RESEARCH ARTICLE
Evaluation of Restoration Measures in a Shallow
Lake through a Comparison of Present Day
Zooplankton Communities with Historical Samples
Gerald Louette,1,2 Steven Declerck,3 Jochen Vandekerkhove,4 and Luc De Meester3
Abstract
Many shallow lakes have lost a large part of their ecological value during the past decades. Human-induced factors
such as eutrophication and inappropriate fish stock management are generally the main causes for this loss. To restore such degraded habitats, several measures are taken,
typically involving a reduction of nutrient loading and
interventions in the aquatic food web functioning (biomanipulation). In this study, we report on the joint effects
of a series of restoration measures in a shallow lake (Lake
Kraenepoel, Belgium, 22 ha) and evaluate these effects
via three different criteria. The first criterion is that the
target condition, being a clearwater phase with submerged
macrophytes, was successfully achieved and persisted for
a period of at least 5 years after restoration. Second, we
detected a substantial change in community structure of
cladoceran zooplankton and an associated increase in spe-
Introduction
During the past decades, a large proportion of lentic freshwater bodies in Europe have suffered from degradation due
to several anthropogenic factors, such as eutrophication,
acidification, metal contamination, unbalanced stocking of
fish communities, and the introduction of nonindigenous
species (e.g., Brouwer & Roelofs 2001; Yan et al. 2003;
Anderson et al. 2005). High nutrient loading, often combined with inappropriate fish stock management, has
resulted in the eutrophication of many shallow lakes in
European lowlands. Eutrophication typically results in the
increased incidence of phytoplankton blooms, reduced
light penetration in the water column, and the loss of submerged macrophytes. There is accumulating evidence that
the loss of macrophytes is one of the major causes for
a diversity decline in aquatic organism groups (Scheffer
et al. 1993; Declerck et al. 2005, 2007). As a result, the restoration of the macrophyte-dominated phase in eutro1
Research Institute for Nature and Forest, B-1070 Brussels, Belgium
Address correspondence to G. Louette, email: [email protected]
Laboratory of Aquatic Ecology and Evolutionary Biology, K. U. Leuven,
B-3000 Leuven, Belgium
4
Department of Genetics and Cytology, University of Gdansk, PL-80-822
Gdansk, Poland
2
3
Ó 2008 Society for Ecological Restoration International
doi: 10.1111/j.1526-100X.2008.00409.x
SEPTEMBER 2009
Restoration Ecology Vol. 17, No. 5, pp. 629–640
cies richness and conservation value following restoration
measures. Finally, we observed that the general structure
of the present day cladoceran zooplankton community resembles well that of the preeutrophication period (1929–
1931). Current species richness, however, tends to be
lower than in the reference period, and some rare species
are still lacking. It is conceivable that, when submerged
macrophytes develop further, a subset of specialist species
may reappear. Overall, the use of historical habitat-specific
samples offers a major opportunity for evaluating restoration success in great detail. Community structures may
directly be compared, the gain or loss of specific species can
accurately be documented, and more insights in the
observed patterns be obtained.
Key words: biomanipulation, Cladocera, community ecology, conservation biology, restoration success.
phied water bodies is an important avenue toward the
restoration of biodiversity in shallow lakes.
The successful restoration of eutrophied shallow lakes
hinges in general on two types of measures, that is, a
reduction in nutrient loading and an enforced alteration of the food web structure (Hosper & Meijer 1993).
Nutrient loading is the result of both internal loading
and external nutrient influx. The reduction of external
loading can be achieved by the purification or diversion
of incoming water and the alteration of agricultural
activities. Internal loading from the sediments can be
effectively reduced through removal of the superficial
nutrient and carbon-rich sediments (Brouwer & Roelofs
2001), although water level drawdown, resulting in mineralization of organic matter, may form a less expensive
alternative in shallow lakes (James et al. 2004). The
reduction of nutrient loading is, however, often only
effective if it is combined with a manipulation of the
food web structure (biomanipulation; Jeppesen et al.
1990; Meijer et al. 1999). In practice, biomanipulation is
most often accomplished through a drastic reduction
(>75%) or complete removal of the planktivorous and
benthivorous fish stocks and also often involves the
stocking of piscivorous fish. Eventually, biomanipulation
comes down to the restoration of the stable clearwater
phase in shallow lakes (Scheffer et al. 1993).
629
Evaluation of Restoration Measures in a Shallow Lake
The success of restoration measures in shallow lakes
is often evaluated as the degree to which the target condition is achieved (i.e., clearwater phase with restoration
of submerged macrophyte vegetations; Anderson et al.
2005). Another criterion is the increase in species richness
or change in community structure before and after the
restoration measure of specific groups of organisms
(Urabe 1994). Some studies have evaluated the success of
restoration measures in systems (Ruiz-Jaen & Aide 2005)
based on the recovery of specific target species that had
disappeared, but were obliged to concentrate on historical
published species lists (Vrba et al. 2003). Other studies
evaluate restoration success through the comparison of
the resulting communities with the contemporary conditions in reference habitats (Keller et al. 2002; Yan et al.
