Effects of Exposed Artiﬁcial Substrate on the
Competition between Phytoplankton and Benthic
Algae: Implications for Shallow Lake Restoration
Hu He 1, *, Xuguang Luo 2, Hui Jin 3, Jiao Gu 1,4, Erik Jeppesen 5,6, Zhengwen Liu 1,6,7 and
Kuanyi Li 1, 6, *
1State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology,
Chinese Academy of Sciences, Nanjing 210008, China; email@example.com (J.G.); firstname.lastname@example.org (Z.L.)
2College of Animal Science, Inner Mongolia Agricultural University, Huhhot 010018, China;
School of Environmental and Civil Engineering, Jiangnan University, Wuxi 214122, China; email@example.com
4University of Chinese Academy of Sciences, Beijing 100049, China
5Department of Bioscience, Aarhus University, 8600 Aarhus, Denmark; firstname.lastname@example.org
6Sino-Danish Centre for Education and Research, Beijing 100049, China
7Department of Ecology and Institute of Hydrobiology, Jinan University, Guangzhou 510632, China
*Correspondence: email@example.com (H.H.); firstname.lastname@example.org (K.L.);
Tel.: +86-25-8688-2237 (H.H.); +86-25-8688-2179 (K.L.)
Academic Editor: Miklas Scholz
Received: 24 October 2016; Accepted: 30 December 2016; Published: 4 January 2017
Phytoplankton and benthic algae coexist in shallow lakes and the outcome of the
competition between these two photoautotrophs can markedly inﬂuence water clarity. It is well
established that exposed artiﬁcial substrate in eutrophic waters can remove nutrients and ﬁne particles
from the water column via the attached periphyton canopy. However, the effects of the introduction
of artiﬁcial substrate on the competition between planktonic and benthic primary producers remain
to be elucidated. We conducted a short-term outdoor mesocosm experiment to test the hypothesis
that the nutrient and light changes induced by exposed artiﬁcial substrate (polythene nets) would
beneﬁt the benthic algae. Artiﬁcial substrate signiﬁcantly reduced total nitrogen and phosphorus
concentrations and water clarity improved, the latter due to the substrate-induced reduction of both
organic and inorganic suspended solids. Consequently, as judged from changes in chlorophyll a
(Chl-a) concentrations in water and sediment, respectively, exposed artiﬁcial substrate signiﬁcantly
reduced the phytoplankton biomass, while benthic algae biomass increased. Our results thus indicate
that exposed artiﬁcial substrate may be used as a tool to re-establish benthic primary production in
eutrophic shallow lakes after an external nutrient loading reduction, paving the way for a benthic- or
a macrophyte-dominated system. Longer term and larger scale experiments are, however, needed
before any ﬁrm conclusions can be drawn on this.
Keywords: artiﬁcial substrate; phytoplankton; benthic algae; resource competition; shallow lakes
Shallow lakes may exist in one of two alternative states—a clear state with an abundant community
of submerged macrophytes and a turbid state characterized by high phytoplankton biomass [
However, in shallow clear water lakes where submerged macrophytes are absent, benthic algae
(epipelon) may dominate primary production and help to maintain a clear water state [2–4].
Light and nutrients are fundamental factors impacting the relative contribution of planktonic
and benthic algae to total primary production in shallow lakes [
]. Excessive nutrient loading often
Water 2017,9, 24; doi:10.3390/w9010024 www.mdpi.com/journal/water
Water 2017,9, 24 2 of 9
boosts the growth of phytoplankton, resulting in reduced light penetration and, with it, decreases in
benthic algae biomass [
]. Moreover, loss of benthic algae promotes phytoplankton growth through
reduced competition for nutrients and enhanced nutrient release from the sediment [
benthic algae often beneﬁt from the enhanced water clarity and decrease the availability of nutrients
for phytoplankton in the overlying water by consuming the resources that these require for growth
and indirectly also by immobilizing nutrients within sediments .
