Aquatic Conservation - 2006 - Peretyatko - Phytoplankton Biomass and Environmental Factors Over A Gradient of Clear To

AQUATIC CONSERVATION: MARINE AND FRESHWATER ECOSYSTEMS
Aquatic Conserv: Mar. Freshw. Ecosyst. 17: 584–601 (2007)

Published online 23 October 2006 in Wiley InterScience
(www.interscience.wiley.com) DOI: 10.1002/aqc.788
Phytoplankton biomass and environmental factors over a

gradient of clear to turbid peri-urban pondsy
ANATOLY PERETYATKOa,*, SAMUEL TEISSIERb, JEAN-JACQUES SYMOENSa

and LUDWIG TRIESTa
a
Plant Science and Nature Management, Department of Biology, Vrije Universiteit Brussel, Brussels, Belgium
b
Laboratoire d ’Ecologie des Hydrosyste`mes, UMR CNRS-UPS 5177, Toulouse, France
ABSTRACT
1. Small lakes and ponds with high nutrient loadings can be clear, turbid or intermediate, with low,
high and intermediate phytoplankton biomass, respectively.
2. A combination of biotic and abiotic factors, such as hydraulic retention time, presence of
submerged vegetation, depth, top-down phytoplankton control, and cascading effects of fish com-
munity structure, play an important role in phytoplankton biomass control when nutrients are not
limiting. Different combinations of these factors lead to different levels of phytoplankton biomass.
3. Identification of the main factors controlling phytoplankton biomass in a particular pond or a
small lake is essential for choosing an appropriate management strategy for the maintenance of a
desired ecosystem state.
4. When a pond or a small lake ecosystem is impaired by eutrophication, a considerable degree of
its ecological quality can be restored through the modification of some environmental factors when a
sufficient reduction in nutrient input is not feasible.
Copyright # 2006 John Wiley & Sons, Ltd.
Received 12 October 2005; Accepted 2 April 2006
KEY WORDS: phytoplankton; ponds; eutrophic; clear; turbid; alternative stable states
INTRODUCTION
Small lakes and ponds represent the overwhelming majority of lentic water bodies in lowland Europe.
Because of their small size less ecological and conservation-related research has been carried out on them.
A number of recent studies have shown their importance for flora, fauna and habitat diversity
*Correspondence to: A. Peretyatko, Plant Science and Nature Management (APNA), Department of Biology, Vrije Universiteit
Brussel, Pleinlaan 2, 1050 Brussels, Belgium. E-mail: Anatoly.Peretyatko@vub.ac.be
y
This article was published online on 23 October 2006. Two errors were subsequently identified and corrected by two errata notices that
were published online only on 28 February 2007; DOI: 10.1002/aqc.848 and 14 June 2007; DOI: 10.1002/aqc.872. This printed version
incorporates the amendments identified by the errata notices.

10990755, 2007, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/aqc.788 by Universidad De Concepcion, Wiley Online Library on [28/05/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
PHYTOPLANKTON IN PERI-URBAN PONDS 585
conservation (Linton and Goulder, 2000; Moss et al., 2003; Angelibert et al., 2004; Sndergaard et al.,
2005). Williams et al. (2003) found that ponds contributed more to biodiversity than other water-body
types, supporting considerably more species in general and more unique and rare species in particular.
Nevertheless, most ponds and small lakes have been heavily affected and disturbed by human activities
leading to eutrophication and drastic decreases in water quality. Many formerly pristine clear-water ponds
and lakes within a few years turned into turbid water bodies with dense algal blooms, bad odour and mucky
bottoms (Proulx et al., 1996; Brönmark and Hansson, 1998; Sand-Jensen, 2001). Many ponds and small
lakes have been lost owing to neglect or direct human intervention (Linton and Goulder, 2000). During the
last few decades, limnologists and conservationists have been increasingly interested in eutrophication and
resulting shifts of vegetation dominance from macrophytes to phytoplankton in shallow freshwater bodies.
It has been shown that food-web manipulation combined with a reduction in nutrient loading may result in
restoration of the clear-water conditions (Shapiro and Wright, 1984; Gulati and van Donk, 2002). Major
conceptual progress was achieved by the development of a model explaining the occurrence of two
alternative stable states (clear and turbid) in shallow lakes, and the relationship between the occurrence of
these states and nutrient loading (Scheffer et al., 1993; Janse, 1997; Scheffer, 1998).
It is generally accepted that nutrient loading is the main factor regulating phytoplankton biomass. When
nutrient concentrations are low, shallow water bodies are clear and characterized by low phytoplankton
biomass and extensive macrophyte vegetation; when high, they are turbid with high phytoplankton biomass
and no macrophytes (van Tongeren et al., 1992; Scheffer et al., 1993; Muylaert et al., 2003). At intermediate
nutrient levels (50–150 mg L1 total phosphorus (TP); Jeppesen et al., 1997) either alternative stable state
can occur and system shifts are possible. Moss et al. (1996) have found that both states can exist over the
range of 25–1000 mg L1 of TP .
Some more recent studies (Sondergaard and Moss, 1998; Van Donk and van de Bund, 2002) have also
shown that submerged macrophytes can maintain a clear-water state through a number of mechanisms
such as shading, increased sedimentation, increased grazing, allelopathy and changing nutrient cycling, and
thus considerably buffer the effects of nutrient enrichment. Submerged macrophytes are also important for
successful biomanipulation in eutrophic or hypereutrophic shallow water bodies as partial or complete
removal of planktivorous fish, not accompanied by revegetation, can lead to a shift in phytoplankton
composition towards larger, colonial or filamentous species, such as bloom-forming cyanobacteria, without
reduction in total phytoplankton biomass (Benndorf et al., 2002).
Several studies have investigated the relationship of phytoplankton biomass and composition as well as
biotic and abiotic environmental factors in shallow lakes and ponds located in large geographic areas (e.g.
Gulati and van Donk, 2002; Bayley and Prather, 2003; Nydick et al., 2003; Szelag-Wasielewska, 2003). These
studies clearly reveal the importance of environmental factors in controlling phytoplankton biomass and
composition. However, in such large-scale studies gross patterns determined by differences in geology,
hydrology and water quality may impede the determination of relative importance of local factors. This study,
as well as a number of others (e.g. Cottenie et al., 2001), have shown that neighbouring and even highly
connected ponds may differ substantially in their trophic structure and biotic and abiotic interactions. The aim
of this study was to estimate the influence of biotic and abiotic factors that operate in a set of peri-urban ponds
located in the same catchment area with high nutrient loadings on the resulting phytoplankton biomass and
composition, as well as the implications of such influence for pond management and restoration. An additional
objective was to verify whether there was an evidence of ‘alternative stable states’ (Scheffer et al., 1993).
METHODS
Study area characteristics
Sixteen ponds located in the immediate periphery of the Brussels urban area (Belgium) were selected for this
study (Figure 1). They are located along the Woluwe River and three of its smaller tributaries flowing
Copyright # 2006 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. 17: 584–601 (2007)
DOI: 10.1002/aqc
586 A. PERETYATKO ET AL.
Figure 1. Location of the sixteen studied ponds in the Woluwe river catchment (Brussels, Belgium).
through the eastern part of Brussels. The Woluwe is a small, 15-km long, tributary of the Senne River
belonging to the Scheldt basin. It ranges from 5 to 30 cm in depth and from 0.5 to 3 m in width within the
study area and drains an area of 9400 ha. Some ponds are connected to the river system (flow-through
ponds); others are fed by the groundwater seepage and small rivulets (overflow ponds). The ponds range in
their surface area from 1800 m2 to 32 400 m2 and in depth from 0.6 to 3 m (Table 1). All ponds were
constructed more than a century ago (Marlier, 1971) with the exception of Malu which was totally restored
in 2000 and converted from an overflow to a flow-through pond. Nine ponds (Hoef, VKn1, VKn2, Vbk1,
Vbk2, WtMl, RKl2, RKl3, RKl5) are located along the forested Woluwe River tributaries and are all of
flow-through type. Two flow-through ponds (Tenr, Malu) and five overflow ponds (MlKl, MlGr, WPk1,
WPk2, TrBr) are located in urban park areas along the midstream river section. More details of the
Woluwe river catchment are given by Triest et al. (2001).
Sampling and sample processing

