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Submerged macrophyte
self-recovery potential
behind restoration treatments:
sources of failure
MichałRybak
1
*, Joanna Rosin
´ska
2
,Łukasz Wejnerowski
3
,
Maria A. Rodrigo
4
and Tomasz Joniak
1
1
Department of Water Protection, Institute of Environmental Biology, Faculty of Biology, Adam
Mickiewicz University, Poznan
´, Poland,
2
Department of Environmental Medicine, Poznan University of
Medical Sciences, Poznań, Poland,
3
Department of Hydrobiology, Institute of Environmental Biology,
Faculty of Biology, Adam Mickiewicz University, Poznan
´, Poland,
4
Integrative Ecology Group,
Cavanilles Institute of Biodiversity and Evolutionary Biology, University of València, Paterna, Spain
When exploring the challenges of restoring degraded lakes, we often do not
observe the expected results despite executing all planned activities. Our study
elucidates the reasons that impede the recovery of submerged macrophytes
despite ameliorated light conditions. When prolonged lake degradation occurs,
subsequent efforts to increase light availability often prove insufficient, resulting in
a persistent turbid water state. In this study, we attempted to determine the
reasons for these failures through a germination test and propagule bank analysis
conducted in bottom sediments from a severely degraded lake, which underwent
restoration. Although the bottom sediments indicate relative potential in the
number of oospores and seeds, their germination efficacy remained dismally
low. Based on the germination test results and factors affecting the development
of submerged macrophytes (physical and chemical parameters, lake morphology),
we stated that improvement of light conditions in the lake could be insufficient to
recover the vegetation, especially when the potential to renew diverse plant
communities from sediments naturally is low. Our findings advocate for a
paradigmatic shift in lake restoration strategies. A holistic approach that includes
propagule bank assessments before embarking on restoration initiatives and
enabling the identification of macrophyte resurgence potentials is
recommended. We also advocate for a multifaceted restoration framework,
emphasizing the indispensability of augmenting natural recovery mechanisms
with targeted interventions. Consequently, in some cases, macrophyte
reintroduction could be the only solution. By reintroducing autochthonic species
to site-specific ecological dynamics, we anticipate an increased success rate in
restituting submerged vegetation, thus catalyzing ecological regeneration within
degraded lake ecosystems.
KEYWORDS
aquatic plant self-recovery, propagule bank, germination test, lakes eutrophication,
lakes restoration
Frontiers in Plant Science frontiersin.org01
OPEN ACCESS
EDITED BY
Marcin Zadworny,
Poznan
´University of Life Sciences, Poland
REVIEWED BY
Irmgard Blindow,
University of Greifswald, Germany
Alice Dalla Vecchia,
University of Parma, Italy
*CORRESPONDENCE
MichałRybak
m.rybak@amu.edu.pl
RECEIVED 22 April 2024
ACCEPTED 27 June 2024
PUBLISHED 16 July 2024
CITATION
Rybak M, Rosin
´ska J, Wejnerowski Ł,
Rodrigo MA and Joniak T (2024) Submerged
macrophyte self-recovery potential behind
restoration treatments: sources of failure.
Front. Plant Sci. 15:1421448.
doi: 10.3389/fpls.2024.1421448
COPYRIGHT
©2024Rybak,Rosin
´ska, Wejnerowski, Rodrigo
and Joniak. This is an open-access article
distributed under the terms of the Creative
Commons Attribution License (CC BY). The
use, distribution or reproduction in other
forums is permitted, provided the original
author(s) and the copyright owner(s) are
credited and that the original publication in
this journal is cited, in accordance with
accepted academic practice. No use,
distribution or reproduction is permitted
which does not comply with these terms.
TYPE Original Research
PUBLISHED 16 July 2024
DOI 10.3389/fpls.2024.1421448
1 Introduction
For several decades, eutrophication has constituted one of the
threats caused by human activity; turbid water, cyanobacteria
blooms, and loss of biodiversity are among the main symptoms
visible in many lake ecosystems around the world that experience
increased anthropogenic pressure (Sand-Jensen et al., 2017;
Klimaszyk and Gołdyn, 2020). Lake eutrophication also leads to
the disappearance of submerged plants and macroalgae (Hilt et al.,
2006;Ozinga et al., 2009). As a result, the lake’s clear-water state
with macrophytes dominance collapses, confronting high turbidity
caused by phytoplankton or competition with free-floating plants
(Scheffer et al., 1993;Meijer, 2000). Macrophytes play an essential
role in the mobilization, transport, and accumulation of nutrients,
and physical stabilization of bottom sediments. They are a source of
food and refuge for macroinvertebrates, zooplankton, and
fish (Short et al., 2016;Brzozowski et al., 2022). The limitation of
macrophyte occurrence to a rush belt (helophytes) is a characteristic
feature of degraded lakes (Kolada, 2016). The lack of bottom
sediment insulation due to submerged plant disappearance
intensifies the resuspension of sediments, and the biogenic
substances are released from substrates into the water column,
further accelerating eutrophication processes (Blindow et al., 2014).
