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Water-level fluctuations regulate the structure and
functioning of natural lakes
VESELA V. EVTIMOVA*
†
AND IAN DONOHUE*
‡
*School of Natural Sciences, Department of Zoology, Trinity College Dublin, Dublin, Ireland
†
Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, Sofia, Bulgaria
‡
Trinity Centre for Biodiversity Research, Trinity College Dublin, Dublin, Ireland
SUMMARY
1. Despite becoming one of the main pressures on aquatic ecosystems globally, understanding of the
ecological impacts of altered water-level regimes in lakes lags far behind that of other human
disturbances (e.g. eutrophication, acidification).
2. We employed a multifaceted approach to explore the potential importance of water-level
fluctuations (WLF) for the structure and functioning of littoral zones and multiple trait responses of
primary producers and benthic consumers across a range of natural lakes.
3. We found that lakes with high WLF had significantly more coarse littoral substrata with less
coverage of macrophyte vegetation in the shallows than in lakes with low WLF. Lakes with high
WLF also had greater proportions of motile diatom species and omnivorous benthic invertebrates
in shallow waters, altered taxonomic and trophic structure of benthic consumers and more
homogeneous algal and benthic invertebrate assemblages.
4. Variation along the littoral depth gradient needs to be examined when assessing the impacts of
hydrological pressures in lakes. We found that depth interacted with WLF in its effects on habitat
structure and mediated the response of both producer and consumer benthic assemblages to WLF.
5. Our results indicate that amplified WLF significantly affect both the structure and functioning of
lake ecosystems. Given the growing importance of WLF as an increasingly pervasive pressure on
lake ecosystems worldwide, our findings have important implications for the conservation and
management of global aquatic biodiversity. Inclusion of both biological traits and sampling along a
depth gradient in existing and in future monitoring programmes could improve significantly the
ability to detect and predict effects of altered patterns of WLF on lake ecosystems.
Keywords: benthic, ecosystem functioning, habitat structure, hydrological disturbance, littoral
Introduction
Hydromorphological pressures are becoming one of the
main threats to the ecological integrity of lake ecosys-
tems globally (Bragg et al., 2003; Solimini et al., 2006;
Wantzen et al., 2008b; Cardinale, 2011). Most lakes are
subject to natural, mostly seasonal, fluctuations in water
levels (Smith, Maitland & Pennock, 1987; Keough et al.,
1999; White et al., 2008, Evtimova, 2013), and natural
water-level variations may support the biodiversity and
productivity of littoral zones (Gafny & Gasith, 1999;
Coops & Hosper, 2002). However, alteration of natural
patterns of WLF can compromise not only the ecological
integrity of lakes (Wantzen et al., 2008b; Zohary & Ostro-
vsky, 2011; Deegan, White & Ganf, 2012; Yin & Yang,
2012), but also the provision of ecosystem goods and
services and the sustainable use and management of
standing water bodies in the face of a multitude of
adverse human impacts (Johnson, Revenga & Echever-
ria, 2001; Coops, Beklioglu & Crisman, 2003; Schmieder
et al., 2004; Beklioglu, 2007; Wantzen et al., 2008b;
Palmer, 2010). This is because the ecological effects of
WLF in lakes are likely to be greatest in littoral zones
(Solimini et al., 2006; Wantzen et al., 2008b), where even
Correspondence: Vesela Evtimova, Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 1 Tsar Osvoboditel
Blvd., Sofia 1000, Bulgaria. E-mail: evtimovv@tcd.ie
©2015 John Wiley & Sons Ltd 251
Freshwater Biology (2016) 61, 251–264 doi:10.1111/fwb.12699
small draw-downs can result in the conversion of large
areas of standing water to air-exposed habitats and vice
versa (Palom€
aki, 1994; Leira & Cantonati, 2008). Further-
more, littoral zones support the significant majority of
biological diversity in lakes (Wetzel, 2001; O’Sullivan &
Reynolds, 2004; Stendera & Johnson, 2008; Vadebon-
coeur, Mcintyre & Zanden, 2011) and provide important
feeding and breeding habitat (Sabo, Finlay & Post, 2009;
Hampton et al., 2011). Thus, impairing lake littoral zones
could cause significant alterations to lake ecosystems,
with consequences for associated terrestrial areas (Van-
der Zanden & Vadeboncoeur, 2002; Wesner, 2011; Yin &
Yang, 2012).
Despite the growing significance of altered WLF as a
global pressure on lakes, relatively little is known about
the importance of different water-level regimes for the
structure and ecological functioning of littoral zones.
Many studies of water-level fluctuations comprise com-
parative studies of macrophytes (Rorslett, 1984; Furey,
Nordin & Mazumder, 2004; Deegan et al., 2012). This
work has indicated that significant WLF may reduce the
diversity and coverage of macrophytes (Rorslett, 1984,
1985; Valdovinos et al., 2007), leading to reduced overall
structural diversity of lake littorals (i.e. loss of habitats
and food resources), increased erosion (Black, Barlow &
Scholz, 2003; Valdovinos et al., 2007), reduced organic
matter availability and modified input of allochthonous
matter from the riparian zone (Wantzen, Junk & Roth-
haupt, 2008a). While previous studies have advanced
understanding of the ecological role of water-level
regimes of lakes, they are all limited in scope, as they
are typically either single-lake studies or comparative
studies of two water bodies with contrasting water-level
regimes, or focus on single biotic groups and/or a par-
ticular assemblage trait.