Quantitative phytoplankton samples accompanied by samples for the main nutrients (TP, SRP, NO3, NO2,
NH4 and SiO2) were collected on 23 occasions in 16 ponds during the 4-year monitoring period (May and
DOI: 10.1002/aqc
Table 1. Environmental variables of the studied ponds. Average and range values are given when relevant. Abbreviations used: SD – Secchi depth, MD – maximum
depth, SA – surface area, RT – hydraulic retention time, FV – floating-leaved vegetation cover, FA – green filamentous algae cover, SM – submerged macrophytes cover,
PF – planktivorous fish density, BF – benthivorous fish density, PsF – piscivorous fish density
TP SRP NH4 NO2 NO3 SiO2 Chl a SD MD RT SA SM FV FA PF BF PsF
Site (mgP L1) (mgP L1) (mg L1) (mg L1) (mg L1) (mg L1) (mg L1) (m) (m) (day) (m2) (scorea) (scorea) (scorea) (CPUE) (CPUE) (CPUE)
Vbk1 0.162 0.022 0.191 0.032 3.607 20.729 2.1 bottom 1.1 2.69 1 800 0 0 1 0 1.13 0
0.01–0.32 0–0.05 0.03–0.54 0.02–0.07 2.49–4.69 10.15–38.34 0.3–6.7 0.9–1.4
Hoef 0.124 0.019 0.033 0.025 0.516 1.61 2.1 bottom 0.7 17.2 7 200 2 0 2 0 1.74 0.29
0.004–0.32 0–0.048 0–0.13 0–0.23 0.001–3.86 0.27–5.09 0.8–4.3 0.5–1.1

Vbk2 0.176 0.047 0.318 0.038 2.349 19.001 6.6 bottom 1.4 4.5 3 600 0 0 1 2.18 5.44 0
0.04–0.32 0.01–0.12 0.05–0.75 0.02–0.07 0.272–4.12 7.87–38.51 1.9–34.2 1.2–1.7
Tenr 0.24 0.104 0.166 0.049 0.757 13.557 3.1 bottom 1.2 2.82 32 400 2 0 2 0.34 1.13 0.23
0.07–0.46 0.02–0.23 0.005–1.06 0–0.22 0.018–3.71 3.74–20.54 1.1–7.5 1–1.5
VKn1 0.166 0.011 0.134 0.020 0.526 12.843 11.4 1.3 1.1 18.25 5 400 0/2b 0 0 33.49 0 0
0.08–0.33 0–0.047 0.001–0.59 0–0.08 0.03–1.85 5.66–20.49 1.1–32.5 0.6–bottom 0.5–1.4
MlGr 0.205 0.018 0.093 0.008 0.171 12.155 30.3 1.1 1.1 29.25 32 400 2 0 1 0 3.18 0
0.06–0.35 0–0.086 0–0.62 0–0.02 0.01–0.54 2.24–24.39 0.6–133.5 0.5–bottom 0.9–1.5
WtMl 0.182 0.028 0.075 0.019 0.717 17.457 8.5 1.5 1.1 6.7 29 700 0/2b 1 1 0 2.2 0
0.04–0.32 0–0.1 0–0.27 0–0.1 0.028–3.81 8.29–33.17 2.4–28.7 0.6–bottom 0.5–1.7
RKl2 0.167 0.006 0.056 0.029 0.81 18.962 27.4 1.1 2 5.86 20 700 0 0 0 0.24 9.99 0.48
0.04–0.31 0–0.014 0.003–0.28 0.001–0.12 0.003–3.78 9.31–41.14 3.7–91 0.6–1.7 1.4–2.3
RKl5 0.226 0.020 0.076 0.018 0.406 18.509 20.4 0.7 0.7 3.02 31 500 0 0 2 0.12 2.31 0
0.08–0.41 0–0.083 0–0.39 0–0.07 0.02–1.09 8.78–41.31 2.5–44.4 0.5–bottom 0.4–1
RKl3 0.16 0.005 0.069 0.017 0.561 17.601 28.1 1.0 2.8 5.39 13 500 0 1 0 57.06 17.9 1.12
0.04–0.32 0–0.016 0–0.24 0–0.11 0–3.82 5.89–41.48 8.5–62.8 0.7–1.6 2.2–3.1
VKn2 0.199 0.006 0.054 0.030 1.393 14.508 54.3 0.8 1 8.68 3 600 0 0 0 4.09 0 0
0.09–0.39 0–0.019 0.005–0.21 0–0.1 0.02–4.36 6.01–19.44 8.2–100.4 0.6–1 0.9–1.1
Malu 0.236 0.022 0.079 0.115 2.39 15.737 80.4 0.8 1.8 0.72 7 200 0 0 0 1.55 2.84 0.26
PHYTOPLANKTON IN PERI-URBAN PONDS
0.07–0.40 0.00–0.05 0.024–0.21 0.011–0.24 0.02–4.39 5.51–27.24 25.7–242 0.7–1 1.1–2.1

