larger zooplankton in danish lakes after cold winters: are winter fish kills of importance?
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SHALLOW LAKES
Larger zooplankton in Danish lakes after cold winters:are winter fish kills of importance?
D. Balayla • T. L. Lauridsen • M. Søndergaard •
E. Jeppesen
Published online: 7 March 2010
� Springer Science+Business Media B.V. 2010
Abstract Winter fish kills can be intense under ice
in shallow lakes, and have cascading effects on the
food web and ultimately on lake water clarity. In
maritime Western Europe, winters are usually mild,
but occasional colder periods may also have strong
effects on lake fish communities. Global warming
may have disproportionate effects by delaying freez-
ing and shortening the period of ice coverage. We
studied differences in zooplankton (cladocerans,
copepods, and rotifers): phytoplankton biomass,
zooplankton community structure, and individual
body size among 37 Danish lakes of various depths,
chemical characteristics, and trophy, by comparing
four winters of different severity (mean winter
temperatures ranging from -1.19�C in 1996 to
?2.9�C in 1995). We found that crustacean mean
body sizes were significantly larger in the summer
following a severely cold winter. The zooplankton
communities in the summer after a cold winter had a
significantly larger proportion of larger-bodied
species and taxa. Phytoplankton biomass, expressed
as chlorophyll-a (chl-a), was lower and zooplankton
herbivory (chl-a:TP index), higher, in the summer
after the severely cold winter of 1995/1996. All these
effects were stronger in shallow lakes than in deep
lakes. Changes in zooplankton during summer 1996,
compared with other years, were likely caused by fish
kills under ice during the preceding severe winter of
1995–1996. Fish kills due to under ice oxygen
depletion would be expected to occur earlier and be
more complete in the shorter water columns of
shallow lakes. With climate change, severe winters
are predicted to become less frequent and the winters
to be milder and shorter. In general, this is likely to
lead to higher winter survival of fish, lower zoo-
plankton grazing of phytoplankton the following
summer and more turbid waters, particularly in
shallow eutrophic lakes.
Keywords Climate change � Winter fish kills �Cladocerans � Body size � Zooplankton:
phytoplankton ratio � Zooplankton community
structure
Introduction
It is important for the future of shallow lakes systems
to be able to predict accurately how climate change
may affect both fish and their zooplankton prey. This
is because fish are key structuring components in
Guest editors: M. Meerhoff, M. Beklioglu, R. Burks, F. Garcıa-
Rodrıguez, N. Mazzeo & B. Moss / Structure and Function of
World Shallow Lakes: Proceedings from the 6th Shallow Lakes
Congress, held in Punta del Este, Uruguay, 23–28 November,
2008
D. Balayla (&) � T. L. Lauridsen � M. Søndergaard �E. Jeppesen
National Environmental Research Institute, Aarhus
University, 25 Vejlsøvej, 8600 Silkeborg, Denmark
e-mail: balayla@liverbula.com
123
Hydrobiologia (2010) 646:159–172
DOI 10.1007/s10750-010-0164-4
temperate shallow lake ecosystems. Zooplankton
abundances and their community composition and
dynamics often respond to changes in fish community
composition and abundance (Brooks & Dodson,
1965; Gliwicz & Pijanowska, 1989; Jeppesen et al.,
1990). By preying on the crustacean zooplankton,
which feed on the phytoplankton, fish can indirectly
have local or whole-lake effects on water transpar-
ency and thereby modify the light climate and
promote the establishment and growth of submerged
vegetation.
In shallow lakes of the temperate zone, the winter
season imposes stresses on fish populations, through
starvation of 0? fish, oxygen conditions under ice
determined by the trophic state of the lakes, the over
wintering macrophyte biomass and the duration of ice
cover (Jackson et al., 2007; Hurst, 2007). Due to the
influence of the North-Atlantic conveyor on ocean
temperatures, winters on the North-western Europe
seaboard are close to the 0�C January isotherm, and
lake freezing is irregular from year to year, both in
likelihood and duration. In addition, many lakes in
this area are shallow and exposed to a large degree to
the influence of air warming and cooling from
surrounding land. Even slightly warmer winters can
have strong effects on the ice covered period and thus
on biological structure.
There is a growing consensus that winters will
become shorter and warmer. A recent study of
temperature extremes based on daily data (IPCC,
2007) reveals that both high-temperature extremes
(hot days, heat waves) have increased over the period
1976–2006 and low-temperature extremes (cold
spells, frost days) have become substantially less
frequent, while winter variability has become smal-
ler. Raisanen et al. (2004) suggest that warming in
Northern Europe will be greatest in winter or late
autumn (Blenckner & Hillebrand, 2002). Projections
from modeling indicate that the greatest reduction in
the occurrence of cold extremes is projected for
northern Europe (Sillmann & Roeckner, 2008).