Almost all undertaken restoration initiatives assume that
reduction of nutrient concentrations in water is a crucial factor
limiting phytoplankton abundance and, consequently, results in
increased light penetration and the development of macrophytes,
especially submerged communities. These organisms can compete
effectively with phytoplankton and bring long-term improvement
(Bakker et al., 2013;Hilt et al., 2018). Among physical factors, light
is necessary for charophyte germination (de Winton et al., 2000),
may enhance plant germination (Lorenzen et al., 2000) and is
crucial factor for seedling development and submerged plant
growth (van den Berg et al., 1998;He et al., 2019). When light
conditions are improved, macrophytes can massively (re)establish
and rapidly develop beds in the lake (van de Haterd and Ter Heerdt,
2007). The vegetation recovery can take from a few weeks to even a
few years. There are many examples of lakes that have been
restored, and the recovery of plants has been observed there (e.g.,
Lake Terra Nova or Lake Zwemlust, Netherlands; Lake Leven,
United Kingdom; Lake Tegel, Germany; Bakker et al., 2013).
Usually, the so-called ‘intermediate recovery state’was noted,
thus the period in which transient colonization by hornworts,
pondweeds, waterweeds or charophytes occurred, especially in
shallow lakes (Hilt et al., 2018). However, the clear-water state
and return of submerged macrophytes and the development of their
diversity are usually slow and often delayed. They can appear many
years later, after limiting the external nutrient load and
implementing complex restoration treatments (Bakker et al.,
2013;Hilt et al., 2018).
However, sometimes improvement of light and trophic
conditions is not followed by macrophyte re-establishment. One
of the critical factors affecting the rate of bottom recolonization by
macrophytes is the density and composition of the propagule bank
(Bakker et al., 2013). There are two functionally different fractions
in a lake propagule bank: i) an active fraction, capable of
germinating under certain conditions (Hilt et al., 2006) and ii) a
passive fraction, temporarily unable to germinate (dormant state,
immaturity, isolation by a too thick sediment layer). The second
fraction should be expected to dominate in degraded lakes with a
permanent turbid water state. Nevertheless, seeds in the sediments
suggest the possibility of natural regeneration of macrophyte
communities once light conditions improve. Some studies have
shown that seed banks from the most degraded lakes can also grow
and have the potential to restore vegetation (de Winton et al., 2000;
Verhofstad et al., 2017). However, the propagule bank in sediments
of degraded lakes usually has a low number of viable seedlings. They
exhibit strong seed dormancy and germinate in response to strict
germination cues. Thus, the chances of recovering submerged
vegetation by germination in such lakes are low (Rodrigo et al.,
2013;Hilt et al., 2018).
Many studies focus on the reconstruction of submerged
vegetation mainly in shallow lakes, while in deep lakes and
reservoirs this aspect is neglected, since macrophytes colonize
only a small part of the bottom. However, the recovery of
submerged plants in deep lakes is as crucial as in shallow lakes
because it also contributes to stabilization of ecological state in them
(Hilt, 2015). Thus, there are still numerous knowledge gaps on
propagule availability and dispersal for the return of submerged
macrophyte vegetation during and after lake restoration treatments
(Bakker et al., 2013;Hilt, 2015), and this problem is especially true
in deep lakes.
The aim of our study was to assess whether meeting the basic
assumption of all restoration projects, which is improving the light
conditions in the lake, is sufficient for the self-recovery of
macrophytes. To elaborate on a suitable basis, we performed a
germination test and propagule bank analysis in sediments
collected from a relatively deep lake that had been degraded for
decades and had undergone restoration treatments. Such an
approach gives a basic understanding of the conditions and
structure of the propagule bank, and therefore its potential ability
to germinate and the recovery of macrophytes. Based on the possible
sources of failure, we proposed some actions that may increase
possibility of macrophyte recovery. We emphasize that the
described problems are underestimated and frequently overlooked.
Awareness of the importance and relationships between predictor
variables describing submerged aquatic vegetation coverage and
composition can significantly facilitate and improve active
protection and restoration efforts for aquatic vegetation recovery.
2 Methods
2.1 Study area
To check the possibilities of plant self-recovery, we collected
sediments from Goreckie Lake (western Poland). This relatively
deep stratified lake had been degraded for many years and had
undergone restoration treatments to improve the quality of water.