WPk2 0.235 0.004 0.049 0.018 0.656 15.074 50.6 0.6 1.1 25.88 19 800 0 0 0 4.37 2.91 0.29
0.14–0.36 0–0.019 0–0.19 0–0.11 0.01–3.38 5.72–31.47 23.5–98.8 0.4–1.2 0.8–1.3
WPk1 0.226 0.004 0.050 0.012 0.455 18.607 41.4 0.6 1.1 39.14 19 800 0 1 0 1.19 1.48 0
0.09–0.36 0–0.014 0–0.33 0–0.05 0.01–2.43 7.55–31.22 22.7–73.6 0.5–1.1 0.9–1.2
MlKl 0.357 0.020 0.016 0.005 0.183 16.086 113.3 0.4 0.9 24.98 8 100 0 0 0 1.91 20.73 0
0.16–0.49 0–0.04 0–0.07 0–0.02 0.005–1.21 5.21–42.83 15.2–225.5 0.3–0.5 0.8–1.1
TrBr 0.384 0.024 0.087 0.068 1.577 14.174 156.9 0.5 1.1 20.05 8 100 0 2 0 11.41 11.41 0.95
0.21–0.51 0–0.10 0 – 0.37 0–0.24 0.02–3.93 0.74–41.56 25.9–415.7 0.3–0.6 0.9–1.5
a
See ‘Methods’ section for scoring system.
b
Before and after manipulation.
587
Aquatic Conserv: Mar. Freshw. Ecosyst. 17: 584–601 (2007)