Many studies link meteorological trends to phe-
nology of phytoplankton and zooplankton in lakes
and suggest that climate change, expressed as
increasing winter temperatures, will further advance
the onset of spring and early summer events (phyto-
plankton spring maxima, zooplankton peaks, fish
recruitment, and clear-water phases). However, pub-
lished work on the effects of global warming on lakes
has focused on large, deep stratifying lakes, and
phytoplankton, with a scarcity of studies on shallow
lakes, zooplankton, and fish (Mooij et al., 2005;
Jeppesen et al., 2004, 2009). Moreover, most studies
including those on fish have focused on the direct
effects of spring temperature on recruitment success
and growth and subsequent predation effects on the
zooplankton (George & Harris, 1985; Mooij, 1996;
Mehner, 2000; Straile, 2000; Benndorf et al., 2001;
Gerten & Adrian, 2002; Winder & Schindler, 2004;
Tirok & Gaedke, 2006), or on overwintering survival
of young-of-the year (YOY) fish (Nyberg et al.,
2001), with a scarcity of studies on the effects of
winter conditions on the whole-year development of
zooplankton.
Studies on potential impacts of climate change on
zooplankton in shallow lakes are far less numerous
than for deep lakes. The emerging pattern is that
impacts will be short-lived and soon taken over by
weather vagaries and biotic interactions (Adrian &
Deneke, 1996; Adrian et al., 1999; Gerten & Adrian,
2000), or that only modest whole ecosystem
responses will be apparent (McKee et al., 2003),
unless extreme future climate scenarios are realized
(McKee et al., 2002; Moss et al., 2003, 2004;
Meerhoff et al., 2007). A recent study using a 4�C
rise in temperature over 2006–2007 values, however,
suggests more serious consequences, with a trend
toward floating plant dominance and extensive fish
kills (Feuchtmayr et al., 2009; Moran et al., 2009).
A controversy exists whether the main driving force
for these patterns is temperature or biotic interactions,
mainly size-selective fish predation on the zooplank-
ton. Zooplankton are often smaller at higher temper-
atures (Atkinson, 1994), both with latitude (Gillooly &
Dodson, 2000) and within lakes in different years
(Adrian & Deneke, 1996). Gyllstrom et al. (2005)
interpreted decreasing zooplankton:phytoplankton
ratios and increasing fish:zooplankton ratios, over an
Arctic to warm-temperate gradient, as lending support
to a weaker fish-zooplankton top–down link in the
warmer, subtropical lakes.
In all of these studies, little or no attention has
been paid to cascading effects of winter fish kills onto
spring and summer zooplankton and phytoplankton.
Although delayed effects of changes in winter
conditions have been investigated abundantly, only
one recent study (Jackson et al., 2007) realizes that
over decades, winter warming may propagate to
160 Hydrobiologia (2010) 646:159–172
123
seasonal succession, structure, and size of zooplank-
ton communities, and ultimately to lake state, through
a diminished likelihood of fish kills in shallow lakes
of the coastal temperate zone.
Here, we examined how extremely cold winters
could affect the spring and summer zooplankton
community in shallow lakes at intermediate latitudes,
where winter ice-cover duration is variable. A set of
37 Danish lakes of various depth, trophy, and
chemical characteristics was analyzed by comparing
winters of different severity. Our specific expecta-
tions of the effect on summer zooplankton of a severe
winter at individual, population, and community
levels were that we would find: (i) larger body sizes
of microcrustaceans, higher proportions of the larger
cladoceran species, and smaller proportions of roti-
fers and small cladoceran species, (ii) lower chloro-
phyll-a (chl-a) per unit of phosphorus and higher
water clarity, and (iii) stronger effects in shallow
lakes than in deep lakes.
Methods
Lake database
We used data from 37 lakes across Denmark
(Table 1; Jeppesen et al., 2000) which are routinely
sampled (fortnightly from April to November and
monthly from January to March; 19 samplings per
year) for zooplankton and analyzed for chemical
variables (total phosphorus (TP), nitrogen, and
ammonia), suspended solids concentration, conduc-
tivity, color, and water temperature; Kronvang et al.,
1993). A pooled water sample from the photic zone
was analyzed for chlorophyll-a using ethanol extrac-
tion (Jespersen & Christoffersen, 1987). For sampling
zooplankton, a Patalas sampler (min. 3 l) was used to
sample from different depths (\2 m, 2–4 m, 4–8 m,
[8 m, and [15 m) and fractions pooled to obtain a
depth-integrated sample from the whole water col-
umn. Depth-integrated samples were taken from three
stations in each lake and pooled. Depending on the
total phosphorus concentration, 4.5–9 l of the pooled
sample were filtered through a 90-lm nytex mesh and
preserved with Lugol’s iodine for later microscope
examination. For rotifer and nauplii counts, the
volumes filtered were 1.8 and 0.9 l from nutrient
poorer and richer lakes, respectively. Crustaceans
were counted under a dissecting microscope at 950
magnification, while rotifers and nauplii were
counted under a compound microscope at 9400.
Fifty plus individuals of the commonest species
(rotifers and nauplii) or 75? individuals (crustaceans)
were counted.
Three of the lakes had been biomanipulated
recently before the study period by removing a large
proportion of the planktivore and benthivore fish, and
were not included in the main analyses. The compo-
sition and relative abundance of pelagic fish was
determined in a sub-sample of lakes by standardized
fishing (Mortensen et al., 1990) using multiple mesh-
sized gill nets (6.25, 8, 9, 12.5, 16.5, 22, 25, 30, 33,
38, 43, 50, 60, and 75 mm). The length and depth of
each section of mesh were 3 and 1.5 m, respectively.
Fishing was conducted in each lake between 15
August and 15 September, as previous trial fishing
indicated that the distribution of the fish populations
was most even then (Mortensen et al., 1990).