Despite a large reduction of the external nutrient loading for the purpose of restoration of
shallow eutrophic lakes, benthic primary producers may take time to recover due to competition by
excessively growing planktonic algae [
], caused by high internal loading and an unfavorable food
web structure [
]. The introduction of exposed artiﬁcial substrate may promote the production
of benthic algae competing with phytoplankton due to changes in nutrient and light conditions
through periphyton colonization on the surface of the artiﬁcial substrate (hereafter referred to as
‘periphyton’). Firstly, periphyton assemblages can remove nutrients, especially phosphorus, from the
water column [
], which may competitively reduce phytoplankton growth [
]. For instance,
Jöbgen et al. (2004) studied the potential of periphyton for phosphorus removal on polypropylene (PP)
ﬂeece in Lake Fühlinger in Cologne, Germany, and found that up to ca. 100 mg total phosphorus was
bound per m
PP-ﬂeece after four months of exposure [
]. Secondly, the periphyton canopy has the
potential of retaining suspended solids in the water column via changes in ﬂow hydraulics or direct
particle trapping and adhesion [
]. For instance, Battin et al. (2003) showed that some forms of
photosynthetically active periphyton produce a ‘sticky’ exopolysaccharide (EPS) matrix that has been
shown to enhance particle deposition [
]. Benthic algae may therefore beneﬁt from enhanced light
penetration via the removal of suspended particles. To date, the effects of exposed artiﬁcial substrate on
nutrient removal and/or particle retention in lakes and rivers are well studied [
the impact of the introduction of artiﬁcial substrate on the competition between pelagic and benthic
primary production remains to be elucidated.
In this study, outdoor mesocosms were used to explore the effects of periphyton on the competition
between planktonic and benthic algae in eutrophic waters mediated by the introduction of artiﬁcial
substrate. We hypothesized that periphyton would reduce nutrient concentrations and enhance water
clarity. The changes in nutrient and light conditions would reduce phytoplankton growth, whereas the
growth of benthic algae would be favored due to the improved light climate.
2. Materials and Methods
The outdoor mesocosm experiment was conducted at the Taihu Lake Laboratory Ecosystem
Research Station (TLLER), which is located in Meiliang Bay, the northern part of Lake Taihu, China
(Figure 1). Lake Taihu is a large (surface area: 2338 km
), shallow (mean depth: 2 m), and hypertrophic
freshwater lake which has suffered severe cyanobacterial blooms (dominated by Microcystis spp.) in
the last two decades [
]. Our experiment was conducted from 5 October 2014 to 11 November 2014.
According to the meteorological data obtained from TLLER, average water temperature in both months
C (Range: 12–20
C). Average wind speed at the site was measured twice, being 2.9 m/s on
14 October and 0.15 m/s on 15 November.
2.1. Experimental Design
Eight cylindrical, high-density polyethylene tanks (depth: 60 cm; upper diameter: 50 cm; bottom
diameter: 40 cm) were placed on the lake shore. Each tank was ﬁlled with a 5 cm layer of sediment
and 70 L water collected from Meiliang Bay. The sediments had previously been sieved (mesh size:
1.7 mm) to remove large invertebrates and mixed to ensure uniformity. The water was screened using
a 64 µm mesh ﬁlter to remove crustacean zooplankton and inorganic particles.
Water 2017,9, 24 3 of 9
Location of Lake Taihu in China (the solid dot shows Taihu Lake Laboratory Ecosystem
Research Station (TLLER) where the mesocosm experiment was conducted).
The artiﬁcial substrates used in the experiment were cylindrical-shaped (40 cm height
diameter) polythene nets with a mesh size of 3 mm. We chose this material not only because it was
a substratum well suited for periphyton settlement [
], but also because it does not affect nutrient
diffusing as do conventionally used artiﬁcial substrates, such as plastic sheets or glass slides. To initiate
the experiment, artiﬁcial substrate was randomly added to four mesocosms. Each tank contained
one net with a total surface area of 0.75 m
of the polythene net exposes 2 m
The artiﬁcial substrates extended through the entire water column and were vertically ﬁxed in the
sediment. The remaining four mesocosms without artiﬁcial substrate functioned as controls.
2.2. Sampling and Analytical Methods
In the morning of day 0 (5 October), 4, 8, 12, 16, 20, 28, and 36 of the experiment, in situ turbidity
was measured in each mesocosm at 20 cm water depth using a YSI 9500 Photometer (YSI, Inc.,
Yellow Springs, OH, USA). After that, a small (1 L) depth-integrated water sample was collected from
each mesocosm using a tube sampler (8 cm diameter, 64 cm length). The water samples were then
analyzed in the laboratory for nutrients, suspended solids, and chlorophyll a(Chl-a).
