The role of light for fish–zooplankton–phytoplankton interactions during winter in shallow lakes–a climate change perspective

The role of light for fish–zooplankton–phytoplanktoninteractions during winter in shallow lakes – a climatechange perspective

METTE ELISABETH BRAMM*, MAJBRITT KJELDAHL LASSEN†, LONE LIBORIUSSEN*,

KATHERINE RICHARDSON ‡, MARC VENTURA* , § AND ERIK JEPPESEN* , –

*Department of Freshwater Ecology, National Environmental Research Institute, University of Aarhus, Silkeborg, Denmark†Department of Marine Ecology, Institute of Biological Sciences, University of Aarhus, Aarhus, Denmark‡The Faculty of Science, University of Copenhagen, Copenhagen, Denmark§Limnology group (CSIC-UB), Centre for Advanced Studies of Blanes (CEAB), Spanish Research Council (CSIC), Catalonia,

Spain–Department of Plant Biology, University of Aarhus, Aarhus, Denmark

SUMMARY

1. Variations in the light regime can affect the availability and quality of food for

zooplankton grazers as well as their exposure to fish predation. In northern lakes light is

particularly low in winter and, with increasing warming, the northern limit of some

present-day plankton communities may move further north and the plankton will thus

receive less winter light.

2. We followed the changes in the biomass and community structure of zooplankton and

phytoplankton in a clear and a turbid shallow lake during winter (November–March) in

enclosures both with and without fish and with four different light treatments (100%, 55%,

7% and <1% of incoming light).

3. In both lakes total zooplankton biomass and chlorophyll-a were influenced by light

availability and the presence of fish. Presence of fish irrespective of the light level led to

low crustacean biomass, high rotifer biomass and changes in the life history of copepods.

The strength of the fish effect on zooplankton biomass diminished with declining light and

the effect of light was strongest in the presence of fish.

4. When fish were present, reduced light led to a shift from rotifers to calanoid copepods in

the clear lake and from rotifers to cyclopoid copepods in the turbid lake. Light affected

the phytoplankton biomass and, to a lesser extent, the phytoplankton community

composition and size. However, the fish effect on phytoplankton was overall weak.

5. Our results from typical Danish shallow eutrophic lakes suggest that major changes in

winter light conditions are needed in order to have a significant effect on the plankton

community. The change in light occurring when such plankton communities move

northwards in response to global warming will mostly be of modest importance for this

lake type, at least for the rest of this century in an IPCC A2 scenario, while stronger effects

may be observed in deep lakes.

Keywords: food availability, global warming, light manipulation, zooplanktivorous fish, zooplanktoncommunity structure

Correspondence: Lone Liboriussen, Department of Freshwater Ecology, National Environmental Research Institute, University of

Aarhus, PO Box 314, DK-8600 Silkeborg, Denmark. E-mail: [email protected]

Freshwater Biology (2009) 54, 1093–1109 doi:10.1111/j.1365-2427.2008.02156.x

� 2008 The Authors, Journal compilation � 2008 Blackwell Publishing Ltd 1093

Introduction

It is widely accepted that predation plays a critical

role in structuring freshwater zooplankton communi-

ties. Planktivorous fish feed selectively on the largest

and most conspicuous zooplankton (Brooks & Dod-

son, 1965) and intense predation often results in a

zooplankton community composed of small-sized

species such as rotifers, small copepods and clado-

cerans (Christoffersen et al., 1993). The strength of the

cascading top–down effect of planktivorous fish on

phytoplankton can be high (Carpenter & Kitchell,

1993) and will vary along a nutrient gradient (Jeppe-

sen et al., 2003). Nutrients and light availability are

critical factors that may restrict the production and

biomass of phytoplankton and thereby limit the

quantity (Gliwicz, 2003) and quality of food for

zooplankton (Sterner et al., 1997; Urabe et al., 2002).

Food limited environments generally promote slow

growing, energetically efficient species that may

continue growth and reproduction at low food con-

centrations at the cost of fast-growing species with

high food requirements and poor ability to tolerate

starvation (Lambert & Muck, 1985; Ventura & Cata-

lan, 2005). Food requirements may also change with

development stage. Juvenile copepods might be more

sensitive to starvation than older copepodites and

adults due to their higher metabolism and, hence,

have greater food requirements (Soto & Hurlbert,

1991a).