Moreover, YOY fish were also large enough to be
included in the catch by this time. The nets were set
in the late afternoon and retrieved the following
morning. Catch per unit effort (CPUE) of planktiv-
orous fish was calculated as mean catch per net.
Table 1 Main morphometric and descriptive variables of the 37 study lakes
Mean (±SD) Median Minimum Maximum
Area (km2) 2.7 (7) 0.6 0.05 39.87
Mean depth (m) 3.5 (3.3) 2.7 0.7 14.96
Maximum depth (m) 7.7 (8.6) 4.5 1.5 37.7
Winter total phosphorus (mg l-1) 0.11 (0.1) 0.02 Undetectable 0.57
Winter* total nitrogen (mg l-1) 3.6 (2.6) 2.8 0.63 11.1
Winter* chlorophyll-a (lg l-1) 39.0 (81.5) 16.8 1.0 190*
Winter is January–March; * excluding the outlier Lake Arresø
Hydrobiologia (2010) 646:159–172 161
123
Winter 1995–1996 was unusually cold, with daily
mean temperatures below 1�C for 90% of the period
1st January to 31st March and ice cover during much
of this period (Fig. 1). The period 1994–1997 was
examined, comparing the 1995–1996 cold winter and
its following summer with corresponding seasons
2 years before and after. We selected a period that
was narrowly adjacent to the cold winter because
lakes were undergoing oligotrophication after nutri-
ent loading reductions, and these also affect the
zooplankton (Jeppesen et al., 2005). Within the
period 1994–1997, there was no trend in N and P
concentrations.
Zooplankton mean individual biomass
and zooplankton:chl-a ratios
For calculating biomass of the zooplankton and for
size structure analyses, size measurements were first
made from a subsample of 25 (crustaceans) or 10
(rotifers) individuals of each species from each
pooled lake sample. When the counting subsample
contained fewer than the requisite number of animals,
the sample was concentrated further and a new
subsample used for size measurements. Rotifer
biovolume formulae, and a dry weight percentage
of 10, except for Asplancha, whose dry weight
percentage was estimated to be 4, were taken from
Ruttner-Kolisko (1977). Crustacean biomass was
calculated using size-weight regressions in Bottrell
et al. (1976), McCauley (1984) and Hansen et al.
(1992).
Zooplankton biomass:chl-a ratios were calculated
for each taxonomic group (Daphnia, cladocerans,
small cladocerans (Bosminidae ? Ceriodaphnia
spp. ? Chydorus spp. ? Diaphanosoma sp. ?
Moinidae), crustaceans (copepods ? cladocerans),
copepods, and rotifers) and per month by dividing
monthly mean zooplankton biomass by the same
month’s mean chl-a concentration. The ratio zoo-
plankton biomass:chl-a concentration is an index of
grazing pressure on phytoplankton which attempts to
eliminate direct positive effects of increased food
concentration (as indicated by chl-a) on zooplankton
biomass.
Mean individual biomass (MIB), a surrogate for
average body size of the zooplankton, was calculated
for each taxonomic group by dividing sums of
biomass for each lake and date combination by
concurrent density. Zooplankton densities were cal-
culated for each relevant taxonomic group and
sampling date by summing the densities separately
for each lake. MIB monthly means were then
calculated for each lake and year.
For MIB, season means were calculated from
monthly means (Winter: January–February–March;
Spring: April–May-June; Summer: July–August–
September; Autumn: October–November–Decem-
ber). For the zooplankton biomass:chl-a ratio, first
the seasonal means for zooplankton biomass and
chl-a were separately calculated and then the sea-
sonal means were used to obtain the ratio. This was
done instead of calculating means of ratios to avoid
artefacts of high ratios during the clear-water phase
determining the summer means.
In order to compare the zooplankton biomass:chl-a
ratio and MIB in the colder 1996 with the periods
before and after, an index for the difference between
years in seasonal means was drawn for each lake.
This was determined as the difference between
seasonal means in different years and those for
1996 (i.e., 1996 vs. 1994, 1996 vs. 1995 and 1996 vs.
1997) divided by the average of the two seasonal
means being compared. Normalization, in this way,
prevented any one lake from having a disproportionate
effect on across-lake index means during statistical
analyses.
1988
1989
1990
1991
1992
1993
1994
1995
1996
1997
1998
1999
2000
2001
2002
2003
2004
2005
2006
2007
2008
Jan
-Mar
ch d
aily
air
tem
per
atu
re (
°C)
-6
-4
-2
0
2
4
6
8
10
Fig. 1 Box plot of daily air temperature in winter (1st January
to 31st March) during the period 1989–2007. The mean and
median temperatures during winter 1996 (arrowed) were -1.18
and -0.6�C, respectively, compared with 2.86 and 2.82�C for
1989–2007 (excl. 1996). All air temperature measurements are
from Copenhagen (Denmark), Danish Meteorological Institute
(DMI)
162 Hydrobiologia (2010) 646:159–172
123
One-sample two-tailed t-tests were then performed
on the standardized lake differences for each of the
three between-year comparisons. Tests examined
whether seasonal differences between years were
significantly greater than 0. Specifically, the hypoth-
esis was that the cold winter 1996 would lead to
larger ratios (except for rotifers and small cladocer-
ans, for which smaller ratios were expected) and
mean animal sizes than the other years, particularly in
the summer months. Because summer top–down
control of phytoplankton by zooplankton can be
stronger in shallow lakes (Jeppesen et al., 2003), and
we expected stronger effects of the cold winter on the
shorter water columns of shallow lakes, the statistical
comparisons were also performed separately for
shallow and deep (defined as Zmax [ 6 m) lakes.