Total suspended solids (TSS) were determined from 200 to 400 mL water samples ﬁltered through
pre-weighed glass ﬁber ﬁlters (GF/C, Whatman International Ltd., Maidstone, UK), which had
been pre-combusted at 450
C for 2 h. The ﬁlters were then dried to a constant weight at 60
for 48 h. After determining TSS, the ﬁlters were combusted in a mufﬂe furnace at 550
C for 2 h,
then cooled in a desiccator, and ﬁnally weighed to determine the inorganic suspended solid (ISS)
concentration. We calculated the organic fraction (OSS) by subtracting ISS from TSS. Total nitrogen
(TN), total phosphorus (TP), total dissolved nitrogen (TDN), and total dissolved phosphorus (TDP)
concentrations were measured according to Chinese standard methods [
]. The Chl-aconcentration
was measured spectrophotometrically from the matter retained on a GF/C ﬁlter after extraction in
a 90% (v/v) acetone/water solution for 24 h . We did not correct for phaeophytin interference.
Water 2017,9, 24 4 of 9
At the end of the experiment (day 36), after the ordinary water sampling, periphyton on the
artiﬁcial substrate and benthic algae were sampled in each mesocosm. For periphyton, each artiﬁcial
substratum was carefully removed, and a vertical 5 cm wide and 35 cm deep strip (from top to
sediment surface area) was cut from each substratum and immediately enclosed in a black zip-lock bag.
In the laboratory, the attachments on both sides of the strip were carefully brushed off into a beaker
with distilled water, mixed thoroughly, and divided equally into two subsamples. One subsample
(100–200 mL) was ﬁltered through pre-weighed, pre-combusted (4 h at 450
C) GF/C ﬁlter and
dried at 105
C for 2 h in order to determine periphyton dry weight, and the other subsample was
used to determine the periphyton Chl-aconcentration of the attachments using the method of water
Chl-ameasurement. For benthic algae sampling, sediments in the center of each mesocosm were
sampled in a small transparent tube (diameter: 2 cm). The upper 0–1 cm sediments were collected
and subsequently ﬁltered through a GF/C ﬁlter. The Chl-aconcentration of benthic algae was also
determined by spectrophotometry without correction for phaeophytin interference, as described above.
At the end of the experiment, the total biomasses of phytoplankton and benthic algae in each
mesocosm were calculated. Total phytoplankton biomass was obtained by multiplying the water Chl-a
concentration by the volume of the water column, total benthic algal biomass by multiplying the Chl-a
concentration of benthic algae by the surface area of the sediment, and total algae biomass by summing
up the total phytoplankton biomass and the total benthic algae biomass. The relative proportions of
phytoplankton and benthic algae to the total algal biomass were then calculated.
Repeated measures analysis of variance (rANOVA) was applied to compare the differences
) in nutrients, suspended solids, and Chl-aconcentrations between the mesocosms with and
without artiﬁcial substrate. Benthic algae were only sampled once. Subsequently, differences in benthic
algae Chl-aconcentrations between the treatments were compared using Student’s t-test (p< 0.05).
When necessary, data were log10 transformed to ensure normality of distribution and homogeneity
of variance before analysis. All statistical analyses were performed with the statistical package SPSS
version 16.0 (IBM Corporation, Somers, NY, USA).
3.1. Nutrients and Turbidity
In mesocosms with artiﬁcial substrate, periphyton dry weight and Chl-aconcentration were
, respectively. The concentrations of TN and TP were both signiﬁcantly
lower in the mesocosms with artiﬁcial substrate than in the substrate-free controls (Table 1; Figure 2a,b),
whereas no signiﬁcant differences were found in dissolved nutrients (TDN and TDP) (Table 1;
Results of Analysis of Variance for repeated measures (rANOVA) for turbidity, suspended
solids, nutrients, and Chl-aof phytoplankton between treatments with and without artiﬁcial substrate.
Artiﬁcial Substrate Time Interaction
F DF pF DF pF DF p
TN 121.86 1 <0.001 299.75 7 <0.001 13.44 7 <0.001
TP 41.57 1 0.003 118.95 7 <0.001 13.71 7 <0.001
TDN 11.43 1 0.015 282.03 7 <0.001 1.15 7 0.352
TDP 11.47 1 0.028 96.71 7 <0.001 9.47 7 0.006
Turb 13.26 1 0.011 29.38 7 <0.001 4.12 7 0.044
TSS 30.12 1 0.002 22.77 7 <0.001 6.89 7 0.012
OSS 61.19 1 <0.001 20.18 7 <0.001 8.59 7 <0.001
ISS 7.71 1 0.038 24.13 7 <0.001 2.77 7 0.095
Chl-a39.18 1 0.001 50.74 7 <0.001 8.32 7 0.002
Notes: TN = total nitrogen; TP = total phosphorus; TDN = total dissolved nitrogen; TDP = total dissolved
phosphorus; Turb = turbidity; TSS = total suspended solids; ISS = inorganic suspended solids; OSS = organic
suspended solids; Chl-a= chlorophyll aof phytoplankton; F = F value; DF = degree of freedom; p=pvalue.