DOI: 10.1002/aqc
August 2002; February, May, June, September and November 2003; and monthly from March to October
in 2004 and 2005). Mixed water samples based on 4–8 random subsamples were taken from each pond with
a plastic tube sampler of 4.5 cm diameter and 70 cm length that closes in the lower part. A special extension
was fixed to the sampler to reach the deeper parts of the ponds when appropriate.
To broaden the characterization of the studied ponds, chlorophyll a (Chl a) and zooplankton samples
were added in 2004 and 2005.
After stirring the collected water, 500 mL were taken for phytoplankton identification and enumeration,
1 L for chemical analyses and 1 L for Chl a analysis.
The samples for Chl a analysis were kept in ice until delivery to the laboratory where they were filtered
onto Whatman GF/C filters and stored at 188C for several days before analysis. Pigments were extracted
in 90% acetone in the dark for 24 hours. Pigment concentrations were measured spectrophotometrically.
Nutrient and Chl a concentrations were measured according to the standard methods (APHA-AWWA-
WEF, 1995). Secchi depth was measured with a Secchi disc of 30 cm diameter. When the Secchi depth was
greater than the depth of the pond, depending on whether the disc was well or partially visible, 0.5 m or
0.1 m was added to the depth value, respectively. The phytoplankton samples were fixed in the field with
alkaline lugol, sodium thiosulfate and buffered formalin (Kemp et al., 1993) and stored at room
temperature in the dark before identification to genus level and enumeration using inverted microscopy.
Biovolumes were calculated using the approximations of cell shapes to simple geometrical forms (Wetzel
and Likens, 1990).
For zooplankton, five subsamples of 1 L were collected randomly in each pond with the same sampler
used for phytoplankton. The subsamples from a given pond were combined, filtered through a 64-mm mesh
net, and preserved in 5% formaldehyde (final concentration) before being identified and enumerated using
inverted microscopy. Different levels of identification were used: rotifers and cladocerans were identified to
genus level; copepods were divided into cyclopoid, calanoid copepods and nauplii. For the analyses,
cladocerans were divided into two groups: large (Daphnia spp. and Moina spp.) and small (Bosmina spp.,
Ceriodaphnia spp. and Chydorus spp.).
Three types of macrophytic vegetation were identified: submerged macrophytes (mainly Potamogeton
pectinatus, Chara spp., Nitella sp. and Ceratophyllum demersum), plants with floating leaves (mainly Nuphar
lutea and Nymphaea alba), and green filamentous algae (mainly Spirogyra spp.). The following scores were
used to quantify the occurrence and abundance of different macrophyte types: 0 ¼ absent; 1 ¼ poorly
developed, 2 ¼ well developed (adapted from Cottenie et al. (2001)).
Semi-quantitative fish samples (catch per unit effort, CPUE) were taken from each pond in April 2004
with two fykenets kept in each pond for 2 days. Seine net fishing was used to verify the species richness
yielded by the first method. All individuals were counted and identified to species level. For data analysis
the fish were lumped into three functional groups: planktivorous, benthivorous and piscivorous.
Morphometric variables of the ponds were measured in the field (depth), or using GIS software (area;
digitized map, ArcView 3.2). Hydraulic retention time was estimated in July 2004 on the basis of the water
discharge measured at the outlet of each pond and the corresponding pond volume.
Incident solar radiation, usually an important factor affecting phytoplankton growth, was not considered
here, for the forest ponds (the most affected by shade), exhibited both low and high phytoplankton biomass
levels and some ponds showed high phytoplankton biomass in February (Secchi depth below 0.5 m) when
solar radiation is at its lowest level suggesting that other factors are more important in its control.
Four ponds were subjected to different types of management intervention during the study period. In
winter 2004–2005 the WtMl and VKn1 ponds were emptied for a few months (WtMl: November 2004–
February 2005; VKn1: February 2005–March 2005) with fish removal. MlGr was subjected to regular
removal of submerged macrophytes in mid-summer by the pond managers considering them as a nuisance
for recreational activities. Malu was converted from an overflow to a flow-through pond in 2000 in order to
improve the water quality and prevent the occurrence of cyanobacterial blooms by decreasing the hydraulic
DOI: 10.1002/aqc
retention time (Brussels Institute of Environment } BIM/IBGE). Continuous monitoring of these ponds
allowed the effects of such management interventions on phytoplankton and ecological status to be
assessed.
Statistical analyses
Phytoplankton biovolume and Chl a data were significantly positively correlated (Spearman R ¼ 0:91;
p50:01) and showed similar spatial–temporal distribution patterns, which suggests that the former gives a
reasonable estimation of phytoplankton biomass. Identified to genus level, phytoplankton biovolume had
greater discriminative power than Chl a; therefore it was used as a proxy for phytoplankton biomass.
Rare phytoplankton genera with an abundance of less than 0.1% of the pond total or occurring only in
one pond were not included in the analyses except for calculating diversity. The Shannon–Wiener index
calculated at genus level was chosen as a diversity measure.
Averaged over the whole or part of the study period data were used in the multivariate tests to avoid a
blurring effect due to occasional shifts in phytoplankton biomass. Only samples taken during the warm part
of the year (May–September) were used in the data analysis as the samples taken during the cold season
were confounding the patterns observed in summer. Besides, cyanobacterial blooms, posing management
problems, occurred only in summer and early autumn.
A hierarchical cluster analysis (farthest-neighbour method) based on Sorensen distance measure (PC-
ORD 4.0; McCune and Mefford, 1999), and redundancy analysis (RDA, CANOCO 4.5; ter Braak and
Smilauer, 1998) were used to explore the phytoplankton data, and to estimate their relation to the measured
environmental variables. RDA analysis was performed on the data of 2004 and 2005 as the environmental
data collected during these two years were more complete than in 2002 and 2003 and these 2 years
represented the conditions before and after the biomanipulation of WtMl and VKn1.
To obtain reliable RDA results, the number of environmental variables should be less than the number of
the ponds included in the analysis (ter Braak and Smilauer, 1998). Therefore the variables showing poor
relationship with the phytoplankton data were excluded from the analysis. Phytoplankton data were log-
transformed. The automatic forward selection procedure was used to select the environmental variables
that contributed most to the explanation of the data.
Because phytoplankton data were not normally distributed even after transformation, phytoplankton
biomass corresponding to pond groups separated by cluster analysis, different vegetation types and the periods
before and after management intervention were compared using the nonparametric Kruskal–Wallis test.
RESULTS
All studied ponds were on average hypereutrophic according to the TP concentrations, whereas Chl a
concentrations covered the range from oligotrophy to hypereutrophy (Table 1; UNEP, 1999).
Phytoplankton biomass showed a clear gradient ranging from several to more than a 100 mm3 L1
(Figure 2). Except for TP increasing with the phytoplankton biomass, nutrient concentrations did not
exhibit any distinct pattern, although considerable temporal and inter-pond variability in nutrient
concentrations was observed (Table 1).
Cluster analysis of 2002–2005 phytoplankton data has constructed three groups of ponds (Figure 3). The
same three groups were constructed by the cluster analysis of different subsets of phytoplankton data. They
can also be outlined on the RDA biplots based on 2004 and 2005 data, except the shift of WtMl and VKn1
from Group 2 to Group 1 after biomanipulation in 2005 (Figure 4). The first two axes of the RDA explain
61.8% and 61.2% of the variation in the 2004 and 2005 phytoplankton data, respectively. The first axes
alone explain 48.3% and 51% (Table 2). The first axes roughly represent the total phytoplankton biomass,
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Figure 2. A gradient of total phytoplankton biomass over the sixteen studied ponds (2002–2005; UBV þ 1:5H5outlier5LBV 1:5H;
UBV þ 3H5extreme5LBV 3H; UBV } the upper value of the box; LBV } the lower value of the box, H ¼ UBV LBV).
Figure 3. Hierarchical cluster analysis results based on the averaged phytoplankton data with ‘farthest neighbour’ as group linkage
method and Sorensen distance as dissimilarity measure (2002–2005).
as indicated by the direction and length of the Secchi depth and Chl a arrows, sub-parallel to the axes, and
the arrangement of the ponds in order of phytoplankton biomass increase. The second axes roughly
correspond to the inverse maximum pond depth. The significant relation of Secchi depth with the
phytoplankton biomass and its orientation with regards to the Chl a arrows indicate that most of the
turbidity in the studied ponds is phytoplankton induced. Of all environmental variables used in the
analyses, only hydraulic retention time had a significant relationship with the phytoplankton data, and TP
was close to a significant level (Table 3). Nutrients explained less than half of the variance in phytoplankton
biomass explained by all environmental factors (21 out of 51% in 2004 and 21 out of 45% in 2005), which
suggests that factors other than nutrients are more important in phytoplankton growth control in the
studied ponds.
Comparison of the phytoplankton biomasses between the three pond groups using the Kruskal–Wallis
test revealed highly significant differences ðp50:01Þ between all groups. The four ponds of the first group
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Figure 4. Redundancy analysis biplots (sites and environmental variables) based on the averaged phytoplankton and environment
data for two consecutive years of the study period, before and after the biomanipulation of WtMl and VKn1 ð2004; 2005Þ: The
biomanipulated ponds shifted from Group 2 to Group 1 in 2005.
(Vbk1, Vbk2, Hoef, Tenr) were clear throughout the study period with the Secchi depth reaching the
bottom. They were characterized by low phytoplankton biomass (mostly below 1 mm3 L1; Figure 2) and,
on average, the lowest phytoplankton diversity. Despite very low phytoplankton biomass, submerged
macrophytes were observed only in Hoef and Tenr (Table 4) covering 60% to 80% of each pond area from
May to September. These two ponds also exhibited occasional profuse growth of green filamentous algae
that remained persistent throughout most of the warmer months of the year in some parts of these ponds,
although the quantity of filamentous algae varied from year to year. No submerged vegetation was
observed in Vbk1 and Vbk2, except for the short-lived but abundant late spring emergences of green
filamentous algae. The phytoplankton assemblages of this group of ponds were dominated by cryptophytes
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Table 2. Summary of the RDA analyses results (2004, 2005)
Axes 1 2 3 4 Total variance