Size structure of populations of cladocerans
and copepods
The size distributions of Cladocera, copepod and
Daphnia populations in the lake database during
1994–1997 were summarized by taking the 10%
(P10), 25% (Q1), 50% (M), 75% (Q3), 90% (P90),
and 99% (P99) percentiles from each date in an
ordered data series, based on monthly means (per
lake) for each size percentile and year, separately for
cladocerans, copepods, and Daphnia. Differences
between years for each month and lake were then
calculated for each percentile, and seasonal means
were estimated from the lake-monthly standardized
means for each between-year comparison (i.e., 1996
vs. 1994, 1996 vs. 1995 and 1996 vs. 1997). One-
sample two-tailed t-tests were performed on the
seasonal between-year mean differences to test
whether differences were significantly different from
zero. Specifically, we tested whether size percentiles
were larger (i.e., size structure was displaced toward
larger animal sizes) in the cold year 1996 than in the
other 3 years. Statistical comparisons were also
performed separately for shallow and deep lakes.
Low percentiles (i.e., P10 and P25) represent smaller
size classes, while high percentiles (i.e., P90 and P99)
represent larger size classes.
Zooplankton community structure
Seasonal means were calculated for the following
ratios of taxa biomass: cladocerans/total zooplankton,
calanoid/total copepods, small cladocerans/total
cladocerans, Daphnia/total cladocerans (excluding
predatory species), and rotifers/total zooplankton.
High values for the ratios calanoid/total copepods,
total cladocerans/total zooplankton and Daphnia/total
cladocerans, and low values of the ratios rotifer/total
zooplankton and small/total cladocerans, suggest low
fish predation pressure on the zooplankton (Jeppesen
et al., 2000). Seasonal means were calculated from
the monthly means and not from the raw data because
the data amount varied within season. Seasonal ratios
were compared between years using paired two-tailed
t-tests. Tests examined whether summer levels of fish
predation pressure were lower in 1996. Statistical
comparisons were also performed separately for
shallow and deep lakes.
Grazing pressure index
The chlorophyll-a:TP concentrations ratio was used as
an index of microcrustacean herbivory on phytoplank-
ton (Mazumder et al., 1990; Jeppesen et al., 2004).
Monthly means of the ratio were calculated by dividing
the monthly means of chlorophyll-a by the monthly
means of TP. A relative difference between monthly
means for each pair of years was then calculated to
prevent any one lake from having a disproportionate
effect on across-lake mean differences during analyses.
Also, a seasonal mean ratio was calculated from
monthly means of chl-a and TP. Relative differences
were calculated for each season and pair of comparison
years and tested using one-sample two-tailed t-tests.
Tests examined particularly whether levels of herbivory
were higher in summer 1996 than in the other summers
during 1994–1997. Statistical comparisons were also
performed separately for shallow and deep lakes.
Results
Zooplankton mean individual biomass
Cladoceran mean individual biomass was larger in
summer 1996 than in the other summers during
1994–1997 (Fig. 2). Differences were significant in
the shallow lakes, but not in the deep lakes (Table 2).
There was a highly significant negative relationship
between the logarithm of lake mean depth and
relative differences in mean size (Fig. 3).
Hydrobiologia (2010) 646:159–172 163
123
Daphnia mean individual biomass was also larger
in summer 1996 than in the other three summers
(Table 2). Differences between summers were not
significant for any of the comparisons in deep lakes,
but were significant for all comparisons in the
shallow lakes (Fig. 2; Table 2). Small cladocerans
were significantly larger in summer 1996 than in the
other three summers, particularly in the deep lakes
(Table 2). Neither copepod nor rotifer mean individ-
ual biomass was significantly different in summer
1996 compared with the other summers (Table 2). On
a seasonal basis, the individual biomass of cladocer-
ans in 1996 tended to be larger in March after ice
melting and again in late summer (August and
especially September) than in the other years.
Size structure
Cladocera
All percentiles of size (lg DW ind-1) were signif-
icantly larger in summer 1996 than in summer of the
other 3 years, except P10 and Q1 in the 1996 versus
1995 comparison (see the example of P90 in Fig. 4).
Differences were larger and more often significant for
the shallow lakes (Table 3). In deep lakes, small size
classes (i.e., smaller percentiles) were more often
significantly larger than large size classes in summer
1996 compared with the other three summers in
1994–1997. In shallow lakes, the higher percentiles
were significantly larger in summer 1996 than in the
other years, while small percentiles were not. Daph-
nia size percentiles were significantly larger in
summer 1996 than in the other three summers in
the shallow lakes, but not in the deep lakes.
Differences were found mainly in the larger size
percentiles, though also in the lower size percentiles.
Copepoda
The higher percentiles (P90 and P99) were signifi-
cantly larger in summer 1996 than in the other three
summers (Table 3). Lower percentiles were not
significantly different between years. Also, the noted
differences between summer 1996 and the other three
summers in 1994–1997 were only significant in the
shallow lakes, not in the deep lakes.