Results of a recent experiment on artificial lakeshores
in large outdoor mesocosms (Evtimova & Donohue,
2014) demonstrated that amplified WLF reduce benthic
algal biomass and both the density and taxonomic dis-
tinctness of littoral benthic invertebrate assemblages.
Furthermore, both the taxonomic and trophic structure
of benthic assemblages was altered significantly in meso-
cosms with extreme WLF. Results of observational stud-
ies in lakes are largely consistent with these findings,
indicating that significant WLF can reduce both the den-
sity and diversity of littoral benthic invertebrate assem-
blages (Hunt & Jones, 1972; Smith et al., 1987;
Jurkiewicz-Karnkowska, 1989; Prus, Prus & Bijok, 1999;
Scheifhacken, Fiek & Rothhaupt, 2007; Valdovinos et al.,
2007; Aroviita & H€
am€
al€
ainen, 2008; Baumg€
artner, M€
ortl
& Rothhaupt, 2008; Brauns, Garcia & Pusch, 2008; White
et al., 2008, 2010; McEwen & Butler, 2010). Evtimova &
Donohue (2014) also found that WLF can modify biotic
assemblages in distinct ways along the littoral depth
gradient. These findings have important implications for
the ecology and biological diversity of standing water
ecosystems but have yet to be tested at larger spatial
scales in natural lakes.
Elucidating the ecological impacts of disturbance on
lake littoral zones is frequently hindered by highly
heterogeneous distributions of organisms, a consequence
of high local-scale variability in a range of factors,
including water chemistry, shore morphology, habitat
structure and biotic interactions (Karjalainen et al., 1999;
Nystrom et al., 2001; Tolonen et al., 2001, 2005; Schindler
& Scheuerell, 2002; Lepp€
a, H€
am€
al€
ainen & Karjalainen,
2003; Brauns et al., 2007; Donohue et al., 2009a). In order
to be able to capture key aspects of functional diversity,
we used simultaneously taxonomy- and trait-based met-
rics of biotic response, as opposed to considering species
mostly individually. Given the spatially heterogeneous
nature of littoral zones within and among lakes, trait-
based approaches (e.g. dietary preferences, motility)
have particularly strong potential for detecting the
impacts of amplified WLF on lakes (Evtimova & Dono-
hue, 2014) and for the ability to generalise findings
across ecosystems (Cavender-Bares et al., 2009; Hille-
brand & Matthiessen, 2009; Menezes, Baird & Soares,
2010). Accordingly, we followed a multi-trait approach
to examine abiotic and biotic differences between sets of
natural lakes that have experienced contrasting ampli-
tudes of WLF over long timescales (at least three dec-
ades). Specifically, we examined whether (i) littoral
habitat structure differed in lakes with contrasting WLF
and, if so, how; (ii) a variety of taxonomy- and trait-
based aspects of littoral benthic communities may reflect
differences in the hydrological regimes of natural lakes
and (iii) the compositional and/or functional hetero-
geneity of biotic assemblages in space is reduced signifi-
cantly in lakes with high WLF.
Methods
Lake selection
We quantified habitat structure and the structure of
algal and macroinvertebrate assemblages along the lit-
toral depth gradient in eight lakes representative of both
ends of the spectrum of WLF in natural lakes in Ireland
(Table 1; Fig. S1) as annual and monthly ranges were
identified as important descriptors of water-level
regimes (Evtimova, 2013). Four of the lakes had high
©2015 John Wiley & Sons Ltd, Freshwater Biology,61, 251–264
252 V. V. Evtimova and I. Donohue
mean annual (>1 m) and monthly (≥0.44 m) amplitudes
of WLF (high WLF) and the remaining four had rela-
tively minor variations in water level (low WLF; mean
annual ranges ≤0.65 m; mean monthly ranges ≤0.21 m;
Table 1, Fig. S1). The lakes were selected for sampling
based on the following criteria: (i) presence of active
water-level recorders, (ii) availability of at least 30 years
of continuous water-level data, (iii) good data quality
with minimal number of missing daily water-level read-
ings and (iv) adequate availability of appropriate and
accessible sampling habitat. Sampling was confined to
stony substrata as they are easy and relatively economi-
cal to sample and their communities are known to
respond to human-induced pressure, including water-
level regulation (Brauns et al., 2007; Aroviita &
H€
am€
al€
ainen, 2008; Donohue et al., 2009a; Tolonen &
H€
am€
al€
ainen, 2010; White et al. 2010). In addition, lakes
with total phosphorus concentrations in excess of
100 lgL
1
or with alkalinity less than 10 mg CaCO
3
L
1
were excluded from the study. Apart from the a priori
determined differences in the amplitudes of WLF, the
selected lakes in both WLF groups exhibited similar
ranges of physical and chemical characteristics (Table 1).
There was no difference in overall water chemistry
between the two WLF groups (MANOVA; F
1,24
=1.17,
P=0.32).
Field sampling and laboratory analyses
Lakes were sampled during an 8-week period between
late May and July 2009, when WLF were relatively low
(Evtimova, 2013), in order to avoid sampling flooded
areas. Four straight-line transects were established in
every lake, orientated perpendicular to the shoreline and
extending to about 1 m water depth. Water samples
were collected using a weighted 5 dm
3
polypropylene
bottle thrown lakewards three times from the deepest
end of each transect (Donohue & Irvine, 2008). Water
column alkalinity (mg CaCO
3
L
1
after titration with
sulphuric acid), pH, conductivity (using a microproces-
sor conductivity meter LF 196 WTW TetraCon
â
GmbH,
Germany), total phosphorus [TP following Eisenreich,
Bannerman & Armstrong (1975)], dissolved total organic
carbon and total nitrogen [DTOC and TN, using a Vario
TOC Cube, Elementar Analysensysteme GmbH (Hanau,
Germany)] and chlorophyll a[quantified colorimetrically
after methanol extraction (Standing Committee of Ana-
lysts, 1983)] were quantified from each site. All filtering
was done immediately upon collection using 47-mm
GF/C glass microfibre filter papers (Whatman
â
, Maid-
stone, UK).