2004
Eigenvalues: 0.483 0.135 0.085 0.064 1.000
Species–environment correlations: 1.000 1.000 1.000 1.000
Cumulative percentage variance
of species data: 48.300 61.800 70.200 76.600
of species–environment relationship: 48.300 61.800 70.200 76.600
Sum of all eigenvalues 1.000
Sum of all canonical eigenvalues 1.000
2005
Eigenvalues: 0.510 0.101 0.078 0.062 1.000
Species–environment correlations: 0.998 0.987 0.990 0.991
Cumulative percentage variance
of species data: 51.000 61.200 69.000 75.100
of species–environment relationship: 54.100 64.800 73.100 79.700
Sum of all eigenvalues 1.000
Sum of all canonical eigenvalues 0.943
Table 3. RDA forward selection results. Marginal effects show the variance explained by each environmental variable alone
(Lambda1); conditional effects show the significance of the addition of a given variable (p) and the stepwise cumulative variance
explained by all the selected variables in the model (LambdaA)
2004 2005
Marginal effects Conditional effects Marginal effects Conditional effects
Variable Lambda1 Variable LambdaA p Variable Lambda1 Variable LambdaA p
SD 0.43 SD 0.43 0.002 SD 0.44 SD 0.44 0.002
Chl a 0.33 RT 0.09 0.012 Chl a 0.28 RT 0.07 0.030
FA 0.30 Chl a 0.06 0.044 TP 0.21 TP 0.06 0.076
TP 0.24 TP 0.06 0.060 RT 0.18 MD 0.05 0.124
RT 0.22 NO2 0.05 0.102 FA 0.17 FV 0.05 0.228
SM 0.13 SM 0.04 0.256 SM 0.17 NO3 0.03 0.322
NH4 0.10 MD 0.04 0.208 SRP 0.14 FA 0.04 0.278
FV 0.08 SRP 0.03 0.264 NH4 0.12 Chl a 0.05 0.080
BF 0.07 FV 0.04 0.378 NO3 0.10 SRP 0.04 0.418
SRP 0.07 FA 0.03 0.262 FV 0.07 SM 0.03 0.402
NO3 0.06 NH4 0.03 0.424 MD 0.05 NO2 0.02 0.468
NO2 0.06 NO3 0.02 0.526 SiO2 0.06 SiO2 0.04 0.342
MD 0.05 SiO2 0.02 0.580 NO2 0.05 NH4 0.02 0.438
PF 0.04 BF 0.02 0.666
SiO2 0.03 PF 0.04 1.000
and diatoms with occasional increases in the density of chrysophytes, chlorophytes, euglenophytes and
cyanobacteria (Pseudanabaena spp. and Oscillatoria spp.) (Figure 5). Most of the phytoplankters were
flagellated or relatively small in size. Zooplankton communities of this group of ponds were represented by
larger forms (Figure 6), especially in May and June, when they were dominated by large cladocerans. This
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Table 4. Macrophyte species richness observed in the vegetated ponds in two consecutive years of the study period, before and after
the biomanipulation of WtMl and VKn1
WtMl VKn1 Hoef Tenr MlGr WPk1 TrBr RKl3 RKl5 Vbk1 Vbk2
June–September 2004
Chara spp. + + +
Ceratophyllum demersum +
Nitella sp. +
Potamogeton pectinatus + + +
Potamogeton pusillus + +
Lemna minor + +
Nuphar lutea + + +
Nymphaea alba +
Spirogyra spp. + + + + + + +
June–September 2005
Callitriche obtusangula +
Chara spp. + + + + +
Ceratophyllum demersum + +
Elodea nuttallii +
Nitella sp. +
Potamogeton pectinatus + + + + +
Potamogeton pusillus + + +
Ranunculus circinatus + +
Zannichellia palustris + +
Lemna minor + + +
Lemna trisulca +
Nuphar lutea + + + +
Nymphaea alba +
Riccia fluitans +
Spirogyra spp. + + + + + + +
group of ponds was characterized by low densities or absence of planktivorous and benthivorous fish and
the presence of pike and perch in the ponds with submerged macrophytic vegetation (Table 1).
The eight ponds forming the second group (MlGr, WtMl, RKl2, RKl3, RKl5, VKn1, VKn2, Malu) had
Secchi depths ranging between 0.5 and 1.7 m, phytoplankton biomass mostly below 20 mm3 L1 (Figure 2)
and, on average, intermediate diversity. Extended stands of submerged macrophytes (mainly P. pectinatus
and Chara spp.) with occasional patches of green filamentous algae were observed in MlGr. Green
filamentous algae were also common for the shallower parts of RKl5 and WtMl. In the latter, scarce growth
of P. pectinatus was observed before it was partially drained in 2004. The remaining five ponds have not
shown any submerged vegetation during the study period, except for VKn1 where submerged macrophytes
recovered after biomanipulation in 2005. Small pockets of floating-leaved vegetation were present in RKl3
and WtMl (Table 4). Phytoplankton assemblages of these ponds were composed of chlorophytes, diatoms,
cryptophytes and chrysophytes alternating in dominance with occasional appearances of euglenophytes,
dinophytes and cyanobacteria (Figure 5). The size of the phytoplankters as well as the ratio of flagellated to
non-flagellated forms varied a lot from pond to pond. Zooplankton communities of this group of ponds
were characterized by small cladocerans, copepods and rotifers with occasional rises in density of large
cladocerans mainly in the ponds located down the phytoplankton biomass gradient (MlGr, WtMl, RKl2,
RKl3; Figure 6). Ponds that were lower down the phytoplankton biomass gradient (MlGr, WtMl, RKl2,
RKl5) and higher up the gradient (VKn1, RKl3, VKn2, Malu) had variable densities of planktivorous and
benthivorous fish. Malu, RKl3 and RKl2 harboured pikeperch, catfish and pike, respectively (Table 1).
DOI: 10.1002/aqc
2002 2003
80 80
Total biovolume
60 60
(mm L ) 40 40
20 20
0 0
100% 100%
Relative biovolume
80% 80%
60% 60%
40% 40%
20% 20%
0% 0%
2004 2005
80 80
Total biovolume
60 60
(mm L )
40 40
20 20
0 0
100% 100%
Relative biovolume
80% 80%
60% 60%
40% 40%
20% 20%
0% 0%
Vbk1
Hoef
Vbk2
Tenr
VKn1
MlGr
WtMl
RKI2
RKl5
RKl3
VKn2
Malu
WPk2
WPk1
MlKl
TrBr
Vbk1
Hoef
Vbk2
Tenr
VKn1
MlGr
WtMl
RKI2
RKl5
RKl3
VKn2
Malu
WPk2
WPk1
MlKl
TrBr
Group 1 Group 2 Group 3 Group 1 Group 2 Group 3
Cyanobacteria Xanthophyta Euglenophyta Dinophyta