Several studies have manipulated predators and

food resources simultaneously to elucidate their

interactive impact on zooplankton biomass and

community structure (e.g. Vanni, 1987). Most studies

have, however, focused exclusively on the summer

period, while little is known about the relative

importance of resource and predator control of

zooplankton in winter (Jeppesen et al., 2004). In

winter, resource control is usually assumed to be

more important than predator control due to lower

irradiance and lower food concentrations (Sommer

et al., 1986). Fish predation may potentially also be

lower during winter than in summer due to a lower

food intake (Keast, 1968) and reduced activity of the

fish (Jacobsen et al., 2002) or reduced abundance of

grazers, as some fish take winter refuge in adjacent

streams or wetlands (Jepsen & Berg, 2002; Hansson

et al., 2007). Nevertheless, some whole-lake stud-

ies have indicated that fish may also control

zooplankton populations during winter, particularly

in eutrophic lakes (Vanni & Findley, 1990; Rudstam,

Lathrop & Carpenter, 1993; Jeppesen et al., 1997,

2004).

Long-term eutrophication of lakes has created a

strong scientific focus on nutrients in controlling

plankton abundance and community composition in

lakes (Jeppesen et al., 2000). Light is, however, the

ultimate energy source for photosynthesis and pro-

duction and is thereby central in, for example,

controlling the total abundance and distribution of

the primary producers and consumers in the lakes.

Consideration of the effect of light on the interactions

between primary producers and consumers is there-

fore important when evaluating the effects of global

warming on lake ecosystems, as communities occur-

ring today at a given latitude in the north temperature

zone will presumably appear at higher latitudes in the

future and here be exposed to lower winter light

regimes than at the lower latitudes where they are

found today. Furthermore, it could be argued that

phytoplankton and zooplankton species, in some

cases, may readily move northwards, while fish may

not, so that local extinctions without species replace-

ment will lead to reduced fish predation in some

lakes, and thus further affect the primary producer–

consumer interactions.

The purpose of this study was to describe how

zooplankton and phytoplankton biomasses and the

zooplankton community structure are affected by

long-term experimental manipulation of light avail-

ability and fish predation in turbid and clear

shallow lakes. We expected that reduced light levels

would reduce the phytoplankton biomass and

change the phytoplankton community structure.

This, in turn, was anticipated to induce reduction

of growth, reproduction and survival of zooplank-

ton and to favour low-food tolerant species.

Reduced light levels were expected to have a larger

impact on the zooplankton community structure in

the clear lake than in the turbid lake, as phyto-

plankton more easily reaches critical levels for

zooplankton when constrained also by nutrient

availability. Finally, reduced light levels were pre-

dicted to reduce the foraging efficiency of fish and,

with it, the predation pressure on zooplankton,

though a longer exposure to predators due to low-

food mediated lower zooplankton growth may

dampen the effects.

1094 M. E. Bramm et al.

� 2008 The Authors, Journal compilation � 2008 Blackwell Publishing Ltd, Freshwater Biology, 54, 1093–1109

Methods

Study sites

The experiment was conducted in two morphometri-

cally similar lakes with contrasting phosphorus con-

centrations: phosphorus-rich Lake Søbygard (56�15¢N;

9�48¢E) and less phosphorus-rich Lake Stigsholm

(55�58¢N; 9�30¢E). Lake Søbygard has a surface area of

0.40 km2, a mean depth of 1.0 m and a maximum depth

of 1.9 m. The mean annual total phosphorus (TP) con-

centration was 0.275 mg L)1 (1997–2001), while total

nitrogen (TN) was 1.78 mg L)1 and chlorophyll-a

(Chl-a) was 0.112 mg L)1. Lake Stigsholm is 0.21 km2

and has a mean depth of 0.8 m and a maximum depth

of 1.2 m. The mean annual TP was 0.096 mg L)1 (1997–

2001), while TN and Chl-a were 2.65 mg L)1 and

0.036 mg L)1, respectively (Liboriussen & Jeppesen,

2003). Within the last decades Lake Stigsholm (termed

clear) has shifted several times between a clear state

with substantial submerged vegetation and a turbid

vegetationless state. By contrast, nutrient-rich Lake

Søbygard (termed turbid) has remained turbid with no

submerged vegetation. The fish community was

numerically dominated by roach (Rutilus rutilus L.)

and perch (Perca fluviatilis L.) in both lakes (Jeppesen

et al., 1998; Jacobsen et al., 2004).