2004; Frost et al. 2006) or with paleolimnological reconstructions of species lists and community structures based
on organic remnants (Pollard et al. 2003; Sarnelle &
Knapp 2004). Historical habitat-specific samples that can
be reanalyzed and directly compared with the newly
formed communities after restoration provide a more
direct approach for the evaluation of restoration success,
but studies using historical samples of shallow lakes are
almost nonexistent.
Long-term effects of gradually executed restoration
measures on the chemical and biological environment
have been monitored both in shallow eutrophied (Moss
et al. 1996; Jeppesen et al. 1998b) and deep acidified lakes
(Fischer et al. 2001; Keller et al. 2002; Yan et al. 2004;
Frost et al. 2006). In the current study, we evaluate the
joint effects of a series of restoration measures on the species richness and community structure of cladoceran zooplankton in a shallow lake. As we have at our disposal the
original samples from a reference period (around 1930)
when the ecological value of the habitat was high, our
study generates the unique opportunity to evaluate resto-
ration success in a straightforward way. We address the
following questions: (1) How did the cladoceran zooplankton community respond to the restoration measures and
at what time scale did changes occur? (2) How does the
community following restoration resembles the community from a reference period?
Methods
Study Site
Lake Kraenepoel (lat 51°059N, long 03°299E, 22 ha surface area, 1.5 m maximum depth) is one of the last
remnants of the many water bodies that occurred in the
former heathlands of northwest Belgium (Fig. 1). The first
records describing the lake date back from the middle of
the 16th century, and it most probably originated from
peat or sandstone extraction. During many centuries, the
lake was exploited as an extensive fish-farming site until
about 1950. During that period, the lake was regularly
drawn down with cycles of 3–5 years to harvest fish
(mainly Common carp [Cyprinus carpio], with bycatches
of Tench [Tinca tinca], Rudd [Scardinius erythrophthalmus], Roach [Rutilus rutilus], Perch [Perca fluviatilis], and
Pike [Esox lucius]). During the period 1920–1940, the lake
was an oligo- to mesotrophic, weakly buffered water body
(circumneutral pH), with no or few emergent macrophytes, and a well-developed submerged macrophyte vegetation on sandy sediments (Luyten 1934). Its high nature
value was displayed by rich Littorelletea vegetations
(Vander Meersch 1874) and diverse cladoceran and desmid communities (Luyten 1934; Van Oye 1941).
After fish culture practices had stopped, the lake was
divided into two sections by an artificial dam in 1957
(Hoste 2001). The northern section (13 ha) kept its clearwater phase (Van Wichelen et al. 2007), probably because
Figure 1. Geographic location of the shallow lake (Lake Kraenepoel, Aalter, Belgium). The lake was divided into a northern section and a
southern section by an artificial dam in 1957. Dark polygons indicate islands within the lake. The lake is fed by a small rivulet in the southern
section, and the water level is regulated by an outlet structure in the northern section. After restoration measures in 2000, the lake was
hydrologically isolated (no incoming water from the small rivulet).
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Restoration Ecology
SEPTEMBER 2009
Evaluation of Restoration Measures in a Shallow Lake
of occasional drawdowns that occurred almost every
decade, and reduced fish densities (planktivorous fish:
6 kg/ha, benthivorous fish: 21 kg/ha) and contributed to
a consolidation of the sediment layer. Submerged macrophytes (mainly narrow-leaved Potamogeton species) persisted over a small proportion in the northern section. The
southern section (9 ha) has never been drained after the
creation of the dam. The influx of nutrient-rich water from
a rivulet caused a shift to the turbid water state (Scheffer
et al. 1993). Before restoration, macrophytes were absent
and the fish community was totally unbalanced due to regular stocking for angling purposes (planktivorous fish: 46
kg/ha, benthivorous fish: 293 kg/ha).
In 2000, several measures were applied to restore the
lake into its original clearwater phase (Table 1). These
restoration measures included: (1) the diversion of a
eutrophied rivulet from the southern section of the lake
(hydrological isolation), (2) the drainage of the lake, (3) the
complete elimination of the fish stocks, (4) the removal of
the sludge on the lake floor (up to 60 cm of organic material
on some places), and (5) the introduction of pike fingerlings
(approximately 2 cm total length) in the northern section of
the lake (500 individuals/ha).
Sampling
The cladoceran zooplankton community of Lake Kraenepoel was sampled during several time periods in the past
century. At these occasions, samples were taken by different methods and in various frequencies: (1) Luyten (1934)
sampled the zooplankton community both qualitatively
and quantitatively on a seasonal basis during the period
1929–1931. For the qualitative samples, he made horizontal hauls from multiple locations at the shore with a conic
plankton net. He collected quantitative samples by filling
a recipient of known volume with lake water at different
depths and filtering the collected water through a plankton
Table 1. Timing of restoration measures that were carried out in
Lake Kraenepoel during the period 2000–2002.