Chrysophyta Cryptophyta Bacillariophyta Chlorophyta
Figure 5. Relative and total phytoplankton biomass distribution along the phytoplankton gradient (averaged per year).
The four ponds of the third group (TrBr, MlKl, WPk1, WPk2) have invariably been turbid during the
warm parts of the study period. They were characterized by Secchi depths generally less than 1 m (often less
than 0.6 m), high phytoplankton biomass exceeding at times 50 mm3 L1, (Figure 2) and, on average, the
highest diversity. All of them have developed persistent cyanobacterial blooms (Planktothrix spp.,
Anabaena spp., Aphanizomenon spp., Microcystis spp., Gomphosphaeria spp.) during the study period, the
most severe in summer 2004. TrBr was less prone to cyanobacterial dominance than the other three ponds,
probably because of extensive floating-leaved vegetation. This is reflected in the results of RDA, which
positions it closer to the second group of ponds (Figure 4) characterized by mixed phytoplankton
composition. Chlorophytes and diatoms played an important role in the phytoplankton assemblages of
these ponds and often exceeded cyanobacteria numerically. Cryptophytes and chrysophytes, although
always present, were relatively less abundant (Figure 5). Large, often colonial, phytoplankters were more
common for this group of ponds than the smaller ones. Floating-leaved macrophytes (Table 4) were typical
for WPk1 and TrBr and were relatively scarce and patchy in the former and covered about half of the
surface of the latter in mid-summer. Neither submerged macrophytes nor green filamentous algae were
observed in these ponds. Zooplankton communities of this group of ponds were dominated by rotifers,
small cladocerans and copepods, mainly cyclopoids (Figure 6), with occasional appearances of large
cladocerans in WPk1 and WPk2. All these ponds harbour relatively high densities of planktivorous and
benthivorous fish; TrBr and WPk2 contain pikeperch (Table 1).
DOI: 10.1002/aqc
Figure 6. Relative zooplankton abundance distribution along the phytoplankton biomass gradient (averaged per year).
The first and the third groups of ponds separated by the cluster analysis correspond to the clear-water
and turbid states respectively. The ponds forming the second group showed intermediate phytoplankton
biomass levels (Figure 2) and because they looked neither clear nor turbid were classified as intermediate.
Cottenie et al. (2001) described a similar situation in a system of interconnected ponds in De Maten, north-
eastern Belgium.
During the cold months of the year the differentiation in phytoplankton biomass and composition
between different pond groups was much less distinct. The ponds with clearer water in the absence
of macrophytes and reduced zooplankton activity tended to increase their phytoplankton biomass
in early spring and autumn. The turbid and, to a lesser degree, intermediate ponds showed a
marked reduction in phytoplankton biomass due to decrease in solar radiation. Phytoplankton
assemblages shifted towards cryptophytes, diatoms and chrysophytes in all ponds, although
chlorophytes and cyanobacteria could persist in some turbid ponds in autumn and became uncommon
in winter and early spring.
Comparison of phytoplankton biomass corresponding to different vegetation types (Table 1) with the
Kruskal–Wallis test showed a highly significant difference ðp50:01Þ between the non-vegetated ponds and
ponds with mixed submerged vegetation or green filamentous algae alone. There was no significant
difference between the ponds with floating-leaved vegetation and non-vegetated ponds ðp > 0:05Þ;
or between the ponds harbouring green filamentous algae and those with mixed submerged vegetation
ðp > 0:05Þ:
DOI: 10.1002/aqc
Management intervention within the four pond ecosystems showed that removing or enhancing factors
controlling phytoplankton biomass might shift them towards the clear or turbid state without changing
external nutrient loadings. Short-term winter emptying of WtMl and VKn1 accompanied by a complete fish
removal led to a remarkable recovery of submerged macrophytes reaching 80% to 90% of the pond surface
cover the following summer. This also had a notable effect on macrophyte species richness. Virtually non-
vegetated during the first 3 years of the study period, these two ponds became the most species-rich in
summer 2005 (Table 4). The biomanipulation-induced revegetation resulted in a significant reduction in
phytoplankton biomass (p50.05) and marked increase in water transparency in both ponds. The result of
the RDA on 2005 phytoplankton and environment data confirms that these two ponds shifted to the group
of the clear-water ponds (Figure 4).
The regular removal of macrophytes from MlGr in mid-summer by the pond managers invariably led to
a significant increase in phytoplankton biomass (p50.05) and in 2002, 2004 and 2005 resulted in
cyanobacterial blooms dominated by Anabaena spp. and Mycrocystis spp. Cyanobacterial blooms might
have occurred in 2003, but the sampling frequency was not sufficient to register them.
Conversion of Malu from an overflow to a flow-through pond resulted in a visible improvement of water
quality (Brussels Institute of Environment } BIM/IBGE, pers. comm.) and although phytoplankton
biomass can still occasionally reach relatively high levels owing to the input of phytoplankton inocula from
the upstream ponds, cyanobacterial blooms were not observed in this pond during the 4-year study period.
DISCUSSION
All the ponds studied are rich in nutrients and therefore have the potential of becoming turbid owing to
high phytoplankton biomass } their normal stable state. Those ponds that are not turbid have deviated
from their stable state owing to the constraints posed on phytoplankton growth by factors other then
nutrient availability, such as the presence of submerged vegetation, low hydraulic retention time, greater
depth in combination with water column mixing, top-down phytoplankton control by grazers and
cascading effects of fish community structure.
Different combinations of these factors are characteristic of the three groups of ponds identified on the
basis of phytoplankton and environmental data analysis. All clear-water ponds are of flow-through type
and, except for Hoef, are characterized by low hydraulic retention time, shorter or comparable to the
generation time of some larger, slow-growing phytoplankton species. Consequently, they are selected
against, shifting the phytoplankton assemblages of these ponds towards smaller, fast-growing and motile
species such as cryptophytes, chrysophytes, small diatoms and chlorophytes. These species happen to be
more palatable to large cladocerans (Reynolds, 1984; Brönmark and Hansson, 1998) that dominate the
zooplankton communities of these ponds in May and June. This is the time of intensive growth of
submerged macrophytes and large zooplankters facilitate their growth by reducing the density of
phytoplankton competing for light and nutrients with them.
Pike and perch in Hoef and Tenr seem to be very efficient in controlling their planktivorous fish
populations (Table 1). No planktivorous fish were caught in Hoef, although some juvenile fish below the
mesh-size of the fishing gear were observed there. Dense submerged macrophytic vegetation of Hoef and