Littoral habitat structure (inclusive of macrophyte
cover), and benthic algae and invertebrate assemblages
were quantified at three sampling sites (1 91 m) along
each transect, with their mid-points being located at
water depths of 0.1 m (shallow), 0.45 m (intermediate)
and 0.8 m (deep site). We assessed habitat structure
in situ by estimating the relative (%) coverage of each of
sand/silt, gravel, pebbles, cobbles, boulders, bedrock,
coarse woody debris (CWD), soil, flooded grass/roots,
leaves/debris and macrophytes using a bathyscope and
a191 m Stafford Frame comprising 25 quadrats of
equal size. The mid-point of the frame was located at
the target water depth.
Table 1 Characteristics of the lakes selected for field surveys, with mean (SD) annual (AR) and monthly (MR) ranges, pH, alkalinity and
total phosphorus concentrations and the year in which the water level recording commenced
WLF Group Lake
Location
(N, W)
Mean
AR (m)
Mean
MR (m)
Records
began
Surface
area (ha) pH
Alkalinity
(mg CaCO
3
L
1
)
TP
(lgPL
1
)
High WLF Anure 55°00012″
8°16024″
1.06 0.17 0.52 0.21 1976 133 6.8 12 37
Eske 54°41037″
8°03032″
1.04 0.07 0.44 0.16 1977 385 7.5 11 6
Muckno 54°06048″
6°40057″
1.43 0.32 0.46 0.27 1976 354 8 47 38
Oughter 54°00032″
7°28016″
2.72 0.38 0.78 0.45 1977 658 7.9 70 72
Low WLF Ennell 53°27054″
7°22046″
0.65 0.17 0.15 0.10 1979 1151 8.1 154 17
Moher 53°43042″
9°32053″
0.59 0.19 0.21 0.12 1977 36 7.3 16 11
Owel 53°34009″
7°21050″
0.58 0.22 0.10 0.06 1975 1018 8.3 96 10
Skeagh 53°57007″
7°00022″
0.65 0.13 0.16 0.09 1975 61 7.3 30 40
©2015 John Wiley & Sons Ltd, Freshwater Biology,61, 251–264
Water-level fluctuations regulate lake ecology 253
Epilithic algae were collected by washing a known
area of the upper surface of stones from each sampling
site (following Cameron, 1997). The samples were fil-
tered for subsequent determination of algal biomass (as
described previously) and organic matter (after loss on
ignition at 550 °C for 3.5 h). Diatom assemblage struc-
ture was quantified from epilithic algal samples that
were preserved with Lugol’s iodine solution and kept in
light-resistant glass bottles at <4°C. Benthic invertebrate
assemblages were sampled from each site by standard
kick sampling (i.e. Ausden, 1997) using a 500-lm Fresh-
water Biological Association hand-held pond net. Faunal
samples were standardised in area and time (1 m
2
,20s)
and were preserved in 75% ethanol. Diatoms and ben-
thic invertebrates were identified to the highest taxo-
nomic resolution practicable. Benthic invertebrates were
assigned to functional feeding (trophic) groups and cate-
gories of locomotive capacity following Cummins &
Klug (1979) and Schmidt-Kloiber et al. (2006). Owing to
logistical constraints, the structure of benthic algae and
invertebrate assemblages was quantified from a random
subset of three of the four transects in each lake.
Data analyses
All statistical analyses comprised two fixed factors:
amplitude of WLF (two levels: low and high) and water
depth (three levels: shallow, intermediate and deep).
Lake and transect number were incorporated as random
factors and nested within, respectively, WLF and lake.
Mixed-model analysis of variance (ANOVA) based on
Type III sum of squares was used to test for differences
in univariate response variables among lakes experienc-
ing high and low WLF. Fisher’s least significant differ-
ence post hoc tests provided pair-wise comparisons
between levels of significant terms. When necessary,
variables were transformed prior to analysis to meet
assumptions of normality and homoscedasticity. Multi-
variate analyses were done with permutational multi-
variate analysis of variance (PERMANOVA, Anderson,
2001; McArdle & Anderson, 2001) with the same model
structure as the univariate analyses. These analyses were
based on either Euclidian distance (habitat structure
data) or Bray–Curtis similarity (biotic data; relative
abundances were log [x +1] transformed) matrices and
were done with 9999 permutations of the residuals
under a reduced model using PRIMER
â
6.1.8 (PRIMER-
E Ltd., Plymouth, U.K.). When the number of possible
unique permutations was less than 100, P-values were
estimated using Monte Carlo simulations (Anderson,
2005; Anderson, Gorley & Clarke, 2008). We used simi-
larity percentage species contributions analysis (SIMPER;
Clarke & Gorley 2006) to investigate the contribution of
different habitat types, individual taxa, functional feed-
ing groups and locomotive categories to the pair-wise
dissimilarity between lakes with low and high WLF.