Restoration Measure
Summer and
fall 2000
Spring 2001
Summer and
fall 2002
Spring 2003
SEPTEMBER 2009
Diversion of nutrient-rich incoming
rivulet
Removal of fish stocks and drawdown
in both sections
Removal of sediment layer of the
northern section
Refilling of both sections
(groundwater and rainwater)
Introduction of piscivorous fish in
northern section
Drawdown of southern section
Removal of sediment layer of the
southern section
Refilling of southern section
(groundwater and rainwater)
Restoration Ecology
net. Based on these samples, he published an exhaustive
species list in a monograph (Luyten 1934). (2) We quantitatively sampled the cladoceran zooplankton communities
during the period before and shortly after the restoration
measures (1999–2002), on a monthly basis during winter
(November to March) and fortnightly during summer
(April to September). By then, the lake was divided into
two sections. In each of these sections, we sampled at
three randomly chosen pelagic locations with a SchindlerPatalas trap (64-lm mesh size). Each location was sampled at two depths (surface and 0.5 m). At each sampling
occasion, all samples per lake section were pooled to form
one integrated sample. In addition, at one occasion (July
2001), the community of the northern lake section was
qualitatively sampled at 15 different locations covering
a wide variety of subhabitat types (e.g., different macrophyte species and sediment types), using a plankton dip
net (64-lm mesh size). (3) In the period after the restoration measures (2003–2005), we took quantitative samples
on a seasonal basis with a tube sampler at eight random
locations in each section. We pooled the samples per section and filtered them through a plankton net (64-lm
mesh size). All the samples from 1929 to 1931 (hereafter
called ‘‘reference period’’ or ‘‘1930’’) and 1999–2005 (hereafter called ‘‘recent survey’’) were preserved in formaldehyde 4%.
For the present study, we worked on a selection of samples from the reference period taken by Luyten (1934)
(stored at the Zoology Museum of the University of Gent,
Belgium), the samples from the period before the restoration measures in the northern and southern sections
(1999–2000, BR-N and BR-S), the samples from the
period shortly after the restoration measures (2001–2002,
AR-N1 and AR-S1), and the samples dating from the
period 2003–2005 (after restoration, AR-N2 and AR-S2).
All samples were processed in a similar way, following
a standardized protocol. In each sample, we identified and
counted the first 300 cladoceran zooplankton individuals
to species level following the key of Flössner (2000). The
abundances of each species were converted to biomass
data using published length–weight regression relationships (McCauley 1984).
Statistical Analysis
We restricted the statistical analyses to samples originating from May (spring) and September (summer) to standardize for seasonal community variation (Abrantes et al.
2006). We estimated species richness and conservation
value in each of these samples. Species richness was
defined as the total number of detected cladoceran species. The conservation value of a sample was determined
by summing the rarity scores of all species occurring in the
sample and dividing this value by the number of species
present. Rarity scores of species were obtained from the
ACFOR scaling applied to the occurrence of species in
631
Evaluation of Restoration Measures in a Shallow Lake
European northwestern lowlands (Louette et al. 2007).
This resulted in rarity scores ranging between 1 and 5,
with a score of 1 for the most abundant species and a score
of 5 for the rarest species. Changes in species richness and
conservation value of samples among different time periods were analyzed by analysis of variance using years as
replicates within each period, followed by a post hoc test
(STATISTICA, StatSoft 2004). We explored patterns in
cladoceran community structure by performing correspondence analysis (CA; CANOCO, ter Braak & Smilauer
2002) on presence/absence data and on log (x 1 1)-transformed biomass data.
Results
We recorded a total of 38 species in the entire set of samples collected during the recent survey (1999–2005). Ten
additional species can be added when taking into account
the list of Luyten (1934), and some species that were
detected by us when reanalyzing a subset of these historical samples. This leads to a total number of 48 cladoceran species observed in Lake Kraenepoel over a period
of 75 years (Table 2). We distinguished several classes
of species based on their occurrence in the samples of
different time periods (Table 2). Ten species were only
detected in the samples of the reference period (1929–
1931). Conversely, seven species were only detected in
the recent survey (1999–2005). We recorded another 12
species in the period after restoration that had been
observed in samples from the reference period but not in
samples dating from the period before restoration (1999–
2000). Finally, 19 species were observed to be always
present.
During the recent survey, the average number of species per sample tended to increase in the period after the
restoration measures compared to the period before the
restoration measures in both the northern and southern
sections of the lake, with a significant difference in spring
among BR-N and AR-N2, and AR-N1 and AR-N2 (p <
0.05; Fig. 2). Before restoration measures, the average species richness of both lake sections was low (approximately
four species), whereas in the period after the restoration
measures, species richness increased to an average of
more than 7 species in spring samples and more than 10
species in summer samples. Species richness in the spring
samples after restoration measures remained significantly
lower than in the samples collected by Luyten (13 species)
(p < 0.05). Species richness of summer samples, however,
approximated well the values derived from the summer
samples of Luyten (11 species). Also the conservation
value increased following restoration both in the northern
and in the southern sections, with a significant difference
in spring among BR-N and AR-N2, BR-S and AR-S2, and
AR-S1 and AR-S2 (p < 0.05; Fig. 3). The conservation
value was only significantly different between the reference period and the period after restoration measures for
the northern section.
