipulation, Aquat. Bot., 2003, 75,
323-337
[46] Shilla D., Dativa J., Biomass dynamics of
charophyte-dominated submerged macrophyte
communities in Myall Lake, NSW, Australia, Chem.
Ecol., 2008, 24, 367-377
[47] Kunii H., Maeda K., Seasonal and long-term changes
in surface cover of aquatic plants in a shallow pond,
Ojaka-ike, Chiba, Japan, Hydrobiologia, 1982, 87,
45-55
[48] Gopal B., Goel U., Competition and allelopathy in
aquatic plant communities, Bot. Rev., 1993, 59,
155-210
[49] Lillie A.R., A quantitative survey of the floatingleafed and submerged macrophytes of Fish Lake,
Dane County, Wisconsin, Trans. Wis. Acad. Sci.
Arts Lett., 1996, 84, 111-125
[50] Best P.E., Boyd A.W., A Simulation Model for Growth
of the Submersed Aquatic Macrophyte Eurasian
Watermilfoil (Myriophyllum spicatum L.), Technical
Report A-99-3, US Army Engineer Research and
Development Center, Vicksburg, Mississippi, 1999,
1-113
[51] Tsuchia T., Nohara S., Iwakuma T., Net primary
production of Nymphoides peltata (Gmel.) O.
Kuntze growing on sandy sediment at Edosakiiri Bay in Lake Kasumigaura, Japan, Am. J. Bot.,
1990, 51, 307-312
[52] Kelly M.S., Distribution and biomass of aquatic
macrophytes in an abandoned nuclear cooling
reservoir, Aquat. Bot., 1989, 35, 133-152
[53] Brock Th.C.M., Arts G.H.P., Goosen I.L.M.,
Rutenfrans A.H.M., Structure and annual biomass
production of Nymphoides peltata (Gmel.) O. Kuntze
(Menyanthaceae), Aquat. Bot., 1983, 17, 167-188
[54] Sand-Jansen K., Borum J., Interaction among
phytoplankton, periphyton, and macrophytes in
256
Unauthenticated
Download Date | 6/16/17 5:09 PM
L. Nikolić, S. Pajević, B. Ljevnaić
temperate freshwaters and estuaries, Aquat. Bot.,
1991, 41, 137-175
[55] Phillips G.L., Eminson D., Moss, B., A mechanism
to account for macrophyte decline in progressively
eutrophicated freshwaters, Aquat. Bot., 1978, 4,
103-126
[56] Schagerl M., Pichler C., Pigment composition of
freshwater charophyceae, Aquat. Bot., 2000, 67,
117-129
[57] Abrahams C., Climate change and lakeshore
conservation: a model and review of management
techniques, Hydrobiologia, 2008, 613, 33-43
257
Unauthenticated
Download Date | 6/16/17 5:09 PM