Additionally, it has been the focus of scientific interest for several
decades, resulting in long-term research results and a well-studied
Rybak et al. 10.3389/fpls.2024.1421448
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vegetation structure (Dambska et al., 1978;Burchardt et al., 2001;
Sobczynski et al., 2012;Rybak et al., 2015). Goreckie Lake (N 52°
16’00”, E 16°47’43”) is endorheic, characterized by an area of 104.1
ha, max. depth of 17.2 m, and mean depth of 8.9 m. The originally
mesotrophic lake underwent accelerated eutrophication from the
1950s to the 1980s due to the inflow of only mechanically treated
wastewater from a sanatorium located on its shore, and the runoff
from the agricultural catchment (Sobczynski and Joniak, 2009). As a
result, the lake was hypereutrophic at the turn of the century
(Sobczynski and Joniak, 2013)–0.160 mg P L
-1
total phosphorus
(TP), 2.70 mg N L
-1
total nitrogen (TN), and 1.1 m Secchi disk
visibility (SDV). During our sampling time surface water was
characterized by 0.046 mg P L
-1
TP, 1.82 mg N L
-1
TN, and 4.2
m SDV. Phytoplankton blooms were reported from early spring to
late autumn, resulting in a substantial reduction in the extent of the
euphotic zone and lack of oxygen in the meta- and hypolimnion
(Sobczynski et al., 2012).
Due to high degradation and poor ecological state, restoration
treatments were applied in April 2010 and were carried out with
varying intensity in 2010 and 2012. To improve water transparency,
oxygenate the bottom waters and reduce phosphorus concentration,
three methods were applied simultaneously: aeration of
hypolimnion waters using a wind-driven aerator, chemical
phosphorus inactivation using iron sulphate salts, and
biomanipulation by removing 3 tons of plankton-eating fish
(Sobczynski et al., 2012). The goal of these activities was to
support the natural defense of the lake, including the recovery of
macrophytes as a factor regulating the circulation of biogenic
elements in the ecosystem. However, the methods employed did
not bring the expected effect on water quality improvement, and
after they were discontinued, the lake returned to its pre-restoration
condition. The main reasons for the low effectiveness of the
treatments were the extensive hypolimnion and strong internal
loading (Rybak et al., 2015;Joniak et al., 2018).
In the early 20
th
century, vegetation reached a maximum depth
of 7m (Figure 1), Chara tomentosa and C. globularis were noted
(Dambska, 1952). In the 1970s Lychnothamus barbatus occurred in
the northern lake part (Dambska et al., 1978). By the early 21
st
century, elodeids depth was 4 m in the northwest area of the lake,
with C. aspera and C. globularis persisting (Burchardt et al., 2001).
In 2013, six phytocoenoses (Charetum contrariae,Myriophylletum
spicati,Najadetum marinae,Nupharo-Nymphaeetum albae,
Potametum pectinati,Potametum perfoliati), indicating eutrophic
waters, covered 7.7% of the phytolittoral zone.
2.2 Field measurement and sampling
Field studies and sampling were conducted in April (time before
germination begins) 2013, one year after restoration treatments
terminated. Sediment samples for the germination test were
collected from 10 sites located in shallow lake parts (1.0–6.0 m),
which were determined based on the submerged vegetation
occurrence in the past (Figure 1;Table 1). Three sediment cores
were collected from each site using the Kajak sampler. The samples
at particular stations represented 8.47 × 10
-3
m
2
sediment surface
and a volume of 1.27 L. The cores were then divided into three
sediment subsamples based on the following strata: 0–5, 5–10 and,
10–15 cm and mixed within the layer. We cut the sediment cores
into layers to assess the abundance and quality of the propagule
bank. Then it was possible to determine whether propagules are
present in a similar amount in the sediment along its entire depth or
whether they are dominant in a particular layer (de Winton et al.,
2000;Boedeltje et al., 2002). The sediments were stored in
polypropylene containers at 4°C and analyzed within 24 hours.
The following physical and chemical variables were analyzed in
the sediment samples: total phosphorus (TP, mg P g
-1
dry weight
(dw)) by the molybdate method (PN-EN ISO 6878:2006) after
mineralization with HCl, organic matter (OM, % dw) as loss on
ignition at 550°C, calcium carbonates (CaCO
3
,%dw)using
Scheibler method with HCl (Van Reeuwijk, 2002) and sediment
hydration (Hydr, %) as fresh water lost on oven drying at 80°C
for 48h.
Photosynthetically active radiation (PAR) was examined at 0.1 m
intervals using a quantum meter with a spherical sensor (LI-193SA,
LiCor Biosciences). Measurements were made in cloudless weather at
FIGURE 1
Bathymetric map of Go
reckie Lake with sampling stations and surface area of the bottom covered by macrophytes in the 1952 –1978 period.