Zooplankton community structure
The total cladocerans:total zooplankton ratio was
significantly larger in summer 1996 than in the
summer of the other 3 years (Fig. 5a; Table 4),
especially in the deep lakes. The proportion of
cladocerans that were Daphnia was also significantly
higher in summer 1996 (Fig. 5b), and the effect was
SHALLOW LAKES
1994
1995
1996
1997
0
2
4
6
8
10
12
1994
1995
1996
1997
0
10
20
30
40
50
DEEP LAKES
0
10
20
30
40
50
60Zoo:Phyto
Su
mm
er C
lad
oce
ra m
ean
siz
e (µ
gD
W in
d-1
)0
5
10
15
20
25Mean size Daphnia
Su
mm
er Zo
o:p
hyto
(µgD
W µg
chla
-1)
0
20
40
60
80
100
120
140
160
0
5
10
15
20
25
1994
1995
1996
1997
0
5
10
15
20
1994
1995
1996
1997
0
20
40
60
80
CladoceraFig. 2 Cladoceran and
Daphnia summer
biomass:chl-a and summer
mean individual biomass
during 1994–1997. Data for
shallow and deep lakes are
shown separately
164 Hydrobiologia (2010) 646:159–172
123
particularly strong in the shallow lakes. Similarly, the
proportion of small cladocerans to total cladocerans
was smaller in summer 1996. This effect was stronger
in the shallow lakes (Fig. 5b; Table 4). The cala-
noid:total copepod ratio was significantly larger in
spring (May–June) in the 1996 versus 1994 compar-
ison and in the 1996 versus 1997 comparison and
differences occurred in both deep and shallow lakes
(Table 4). There were significantly fewer rotifers in
the zooplankton community in summer 1996 than in
the other summers (Fig. 5a), and this effect was
particularly strong in the deeper lakes (Table 4).
Zooplankton:phytoplankton
Cladocera biomass:chl-a ratios were generally larger
in summer 1996 than in the other 3 years during
1994–1997. In the deeper lakes, differences were
Table 2 Results of statistical comparisons between summer and spring 1996 and corresponding seasons in other years during 1994–
1997
All lakes Deep lakes Shallow lakes
Summer
Zooplankton:phytoplankton
Cladocera */–/– */*/– –/–/–
Daphnia –/*/* –/–/– –/–/–
Small Cladocera –/–/– (*)/(***)/– –/–/–
Copepods –/–/– –/–/– –/–/*
Rotifers –/–/– –/–/– –/–/–
Rotifers (biomass) –/*/* */***/* –/–/–
Mean individual biomass
Cladocera */*/** –/–/– */*/**
Daphnia */*/* –/–/– –/**/*
Small Cladocera **/*/* */*/– */–/–
Copepods –/–/– –/–/(*) –/–/*
Rotifers –/–/– –/–/– –/–/–
Spring
Zooplankton:phytoplankton
Cladocera –/–/– –/–/– –/–/–
Daphnia –/–/(*) –/–/– –/–/–
Small Cladocera –/–/* –/–/– –/–/*
Copepods */–/– –/–/– –/–/–
Rotifersa */**/– –/*/– –/*/–
Rotifersa (biomass) –/**/* –/–/– –/*/–
Mean individual biomass
Cladocera –/–/– –/–/– –/–/–
Daphnia –/–/– –/–/– –/–/–
Small Cladocera –/–/– –/–/– –/–/–
Copepods –/–/– –/–/– (*)/–/–
Rotifers –/–/– –/–/– –/–/–
Zooplankton:phytoplankton biomass ratios and mean individual biomass are shown for main taxa (Cladocera, Daphnia, small
cladocerans, Copepoda, Rotifera) in summer (July–August–September) and spring (April–May–June) in deep and shallow lakes
during 1994–1997. In each cell, statistical significances (* P \ 0.05; **P \ 0.01; *** P \ 0.001; – not significant) are shown for
one-sample t-tests comparing relative differences between either summer (July–August–September) or spring (April–May–June) in
1996 with each of the other three years during 1994–1997: 1996 versus 1994/1996 versus 1995/1996 versus 1997. In parentheses,
opposite differences between shallow and deep lakes (see text for details)a Significances refer to larger spring 1996 values
Hydrobiologia (2010) 646:159–172 165
123
statistically significant (Table 2). Daphnia bio-
mass:chl-a ratios were larger in summer 1996 than
in summers 1995 and 1997. Copepod biomass:chl-a
ratios overall were not significantly different between
Log(Zmean + 1)
0,0 0,5 1,0 1,5 2,0 2,5 3,0
Rel
ativ
e d
iffe
ren
ce in
m
ean
ind
ivid
ual
bio
mas
s
-1,5
-1,0
-0,5
0,0
0,5
1,0
1,5
2,0
r2=0.17 (all); p<0.0001
Fig. 3 Relationships between summer cladoceran mean size
(lg DW ind-1) and lake depth. Each symbol in the plot is one
lake for each between-year comparison (1996 vs. 1994—filledcircles, vs. 1995—empty squares and vs. 1997—filled trian-gles). The same lake set is used in each comparison (N = 29).