Experimental design

Planktivorous fish abundance and light were manipu-

lated in 24 clear cylindrical polyethylene enclosures in

each of the two lakes. The enclosures (diameter 1.2 m)

were placed along a bridge (12 on each side) 4–5 m from

the littoral zone. They were open to the atmosphere and

to the sediment. An aluminium ring fixed each enclo-

sure in the sediment, while a hard plastic ring mounted

on poles secured the top above the water surface. To

prevent water exchange between the enclosure and the

lake, the walls projected approximately 40 cm above

the water surface. The water level in the enclosures was,

on average, 0.8–0.9 m, giving a total water volume of

approximately 1000 L. Before the enclosures were

established, submerged macrophytes were removed

from the area. Adult fish and larvae were prevented

from entering the enclosures during set-up by covering

the open bottom with a nylon net (mesh size 0.5 cm),

thus filtering the incoming water while filling up the

mesocosm. The nylon net was subsequently removed

when fixing the lower ring into the sediment.

A 2 · 4 factorial design with three replicate enclo-

sures per treatment was employed. Light intensity in

the enclosures was adjusted to one of four levels: high

(H), medium (M), low (L) and scarce (S), correspond-

ing to 100%, 55%, 7% and <1% of the incoming light,

respectively. Light was controlled by covering the

enclosures with black and grey cloth nettings and a

polyethylene net tied onto wooden frames placed just

above the enclosures. The covers extended approxi-

mately 0.5 m into the water on all sides of the

enclosures. High light enclosures were screened with

simple nets to prevent bird access. Planktivorous fish

were stocked in half of the enclosures (+), while the

other half remained fish-free ()). Fish were caught in

the study lakes using electro fishing and plexiglass

traps and were subsequently stored in keep-nets for

a minimum of 10 days prior to stocking in the

enclosures to ensure that they had survived the

handling. Seven 0+ roach (c. 6 individuals m)2 or c.

15.5 g WW m)2) were added to each of the fish

enclosures one week after set-up. When dead fish

were observed in the enclosures, they were removed

and replaced. Thus, eight triplicate treatments were

used in the overall experimental design: +H, )H, +M,

)M, +L, )L, +S and )S.

Sampling

The initial sampling for analysing community struc-

ture and abundance was conducted on the day that

the fish were added to the enclosures, while the first

sampling was made a week later. Subsequent samples

were taken monthly from October 2000 to March 2001,

however, with a 10-day delay in January due to ice

coverage. Both lakes were ice-covered for approxi-

mately 2 weeks in mid–late January and again from

late February to the beginning of March.

In each enclosure, water samples integrating the

entire water column were collected at five equidistant

locations along the mid-line of the enclosures using a

tube sampler (6.7 cm in diameter), sampling being

conducted from the water surface to just above the

sediment. From the first sample (c. 14 L) taken in the

centre, sub-samples were taken for TP, TN, Chl-a and

phytoplankton analysis. From a pooled water sample,

6 L were filtered through a 50 lm mesh net to obtain

material for zooplankton analysis. The zooplankton

samples were fixed immediately in Lugol’s iodine.

Unused water was returned to the enclosures.

Winter dynamics of plankton 1095


On each sampling occasion, water transparency was

estimated by simultaneous measurements on two

photosynthetically active radiation sensors, one in

the air (Li-190SA) and one in the water (Li-192SA;

Licor, Lincoln, NE, U.S.A.), taken at 10 cm intervals

vertically through the water column. From triplicate

light profiles, the vertical attenuation coefficient (Kd)

for the water column was calculated from the slope of

the log-transformed light measurements. The covers

inducing low and scarce light were removed during

the measurements in order to reduce the biases caused

by the low light intensities under the covers. The

shading induced by the covers was determined reg-

ularly by conducting parallel light measurements in

the water column with and without the covers. Water

temperature was measured at each sampling occasion.