Tenr stabilizes the water column thus increasing sedimentation of larger non-motile phytoplankters
(Reynolds, 1984, 1998). It can also inhibit phytoplankton growth by allelopathic activity (Gross, 1999;
Gross et al., 2003) and shading (van Donk and van de Bund, 2002). Vbk1 and Vbk2 lack macrophytic
vegetation, most likely because of bird herbivory and shading by green filamentous algae (Irfanullah and
Moss, 2004). These ponds are very small in size and well sheltered by the surrounding forest from wind,
Vbk2 having an island in the middle. Their water columns should be very stable, leading to the increased
loss of non-motile phytoplankters to the sediments. The late spring emergence of green filamentous algae,
DOI: 10.1002/aqc
characteristic of these two ponds, coincided with the peaks in large cladoceran populations, which suggests
that aggregations of green filamentous algae serve as a shelter to zooplankters against fish and invertebrates
and thus contribute to maintaining the clear water. This is confirmed by the results of the comparison of
phytoplankton biomass corresponding to different vegetation types in the Kruskal–Wallis test. The ponds
with green filamentous algae showed significantly lower phytoplankton biomasses compared with the non-
vegetated ponds. It is difficult to tell which factor has greater impact on phytoplankton biomass when
several of them act together; only that different combinations of low hydraulic retention time, extensive
cover of submerged macrophytes and/or green filamentous algae, and high densities of large zooplankters
and piscivorous fish, prevented the development of high phytoplankton biomass in the clear-water ponds
despite high nutrient loadings.
Besides the lowest phytoplankton biomass, these ponds also showed the lowest average phytoplankton
diversity. This could be attributed in part to the scarce phytoplankton inocula due to their upstream
location. However, the fact that some other ponds that are mostly groundwater-fed and have no ponds
upstream (TrBr and WPk1) have shown high phytoplankton biomass and diversity suggests that other
factors are more important in their control than location relative to other ponds. Rather, the clear-water
ponds do not offer the conditions for the richer inocula to be established there.
The four turbid ponds have the opposite properties to those of the clear-water ponds described above. All
of them are of overflow type, which means that they are not connected, except for WPK1 and WPK2, and
are characterized by high retention times ranging from 20 to 39 days (Table 1). They also contain higher
densities of planktivorous and benthivorous fish and lack any submerged vegetation. The presence of
floating vegetation in some of them seems to have no effect on phytoplankton biomass, as indicated by the
comparison of the phytoplankton biomass corresponding to different vegetation types with the Kruskal–
Wallis test. They are generally larger, and are more open to wind. Given their low depth (51.5 m, mostly
51 m) and high densities of benthivorous fish, their water columns should be mostly well mixed. This
reduces phytoplankton loss caused by sinking. Because of high densities of planktivorous fish and lack of
shelter, zooplankton communities of these ponds are dominated by smaller forms having narrow food-size
range (Reynolds, 1984; Brönmark and Hansson, 1998). The lack of large zooplankton during late spring in
these ponds is probably partly responsible for the absence of macrophytic vegetation as it is outcompeted
by phytoplankton. This assumption is confirmed by the germination of submerged macrophytes from the
sediments of some turbid ponds in a laboratory experiment (Triest, unpublished data).
The presence of pikeperch in TrBr apparently has little effect on planktivorous fish populations. The
occasional appearance of large cladocerans in WPk2 suggests that the presence of piscivorous fish in this
pond has an effect on the fish community structure, biasing it towards older, larger fish not feeding on
zooplankton. Nevertheless, this does not seem to be enough to allow efficient zooplankton control of
phytoplankton.
Thus, the environmental conditions and fish community structures of the turbid ponds allowed large,
often colonial phytoplankters (mostly chlorophytes and cyanobacteria) to take advantage of high nutrient
concentrations and reach very high biomass. It appeared that in the second half of the summer this led to
nitrogen limitation, as indicated by the concurrent low nitrogen species concentrations and appearance of
heterocystous cyanobacteria (Anabaena spp. and Aphanizomenon sp.).
The remaining eight ponds, classified as intermediate, had the characteristics of both types of ponds
described above. Some of them had more similarities to the clear-water ponds, while others to the turbid
ones. Most of these ponds were characterized by the intermediate hydraulic retention times relative to the
clear-water and turbid ponds. MlGr, having high retention time, contained extended submerged
macrophytic vegetation, which, in combination with the lack of planktivorous fish, offset the effect of
very low flushing rate on phytoplankton biomass. Malu, with a very low retention time, is the last pond on
the Woluwe River receiving phytoplankton inocula from the upstream ponds. This is confirmed by the
occasional elevated concentrations of cyanobacteria similar in composition and concurrent with the
DOI: 10.1002/aqc
cyanobacterial blooms in TrBr and WPk2 located less then 2 km upstream (Figure 1), which otherwise have
no time to develop in a pond with hydraulic retention time of approximately 1 day (Reynolds, 1984). Thus,
the incoming inocula and the presence of planktivorous fish controlling the phytoplankton grazers
outweigh the effect of very low retention time, shifting the phytoplankton biomass just next to those of the
turbid ponds (Figure 2).
Some of the intermediate ponds (RKl2, RKl3 and to a lesser degree Malu) are more than 1.5 m deep over
a greater part of the surface they cover. Given their relatively large size and openness to wind, the mixed
depths of these ponds can exceed the euphotic depths of some algae, thus selecting against the non-motile or
non-shade-adapted phytoplankton species (Reynolds, 1984; Kallf, 2002). It can probably explain why RKl2
and RKl3 did not develop higher phytoplankton biomass despite relatively high hydraulic retention time,
high densities of planktivorous and benthivorous fish, and absence of submerged vegetation.
Some of these ponds harboured extensive growth of green filamentous algae, which seem to have a
negative effect on phytoplankton growth, although not as strong as that of submerged macrophytes. That is
probably due to the predominantly benthic nature of filamentous algae and their confinement to the
shallower parts of ponds leaving the deeper parts largely unaffected.
Phytoplankton assemblages of the intermediate ponds differed considerably from pond to pond as a
result of the difference in habitat conditions. The assemblages were composed of a mix of different
phytoplankton groups competing for dominance. In summer, chlorophytes, diatoms and cryptophytes
played an important role in all of them, while cyanobacteria were hardly present.
Occasional appearances of large cladocerans against a background of zooplankton communities