632
There was a dramatic shift in the species list (presence/absence data) and biomass structure of the cladoceran communities between the reference period and
the period before restoration measures (Figs. 4 & 5).
There were also pronounced changes in the communities
of both lake sections upon restoration. According to the
CA on the presence–absence data, all samples belonging
to the period after restoration resembled each other and
differed considerably with the samples from the reference period and the period before restoration. A similar
pattern emerged from the biomass data obtained from
spring samples but not from summer samples. Biomass
structure of summer samples after restoration measures
differed considerably with samples from the period
before restoration but showed high resemblance with
samples from the reference period. There was only one
sample that did not accord to this pattern, that is, the
sample that was taken in the southern section immediately after restoration (AR-S1).
The shifts in community structure are further illustrated
in Figure 6. In the reference period (1929–1931), communities were dominated by chydorids and Diaphanosoma
(together >80% of total cladoceran estimated biomass).
The period before restoration measures (1999–2000) was
in both lake sections characterized by the presence of
Bosmina and small daphniids (mainly Daphnia galeata,
D. ambigua, and Ceriodaphnia pulchella) (>90% of cladoceran biomass). After restoration measures (2003–
2005), the most important taxa (>70% of the biomass) in
the community during spring were Diaphanosoma and
daphniids (both large species like Daphnia pulex, D.
magna, D. obtusa, Simocephalus vetulus and small Daphnia
species). During summer, large daphnids and Diaphanosoma dominated (>70% of the biomass). The proportion
of large daphnids (mainly D. pulex) after restoration
measures during summer was substantially larger in the
southern section than in the northern section.
Discussion
Community Responses to Restoration Measures
We observed a low species richness and conservation
value of the cladoceran communities in both lake sections
before restoration measures. High levels of primary productivity (Jeppesen et al. 2000; Declerck et al. 2007) combined with a high fish predation pressure and a lack of
submerged macrophytes, which can serve as substrate
and refuge against fish predation (Jeppesen et al. 1998a;
Declerck et al. 2005), were probably responsible for the
low species richness. In both lake sections, the cladoceran communities were dominated by small-sized species
(Bosmina, Ceriodaphnia pulchella, Daphnia ambigua, and
D. galeata) that are known to inhabit eutrophic systems
and coexist with fish.
After restoration measures had taken place, species
richness increased gradually in both sections and this
Restoration Ecology
SEPTEMBER 2009
Evaluation of Restoration Measures in a Shallow Lake
Table 2. Complete list of cladoceran zooplankton species that have been observed in Lake Kraenepoel in the time span between 1929 and 2005.
Luyten (n ¼ 38)
Disappeared
Acantholeberis curvirostris
Alonella excisa
A. nana
Ceriodaphnia laticaudata
Daphnia longispina
Drepanothrix dentata
Lathonura rectirostris
Monospilus dispar
Polyphemus pediculus
Rhynchotalona falcata
Recovered
Alona costata
A. guttata
Alonella exigua
Ceriodaphnia quadrangula
Eurycercus lamellatus
Graptoleberis testudinaria
Leydigia acanthocercoides
L. leydigi
Oxyurella tenuicaudis
Pleuroxus laevis
Scapholeberis mucronata
Sida crystallina
Always present
Acroperus harpae
Alona affinis
A. quadrangularis
A. rectangula
Bosmina longirostris
Camptocercus rectirostris
Ceriodaphnia pulchella
Chydorus sphaericus
Daphnia cucullata
D. galeata
Diaphanosoma brachyurum
Disparalona rostrata
Ilyocryptus agilis
I. sordidus
Pleuroxus aduncus
P. trigonellus
P. truncatus
Pseudochydorus globosus
Simocephalus vetulus
New
Daphnia ambigua
D. magna
D. obtusa
D. pulex
Macrothrix laticornis
Pleuroxus denticulatus
P. uncinatus
BR-N (n ¼ 14)
BR-S (n ¼ 14)
AR-N (n ¼ 60)
AR-S (n ¼ 40)
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Species are grouped into classes (disappeared, recovered, always present, and new) according to their occurrence in the different periods. Cross marks indicate the
presence of species in each of the distinguished periods. Luyten: species list of Luyten (1934), completed with species that were found by us during a reanalysis of a subset of his samples (n ¼ 5); BR-N and BR-S: the period before restoration in the northern and southern sections (1999–2000); AR-N and AR-S: the period after restoration in the northern and southern sections (2001–2005). Total numbers of samples for each period are given within parentheses.
process occurred in a relatively short time span. We are
aware that part of the changes may be due to differences
in sampling methodology, as in the period 1999–2002
SEPTEMBER 2009
Restoration Ecology
(before restoration and shortly after restoration), zooplankton was sampled with a Schindler-Patalas trap,
whereas a tube sampler was used between 2003 and 2005.