Water 2017,9, 24 5 of 9
Comparisons of concentrations of (
) total nitrogen (TN); (
) total phosphorus (TP); (
dissolved nitrogen (TDN); and (
) total dissolved phosphorus (TDP) between treatments with and
without artiﬁcial substrate during the experiment.
Artiﬁcial substrate signiﬁcantly reduced the turbidity in the water column, turbidity being twice
as high in the controls as in the artiﬁcial substrate mesocosms at the end of the experiment (Table 1;
Figure 3a). Periphyton on artiﬁcial substrate also signiﬁcantly reduced the concentrations of suspended
solids, TSS (Figure 3b), OSS (Figure 3c), and ISS (Figure 3d) (Table 1).
Comparisons of (
) turbidity; (
) total suspended solids (TSS); (
) organic suspended solids
(OSS); and (
) inorganic suspended solids (ISS) concentrations between treatments with and without
artiﬁcial substrate during the experiment.
Water 2017,9, 24 6 of 9
3.2. Biomass of Phytoplankton and Benthic Algae
Addition of artiﬁcial substrate signiﬁcantly reduced the phytoplankton biomass, with water
Chl-aconcentrations being signiﬁcantly lower in the artiﬁcial substrate mesocosms than in the control
mesocosms (Table 1; Figure 4a). For instance, at the end of the experiment, water Chl-aconcentrations
were ﬁve times higher (30.57
g/L) in the control treatment than in the artiﬁcial substrate
g/L) (Figure 4a). In contrast, the Chl-aconcentrations of benthic algae were
signiﬁcantly lower in the control mesocosms (1.23
) than in the mesocosms with artiﬁcial
substrate (4.00 ±0.37 µg/cm2) (t-test, F(1,5) = 79.00; p= 0.001; Figure 4b).
Comparison of chlorophyll a(Chl-a) concentrations of (
) phytoplankton; and (
algae at the end of experiment with and without artiﬁcial substrate.
In addition to the changes in overall abundance, the relative proportions of phytoplankton
and benthic algae of total algal biomass varied between treatments (Figure 5). Artiﬁcial substrate
signiﬁcantly increased the proportions of benthic algae (from 46.6% to 93.3%) (Figure 5).
Contribution of phytoplankton and benthic chlorophyll a(Chl-a) to total biomass in the two
treatments by the end of the experiment.
Water 2017,9, 24 7 of 9
As expected, the artiﬁcial substrate signiﬁcantly reduced nutrient concentrations (Figure 2) and
the biomass of phytoplankton (Figure 4a) while water clarity increased (Figure 3a), as did the biomass
of benthic algae (judged from changes in Chl-a) (Figure 4b). Artiﬁcial substrate may therefore pave the
way for a benthic-dominated or in the longer term a macrophyte-dominated system via changes in
water chemical–physical conditions.
We found signiﬁcantly lower nitrogen and phosphorus concentrations in the mesocosms with
artiﬁcial substrate than in the controls (Figure 2a,b). Similarly, Vymazal (1988), studying the nutrient
removal efﬁciency of periphyton communities on nylon screens in polluted streams, found high
maximum efﬁciencies of ammonium and orthophosphate removal (80% and 70%, respectively) [
Also Adey et al. (1993), Dodds (2003), and Jöbgen et al. (2004) recorded that exposed artiﬁcial
substrate in lakes or streams removed a large amount of phosphorus from the water column [
However, in our study, dissolved nutrient levels (TDN and TDP) did not differ signiﬁcantly between
the treatments (Figure 2c,d), possibly reﬂecting a rapid uptake of accessible inorganic nutrients by the
primary producers in the mesocosms.
Artiﬁcial substrate also resulted in lower concentrations of particulate organic and inorganic
particles and thereby improved the water clarity (Figure 3a). Others, for example Sansone et al.