The mean light level in the enclosure was determined

by: surface light, water transparency given as Kd and

the shading induced by the covers. As all enclosures

were subjected to exactly the same surface light the

integrated light within the water column (Im) can be

estimated as the dimensionless factor with the formula:

Im ¼1� e�KdZm

KdZm

(Sterner et al., 1997), using Zm = 0.5 m (half of the

maximum depth of the enclosures) and Kd corrected

by the covers applied to each enclosure; corresponding

to either 100%, 55%, 7% or <1% of the incoming light.

Analyses

Water samples for Chl-a analysis were filtered onto

47 mm Whatmann GF ⁄C filters (Whatman Internati-

onal Ltd., Maidstone, U.K.) and frozen until extraction.

Chlorophyll-a was then determined spectrophoto-

metrically (Shimadzu, UV-160; Shimadzu Corporation,

Kyoto, Japan) after extraction in 96% ethanol (DS 2201,

1986). Water chemistry (TP and TN) was analysed

monthly from October to March immediately after

sampling and according to Koroleff (1975a,b).

Phytoplankton, sampled in October and February,

was counted using an inverted microscope at 400·magnification using the Utermohl technique (Uter-

mohl, 1958). In addition, the linear dimensions of 5–10

cells of each species were measured. Cell volume for

each measured cell was determined by using the

formula for the appropriate geometric shape (Olrik,

1991). Carbon biomass was calculated using a conver-

sion factor of 0.13 pg C lm)3 for the dinoflagellates

and 0.11 pg C lm)3 for all other phytoplankton (Olrik,

1991). Furthermore, carbon biomass was estimated

from Chl-a at each sampling date by using a conversion

factor of 35 (Reynolds, 1984). Conversion to dry weight

was made using a factor of 0.29 (Reynolds, 1984).

Species in each zooplankton sample were identified

and counted using a stereomicroscope until at least 50

individuals of the most dominant species had been

counted (Hansen et al., 1992). In samples with high

densities, zooplankton (mainly rotifers) were identified

and counted in sub-samples. Between 2% and 100% of

each sample was counted. Copepods were counted as

adults (according to sex and females with or without

eggs), copepodites and nauplii. Zooplankton samples

were enumerated once a month from October to March.

To estimate zooplankton biomass, length measure-

ments were made of at least 30 rotifers, 30 cladocerans,

30 copepodites and 15 adult copepods using a digita-

lised micrometer connected to the microscope. The

biomasses of copepods, cladocerans and rotifers were

estimated from length–weight relationships (Dumont,

Van de Velde & Dumont, 1975; Bottrell et al., 1976; and

McCauley, 1984; respectively). The biomasses of cyclo-

poid and calanoid nauplii were set to 0.26 lg DW indi-

viduals)1 (Culver et al., 1985) and dry weight for

rotifers was set to 4% of the wet weight for Asplanchna

and to 10% for all other rotifers (Bottrell et al., 1976).

Statistics

Repeated-measures ANOVAANOVA (SAS General Linear

Models routine of SAS Institute Inc., 1990) was used

to elucidate the impact of fish, light, sampling date

and lake type on water chemistry, Chl-a, total

zooplankton biomass and biomasses of major zoo-

plankton groups. All data were log10-transformed

before conducting the analyses in order to stabilise

variance. When significant effects were found, treat-

ment means were compared using the Least Squares

MEANS (LSMEANS) procedure (Sokal & Rohlf, 1995).

Results

Chemical and physical variables

Initially, higher TP and lower TN concentrations were

found in turbid Lake Søbygard than in clear Lake



Stigsholm. However, for the remainder of the study,

the nutrient concentrations did not differ between the

two lakes (see details in Liboriussen et al., 2005). The

light treatments significantly affected both the TP and

the TN concentrations in the two lakes (Tables 1 & 2),

as these nutrients were generally lower at high and

medium than at low and scarce light levels. With a

few exceptions the presence of fish decreased the TP

concentrations in the enclosures in both lakes, while

higher TN concentrations were found in the clear lake

when fish were present. Water temperatures ranged

between 3.3 �C (January) and 10.5 �C (October) in

both lakes.