ANOVAs of linear regressions: 1996 versus 1994, F = 5.74,
P \ 0.05; 1996 versus 1995, F = 2.32, P = 0.1393; 1996
versus 1997, F = 9.22, P \ 0.01. R2 were 0.17, 0.05 and
0.25, respectively. All comparisons: N = 86, R2 = 0.1714,
P \ 0.0001
Su
mm
er P
90 s
ize
(µg
DW
ind
-1) 0
5
10
15
20
25
0
2
4
6
8
10
12
Daphnia
-1,5
-1,0
-0,5
0,0
0,5
1,0
1,5
1996 vs.
Relative d
ifference b
etween
years
-1,5
-1,0
-0,5
0,0
0,5
1,0
1,5
2,0Shallow lakesDeep lakes
*
Cladocera*
*
***
Cladocera
1994
1995
1996
1997
0
2
4
6
Copepoda
1994
1995
1996
1997
0
2
4
6
Daphnia
0
10
20
30
0
5
10
15
20
Copepoda
1994 1995 1997-1,5
-1,0
-0,5
0,0
0,5
1,0
1,5
Fig. 4 Box plots of
summer (July–September)
P90 size (lg DW ind-1) in
deep (Zmax [ 6 m) and
shallow lakes for Cladocera,
Daphnia and Copepoda.
The thicker line in each plot
indicates the mean for that
plot. The three rightmost
plots show relative (to poles
of comparison) differences
between summer size in
1996 and in the other three
years in the period 1994–
1997, separately for deep
and shallow lakes. For
Cladocera and Copepoda,
14 deep lakes and 16
shallow lakes were included
in analyses; for Daphnia, 11
deep lakes and 11 shallow
lakes. Statistical
significances for one-
sample t-tests comparing
the mean relative difference
to 0 are indicated above the
appropriate box plots:
* P \ 0.05 and ** P \ 0.01
Table 3 Size structure as given by percentiles (P10, Q1,
M-median, Q3, P90 and P99) of actual size measurements
Size percentile P10 Q1 M Q3 P90 P99
Deep lakes
Cladocera –/–/– */–/* */–/– –/–/– –/–/– –/–/–
Daphnia –/–/– –/–/– –/–/– –/–/– –/–/– –/–/–
Copepoda –/–/– –/–/– –/–/– –/–/– –/–/– –/–/–
Shallow lakes
Cladocera –/–/* –/*/* –/*/** –/*/** –/*/* –/**/**
Daphnia –/–/– –/–/– –/*/– –/*/* –/–/* –/–/*
Copepoda –/–/– –/–/– –/–/– –/–/– **/–/* */–/*
Comparisons between summer 1996 and summer 1994, 1995
and 1997 from one-sample t-tests are shown. See text for
details
– not significant; * P \ 0.05; ** P \ 0.01
166 Hydrobiologia (2010) 646:159–172
123
years in either spring or summer 1996. However,
there were large, albeit short-lived, differences in late
spring-early summer. The small Cladocera bio-
mass:chl-a ratio was larger in summer 1996 in the
deep lakes, but not in the shallow lakes. In the
shallow lakes, the ratio was significantly smaller in
spring 1996 than in the spring seasons of 1995 and
1997. Rotifer biomass:chl-a ratios were not signifi-
cantly different in summer 1996 than in the other
summers, but were significantly larger in spring 1996
than in the spring seasons of the other 3 years
(Table 2). Also, rotifer biomass in summer 1996 was
significantly smaller than in summer of the other
3 years, and differences were mainly driven by those
in the deep lakes.
Chl-a and Chl-a:TP
The chl-a concentration, a proxy for phytoplankton
biomass, tended to be smaller in summer 1996 than in
the other 3 years (Fig. 6a), although differences were
not significant. The chl-a:TP index was overall
smaller (higher grazing by zooplankton) in summer
1996 than during the other summers. Differences
were more substantial in the deep lakes, with
significant differences between summers 1996 and
1994 (N = 14, t = -2.56, P \ 0.05) and summers
1996 and 1995 (N = 14, t = -2.18, P \ 0.05).
Fish
Mean total CPUE of surveys conducted in Danish
lakes during the sampling period (not the same lakes
every year) tended to be lower in summer 1996 than
in the other summers. However, there was no
indication that the mean proportion of fish \10 cm
(Fig. 6b) was lower in summer 1996 than in other
years. Summer total phosphorus concentrations were
similar all years (Fig. 6b), indicating lake sets each
year were sufficiently similar for meaningful com-
parisons with regard to gross estimates of fish
abundance and size structure.
Discussion
The cold winter 1995–1996 apparently had strong,
albeit short-lived, effects on the pelagic structure and
dynamics of shallow lakes in Denmark. Several of the
biological variables examined suggest that, during the
summer after this cold winter, the predation pressure
on zooplankton was much less intense than in normal
years. Thus, we found: (i) increased proportions of
large zooplankton species (Fig. 5; Table 4), (ii) larger
mean and individual sizes of the main zooplankton
taxa (Figs. 2, 4; Table 3), (iii) indications of enhanced
crustacean grazing on phytoplankton (lower chl-a and
chl-a:TP ratios; Fig. 6a), and (iv) fewer planktivorous
fish (Fig. 6b).
Daphnia:Total clad.
1994
1995
1996
1997
Rotifers:Total zoo.