Taxon richness, Shannon’s index of diversity and Pie-
lou’s evenness were used as metrics of diatom and ben-
thic invertebrate assemblage diversity. Taxon richness
was rarefied to the minimum number of individuals
found in a sample (diatoms: 12; invertebrates: 27) to
remove the confounding influence of abundance on esti-
mates of richness (Hurlbert, 1971). The importance of
WLF for phylogenetic and taxonomic richness of algal
and invertebrate assemblages was examined by quanti-
fying each of their total phylogenetic diversity (PD), tax-
onomic distinctness (TD) and total taxonomic
distinctness (TTD) using PRIMER
â
6.1.8. Phylogenetic
diversity was calculated as the sum of the phylogenetic
branch lengths among species (Faith, 1992), TD was cal-
culated as the mean taxonomic distance between all
pairs of taxa, while TTD is a modification of species
richness that incorporates family inter-relatedness explic-
itly (Clarke & Warwick, 2001; Salas et al., 2006). Hierar-
chical Linnaean classification served as a proxy for
cladograms and a basis for measuring relatedness. The
highest taxonomic resolution practicable across all taxa
found was used (genus for benthic diatoms and family
for the invertebrates). Equal weights were assigned to
each of the principal taxonomic levels.
We investigated the potential of established metrics of
aquatic disturbance as indicators of WLF in lakes by
focusing on two metrics that have been shown to
respond to a range of different pressures in both rivers
and lakes (Wallace, Grubaugh & Whiles, 1996; Sandin &
Johnson, 2000; Schmidt-Kloiber et al., 2006; O’Toole et al.,
2008); the average Biological Monitoring Working Party
score per taxon (ASPT; Armitage et al., 1983) and the
richness and percentage of abundance classes of Ephe-
meroptera, Plecoptera and Trichoptera (EPT scores;
Lenat, 1988).
To test hypotheses regarding the importance of con-
trasting regimes of WLF for compositional and func-
tional heterogeneity of biotic assemblages at local spatial
scales in natural lakes, we quantified spatial variability
along the depth gradient as the coefficient of variation
(CV; expressed as a percentage) calculated among sam-
ples within transects for univariate variables (benthic
chlorophyll aand organic matter concentrations) and as
the Euclidian distance among samples in Bray–Curtis
similarity space [after log(x +1)-transformation] for
multivariate analyses of benthic community structure.
©2015 John Wiley & Sons Ltd, Freshwater Biology,61, 251–264
254 V. V. Evtimova and I. Donohue
Statistical analyses were done using ANOVA following
the statistical models described previously. We tested
whether high WLF reduce the compositional and/or
functional heterogeneity of benthic assemblages among
lakes by comparing the Euclidian distances between
samples taken at each depth in lakes with high and low
WLF to their respective centroid in multivariate Bray–
Curtis space (see Donohue et al., 2009b). Significantly
lower distances to centroids in lakes with high WLF
would indicate that high WLF homogenise biotic assem-
blages among lakes.
Results
Habitat structure
Littoral habitat structure varied significantly with WLF
along the depth gradient (PERMANOVA; interaction
between WLF and water depth: pseudo F
2,60
=3.09,
P=0.003). Post hoc tests revealed that habitats differed
significantly between lakes with high and low WLF at
the shallow sampling depth (pseudo t=2.18, P=0.003),
while differences at the intermediate depth were
bordering on statistical significance (pseudo t=1.58,
P=0.073). SIMPER analysis (Table 2a) revealed
that lakes with high WLF had greater proportions of
pebble, cobble, boulders and bedrock at the shallowest
depth than lakes with low WLF. There was also a more
than three-fold reduction in the percentage of gravel
and macrophytes in lakes experiencing high WLF
(Table 2a).
Benthic algae
A total of 222 benthic diatom taxa were recorded from
the sampled lakes (Table S1). Of these, 54 taxa were
found only in lakes with low and 28 in lakes with high
WLF. No significant main or interactive effects of WLF
were found on periphyton biomass or any measure of
diatom diversity (taxonomic or phylogenetic). However,
the interaction between WLF and water depth on ben-
thic diatom assemblage structure was bordering on sta-
tistical significance (PERMANOVA; pseudo F
2,44
=1.37,
P=0.064). We found that the percentage abundance of
motile diatom taxa varied significantly with WLF along
the depth gradient (ANOVA; F
2,44
=5.86, P=0.006;
Fig. 1a). Post hoc tests revealed that the relative abun-
dance of motile diatoms was significantly greater at the
shallowest (t=3.47, P=0.01) and intermediate (t=6.80,
P≤0.0001) depths in lakes with high WLF (Fig. 1a,
Table S1).
Benthic invertebrates
One hundred and thirty taxa of littoral benthic inverte-
brates were recorded from the surveyed lakes (Table S2).
Thirty-five invertebrate taxa were found only in lakes
with low and 32 only in lakes with high WLF. Of these,
six gastropod species were found only in lakes with low
WLF. Non-operculate gastropod species were found in
high densities at the shallowest depth of lakes with low
WLF, while in lakes with high WLF these species
together with the operculate gastropods Bithynia tentacu-
lata and Viviparus viviparus were recorded mostly at the
intermediate or deep sampling sites.
There was no detectable difference between lakes
experiencing low and high WLF in the total number of
taxa, total density, taxonomic or phylogenetic diversity
of benthic invertebrates or either of the two established
metrics of disturbance (ASPT and EPT scores) that we
quantified. However, the amplitude of WLF interacted
significantly with water depth in their effects on both
the evenness (ANOVA; F
2,44
=2.91, P=0.037) and
taxonomic structure (PERMANOVA; pseudo F
2,44
=2.24,
P<0.001) of benthic invertebrate assemblages, although
the post hoc tests were inconclusive (at P<0.05).