Rybak et al. 10.3389/fpls.2024.1421448
Frontiers in Plant Science frontiersin.org03
the time of maximum solar height above the horizon. Additionally,
measurements were repeated during the peak of vegetation season in
July. The light extinction coefficient (K
d(PAR)
) was calculated
according to Kirk (2010):Kd(PAR)=lnI0−lnId
d, where dis the water
depth, I
0
and I
d
are PAR values at the water surface and at depth d,
respectively. Data to measure the width of the reed belt and slope
measurements (edge points and water depth) were collected with a
Garmin Dakota 20 GPS and compiled using QGIS 3.12.
2.3 Germination test
We conducted the laboratory test using lake sediments based on
the studies on germination potential, which have been assessed under
different conditions (laboratory, greenhouse, outdoor) and onvarious
substrates (e.g., natural sediments, sand, artificial substrate)
(Thompson et al., 1997 and cited there). The germination test
carried out during study employed methods used by de Winton
et al. (2000) and Dugdale et al. (2001). It was performed in a
cultivation chamber in glass cylinders. The cylinders were filled
with filtered lake water (GF/F filters, Advantec) up to 25 cm of the
water column height. The temperature was constant at 17.5°C, while
the light regime was set at 10: 14 h (light: darkness). Light intensity at
the water surface was 34.5 μmol m
-2
s
-1
. This simulated lake
conditions in the early spring period. Ninety transparent
polypropylene plastic pots (120 cm
3
)werefilled with 40 cm
3
(2 cm
height) of sediment subsamples from the particular layer. Each single
pot was inserted in a single cylinder. Every layer from each station
was replicated three times, which created a 0.165 m
2
sediment area.
Individuals of Daphnia magna L. from a long-term laboratory culture
(Bdem2) were introduced in the cylinders to reduce the growth of
phytoplankton (three per cylinder). Growths of filamentous algae
were removed daily. The cultivation trial was carried out for 50 weeks.
The dissolved oxygen (HI 9146–04, Hanna Instruments),
temperature, pH and electric conductivity (HI 98129, Hanna
Instruments) were measured every two weeks. After 25 weeks,
sediments were gently mixed to move potentially buried propagules
closer to light. Emergence was defined as developing a germinated
seedling to a stage where it could be identified. At the end of the test,
each sediment sample was sieved by 250 μm aperture mesh, and the
extract was observed using a stereoscopic microscope (Zeiss Stemi
2000-C) to identify and quantify the seeds and other propagules (e.g.
charophyte oospores). Data of propagule numbers and seedlings were
standardized to individuals per m
2
(ind. m
-2
).
2.4 Statistical analyses
The differences in the number of propagules among sediments
layers were analyzed with generalized linear mixed effect models
from glmmTMB library (Brooks et al., 2017). Sampling station was
incorporated as a random effect and the gamma family with log-link
function was used to describe the data distribution. Non-parametric
Kruskal-Wallis test (stats library) was used to check the differences
of physicochemical features among sediment layers (TP, OM, Hydr,
and CaCO
3
content). Q-Q plot and residual plot were used to test
the normality of the data.
The Principal Component Analysis (PCA) with factors grouping using
k-means clustering (both in the stats library) was performed to visualize the
data cloud, which allowed the identification of the distribution patterns of
physical-chemical factors (water depth, fresh sediment depth, organic
matter, hydration, total phosphorus, calcium carbonate, and availability
of photosynthetic active radiation) and propagules and group them. The
clusternumberanditscontentwasestimatedusingparallelanalysisinthe
paran package (Dinno, 2018). Statistical analyses were performed using the
R software (ver. 3.5; R Development Core Team).
TABLE 1 Density of diaspores in bottom sediments and physical characteristics of sampling stations of Go
reckie Lake.
Station
Density of
diaspores
(thous. ind. m
-2
)Depth of
water(m)
Slope angle
(°)
Width of the
reed bed (m)
Thickness of
fresh
sediment
(cm)
% PAR availability at
the bottom
Oospore Seed spring summer
1 12.31 1.54 6 8 16 5 1 0
2 3.59 0.51 6 11 14 15 1 0
3 16.92 2.05 4 9 14 3 4 1
4 14.87 0.51 4 9 14 3 4 1
5 160.00 5.64 2 10 14 3 16 8
6 8.72 0.51 5 7 14 3 2 0
7 38.46 2.05 3 12 16 2 9 2
8 30.26 lack 2 3 29 7 16 8
9 42.05 4.62 2 11 21 5 16 8
10 1.54 2.05 1 11 79 4 47 46
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3 Results
3.1 Environmental factors and
sediment structure
The maximum PAR penetration depth in the lake was 10.5 m in
spring. The percentage of the incident light at the bottom of the
sampling stations ranged between 1% (12 μmol m
-2
s
-1
)at6mand
47% (425 μmol m
-2
s
-1
) at 1 m depth, with an average K
d(PAR)
of 2.3 ±
1.0 m
-1
(Table 1). All stations were in range of the euphotic zone
where an average K
d(PAR)
of 0.614 ± 0.092 m
-1
. At the peak of the
growing season, the maximum light penetration depth was 5.5 m
including euphotic zone depth of 3.3 m and an average K
d(PAR)
=
1.449 ± 0.096 m
-1
. The light reaching the phytolittoral bottom was ca.