Phytoplankton

Total available phytoplankton carbon (estimated from

Chl-a) in winter ranged between 0.85 and

1.93 mg C L)1 at high and medium light (Table 3)

and between 0.08 and 0.18 mg C L)1 at low and scarce

light. However, the availability of edible phytoplank-

ton carbon (based on both edible sizes and taxa) was

markedly lower, reaching levels as low as 0 mg C L)1

at the most extreme (Table 3). Only in the full light

treatment did the enclosures with fish have a signif-

icantly higher phytoplankton biomass than the enclo-

sures without fish (LSMEANS, P < 0.01) (Fig. 1a). In

contrast, there was no relationship between TP and

Chl-a for any of the treatments (Fig. 1b) or between

Chl-a and TN (data not shown), indicating that light

was the main driver of phytoplankton growth.

The phytoplankton communities in clear Lake

Stigsholm consisted mainly of cryptophytes, whereas

turbid Lake Søbygard had more diverse communities

that were quantitatively dominated by small flagel-

lates, diatoms and chlorophytes. The phytoplankton

community structure (Fig. 2a) and size distribution

(Fig. 2b) were influenced by light, especially in the

clear lake, whereas the response to fish was weak in

both lakes. The small (£20 lm) unidentified flagellates

generally constituted higher proportions of the total

phytoplankton biomass at low and scarce light

levels, while cryptophytes (Cryptomonas sp. (<30 lm),

Cryptomonas reflexa and Rhodomonas sp.) and

Table 2 Summary of repeated measures A N O V AA N O V A tests analysing if winter TP, TN and phytoplankton biomass (Chl-a) in 24 enclo-

sures in clear Lake Stigsholm and turbid Lake Søbygard are affected by sampling date, fish and light

Lake n Date Fish Light Fish · date Light · date Light · fish Light · fish · date

TP Stigsholm 5 *** *** ** ** ns ns ns

Søbygard 6 *** * *** ** ns ** ns

TN Stigsholm 6 ns * *** ns ns ns ns

Søbygard 6 *** ns *** ns ns ** ns

Chl-a Stigsholm 12 *** ** *** * *** * ns

Søbygard 12 *** *** *** *** *** ns ns

The 24 enclosures in each lake were either with fish or without fish and exposed to one of four light levels (high, medium, low or scarce

light). Samples were taken from mid-October to March.

TP, total phosphorus; TN, total nitrogen; Chl-a, chlorophyll-a; ns, non-significant.

*P < 0.05; **P < 0.01; ***P < 0.001.

Table 1 Winter total phosphorus and total nitrogen (mean November–March, ±1 SE) in turbid Lake Søbygard and clear Lake

Stigsholm (n = 5)

Lake Light

Total phosphorus (mg L)1) Total nitrogen (mg L)1)

+Fish )Fish +Fish )Fish

Søbygard High 0.233 ± 0.02 0.262 ± 0.01 0.737 ± 0.08 0.620 ± 0.09

Medium 0.203 ± 0.02 0.253 ± 0.03 1.220 ± 0.14 1.323 ± 0.08

Low 0.210 ± 0.03 0.287 ± 0.03 1.460 ± 0.28 1.403 ± 0.24

Scarce 0.303 ± 0.02 0.264 ± 0.01 1.140 ± 0.07 1.570 ± 0.12

Stigsholm High 0.210 ± 0.01 0.310 ± 0.01 0.830 ± 0.16 0.743 ± 0.07

Medium 0.277 ± 0.03 0.258 ± 0.04 0.987 ± 0.19 0.943 ± 0.06

Low 0.251 ± 0.02 0.435 ± 0.05 1.753 ± 0.32 1.513. ± 0.26

Scarce 0.268 ± 0.06 0.395 ± 0.06 1.870 ± 0.18 1.493 ± 0.15



Euglenophyceae were quantitatively more important at

high and medium light. The relative importance of

the small and large nanoplankton groups (2–20 lm)

tended to increase with decreasing light at the expense

of, in particular, the small microplankton group

(21–64 lm) in both lakes.