Table 2 Results of SIMPER analyses identifying the contribution
(%) of different (a) fractions of littoral habitat structure, (b) trophic
groups of benthic invertebrate consumers at the shallowest water
depth sampled and (c) locomotive categories of benthic inverte-
brates at the deepest sampling depth to the dissimilarity between
lakes with low and high water-level fluctuations. Untransformed
data are shown for clarity
Response variable
Mean density (%) Contribution to
dissimilarity
(%)Low WLF High WLF
(a) Habitat structure
Gravel 46.3 17.8 32.5
Pebble 27.5 40.2 19.8
Cobble 5.2 17.7 17.6
Macrophytes 7.6 2.6 8.6
Soil 3.4 0.7 4.5
Bedrock 0 4.1 4.5
Boulder 0 6 4.1
Coarse woody debris 4.1 2.2 3.1
(b) Trophic structure
Shredders 24.1 11.2 28.9
Gatherers/Collectors 46.5 46.5 26
Grazers and scrapers 15.1 17.1 16.7
Predators 7 10 11.2
Filter feeders 3.9 8.6 9.7
(c) Locomotive category
Swimming 26.4 15.1 27.6
Burrowing/boring 11.1 21 27
(Semi) sessile 16.8 23.7 25.2
Sprawling/walking 45.7 40.2 20.3
©2015 John Wiley & Sons Ltd, Freshwater Biology,61, 251–264
Water-level fluctuations regulate lake ecology 255
SIMPER analysis (Table S3) revealed that lakes with
higher WLF had higher densities of chironomids (at all
sampling depths) and oligochaetes (at the deep sam-
pling depth). Furthermore, we found notably lower den-
sities of the native isopods and the amphipod Gammarus
duebeni at all depths in lakes with high WLF. In contrast,
densities of the non-native amphipods Crangonyx pseudo-
gracilis and G. pulex were considerably higher at the
shallow and intermediate depths in lakes with high
WLF. Neither of the latter two species was found at the
deep sampling sites in any of the lakes we surveyed.
The trophic structure of benthic invertebrate assem-
blages varied significantly between lakes with low and
high WLF, regardless of littoral water depth (PERMA-
NOVA; pseudo F
1,44
=4.15, P=0.043). The relative
abundance of shredders was lower and predators higher
in lakes with high WLF (Table 2b). Moreover, the rela-
tive abundance of omnivorous species was significantly
greater in lakes with high compared with low WLF
(ANOVA; interaction between WLF and water depth:
F
2,44
=3.57, P=0.037) at the shallow water depth (post
hoc test: P=0.0005; Fig. 1b). However, the reverse
occurred at intermediate water depths (P=0.022). The
locomotive structure of benthic invertebrate assemblages
also varied significantly along the depth gradient in
lakes with contrasting WLF (PERMANOVA; pseudo
F
1,44
=2.81, P=0.045). Pair-wise tests revealed signifi-
cant differences between lake groups at the deepest sam-
pling sites (pseudo t=2.10, P=0.039) with no
difference detected at any of the other depths. This shift
in locomotive structure was attributable to a decrease in
the relative abundance of swimming and sprawling/
walking species coupled with an increase in the relative
abundance of burrowing, boring and semi-sessile taxa in
lakes with high WLF (Table 2c).
Spatial heterogeneity
Benthic chlorophyll aconcentrations varied significantly
less along the depth gradient (i.e. within transects) in
lakes with high than in lakes with low WLF (ANOVA;
F
1,24
=6.53, P=0.043; dependent variable log-trans-
formed; Fig. 2a), while similar results for organic matter
were bordering on statistical significance (ANOVA;
F
1,24
=5.09, P=0.065; dependent variable log-trans-
formed). The interactive effect of high WLF and depth
in reducing the compositional heterogeneity of benthic
diatom assemblages along the depth gradient was also
bordering on statistical significance (ANOVA;
F
1,22
=3.67, P=0.068). We found no difference between
the WLF groups in the heterogeneity of any of the taxo-
nomic, functional or locomotive structure of benthic
invertebrate assemblages along the depth gradient.
At among-lake scales, the taxonomic structure of ben-
thic invertebrate assemblages in lakes with high WLF
was significantly more homogeneous than in lakes that
experienced relatively low WLF, irrespective of water
depth (ANOVA; F
1,66
=4.87, P=0.031; Fig. 2b), with the
similar effect on trophic structure bordering on statistical
significance (ANOVA; F
1,66
=3.54, P=0.064). Somewhat
in contrast to these results, benthic invertebrate assem-
blages in lakes with high WLF had more variable loco-
motive structure at the intermediate sampling depth
compared to lakes with low WLF (ANOVA; F
2,66
=3.85,
P=0.026; post hoc test for differences at the intermediate
depth: P=0.024). There was no difference between WLF
0
10
20
30
40
50
60
(a)
(b)
Shallow Intermediate Deep
Percentage of motile diatoms
** ***
0
10
20
30
40
50
60
70
Shallow Intermediate Deep
Percentage of omnivorous taxa
*** *
Fig. 1 Percentage of (a) motile diatoms and (b) omnivorous benthic
invertebrate consumers (mean +SE, n=4) at different water
depths in lakes with low (grey bars) and high (black bars) water-
level fluctuations. Untransformed data are shown here for clarity.
