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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