Zooplankton biomass

Total zooplankton biomass was generally higher in

Lake Stigsholm than in Lake Søbygard (Fig. 3) and in

both lakes the biomass was significantly affected by

fish, light and date, which also exhibited significant

interactions (Table 4). Fish reduced the total zoo-

plankton biomass at all light treatments, but a more

pronounced impact was seen at high and medium

light levels than at low and scarce light. The effect of

fish on the total zooplankton biomass was apparent

within 1 month after initiation of the experiment

(Fig. 3) and it remained significant throughout the

rest of the study period. At low and scarce light levels,

the total zooplankton biomass was significantly lower

than at high and medium light (LSMEANS, P < 0.01),

and this effect was obvious already within the first

Table 3 Phytoplankton carbon contents estimated from: chlorophyll-a [mean November–March, ±1 SE (n = 9)], the edible phyto-

plankton size fraction (December and February) and the edible phytoplankton taxa (December and February)

Lake Light

Phytoplankton carbon content (mg C L)1)

Chlorophyll-a* Edible size fraction† Edible taxa†

+Fish )Fish +Fish )Fish +Fish )Fish

Søbygard High 1.84 ± 0.54 1.06 ± 0.39 0.24 (0.81) 0.33 (0.57) 0.01 (0.35) 0.06 (0.06)

Medium 1.22 ± 0.35 1.27 ± 0.28 0.10 (0.18) 0.39 (0.16) 0.23 (0.53) 0.06 (0.14)

Low 0.17 ± 0.06 0.18 ± 0.08 0.04 (0.03) 0.06 (0.02) 0.01 (0.01) 0.04 (0.02)

Scarce 0.09 ± 0.02 0.08 ± 0.04 0.03 (0.02) 0.04 (0.02) 0.01 (0.00) 0.01 (0.00)

Stigsholm High 1.93 ± 0.67 1.22 ± 0.31 0.06 (0.74) 0.10 (0.27) 0.06 (0.39) 0.16 (0.48)

Medium 1.02 ± 0.20 0.85 ± 0.28 0.04 (0.26) 0.06 (0.77) 0.03 (0.12) 0.07 (1.52)

Low 0.13 ± 0.03 0.11 ± 0.03 0.01 (0.09) 0.01 (0.01) 0.01 (0.02) 0.02 (0.05)

Scarce 0.09 ± 0.03 0.11 ± 0.03 0.02 (0.01) 0.02 (0.01) 0.01 (0.02) 0.00 (0.01)

*Converted from chlorophyll-a using a conversion factor of 35 (Reynolds, 1984).†Based on phytoplankton biomass data (lg C L)1). The size fraction of 2–20 lm was classified as edible phytoplankton for particularly

rotifers and calanoid copepods (Gliwicz, 1969; Pourriot, 1977), whereas phytoplankton belonging to cryptophytes, chrysophytes,

diatoms, green flagellates and unidentified flagellates were classified as edible phytoplankton taxa for the herbivorous and omniv-

orous stages of cyclopoid copepods (Kniesly & Geller, 1986; Toth et al., 1987).

Chl

orop

hyll

a (µ

g L–1

)

Light (Im) Total phosphorus (mg L–1)

Lake Søbygård

Lake Søbygård

Lake Stigsholm

Lake Stigsholm

0

20

40

60

80 (a) (b)

0 0.2 0.1 0.4 0.3 0.6 0.5 0 0.2 0.4 0.8 0.6

+Fish

–Fish

Fig. 1 Relationship between chlorophyll-a and (a) light (Im) and (b) total phosphorus in the presence (+, filled symbols) and

absence (), empty symbols) of fish in turbid Lake Søbygard (circles) and clear Lake Stigsholm (squares). Points are averages and error

bars are standard errors for the whole experimental period (October–March). See the text for details on Im.



2 weeks after the enclosures were shaded and irre-

spective of the occurrence or not of fish predation

(Fig. 3).

The zooplankton : phytoplankton biomass ratios

were generally low but, on average, almost twice as

high in Lake Stigsholm as in Lake Søbygard, as

indicated by the slope of the linear regression between

the fit of the two parameters (Fig. 4a). The presence of

fish lowered the zooplankton : phytoplankton ratio in

both lakes and to a similar magnitude (a decrease in

the ratio from 0.09 to 0.02 for Lake Stigsholm and from

0.04 to 0.01 in Lake Søbygard; Fig. 4a, Table 4). The

change of the ratio through time, measured as the

slope of the regression on each sampling occasion,

showed that the ratio was highest in the fishless

enclosures in both lakes, and, especially in Lake

Stigsholm, the ratio tended to increase towards the

end of the experiment (Fig. 4b).

Zooplankton community composition

Overall, the presence of fish led to low crustacean

biomass, high rotifer biomass and changes in the life

history of copepods. The strength of the fish effect on

zooplankton biomass diminished with decreasing

light intensity and the effect of light was strongest in

the presence of fish (Fig. 5).