Asterisks indicate the level of significance for the individual depths
(*P<0.05; **P<0.01; ***P<0.001).
©2015 John Wiley & Sons Ltd, Freshwater Biology,61, 251–264
256 V. V. Evtimova and I. Donohue
groups in the compositional heterogeneity of benthic
diatom assemblages at among-lake scales.
Discussion
Our results indicate clearly that contrasting water-level
regimes drive significant differences in the ecology of
lake littoral zones, affecting not only the structure and
functioning of benthic assemblages, but also littoral habi-
tat structure. Most, though not all, of the differences
between lakes with high and low amplitudes of WLF
were mediated by the depth gradient, being generally
strongest in the zone of water fluctuation (i.e. at the
shallowest and to a lesser extent the intermediate water
depths). Our findings suggest that contrasting WLF gen-
erated a suite of community responses, altering the taxo-
nomic and trophic structure of benthic consumers and
homogenising algal and benthic invertebrate assem-
blages. These findings are consistent with those of the
experimental mesocosm study by Evtimova & Donohue
(2014) and demonstrate clearly the strong potential to
link multivariate (community) and trait-based (e.g. diet-
ary preferences or motility) biological responses to
changes in patterns of WLF. Given this, our findings
should facilitate the development of robust tools for
assessment of impacts of WLF across a broad range of
lake types and locations.
Littoral habitat structure in lakes experiencing high
WLF differed from that in lakes with low fluctuations at
the shallowest sampling depth. Higher monthly and
annual amplitudes of WLF were associated with
decreased contributions of smaller sized substratum
fractions, consistent with the observations of Furey et al.
(2004). Furthermore, the largest sized fractions at the
shallow depths were found only in lakes with high
WLF. This probably reflects the altered position of the
more turbulent upper littoral zone as a result of a rise
(conversion of terrestrial into aquatic habitat) or drop
(shift of the littoral zone lakewards) in water levels win-
nowing the fine particles from the shore zone. Therefore,
extreme WLF appear to modify directly the particle size
distribution of benthic substrata in lake littoral zones
and are responsible for increased physical stress and
related habitat displacement and loss. These findings are
consistent with the speculations of Hofmann, Lorke &
Peeters (2008) that long-term WLF could induce a slow
shoreline displacement, with continuous interplay
between short-term (weekly/monthly) and long-term
(annual/decadal) fluctuations being responsible for
shaping shore morphology and sediment grain size dis-
tribution. Both Black et al. (2003) and Valdovinos et al.
(2007) suggested that significant WLF might also
increase erosion through impairing macrophyte assem-
blages. Lakes are much less dynamic physical environ-
ments than rivers, with residence times that are orders
of magnitude longer. Thus, multi-annual patterns pre-
sumably have a much stronger influence on habitat
structure in lakes than in rivers (Wantzen et al., 2008a;
Garc
ıa Molinos & Donohue, 2014).
A myriad of environmental factors shape habitat
structure (Dodds, 2002; Hofmann et al., 2008). Aquatic
and near-shore faunal distribution depends largely on
the environment, with high diversity of habitats and
food resources generating correspondingly diverse lit-
toral communities (Wallace, 1996; Weatherhead & James,
2001; Schindler & Scheuerell, 2002; Stendera & Johnson,
2008; Tolonen & H€
am€
al€
ainen, 2010). Alteration of sub-
strata may trigger changes in lake geomorphology or
wave dynamics, thus affecting vegetation zonation indi-
rectly (Schmieder, 2004). Extreme WLF have been shown
to have an adverse effect on macrophytes, decreasing
0
20
40
60
80
100
120
Spatial CV (%)
*
0
10
20
30
40
50
60
Distance to centroids
*
Fig. 2 Spatial heterogeneity of benthic (a) chlorophyll aconcentra-
tion (measured as spatial CV) among sampling depths within tran-
sects and (b) regional scale (i.e. among lake) spatial heterogeneity
in taxonomic structure in lakes experiencing low (grey bars) and
high (black bars) amplitudes of water-level fluctuations.
©2015 John Wiley & Sons Ltd, Freshwater Biology,61, 251–264
Water-level fluctuations regulate lake ecology 257
their diversity and cover, with associated decreases in
the structural diversity and productivity of littoral habi-
tats (Rorslett, 1984, 1985; Hellsten, 2002; Acreman et al.,
2005; Valdovinos et al., 2007). Our findings of reduced
macrophyte cover at shallow depths in lakes experienc-
ing high WLF are consistent with this. Associated reduc-
tions in the structural diversity, and hence niche
availability, of littoral habitats probably affect further
lake biodiversity and impoverish ecosystems, reducing
the resistance and resilience of lakes to the ecological
impacts of anthropogenic disturbances (Cardinale, 2011;
Donohue et al., 2013).