50% lower than in spring, and the K
d(PAR)
increased to 4.8 ± 2.2 m
-1
.
The thickness of the fresh sediment layer ranged from 2 up to 15 cm
(Table 1). In zones with the highest bottom slopes, the sediments
contained a thin fresh layer. In areas with a lower slope, this layer was
thicker. However, these differences did not significantly affect the analyzed
physical and chemical features in the whole lake context (Table 2).
Variables describing sediments clearly indicated factors positively
correlated with propagule bank abundance in the PCA ordination space
defined by the first and second principal components (Figure 2). Both
components accounted for more than 61% of the variance observed in the
structure of the analyzed stations. The clustering algorithm revealed that
environmental factors related to diaspore abundance could be divided into
three groups. The first group includes factors positively correlated with
propagule abundance: PAR availability, slope angle, and CaCO
3
content.
Factors in the second group were negatively correlated with propagule
number, including water depth and fresh sediment layer thickness. The
third group includes factors which were not correlated with propagules:
sediment hydration, total phosphorus, and organic matter content.
3.2 Germination test
Water pH during the entire trial was constant and reached 8.5 ± 0.5.
Dissolved oxygen in the first eight weeks was 6.5 ± 0.1 mg O
2
L
-1
and
increased during the trial up to 9.7 ± 0.1 mg O
2
L
-1
in the last 4 weeks.
Electric conductivity decreased from 800 ± 4 μS cm
-1
in the first month
to 640 ± 2 μS cm
-1
at the end of assay.
Seedlings appeared after 6 weeks from station 8: Chara virgata
Kütz. –18 ind. m
-2
from 0–5 cm and 36 ind. m
-2
from layer 5–10
cm. After this time no new seedlings were noted nor did the
sediment stirring induced emergence of new ones.
Charophytes’oospores were significantly more abundant than
seeds in the propagule banks (F-ratio = 8.39, p<0.01) (Table 1).
Considering the number of diaspores in particular layers, the highest
number was noted in 5–10 cm (18 769 ± 9 960 oospores and 1 795 ±
702 seeds m
-2
;mean±SE)andthelowestin10–15cminthecaseof
seeds (150 ± 150 ind. m
-2
)and0–5 cm in the case of oospores (6 205 ±
2317ind.m
-2
). Statistical analysis did not reveal significant differences
between sediment layers and sampling stations (Figure 3).
Microscopic analysis showed physical damage to about 80% of
the seed pool (splitting, gnawing) and revealed that 70% of the
oospores were empty carbonate encrustations with no biotic part.
4 Discussion
4.1 The propagules origin and the success
of germination
Although we employed a standard methodology (de Winton
et al., 2000;Dugdale et al., 2001) in the germination test conducted
on sediments from Goreckie Lake, the results were significantly
different from comparable studies. A key aspect that gives very good
results in germination success, both in terms of germling density
and plant taxonomic diversity, is the origin of the sediments.
Ecosystems without signs of permanent degradation and aquatic
vegetation occurrence are characterized by undisturbed production
of diaspores (see e.g., Finlayson et al., 1990;Skoglund and
Hytteborn, 1990;de Winton et al., 2000). If the lake has been
degraded due to unnaturally fast eutrophication (such as Goreckie
Lake), the inhibition of diaspore production and the replenishment
of the propagule bank are the main problems (Lu et al., 2012). The
density of propagules in Goreckie Lake ranged from ca. 500 (seeds)
to 160 000 (oospores) ind. m
-2
, with the highest number in the 5–10
cm sediment layer. This proves the presence of a well-developed
flora in the recent past. A relatively high number of diaspores,
together with their potential survival (up to 50–60 years described
by other authors; Lu et al., 2012;Rodrigo and Alonso-Guillen,
2013), seems to ensure the macrophytes return (Bakker et al., 2013).
However, both the restoration treatments applied in the field and
the laboratory germination test resulted in an infinitesimal success
rate. A similar diaspore distribution pattern in the sediments was
described in lakes where submerged plants were absent for years,
however, viable seeds have been found (Hilt et al., 2006;Lu et al.,
2012). The sediment analysis of Goreckie Lake demonstrated that
the upper layer contained fewer seeds, which seems to be due to the
very poor representation of elodeids in the lake, whereas this layer is
crucial in terms of germination initiation potential. Seeds and
oospores located deeper, even if numerous, exhibit lower
germination potential and can only play an ecologically
TABLE 2 Vertical changeability of physicochemical parameters (mean ±
stand. dev.) of bottom sediments of Go
reckie Lake (TP –total
phosphorus, OM –organic matter, Hydr –hydration, CaCO
3
–calcium
carbonate; Z –Kruskal-Wallis test).