In both lakes, rotifers exhibited higher biomass

when exposed to fish predation, while reduced light

levels negatively impacted the rotifer biomass (Fig. 5).

At low and scarce light levels, the rotifer biomass was

not affected by the presence of fish (LSMEANS,

P < 0.05). The effect of fish on rotifer biomass was

also significantly related to the phytoplankton bio-

mass on all sampling occasions for both lakes and fish

treatments (Fig. 4d). The rotifer : phytoplankton bio-

mass ratio was higher when fish were present on all

sampling occasions from as early as November in

Lake Søbygard and from December in Lake Stigsholm

(Fig. 4d). The crustacean : phytoplankton biomass

ratio was much higher when fish were absent. The

presence of fish decreased the crustacean biomass

differentially at the different light treatments, having

a stronger effect in the higher light treatments

(Fig. 4c). In contrast, in the enclosures without fish,

there was a positive correlation between crustacean

Others Conjungatophyceae Chrysophyceae Cyanophyceae Dinophyceae Euglenophyceae Diatomophyceae Chlorophyceae Cryptophyceae Flagellates

>64 µm 21–64 µm 11–20 µm 2–10 µm

0

20

40

60

80

100 S L M H S L M H S L M H S L M H S L M H S L M H S L M H S L M H +Fish –Fish +Fish –Fish

0

20

40

60

80

100

(a) Taxa

Phy

topl

ankt

on b

iom

ass

dist

ribut

ed a

mon

g ta

xa a

nd s

ize

clas

ses

(%)

Lake Søbygård – turbid Lake Stigsholm – clear

(b) Size classes

October February October February October February October February

Fig. 2 (a) Relative contribution (%) of different phytoplankton taxa to total phytoplankton biomass in October and February. ‘Others’

consist of taxa contributing less than 5% of the relative biomass. ‘Flagellates’ are unidentified specimens £20 lm. (b) Relative

contribution (%) of biovolume of 4 different size classes to total phytoplankton biovolume in October and February. Treatment

abbreviations are (+) presence and ()) absence of fish at the different light intensities, high (H)-, medium (M)-, low (L) and scarce (S)

light, in turbid Lake Søbygard (left) and clear Lake Stigsholm (right).



Tota

l zoo

plan

kton

bio

mas

s (µ

g D

W L

–1)

0

200

400

600

800

0

50

100

150

200 372

Lake Søbygård – turbid Lake Stigsholm – clear

October November December January February March October November December January February March

H

H

M

M

+Fish

–Fish

L

L

S

S

+Fish

–Fish

Fig. 3 Total zooplankton biomass (lg DW L)1, ±1 SE) in high (H) and medium (M) light (top), and low (L) and scarce (S) light

(bottom) in the presence (+) and absence ()) of fish in turbid Lake Søbygard (left) and clear Lake Stigsholm (right). Note the difference

in scale between the H–M and L–S enclosures.

Table 4 Summary of repeated measures A N O V AA N O V A tests analysing if the biomass of zooplankton, cladocerans, rotifers, cyclopoids,

calanoids and the ratio of zooplankton to phytoplankton and calanoid to total number of copepods in clear Lake Stigsholm and turbid

Lake Søbygard are affected by planktivorous fish, available light conditions and sampling date during winter

Lake n Date Fish Light Date · fish Date · light Fish · light Date · fish · light

Biomass

Zooplankton Stigsholm 5 *** *** *** *** ns *** ns

Søbygard 7 *** *** *** *** *** ** ns

Cyclopoid copepods Stigsholm 6 *** *** *** *** * * ns

Søbygard 7 *** *** *** *** ns ns ns

Calanoid copepods Stigsholm 5 ** ns ** ns ns ns ns

Søbygard – – – – – – –

Cladocerans Stigsholm 7 ns *** * ns ns ns ns

Søbygard 7 ns *** ns ns ns ns ns

Rotifers Stigsholm 5 ** *** *** ns ns *** *

Søbygard 6 *** *** *** ** * *** *

Ratios

Zooplankton :

phytoplankton

Stigsholm 6 ns *** ns * ns ** ns

Søbygard 7 *** *** ns *** *** * ns

Calanoid : copepods Stigsholm 5 * *** * ** ns *** ns

Søbygard – – – – – – –

The 24 enclosures in each lake were either with planktivorous fish or without fish and exposed to one of four light levels (high,

medium, low or scarce light).

ns, non-significant; –, no data.