1994
1995
1996
1997
Clad.:Total zoo.
1994
1995
1996
1997
Per
cen
tag
e
0
20
40
60
80
100
Sm
all c
lad
oce
ran
s:to
tal c
lad
oce
ran
s
0
20
40
60
80
100Shallow lakesDeep lakes
Dap
hn
ia:
tota
l cla
do
cera
ns
19941995
19961997
Per
cen
tag
e
0
20
40
60
80
19941995
19961997
+ * **nsns ns
*ns **
ns nsns
a
b
Fig. 5 Effect of the cold winter on summer zooplankton
community structure. Box plots of percentage of cladoceran
biomass of total zooplankton biomass, Daphnia biomass of
total cladoceran biomass and rotifer biomass of total zoo-
plankton biomass are shown for the whole-lake database
(excluding biomanipulated lakes) in which they were found.
The across-lake mean for each year in 1994–1997 is shown
within each box plot (thicker line). ? P \ 0.1; * P \ 0.05;
** P \ 0.01; ns-not significant
Hydrobiologia (2010) 646:159–172 167
123
Effects identified in summer 1996 are consistent
with the occurrence of fish kills during the unusually
long period of ice cover in 1995–1996, likely
reflecting oxygen depletion, as seen elsewhere
(Meding & Jackson, 2003; for review, see Hurst,
2007). Although not quantified, several Danish water
authorities reported numerous dead fish after the ice
melted in 1996. Accordingly, we see a tendency to a
temporary decline in fish abundance (total mean
CPUE) in summer 1996 compared with other years,
although we cannot exclude other factors because it
was not the same set of lakes that was monitored for
fish in the different years. The decline could not be
explained by a particularly weak year class in 1996,
as the mean CPUE of small fish was not lower in this
year. The suggestion is that a lower survival of fish
during winter leads to lower total fish abundance
during summer. Larger-bodied and more abundant
zooplankton will then have stronger grazing impacts
on phytoplankton, helping to create, and sustain a
clear-water state. Many of the effects identified were
substantially stronger and more highly significant in
the shallow lakes (Fig. 3; Tables 2, 3, 4). Fish kills
during winter, related to under ice oxygen depletion,
would be expected to occur earlier and be more
complete in the shorter water columns of shallow
lakes, while direct effects of low winter temperature
on fish feeding activity can be expected to be similar
in lakes of all depths.
Cladocerans tended to be larger-bodied both after
the ice melted and during the summer following the
cold winter (Tables 2, 3), suggesting that fish preda-
tion levels had been lower early in the season and
also during summer. In our study, differences in mean
body size between years were greatest in August–
September. Stronger fish predation pressures are
often observed in late summer in shallow lakes
(McQueen et al., 1986; Whiteside, 1988; Luecke
et al., 1990; Rettig, 2003), as the YOY grow to a
sufficient size to eat the zooplankton. However,
several studies suggest that both adult and larval fish
can have impacts on zooplankton community struc-
ture in spring and in summer (Link et al., 2004;
Jeppesen et al., 2004; Hansson et al., 2007).
A commonly reported effect of climate change on
fish recruitment is through the projected higher spring
air temperatures and their translation to better con-
ditions for fish egg hatching and growth of the YOY
fish (Mooij, 1996). In our study, air temperatures
following the cold event in spring and summer were
not lower than during the other years in the period
1994–1997. Moreover, the proportion of small fish
(\10 cm) was not higher in 1996 than in the other
years, indicating that a lower predation on large-
bodied zooplankton in 1996 was the result of a lower
biomass of both small and large-bodied fish.
We found a different response in deep and shallow
lakes. Cladoceran and copepod body sizes were
Table 4 Comparison of descriptors of spring (April ? May ? June) and summer (July ? August ? September) community
structure in deep and shallow lakes during 1994–1997
All lakes Deep lakes Shallow lakes
Spring (April ? May ? June)
Calanoid:total copepod –/–/– –/–/– –/–/–
Cladocera:total zooplankton –/–/– –/–/– –/–/–
Small Cladocera:total Cladocera –/–/– –/–/– –/–/–
Daphnia:total Cladocera –/–/* –/–/– –/–/*
Rotifers:total zooplankton –/–/– –/–/– –/–/–
Summer (July ? August ? September)
Calanoid:total copepod –/–/– –/–/– –/–/–
Cladocera:total zooplankton */*/– */*/– –/–/–
Small Cladocera:total Cladocera –/*/– –/–/– –/*/**
Daphnia:total Cladocera –/–/– –/–/– */–/**
Rotifers:total zooplankton */*/* –/*/– –/–/–
In each cell, statistical significances (* P \ 0.05; ** P \ 0.01; - not significant) are shown for paired t-tests comparing 1996 with
each of the other three years in 1994–1997: 1996 versus 1994/1996 versus 1995/1996 versus 1997
168 Hydrobiologia (2010) 646:159–172
123
generally larger in the shallow lakes in summer 1996
than in the other years, while in the deep lakes,
effects were either restricted to the smaller percen-
tiles of body size or were negligible (Table 3), which
is consistent with the expected stronger fish kill in the
shorter water columns of shallow lakes. Furthermore,
because fish biomass m-3 of lake bottom is larger
in shallow lakes than in comparable deep lakes
(Jeppesen et al., 2000), stronger effects of fish kills
can be expected in the shallow lakes. The role of
depth is supported by the relationship between lake
mean depth and changes in cladoceran mean size
among years (Fig. 3), which decreases with increas-
ing lake depth.