(1998), Battin et al. (2003), and Salant et al. (2011), have shown that periphyton captured or trapped
ﬁne particles by modifying shear stress and surface adhesion [
]. The lower OSS concentration
(Figure 3c) in the artiﬁcial substrate mesocosms may in part reﬂect a lower phytoplankton biomass
(Figure 4a). Moreover, we also calculated non-algal organic suspended solids by subtracting the
contribution of phytoplankton to OSS (using a conversion factor from Jeppesen et al., 2003 [
Furthermore, non-phytoplankton OSS was also signiﬁcantly lower than in the controls (data not
shown), indicating that artiﬁcial substrate also decreases the amount of other organic particles, such as
detritus, in the water column. The observed decrease in inorganic particles (ISS) in the mesocosms with
artiﬁcial substrate (Figure 3d) may be attributed to the adhesion effect [
] exerted by the periphyton
canopy (Figure 4b). Supporting this view, in a study exploring the inﬂuence of streambed periphyton
on particle deposition and inﬁltration using a series of ﬂume experiments, all periphytic diatom surface
samples were found to have signiﬁcantly higher inorganic contents than non-periphyton surfaces [
We found a lower phytoplankton biomass in the mesocosms with artiﬁcial substrate (Figure 4a)
than in the controls, likely reﬂecting the reduced nutrient concentrations (Figure 2). Concurrently with
the subsequently lower turbidity in these mesocosms, Chl-ain the sediment was higher and the share
of algae in the sediment substantially higher than in the controls (Figure 4b). By being able to take
up nutrients from sediments, benthic algae are favored when water clarity is high [
]. However, we
cannot exclude that part of the higher Chl-ain the sediment in the mesocosms with artiﬁcial substrate
derived from settling of periphytic material. Such material, when continuing growth on the sediment,
is expected to reduce also the phosphorus release from the sediment as well as phytoplankton growth.
Our study has limitations. Firstly, the experimental period only covered one season—the autumn.
The growth rate for phytoplankton in this season may be lower than in summer. However, in
subtropical Lake Taihu, previous studies have shown phytoplankton to grow actively in October [
Secondly, we did not add nutrients during the experiment period, which resulted in signiﬁcant declines
in TN and TDN (Figure 1). Nonetheless, the ﬁnal TN and TDN concentrations in the treatment with
artiﬁcial substrate were 0.88 and 0.70 mg
, respectively. The high TDN levels, moreover, indicate
that the decreased growth of phytoplankton in the mesocosms with artiﬁcial substrate was not caused
by insufﬁcient N for growth. Finally, our experiment was of short-term duration, covering a build-up
phase of periphyton. Whether the effect will be maintained if the artiﬁcial substrate be exposed for
longer time is unclear and warrants further studies.
Measures taken to restore shallow eutrophic lakes frequently involve attempts to re-establish
benthic primary producers, especially submerged vegetation [
]. Prior to such restoration,
improvement of water physical–chemical conditions, for instance light (+) and nutrient levels (
Water 2017,9, 24 8 of 9
recommended. Our study revealed that exposed artiﬁcial substrate in eutrophic waters signiﬁcantly
reduced nutrient levels and enhanced water clarity in the water column. These changes led to enhanced
benthic algae growth and reduced phytoplankton biomass. Additionally, artiﬁcial substrate exposed
in eutrophic waters may also have other effects reinforcing a shift to the clear-water state. For instance,
studies from temperate lakes have shown artiﬁcial plant beds to act as a daytime refuge for large-bodied
]. Other studies have demonstrated that artiﬁcial plants substantially increased
macroinvertebrate food resources for piscivorous ﬁsh, for instance perch (
Perca ﬂuviatilis L.
Thus, when combining the results of these studies with ours, we conclude that introduction of artiﬁcial
substrate may be a valuable restoration tool in shallow eutrophic lakes after an external nutrient loading
reduction in order to speed up recovery and the establishment of natural submerged macrophyte beds.
However, the small scale and short duration of our experiment obviously prevent a direct transfer of
our results to the whole-lake level. Thus, large-scale and long-term experiments are required before any
ﬁrm conclusions can be drawn about the usefulness of artiﬁcial substrate as a lake restoration method.
The authors wish to express their gratitude to Xiaoxia Chen and Ruijie Shen for ﬁeld and
laboratory support and to Anne Mette Poulsen for language assistance. This study was supported by the
National Science Foundation of China (31500379, 31370477 and 41571086), by the MARS project (Managing
Aquatic ecosystems and water Resources under multiple Stress) funded under the 7th EU Framework Programme,
Theme 6 (Environment including Climate Change), Contract No. 603378 (http://www.mars-project.eu), and
CLEAR (a Villum Kann Rasmussen Centre of Excellence project).
Hu He, Xuguang Luo and Kuanyi Li designed the study, Hu He, Jiao Gu and Hui Jin
undertook the sampling, Hu He, Erik Jeppesen, Kuanyi Li and Zhengwen Liu conducted the data analyses and
wrote the paper.
Conﬂicts of Interest: The authors declare no conﬂict of interest.
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