Parameter,
unit 0–5cm 5–10 cm 10–15 cm Z pn
TP, mg P g
-1
dw 10.1
± 7.0 8.7 ± 7.6 6.0 ± 6.2 1.3 >0.05 30
OM, % dw 12.1
± 13.3 9.0 ± 8.5 12.3 ± 10.7 0.4 >0.05 30
Hydr, % 66.0
± 25.8
62.2
± 16.9 68.2 ± 16.1 3.6 >0.05 30
CaCO
3
,%dw 16.3
± 22.0
25.1
± 22.7 26.7 ± 25.3 0.3 >0.05 30
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significant role in a situation of sediment disturbance. However,
they must be disregarded when considering rapid vegetation
regeneration (Dugdale et al., 2001;de Winton et al., 2004).
de Winton et al. (2000), collected 15 cm sediment cores divided into 5
cm layers; sediments were collected from lakes that supported seed
production and lakes in which vegetation had disappeared (de-vegetated).
The first seedlings were recorded after 5 weeks, and the highest number was
found in the sediment of the 5–10 cm layer, however only in lakes with
present vegetation. No seedlings were recorded from lakes classified as de-
vegetated. These results are in line with our study, in which sediments origin
from Goreckie Lake which could be classified as de-vegetated, considering
submerged vegetation. Moreover, even mixing of the sediments in the
germination test as described by van Zuidam et al. (2012),didnotprovide
beneficial effects and did not contribute to seedling appearance.
Although the composition of the submerged propagule bank
does not have to match the vegetation presence exactly (Arthaud
et al., 2012), its condition indicates a new macrophyte emergence
after a significant disturbance (Combroux et al., 2001). Thus, the
FIGURE 2
PCA output for the relationships between environmental variables with clustering algorithm results (denoted by color); depth –water depth, FsD –
fresh sediment depth, OM –organic matter, Hydr –hydration, TP –total phosphorus, CaCO3 –calcium carbonate, PAR –availability of
photosynthetic active radiation. Dots 1–10 –sampling stations according to Figure 1 (the size indicates contribution of the variables to the principal
components –up to 20%).
FIGURE 3
Densities of oospores (left) and seeds (right) in the bottom sediments used in the laboratory trial. For each layer 30 observations. Box-and whisker
plots boxes represent median, first and third quartiles with whiskers extending until respectively the values that are within 1.5 × inter-quartile range;
red dots represent the mean value, black dots represent outliers; oospores extreme of 160 thous. ind. m
-2
not present (see Table 1).
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spontaneous return of submerged macrophytes depends, at least
partly, on the quality of the propagule bank. Viable propagules of
non-dominant species, including charophytes, are usually found in
most sediments. This means that when the dominant species
disappears, there is a local potential for the development of
diverse aquatic plants (Verhofstad et al., 2017), and species can be
easily spread from neighboring ponds and water bodies (Barrat-
Segretain, 1996). The data from lake sediments indicate that
particularly propagules from Characeae and Potamogeton species
are very abundant, and frequently appear in many restored lakes, as
they can survive in turbid water (Bakker et al., 2013;Hilt et al.,
2018). Corroborating this, the emergence of C. virgata seedlings
from the oospores in Goreckie Lake sediments seems to be a result
of dispersal by waterfowl (Vivian-Smith and Stiles, 1994;Linton
and Goulder, 2000;Reynolds and Davies, 2007) from neighborhood
ponds where C. virgata was present (Gabka, 2009). In other lakes,
e.g., Steinhuder Meer (Germany) the dominance of Elodea nuttallii
was noted after a sudden improvement in water transparency
approximately 40 years after the disappearance of plants. The
species was not observed earlier in this lake and spread mainly by
vegetative fragments (Hilt et al., 2006). Plants can also develop by
expanding local remnant populations, as seen in Lake Fure,
Denmark, where macrophytes spread through clones of several
species from pre-eutrophication times (Bakker et al., 2013). If the
dispersal inflow from external sources does not compensate a poor
bank of propagules, the success in macrophyte establishment and
development will gradually decrease (Van Onsem and Triest, 2018).
As a result, passive fractions and the active propagule bank remains
became critical bottlenecks for maintaining a clear-water state. In
such a situation, the only way to restore vegetation in lake is
artificial support of submerged macrophyte development through
reintroduction of the most successful native species (Hilt et al.,
2006;Rodrigo and Carabal, 2020).