dominated by smaller forms were characteristic of these ponds, but they rarely reached the levels observed
in the clear-water ponds and mostly occurred in the ponds tending towards clear water.
It seems that the combinations of factors inhibiting and favouring phytoplankton growth led to
intermediate phytoplankton biomass in this group of ponds. Relative importance of one factor type over
another determined whether they were closer to the clear or the turbid state. Dense stands of submerged
macrophytes, once established, could maintain clear water in Hoef and Tenr. MlGr, a pond with extensive
submerged macrophyte cover, was classified as intermediate owing to the regular removal of macrophytes
by managers in mid-summer. Macrophyte removal invariably resulted in phytoplankton biomass increase
and in 2002, 2004 and 2005 in the development of cyanobacterial blooms dominated by potentially toxic
genera, making the pond unsuitable for recreation. This case shows the importance of submerged
macrophytes for the maintenance of the clear-water state and the risks posed by management driven
primarily by public amenity concerns and ignoring ecosystem integrity.
The three groups of ponds were stable during the 4-year study period. No pond shifts from one group to
another were observed except for the WtMl and VKn1 that shifted to the clear-water state as a result of
drainage and fish removal. The clear and turbid ponds studied roughly correspond to the two alternative
stable states described by Scheffer et al. (1993) except that they occur at comparable nutrient loadings.
However, half of the studied ponds exhibiting intermediate phytoplankton biomass levels imply a gradient
rather than a ‘jump’ from one state to the other. This situation corresponds better to the three alternative
equilibria concept proposed by Scheffer (1998) with aquatic vegetation, mixed phytoplankton and
cyanobacterial dominance, respectively, suggesting that at least for ponds and small lakes the identification
of an intermediate state is justified. It should be noted though that Scheffer considered that the three
alternative stable states are more likely to occur in ‘somewhat deeper lakes’ whereas very shallow lakes would
have only vegetation or cyanobacterial dominance. This apparent contradiction can probably be explained by
the fact that in large shallow lakes, like those treated by Scheffer (1998), factors such as hydraulic retention
time or profuse growth of green filamentous algae are much less important than in the small lakes and ponds
where they can produce a similar effect on phytoplankton growth to that of greater depth.
These results also show that phytoplankton biomass is poorly related to nutrient concentrations when
nutrient loadings are high. TP concentrations, on average, are well above the proposed critical value of
DOI: 10.1002/aqc
150 mg L1 (Jeppesen et al., 1997), confirming the finding of Moss et al. (1996) that the alternative stable
states can exist over a much wider range of TP concentrations.
Therefore, in agreement with Carpenter et al. (1996, 2001), Reynolds (1998), Nydick et al. (2003) and
Sndergaard et al. (2005) we consider that determining the controls on phytoplankton biomass and
composition in ponds and small lakes should not be confined to the nutrients available but should take into
account a number of factors. The environmental factors dealt with in this study can be split into two
groups: those leading to low phytoplankton biomass and clear-water state } low hydraulic retention time,
dense submerged macrophyte and/or green filamentous algal growth, high densities of large zooplankters
and piscivorous fish, mixed depth exceeding euphotic depth } and those leading to high phytoplankton
biomass and turbid state } high hydraulic retention time, high densities of planktivorous and benthivorous
fish, exposure to wind in combination with low depth and input of phytoplankton inocula from upstream
water bodies. When nutrients are not limiting, it is the interplay of these factors that determines the
ecological make-up of a pond or a small lake.
Although a number of other factors negatively affect phytoplankton biomass, submerged macrophytes
seem to be crucial for the maintenance of the clear-water state and prevention of cyanobacterial blooms in
shallow eutrophic water bodies. Their revegetation with submerged macrophytes has proved to be essential
for the restoration of their ecological quality. Hydraulic retention time is another very important factor for
small water bodies. The modification of the hydraulic regime of a pond or a small lake in order to reduce
the retention time below the generation time of bloom-forming cyanobacteria can prevent the occurrence of
potentially toxic blooms when an adequate reduction in nutrient loading is not feasible. Profuse growth of
green filamentous algae, although an indicator of degraded ecological quality due to eutrophication
(Irfanullah and Moss, 2004), might be considered as a preferred state to that of phytoplankton dominance.
Maintenance of a balanced trophic structure through fish community manipulation can enhance the effects
of other factors.
Because restoration of small lakes and ponds subjected to diffuse sources of pollution is a very long
process (Carpenter, 2005) the water bodies affected by eutrophication should be managed in such a way
that a clear-water or, at least, an intermediate state is maintained. This can be achieved by enhancing the
role of biotic and abiotic factors having a negative effect on phytoplankton biomass. The identification of
the main driving forces operating in a particular ecosystem is essential for choosing an appropriate strategy
for management, restoration or biodiversity conservation in ponds and small lakes. This approach cannot
reverse eutrophication, though; it can only mitigate some of its consequences.
ACKNOWLEDGEMENTS
The authors thank the Brussels Institute for Promotion of Scientific Research and Innovation (IWOIB) for financing
the research grants of Dr Samuel Teissier (Research in Brussels Action 2002) and Anatoly Peretyatko (Prospective
Research for Brussels 2002–2005). We also thank Helmuth Van Pottelbergh, Lea Katherine Acera and Paola Eulalio
for their participation in the collection of zooplankton and fish data. The Brussels Institute of Environment (BIM/
IBGE) provided interesting data on the pond use and management. Two anonymous reviewers provided very useful
comments and suggestions.
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DOI: 10.1002/aqc

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AQUATIC CONSERVATION: MARINE AND FRESHWATER ECOSYSTEMS

Aquatic Conserv: Mar. Freshw. Ecosyst. 17: 584–601 (2007)

Phytoplankton biomass and environmental factors over a

ANATOLY PERETYATKOa,*, SAMUEL TEISSIERb, JEAN-JACQUES SYMOENSa

Received 12 October 2005; Accepted 2 April 2006

Copyright # 2006 John Wiley & Sons, Ltd.

Sampling and sample processing

Copyright # 2006 John Wiley & Sons, Ltd.

0.07–0.40 0.00–0.05 0.024–0.21 0.011–0.24 0.02–4.39 5.51–27.24 25.7–242 0.7–1 1.1–2.1

Aquatic Conserv: Mar. Freshw. Ecosyst. 17: 584–601 (2007)

Table 2. Summary of the RDA analyses results (2004, 2005)

Axes 1 2 3 4 Total variance

Cyanobacteria Xanthophyta Euglenophyta Dinophyta

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