633
Evaluation of Restoration Measures in a Shallow Lake
Spring
Summer
B
14
14
12
12
Species richness
Species richness
A
10
8
6
4
10
8
6
4
2
2
(3)
0
0
193
(2)
(3)
-N1
-N2
(2)
N
BR- AR
AR
(2)
(3)
-S1
-S2
(2)
S
BR- AR
(2)
0
0
193
AR
(2)
(3)
-N1
-N2
(1)
N
BR- AR
AR
(1)
(3)
(1)
-S1
S
BR- BR
S2
BR-
Figure 2. Average species richness of cladoceran communities estimated for different time periods during the past century (1930: reference
period; BR-N and BR-S: before restoration in the northern and southern sections; AR-N1 and AR-S1: shortly after restoration in the northern
and southern sections; AR-N2 and AR-S2: after restoration in the northern and southern sections) in spring (A) and summer (B). Error bars
represent interannual variability in species richness and denote the SE of the mean. Total numbers of samples for each period are given within
parentheses.
In contrast to the tube sampler, the Schindler-Patalas trap
is not very effective when used within macrophyte beds
and may potentially yield an underestimation of species
richness in the period before 2003. There were, however,
no submerged macrophytes in the southern lake section
before restoration measures, so it is unlikely that the
increase in species richness in this section resulted from
lower sampling efficiency. Furthermore, as in both periods, samples were taken at various randomly chosen locations in the water body and a similar standardized analysis
protocol was followed for all samples (identification of the
Summer
Spring
A
3.0
2.5
Conservation value
Conservation value
3.0
same number of individuals in each sample), we are confident that the patterns are well assessed.
The community structure also responded to the restoration measures in terms of biomass structure with an
increased dominance of large-bodied species (e.g., Diaphanosoma but also Daphnia magna, D. pulex, and Simocephalus vetulus). This is in agreement with the patterns
observed in the literature (Jeppesen et al. 1990; Moss
et al. 1996), where large daphniids increased after restoration of eutrophied shallow lakes. The near absence of fish
(Louette et al. unpublished data) in both sections during
2.0
1.5
B
2.5
2.0
1.5
(1)
1.0
(3)
0
193
(2)
(2)
(3)
1
2
N
BR- AR-N AR-N
(2)
(2)
(3)
1
2
S
BR- AR-S AR-S
1.0
(2)
0
193
(2)
(3)
1
2
N
BR- AR-N AR-N
(1)
(1)
(3)
1
2
S
BR- AR-S AR-S
Figure 3. Average conservation value of cladoceran communities estimated for different time periods during the past century (1930: reference
period; BR-N and BR-S: before restoration in the northern and southern sections; AR-N1 and AR-S1: shortly after restoration in the northern
and southern sections; AR-N2 and AR-S2: after restoration in the northern and southern sections) in spring (A) and summer (B). Error bars
represent interannual variability in conservation value and denote the SE of the mean. Total numbers of samples for each period are given
within parentheses.
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Restoration Ecology
SEPTEMBER 2009
2
2
Evaluation of Restoration Measures in a Shallow Lake
A
B
BR-N
CA axis II (13% of variance)
BR-S
Aaf
Csp
Blo
Dga
Iso
AR-N2
AR-S1
AR-S2
Ana
Gte
1930
AR-N1
Ela
Dam
Aqu
Dbr
Aha
-2
-2
Sve Cre
-2
2
-2
2
2
2
CA axis I (25% of variance)
C
D
BR-N
Cpu
CA axis II (13% of variance)
BR-S
Blo
Dam Csp
AR-N1
Dga
AR-N2
Ela
Gte
1930
AR-S2
Cre
Sve
Pla
Aaf
Dro
Aha
Aqu
Dbr
Cqu
-2
-2
-2
AR-S1
CA axis I (38% of variance)
2
-2
2
Figure 4. Biplot representation of compositional changes in the cladoceran communities among the reference period (1929–1931), the period
before the restoration measures (1999–2000), and the periods after restoration measures (2001–2005). Biplots were obtained by performing CAs
on the presence/absence data of spring samples (A and B) and summer samples (C and D). A and C represent sample scores and B and D represent species scores (only species with a weight >10% are displayed). 1930: reference period (n); BR-N and BR-S: before restoration in the northern ()) and southern (3) sections; AR-N1 and AR-S1: shortly after restoration in the northern (h) and southern (s) sections; AR-N2 and
AR-S2: after restoration in the northern (1) and southern (,) sections. Aaf, Alona affinis; Aha, Acroperus harpae; Ana, Alonella nana; Aqu, Alona
quadrangularis; Blo, Bosmina longirostris; Cpu, Ceriodaphnia pulchella; Cqu, Ceriodaphnia quadrangula; Cre, Camptocercus rectirostris; Csp,
Chydorus sphaericus; Dam, Daphnia ambigua; Dbr, Diaphanosoma brachyurum; Dga, Daphnia galeata; Dro, Disparalona rostrata;
Ela, Eurycercus lamellatus; Gte, Graptoleberis testudinaria; Iso, Ilyocryptus sordidus; Pla, Pleuroxus laevis; Sve, Simocephalus vetulus.