4.2 Physical and chemical factors
promoting successful germination
The submerged macrophyte distribution is regulated by a series
of biotic and abiotic factors. Despite light availability (Cronin and
Lodge, 2003) and nutrient concentration in both water and sediments
(Feijoo et al., 2002;Li et al., 2007), water movement (Atapaththu and
Asaeda, 2015), sediment anoxia (Zaman and Asaeda, 2013), and
water column hypoxia (Summers et al., 2000) are pointed out as
crucial. However, they always should be considered comprehensively.
The failure of macrophyte recruitment suggests that the
environmental conditions of Goreckie Lake were not beneficial for
germination or the growth of submerged plants (Hay et al., 2008;
Nonogaki, 2014). This is confirmed by the range of the euphotic zone
in Goreckie Lake in spring and summer (10.5 and 5.5 m,
respectively). Although the sediment illumination was sufficient, the
submerged plant growth was strongly inhibited. Moreover, our
germination potential test also exhibited negligible results. This
underlines that many conditions must be met for successful
germination. In many lakes, reducing nutrient concentrations and
deepening the euphotic zone is sometimes not enough for renewal of
macrophyte communities from the seed bank (Middelboe and
Markager, 1997;Cronin and Lodge, 2003), as it is often assumed
before restoration treatments.
The structure of the sediments in Goreckie Lake strictly
reflected changes in trophic level. The organic layer was created
mainly as a result of dead phytoplankton sedimentation, which
developed substantial biomass during the vegetation season, and
poor oxygen conditions in bottom waters prevented its
decomposition (Rabalais et al., 2010;Sobczynski et al., 2012).
Although low oxygen conditions might have positive effects on
seed germination for some species (e.g. Typha latifolia and Zostera
marina; Bonnewell et al., 1983;Moore et al., 1993), in general
insufficient dissolved oxygen inhibits plant growth and intensifies
other stressors, e.g., hydrogen sulfide (Parveen et al., 2017;Zhao
et al., 2021). The mineral layer lying below referred to a higher
calcium concentration, which was accumulated in sediments due to
calcium carbonate precipitation on charophytes and macrophytes
(Cicerone et al., 1999;Kufel et al., 2013;Pełechaty et al., 2013). The
maximum sediment accumulation rate in the littoral zone was
determined at 3.6 mm yr
-1
. This is a theoretical value on which
many factors have an impact (Benoy and Kalff, 1999). Nevertheless,
based on this rate, it can be assumed that the collected core
sediments developed for ca. 40 years, and they date back to the
period with well-developed macrophytes communities.
Subsequently, accelerated eutrophication occurred leading to
macrophyte disappearance and further lake degradation. On the
other hand, the amount of the formed sediment can also be a factor
that significantly influences germination. Seeds of some species (e.g.
Typha domingensis) do not germinate when covered by sediment,
however in contrast, others are able to grow through a thin layer of
sediment or detritus (e.g. Cladium jamaicense) or could even
withstand relatively thick sediments deposit, such as M. spicatum
–up to 2 cm (Hartleb et al., 1993;Lorenzen et al., 2000), which was
the sediment thickness in our germination test.
4.3 The importance of lake morphology
in germination
The morphological, hydrographical, and catchment conditions
of lakes may influence the trend and rate of theoretical changes in
aquatic vegetation patterns. Since the macrophyte spatial
distribution strongly depends on the water depth and light range,
the maximum depth of a lake is one of the most critical factors
determining the potential area covered by plants (Søndergaard
et al., 2013). Consequently, propagule dispersal to the target
habitat and successful germination in it are functional processes
controlling plant community structure (Nilsson et al., 2010). It was
demonstrated that a littoral slope over 2% caused a steep decrease in
light availability and, in consequence, a rapid decrease in the
vegetation distribution, abundance, and biomass (Duarte and
Kalff, 1986;He et al., 2019). Differences in plant cover have also
been shown between lakes with gentle slopes (shallow and deep
regular-shaped) and ribbon-shaped lakes with steeper slopes
Rybak et al. 10.3389/fpls.2024.1421448
Frontiers in Plant Science frontiersin.org07
(Kolada, 2014). This characteristic of the littoral area also
determines the physical properties of sediments (nutrient poor)
and the spatial differentiation of matter deposition, thus affecting
the extent of vegetation. For example, sharp bottom slopes, which
occur in Goreckie Lake, cause the top layer of sediments with
propagules to slide down to the deeper zones of the lake and remove
some parts of the propagules from the active seed bank. Thus, in
lakes with a very steep bed slope, the abundance of macrophyte
development may be naturally limited, even irrespective of water
quality (Kolada, 2014). This was confirmed by the PCA analysis
performed in our study, which showed that the number of diaspores
in the sediment was related to the amount of light reaching it, which
was inversely correlated with the depth and amount of fresh
sediment (lake turbidity state phase). At the same time, it
confirmed that the density of oospores was related to the amount
of calcium carbonate intensively precipitated by charophytes and
indicative of their abundant presence in the past. Correlating with
the slope of the bottom, it indicates that diaspores may descend with
the sediment to greater depths at the sharp slopes of the lake basin.