Many studies (Townsend, Scarsbrook & Doledec,
1997; Statzner, Dol
edec & Hugueny, 2004; Bjelke, Boh-
man & Herrmann, 2005; Hillebrand & Matthiessen, 2009;
Menezes et al., 2010; C
er
eghino et al., 2012; Lange,
Townsend & Matthaei, 2014) have suggested that using
biological traits might provide greater insight into
revealing the impacts of environmental conditions and
habitat changes in lake biota. We found that lakes with
high WLF had greater proportions of motile diatom spe-
cies (Table S1) and omnivorous benthic invertebrates in
the shallows (i.e. Bithynia tentaculata,Galba truncatula,
Potamopyrgus antipodarum,Gammarus pulx,Asellus aquati-
cus). This is most likely a consequence of species with
these traits being more adaptable to dynamic water
levels and better able to cope with moderate draw-
downs or rising of water levels. Omnivory (i.e. benefit-
ing from resources from more than one trophic level) is
characteristic of animals that display functional plasticity
and possess physiological, morphological and beha-
vioural adaptations necessary to forage and process
resources that differ in chemical composition, morphol-
ogy and nutritional value (Lancaster et al., 2005). How-
ever, increased prevalence of omnivory in lakes with
high WLF may reduce the stability of these systems and
increase their susceptibility to other disturbances with
strong and (occasionally) intermediate omnivory desta-
bilising the system (Gellner & McCann, 2012).
We found highly significant differences in the taxo-
nomic structure of benthic invertebrate assemblages
between lakes with low and high WLF. There was an
overall lower density of crustacean species at all sam-
pling depths in lakes with high WLF, consistent with
the findings of Evtimova & Donohue (2014). Loss of lit-
toral species may be followed by re-colonisation pro-
vided water levels are stable (Hunt & Jones, 1972;
Hynes & Yadav, 1985), thus giving the opportunity for
new (including alien) species to establish in the ecosys-
tem as a result of freeing-up habitat niches. Altered
water-level regimes have been associated not only with
reductions in species richness but also with frequent
dominance by invasive plant species (Van Geest et al.,
2005). We found lower densities of both native amphi-
pods and isopods in lakes with high WLF, coincident
with greater densities of the invasive amphipod Cran-
gonyx pseudogracilis.Gammarus pulex, another alien
amphipod (Dick, Elwood & Irvine, 1990; Costello, 1993;
Dick, Macneil & Anderson, 1999; Dick, 2008), and the
invasive alien bivalve Dreissena polymorpha were
recorded only from lakes experiencing high WLF. High
amplitudes of WLF are likely to disturb oxygen regimes
(Acreman et al., 2005; Hofmann et al., 2008) and modify
food sources for macroinvertebrates (Wantzen et al.,
2008a). These, in tandem with intraguild predation, the
more aggressive nature of G. pulex and its greater rate of
population growth, probably facilitate the replacement
of the native G. duebenii by G. pulex (Dick et al., 1990;
Costello, 1993; Macneil, Dick & Elwood, 1997; Dick,
2008). These results suggest that the amplification of
WLF increases the susceptibility of lakes to successful
colonisation by invasive species.
We found more gastropod taxa in lakes with low
WLF, and non-operculate snails were found exclusively
in this group. On the rare occasions when recorded in
lakes with high WLF, gastropods were found at the
intermediate or deep sites. In addition to the direct
physical disturbance through shifting of the littoral zone,
gastropods in lakes with high WLF may also be sub-
jected to trophic stress. They rely partially on macro-
phytes as a food source (Cummins & Klug, 1979) and,
as demonstrated here and elsewhere (Hill, Keddy &
Wisheu, 1998; Mastrantuono et al., 2008; Wantzen et al.,
2008b), WLF are associated with reductions in macro-
phyte biomass and diversity. Moreover, both gastropod
species found only in lakes with high WLF had an oper-
culum, enabling them to resist desiccation (Gibson,
1970), survive periods of drought and thus a probable
displacement of the littoral zone. These results are con-
sistent with those of Evtimova & Donohue (2014), and
suggest that gastropods could be useful biological indi-
cators of the magnitude and timing of WLF (Mastran-
tuono et al., 2008).
The trophic structure of invertebrate assemblages dif-
fered significantly among WLF groups, owing mostly to
a more than two-fold decrease of shredders in lakes
with high WLF. This is attributable to reduction in food
availability (i.e. benthic algae, macrophytes, riparian
vegetation and leaf litter). These specialised feeders are
typically sensitive to perturbations owing to their more
restricted range of available food sources (Rawer-Jost
et al., 2000). Shredders feed on coarse particulate matter
©2015 John Wiley & Sons Ltd, Freshwater Biology,61, 251–264
258 V. V. Evtimova and I. Donohue
with preferences for the most microbially colonised
material (Cummins & Klug, 1979). They depend on the
input of allochthonous matter from the riparian zone,
which could be impeded by shifting of the littoral zone
in lakes with high WLF (Weatherhead & James, 2001;
Wantzen et al., 2008b). On the other hand, higher densi-
ties of generalist feeders (i.e. gatherers, collectors and fil-
ter feeders) in lakes with high WLF could be attributed
to their ability to employ various feeding strategies and
to tolerate changes in food availability owing to their
broad range of potential food sources (Cummins &
Klug, 1979; Barbour et al., 1996). The significantly higher
percentage of predators in lakes with high WLF was
likely to be driven by the potentially high availability of
prey organisms, both aquatic and terrestrial, that were
unable to track the more rapid fluctuations of water
levels. These results are consistent with the experimental
findings of Evtimova & Donohue (2014) and with results
for rivers (Marks, Power & Parker, 2000).
We found a decrease in the relative abundance of
motile invertebrate species at the deepest sites. This shift
in locomotive structure could be an indirect effect of
high WLF, associated with the reduction of aquatic
macrophytes and decreased contributions of smaller
sized substratum fractions that resulted from high fluc-
tuations in water level. Alteration of key aspects of func-
tional diversity (e.g. trophic or locomotive structure) of
benthic consumers could not only affect essential ecosys-
tem services that support human well-being, such as
fisheries (Menezes et al., 2010), but could also trigger
changes throughout entire lake ecosystems. Littoral
invertebrates occupy an intermediate position in energy
and matter flow in lakes and lake littoral zones provide
important food subsidies both to adjacent terrestrial
habitats and to associated aquatic ecosystems (Vander
Zanden & Vadeboncoeur, 2002; Sabo et al., 2009; Wesner,
2010, 2011; Kaufmann et al., 2014).