the period after restoration allowed large-sized cladoceran
species to thrive, as they are better competitors in the
absence of fish predation (Gliwicz 1990). In general, community structure was similar for both sections despite their
SEPTEMBER 2009
Restoration Ecology
physical isolation (artificial dam), suggesting deterministic
recovery trajectories. However, in the summer immediately following the restoration, samples of the southern
lake section (AR-S1) deviated strongly from all other
635
2
2
Evaluation of Restoration Measures in a Shallow Lake
A
B
Blo
BR-S
CA axis II (18% of variance)
BR-N
Aaf
Csp
1930
Gte
Dga
AR-S1
Ptru
AR-N1
AR-N2
Iso
AR-S2
Dbr
Aha
Sve
Cre
-2
-2
-2
2
-2
2
2
2
CA axis I (28% of variance)
C
CA axis II (22% of variance)
Ela
D
AR-S1
Dpu
Dga
Aex
1930
AR-N1
AR-S2
Dlo
Sve
Cqu
Aha
Dbr
AR-N2
Csp
Blo
Cpu
BR-N
BR-S
-2
-2
Dam
-2
CA axis I (28% of variance)
2
-2
2
Figure 5. Biplot representation of compositional changes in the cladoceran communities among the reference period (1929–1931), the period
before the restoration measures (1999–2000), and the periods after restoration measures (2001–2005). Biplots were obtained by performing CAs
on the log (x 1 1)-transformed biomass data of spring samples (A and B) and summer samples (C and D). A and C represent sample scores and B
and D represent species scores (only species with a weight >10% are displayed). 1930: reference period (n); BR-N and BR-S: before restoration
in the northern ()) and southern (3) sections; AR-N1 and AR-S1: shortly after restoration in the northern (h) and southern (s) sections;
AR-N2 and AR-S2: after restoration in the northern (1) and southern (,) sections.Aaf, Alona affinis; Aex, Alonella excisa; Aha, Acroperus harpae;
Blo, Bosmina longirostris; Cpu, Ceriodaphnia pulchella; Cqu, Ceriodaphnia quadrangula; Cre, Camptocercus rectirostris; Csp, Chydorus sphaericus;
Dam, Daphnia ambigua; Dbr, Diaphanosoma brachyurum; Dga, Daphnia galeata; Dlo, Daphnia longispina; Dpu, Daphnia pulex;
Ela, Eurycercus lamellatus; Gte, Graptoleberis testudinaria; Iso, Ilyocryptus sordidus; Ptru, Pleuroxus truncatus; Sve, Simocephalus vetulus.
samples. This was because the cladoceran community
was strongly dominated by D. pulex (and to a lesser extent
D. magna) (>70% of total cladoceran biomass). The
636
strong increase of these large-bodied species after restoration measures were most probably due to the removal of
the fish community. Population densities of these species
Restoration Ecology
SEPTEMBER 2009
Evaluation of Restoration Measures in a Shallow Lake
Chydoridae
Daphniidae (large)
Daphniidae (small)
Diaphanosoma
Bosmina
Other species
% of Cladocera biomass
100
A
80
60
40
20
0
% of Cladocera biomass
100
1930
BR-N
BR-S
AR-N
AR-S
1930
BR-N
BR-S
AR-N
AR-S
B
80
60
40
20
0
Figure 6. Relative contribution of the most abundant taxa to the
total cladoceran zooplankton biomass (averages over years within
periods) during spring (A) and summer (B). 1930: reference period;
BR-N and BR-S: period before restoration in the northern and
southern sections (1999–2000); AR-N and AR-S: period after
restoration in the northern and southern sections.
were, however, reduced in the following years, after sediments had also been removed from the southern lake section. Large Daphnia are known to grow best in very
productive systems (Moss et al. 2005; Declerck et al. 2007).
The oligotrophication that was achieved by the removal of
sediment-associated nutrients probably resulted in a more
pronounced P limitation, which favored a shift to a dominance of Diaphanosoma (Kyle et al. 2006).