The spring rotifer peak in 1996 (Table 4) was
followed by a rapid decrease in summer, coinciding
with an increase in the abundance of cladocerans and
particularly also the Daphnia species. Other changes
were a larger proportion of cladocerans in the
zooplankton, a general increase of the fraction of
Daphnia biomass among cladocerans and a decrease
of the contribution of rotifers to the summer
zooplankton community (Fig. 5a). These effects were
substantial in both deep and shallow lakes, likely
indicating that fish kills had occurred in both types of
lake.
The Cladocera biomass:chl-a ratios also differed in
the deep lakes, being higher in 1996 than in the other
years. This indicates higher grazing on phytoplankton
this year, also evidenced by the lower chl-a:TP ratios.
The effect on zooplankton biomass:chl-a ratios was
less clear than for Cladocera biomas:chl-a ratios,
reflecting that only small changes occurred in the
ratios for rotifers and copepods. This is consistent
with an overall lower fish predation risk for rotifers
and cyclopoid copepods (Gliwicz & Pijanowska,
1989).
Although, we see clear indications of reduced fish
predation in 1996, following the cold winter, effects
are modest when compared with observations from
shallow Canadian prairie lakes (Jackson et al.,
2007). In these lakes, which are under ice for up
to 5 months each year, fish abundance is very low
due to the intense fish kills. An average chl-a:TP
ratio of 0.11 and high zooplankton:chl-a ratios have
been found from a set of 30 Canadian lakes,
compared with an average of 0.43 and much lower
zooplankton:chla-a ratios in a set of 222 Danish
lakes (Jackson et al., 2007). By comparison, in our
-Shallow lakes- -Deep lakes-
Grazing (chl-a:TP)
Gra
zin
g in
dex
(ch
l-a:
TP
)
0,0
0,2
0,4
0,6
0,8
1,0
1,2
Grazin
g in
dex (ch
l-a:TP
)0,0
0,2
0,4
0,6
0,8
1,0
1,2
Chl-a
[Ch
l-a]
(µg
l-1)
0
50
100
150
200
250
300 Grazing (chl-a/TP) Grazin
g in
dex (ch
l-a:TP
)
0,0
0,2
0,4
0,6
0,8
1,0
Chl-a
1994
1995
1996
1997
[Ch
l-a]
(µg
l-1)
0
50
100
150
200
1994
1995
1996
1997
[Ch
l-a] (µg l -1)
0
50
100
150
200
250
300
350
-All lakes-
1994 1995 1996 1997
Cat
ch p
er u
nit
eff
ort
(n
o/n
et)
0
100
200
300
400
500
600 Mean
pro
po
rtion
(%) o
f <10 cm fish
25
30
35
40
45
50
55
60
Mean
[TP
] (mg
/l)
0,0
0,2
0,4
0,6
0,8
1,0
1,2Mean totCPUEMean proportion of <10 cm fishMean total P conc.
14 1120
14
a
b
Fig. 6 a Box plots comparing chlorophyll-a and grazing index
(chl-a/TP) in July 1994–1997 across the lake database
(N = 29). Grazing levels (middle plot) and chlorophyll-aconcentrations (bottom plot) are also compared in different
years in shallow (max. depth \6 m) and deep lakes in the
database. The thicker line in each plot indicates the mean for
that plot. b Fish mean total catch per unit effort (CPUE, in
number/net) ± S.E. from summer surveys conducted during
1994–1997 in Danish lakes. The line shows the proportion of
small fish (\10 cm) CPUE. The summer mean TP concentra-
tion ± S.E. is also shown, suggesting that lake sets (number of
lakes within each bar) each year were comparable as regards
fish abundance
Hydrobiologia (2010) 646:159–172 169
123
study, we estimated a change from an average of
0.41 after warm winters to 0.35 after the 1995/1996
cold winter.
In conclusion, in high-latitude regions of the
oceanic seaboard, where the period of lake ice-cover
in winter is irregular from year to year, climate
change may have profound effects on shallow lake
ecosystems as winters are predicted to become
shorter and less cold. The present study indicates
that future changes in climate and weather patterns
influencing winter icing behavior may affect the size,
abundance, and structure of summer zooplankton.
Shortening of the winter season due to global
warming could lead to increased predation by fish
in summer as more cyprinid fish survive the winter.
This could lead to less grazing on phytoplankton and
more turbid water.
Acknowledgments We would like to thank all staff from the
National Environment Research Institute (NERI) and the Danish
Counties, who collected the data from the set of lakes used in this
article. Many thanks are due to a number of colleagues at NERI
for interesting discussions and help: Thomas B. Kristensen,
Sandra Brucet, Marc Ventura, Carolina Trochine, Liselotte
Sander Johansson, Lone Libourissen, Lissa Skov Hansen, Ulla
Kvist Pedersen, and Ole Sortkjær. Thanks are due to Søren
Larsen for advice on SAS programming for size structure
analyses and to Anne Mette Poulsen for revising the English.
The analyses were funded by the European Commission
project ENDURE (Marie Curie Individual fellowship
MEIF-CT-2006-038366).
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