Benthic chlorophyll aconcentrations were significantly
less variable along the littoral depth gradient in lakes
experiencing high WLF. This is consistent with results
from mesocosms (Evtimova & Donohue, 2014) and indi-
cates potential for inclusion as an indicator of high WLF
in lakes. Our results also indicate that high monthly and
annual WLF homogenise benthic consumer assemblages
among lakes. These results have important implications
for the conservation and management of global aquatic
biodiversity, owing to the growing importance of WLF
as an increasingly pervasive pressure on lake ecosystems
worldwide. This, together with associated reductions in
diversity at among-lake scales, may have unpredictable
effects on whole aquatic ecosystems, with potentially
considerable ecological and evolutionary consequences
(Olden et al., 2004; Donohue et al., 2009b).
Although the experimental mesocosm study of Evti-
mova & Donohue (2014) found highly significant
effects of amplified WLF on many univariate taxo-
nomic and phylogenetic diversity metrics, our field
surveys found no such differences between lakes with
high and low WLF. The scaling-up of this study to
incorporate the complexity of whole-lake ecosystems,
and the consequent inclusion of significant abiotic and
biotic heterogeneity both within and among lakes,
undoubtedly reduced the ability of our study to detect
many of the perhaps more subtle effects of amplified
WLF. A key strength of our study is that the variabil-
ity both within and among lakes was accounted for
explicitly in our statistical models and any effect of
WLF was over and above these differences among
lakes. Thus, we have identified key effects of contrast-
ing patterns of WLF that were consistent and signifi-
cant across a range of lakes with a variety of biotic
and abiotic characteristics. This suggests that our find-
ings are likely to be broadly relevant and applicable
to a wide range of lakes.
Our results demonstrate the potential of linking both
trait- and multivariate community-based responses to
hydrological disturbance to expand biomonitoring
approaches beyond traditional taxonomically based
assessments that identify ecological effects. Another key
finding of our study is that the littoral depth gradient
needs to be taken into account when studying the
impacts of hydrological pressures. Depth mediated the
response of both primary producer and consumer ben-
thic assemblages to fluctuations in water level and inter-
acted with WLF in moderating habitat structure. The
importance of depth pertains to the physical shifting of
the littoral zone, resulting either in the conversion of
terrestrial habitats into aquatic ones, or converting the
sub-littoral into eulittoral. In addition, incorporating the
timing of extreme events and amplitude of fluctuations
at various temporal scales (Evtimova, 2013; Garc
ıa Moli-
nos & Donohue, 2014; Garc
ıa Molinos et al., 2015) into
field sampling programmes, coupled with sampling on
more than one occasion, could enhance significantly our
knowledge and assist in developing robust metrics for
quantifying impacts of hydrological disturbances. Poten-
tial alterations to the amplitude or seasonality of WLF
impact not only on ecosystem health and stability, but
also have important implications for flood risk assess-
ment, water management (Fitzpatrick & Bree, 2001; Jack-
son et al., 2001; Johnson et al., 2001; Baron et al., 2002;
Brown et al., 2010) and the delivery of ecosystem goods
©2015 John Wiley & Sons Ltd, Freshwater Biology,61, 251–264
Water-level fluctuations regulate lake ecology 259
and services, including water supply, fisheries and
agricultural and recreational activities (Kosarev &
Yablonskaya, 1994; Graynoth, 1999; Brunberg & Blomq-
vist, 2003; Okun, Lewin & Mehner, 2005; Okun & Meh-
ner, 2005).
In conclusion, our study indicates clearly that includ-
ing both biological traits and sampling along a depth
gradient in existing and in future monitoring pro-
grammes could improve significantly the ability to
detect and predict effects of altered patterns of WLF on
lake ecosystems. Furthermore, it comprises an important
step towards improved understanding of the ecological
effects of modified WLF and, therefore, towards
improved ability to assess and predict the ecological
impacts of this globally important pressure on standing
water ecosystems.
Acknowledgments
This work was funded as VE’s PhD project by the Irish
Research Council, with further support from the School
of Natural Sciences, Trinity College Dublin and Dublin
City Council. We thank Peter Stafford for his precious
assistance, as well as Tamara Jurca, Jorge Garc
ıa Moli-
nos, Yesim Tunali, Erna King, Alison Boyce, Marjolein
Kamermans and Mafalda Viana for assistance with field
sampling.
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Supporting Information
Additional Supporting Information may be found in the
online version of this article:
Figure S1. Long-term time-series plots of (a) annual
(AR) and (b) monthly (MR) ranges for the sampled
lakes.
Table S1. Benthic diatom taxa found in the surveyed
lakes.
Table S2. Benthic macroinvertebrate taxa found in the
surveyed lakes.
Table S3. Results of SIMPER analysis identifying the
five benthic invertebrate taxa that contributed most
strongly to the dissimilarity between lakes with low and
high amplitudes of water-level fluctuations along the
depth gradient.
(Manuscript accepted 12 November 2015)
©2015 John Wiley & Sons Ltd, Freshwater Biology,61, 251–264
264 V. V. Evtimova and I. Donohue