An important question is whether the origin of species
in the restored habitat is mainly arising from external
sources (neighboring water bodies) or rather from internal
sources (dormant propagule bank). This question can only
unequivocally be answered with genetic analysis (Pollard
et al. 2003). For degraded deep lakes, an internal origin of
SEPTEMBER 2009
Restoration Ecology
species that dominate after restoration is in most cases not
obvious as the dormant egg bank is often covered by the
sediment, and main stressors in these environments such
as acidification and metal contamination affect the viability of propagules (Angeler & Garcı́a 2005). Furthermore,
due to the gradual increase in habitat quality in those systems, it is very difficult to determine whether the occurrence of a species can be dedicated to its arrival capacity
from external sources or to improving hatching conditions
during restoration. The successful reoccurrence of species,
which have been shown to originate from internal sources
(dormant egg bank, refuge populations), is often delayed
(up to almost a decade) by competitive interactions with
the alternate active community (Keller & Yan 1998;
Keller et al. 2002; Binks et al. 2005). Overall, recovery
trajectories in these systems have been shown to be stochastic (Frost et al. 2006). In the present case, there are
a number of indications that new species in postrestoration communities originate from the dormant propagule
bank. Many cladoceran taxa have high dispersal abilities
(Louette & De Meester 2005; Vandekerkhove et al.
2005b), but the short time span between the restoration
measures of the habitat and the occurrence of a rich community (in the first years after restoration) suggests an
important role of the dormant egg bank (Keller & Yan
1998). Among the species observed, there were also species that are not known to readily colonize new habitats
(Eurycercus, several other chydorids, Diaphanosoma)
(Louette & De Meester 2005). Overall, the phenomenon
of a rapid community development after sediment removal can be compared with heathlands, where typical
species emerge from the dormant seed bank after creating
suitable environmental conditions (sod cutting) (Dorland
et al. 2005).
Evaluation of Restoration Success
The restoration measures conducted in the shallow lake
consisted of an intervention in the food chain (removal of
planktivorous and benthivorous fish, introduction of piscivores) and a reduction of the internal and external nutrient loading (diversion of eutrophied inlet and removal of
the anoxic and nutrient-rich organic sludge layer). Our
data allow the assessment of restoration success by three
different criteria as follows: (1) the achievement of a target
condition (balanced ecosystem functioning, i.e., stabilization of a clearwater state), (2) the increase of species richness and conservation value, and (3) the approximation of
a historical reference (high nature value) period.
Restoration was successful according to the first criterion. Restoration measures restored the clearwater phase,
with an increase in submerged vegetation and a substantial
reduction in nutrient levels and phytoplankton biomass
(Table 3). Also for the second criterion, restoration can be
regarded as successful. We are aware that inference of the
data should be done with care, as different years within
each period were used as replicates (pseudoreplication),
637
Evaluation of Restoration Measures in a Shallow Lake
Table 3. Mean values for the most important abiotic and biotic
parameters for both sections of Lake Kraenepoel.*
NO3-N (lg/L)
PO4-P (lg/L)
Suspended solids (mg/L)
Phytoplankton (lg/L)
Macrophyte cover
of lake bottom (%)
BR-N
BR-S
AR-N
AR-S
392
207
7
737
40
632
210
33
1,874
—
24
13
12
85
55
63
158
18
521
—
BR-N and BR-S: the period before restoration in the northern and southern
sections (1999–2000); AR-N and AR-S: the period after restoration in the
northern and southern sections (2001–2002).
* Source: Adopted from Van Wichelen et al. (2007).
but can assume that species richness and conservation
value, which were low before restoration, tended to
increase considerably and on a short term after restoration. The restoration may also be considered successful
regarding the third criterion. Restoration resulted in the
reappearance of about 55% of the species that had disappeared since the 1929–1931 survey (12 recovered species
out of 22 species). Furthermore, according to the CA
results, restoration also resulted in a shift in the biomass
structure of the cladoceran communities in the direction
of the community structure as it was observed in samples
dating from the reference period, especially for the summer season. The resemblance between the restored communities and the reference communities seems, however,
mainly the result of a strong increase in relative biomass
of one species, that is, Diaphanosoma brachyurum. This
species indicates a low availability of algae (low nutrient
conditions) (DeMott 1985) and is a good competitor at
high water temperatures (Hart 2000). Recovery of this
species after oligotrophication of eutrophied lakes has
also been reported in other studies (Stich 2004).
In particular, the restoration of populations of chydorid
(e.g., Alonella, Monospilus, and Rhynchotalona) and macrothricid (e.g., Acantholeberis, Drepanothrix, and Lathonura) species was not entirely successful. A comparison of
the species list of the reference period with the one after
restoration shows that although a majority of chydorid
species have reappeared, occurrences are often sporadic
and population densities low. Possibly, suitable habitat
conditions (well-developed layer of submerged macrophytes) are still marginal or lacking. Some species may
also have failed to recover from the dormant propagule
bank, and some may also have been missed during the
sampling. Nowadays, some of these species have become
very rare in European northwestern lowlands (e.g., Drepanothrix, Lathonura, Monospilus, and Rhynchotalona;
Louette et al. 2007), and it may take a long time before
these species are able to reach the shallow lake again.
The recent survey (1999–2005) also revealed some species that were not reported from the reference period.