4.4 Broader perspective
Plant development was assumed to have a self-renewal
characteristic due to the ecological state amelioration. However,
these expectations may be illusory or may never come true without
a proper propagule bank diagnosis and appropriate treatments to
facilitate germination or macrophyte reintroduction (Rodrigo,
2021). The reduction of nutrient loading and biomanipulation
(mainly fish removal) can bring a rapid response to improved
light conditions and macrophyte development (Lauridsen et al.,
2003). However, some treatments could also have a negative impact
on plant recovery. For example, sediment removal may cause the
removal of propagules or isolate them below the viable germination
zone, and chemical phosphorus inactivation may inhibit
charophyte generative reproduction (Hilt et al., 2006;Rybak et al.,
2017,2020). Climate changes should also be taken into account
during restoration activities, because they affect plants, directly
inducing morphological and physiological responses and
indirectly interfering with biotic interactions, affecting the
population dynamic (Tylianakis et al., 2008;Olsen et al., 2016).
The stabilization of clear water phase by macrophytes might be
limited in the hotter and carbon dioxide rich climate in the future.
Considering climate change and the consequence of bloom-forming
cyanobacteria domination in the phytoplankton community
structure, only submerged vegetation with lower requirements for
critical environmental factors can better withstand climate- and
cyanobacteria-caused disturbances in the ecosystem. Surprisingly,
charophytes seem to be good candidates as they can diminish the
share of cyanobacteria in the lake phytoplankton more effectively
than submerged vascular macrophytes and exhibit the potential to
mitigate the effects of climate change (Pełechata et al., 2023).
Therefore, future global warming effects should be considered in
planning, management, and restoration since strategies may need to
be refined and adapted to preserve or improve the present-day lake
water quality (Trolle et al., 2011).
5 Conclusions and recommendations
We conclude that improving the light conditions in the lake
may not be enough to recover vegetation, especially when the
potential to naturally recover plant communities from sediments
is low. We highlight that:
•Understanding the propagules germination-environmental
factors-macrophytes occurrence interactions, offers a tool
for improvement of the revegetation and management of
many degraded lacustrine ecosystems.
•Analysis of the propagule bank before applying restoration
treatments should be a standard procedure to recognize the
possibility of macrophyte recovery from internal sources,
particularly in lakes where no submerged plants are observed.
•The germination test should be done to assess the rate of
germination success. Although many plants can reproduce
clonally and spread without seed production, recruitment of
seeds remains extremely important in the lake renewal or
restoration context.
•If the oospores and seeds present in the propagule bank are not
of high quality or viable, the only way to restore vegetation is
artificial support of submerged macrophyte development
through reintroduction of the most successful native species.
Such a strategy allows for better adjustment of restoration
methods and saves time and resources in the event of the need
for macrophyte reintroduction.
Data availability statement
The raw data supporting the conclusions of this article will be
made available by the authors, without undue reservation.
Author contributions
MR: Conceptualization, Formal analysis, Investigation,
Methodology, Resources, Visualization, Writing –original draft,
Writing –review & editing. JR: Formal analysis, Investigation,
Writing –original draft, Writing –review & editing. ŁW: Formal
analysis, Investigation, Writing –original draft, Writing –review &
editing. MAR: Formal analysis, Investigation, Writing –original
draft. TJ: Conceptualization, Formal analysis, Investigation,
Methodology, Resources, Validation, Writing –original draft,
Writing –review & editing.
Rybak et al. 10.3389/fpls.2024.1421448
Frontiers in Plant Science frontiersin.org08
Funding
The author(s) declare that no financial support was received for
the research, authorship, and/or publication of this article.
Acknowledgments
We want to thank Prof. Mariusz Pełechaty (Adam Mickiewicz
University) for his suggestions and fruitful discussions; Prof.
AMU Bartłomiej Gołdyn (AMU) for help in statistical analyses;
MSc. Kaira Kamke for the manuscript proofreading; and two
reviewersfortheirusefulcommentsonanearlierversionof
the manuscript.
Conflict of interest
The authors declare that the research was conducted in the
absence of any commercial or financial relationships that could be
construed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the authors
and do not necessarily represent those of their affiliated organizations,
or those of the publisher, the editors and the reviewers. Any product
that may be evaluated in this article, or claim that may be made by its
manufacturer, is not guaranteed or endorsed by the publisher.
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