Several of these (e.g., D. ambigua and Pleuroxus denticulatus) are nonindigenous species that were introduced in
638
Belgium after the study of Luyten (1934). Large-bodied
species, like D. magna, D. pulex, or D. obtusa, were also
lacking in the samples of the reference period. The
absence of these large daphniids is probably the result of
lower productivity in those days (Louette et al. 2007)
rather than fish predation, as these species were observed
before the restoration measures when fish predation was
intensive.
We demonstrate that comparisons of historical habitatspecific samples (often representing a reference period of
good ecological quality) with newly formed communities
after restoration provides very valuable information for
evaluating the restoration success of habitats. Compared
to achieving a target condition, or merely demonstrating
a change in species richness following restoration, the
advantages of analyzing historical samples are substantial,
as very detailed information can be obtained. Community
structures may directly be compared and differences in
structure be related to changes in environmental conditions (e.g., climate, land use, food web structure). Additionally, the gain or loss of specific species can accurately
be documented, dated, and related to local or regional factors (e.g., the absence of specific species despite the trophic structure recovery, potentially as a result of dispersal
limitation). Drawbacks of comparing sets of samples
among different periods involve the often different sampling gear applied; however, these may partly be overcome by a standardized analysis of samples. Another
obstacle is that samples from historical times are in many
cases not readily available, so one has to rely on historical
published species lists (Vrba et al. 2003), contemporary
conditions in reference habitats (Keller et al. 2002; Yan
et al. 2004; Frost et al. 2006), or paleolimnological reconstructions based on organic remnants (Pollard et al. 2003;
Sarnelle & Knapp 2004), which makes direct interpretations more difficult. Overall, it is clear that for future lake
restoration efforts, evaluation of the applied measures will
benefit substantially when comparisons with reference
conditions are performed, ideally after processing historical habitat-specific samples, alternatively after paleolimnological reconstructions or analysis of other reference
habitats.
Conclusions
Biological recovery of degraded systems may follow the
restoration of the physical and chemical environment
(Yan et al. 2003). Whether, and on what time span this
biological recovery occurs, depends on the accuracy with
which restoration measures were executed and the colonization potential of the model group under study. Our
study demonstrates that partial recovery of cladoceran
zooplankton communities in restored shallow lakes can
take place rapidly and suggests that recovery trajectories
may follow a deterministic path. The restoration of the original environment (removal of sediment layer, elimination
of fish stocks, and stimulation of macrophyte vegetation)
Restoration Ecology
SEPTEMBER 2009
Evaluation of Restoration Measures in a Shallow Lake
and the availability of a large species pool in the dormant
propagule bank (Vandekerkhove et al. 2005a) have probably allowed the cladoceran communities to assemble rapidly through the process of species sorting (Cottenie & De
Meester 2004; Louette et al. 2006).
The success of the restoration measures in Lake Kraenepoel can be considered high according to different criteria. Restoration measures succeeded in achieving the
intended target of restoring a clearwater state. The richness and conservation value of at least one organism
group, the cladoceran zooplankton, increased upon restoration. Furthermore, community structure shifted back in
the direction of that recorded from samples from a historical reference period. Additionally, an important fraction
of species that seemed to have disappeared since the reference period reappeared after restoration. Nevertheless,
restoration measures did not result in a complete restoration of the habitat, as some species remained absent in the
communities. This may partially be due to the still relatively marginal development of structural habitat (submerged macrophytes). We expect that recovery can reach
completeness as soon as submerged macrophytes have
developed, and species richness levels will last when the
lake remains properly managed (e.g., balanced fish stocks,
regular drawdown).
Implications for Practice
Restoration of shallow lakes will have the highest
chance on success when measures concentrate on the
(1) reduction of the nutrient load and (2) alteration
of the food web structure.
d Restoration success can be evaluated by different criteria, such as (1) reaching a target condition, (2)
increase of diversity levels and conservation value,
(3) comparisons with the community structure originating from periods before lake deterioration.
d When
shallow lakes remain properly managed
(maintaining low nutrient levels, fish stocks in equilibrium), a distinct recovery can occur on a relatively
short time interval.
d For the evaluation of future lake restoration efforts,
comparisons between actual communities and those
from a reference (pristine) state, ideally from historical habitat-specific samples, alternatively from paleolimnological reconstructions or other reference
habitats, offer an important added value.
d
Acknowledgments
This study was carried out in the framework of LIFE project (LIFE98NAT/B/5172) ‘‘Restoration and management
of Lake Kraenepoel (Aalter)’’ and financially supported
by the European Union (EU), the Flemish (ANB), and
local (Aalter) government. We thank the Pettiaux family,
SEPTEMBER 2009
Restoration Ecology
owners of the northern section of the lake, for their cooperation, and the many people who helped with sampling and sample processing. S.D. is a postdoctoral fellow
of the Fund for Scientific Research—Flanders (FWOVlaanderen). J.V. is an experienced researcher within
the EU Research Training Network (FP6-512492).
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