*P < 0.05; **P < 0.01; ***P < 0.001.



zooplankton and phytoplankton biomass. This rela-

tionship was already significant in November.

Total cladoceran biomass, although low, was sig-

nificantly reduced by the presence of fish in both lakes

(Table 4). Initially, several cladoceran species were

present in the enclosures in both lakes but, after only

1 week, Chydorus sphaericus (Mueller, 1785) dominated

the cladoceran biomass, both in the presence and in

the absence of fish. A general decline in cladoceran

biomass was associated with the reduced diversity of

the cladoceran community (data not shown). The light

effect on the community composition was less pro-

nounced than fish presence, but there was a tendency

towards a higher proportion of cyclopoids and

cladocerans with reduced light when fish were pres-

ent (Fig. 5). Initially, Cyclops vicinus (Uljanin, 1875)

and rotifers dominated the zooplankton community

in Lake Søbygard, while no calanoid copepods were

found. In this lake reduced light led to a shift from

dominance of rotifers to cyclopoid copepods when

fish were present. In Lake Stigsholm, the zooplankton

community was more diverse than in Lake Søbygard

and it was quantitatively dominated by the calanoid

copepod Eudiaptomus gracilis (G. O. Sars, 1863),

rotifers and, to a lesser extent, by cyclopoid copepods

and cladocerans. In Lake Stigsholm, a reduction of the

light shifted the community from dominance by

rotifers to calanoid copepods (E. gracilis) when fish

were present, while a shift towards a larger propor-

tion of calanoids at the expense of cyclopoids

occurred when fish were absent (Fig. 5). The ratio of

calanoid copepods to the total number of copepods

(calanoid : copepod ratio) in Lake Stigsholm was

higher in enclosures with fish than in those without

fish as early as in November (Fig. 6). In addition, the

calanoid : copepod ratio in the lake was significantly

lower at the high and medium light treatments than at

low and scarce light in the fish-free enclosures

(Table 4).

October November December January February March

0

0.04

0.08

0.12

0.16

0

0.04

0.08

0.12

0.16

0

0.01

0.02

0.03

0.04

0.05

Zoo

plan

kton

: ph

ytop

lank

ton

Cru

stac

ean

: phy

topl

ankt

on

Rot

ifer

: phy

topl

ankt

on

0

0.1

0.2

0.3

0.5 (a)

(b)

(c)

(d)

0.4

0 2 4 6 8 10

s = 0.09 s = 0.04

s = 0.02

s = 0.01

Zoo

plan

kton

(µ

g D

W L

–1)

Phytoplankton (µg DW L–1)

Lake Søbygård Lake Søbygård Lake Stigsholm Lake Stigsholm

+Fish –Fish

Fig. 4 (a) Relationship between zooplankton and phytoplankton

biomass in the presence (+, filled symbols) and absence (), open

symbols) of fish in turbid Lake Søbygard (circles) and clear Lake

Stigsholm (squares). Points are averages and error bars are

standard errors for the whole experimental period (November–

March) excluding the initial conditions. Straight lines are the

linear regression fit of the averages (all regressions were

significant at P < 0.05 and r2 > 0.93) and ‘s’ is the slope of the

regressions for each line. Lower panels are the temporal changes

in the (b) total zooplankton : phytoplankton, (c) crustacean

zooplankton : phytoplankton and (d) rotifers : phytoplankton

biomass ratios. The ratios are the slope of fitting a linear

regression (as in a) on each sampling occasion between the

zooplankton and phytoplankton biomass. Only significant

regression slopes are included.



Copepod life history changes

The abundance of adult cyclopoid copepods was

strongly affected by the presence of fish. At all light

levels and in both lakes, both male and, particularly,

female cyclopoids made up a smaller proportion of

the total cyclopid biomass (mostly dominated by

C. vicinus in both lakes) when the community was

exposed to fish predation (Fig. 7). No egg-bearing

cyclopoid females were found in enclosures with fish,

0

20

40

60

80

100

Start November– December

January– February

March Start November– December

January– February

March

S L M H S L M H S L M H S L M H S L M H S L M H S L M H S L M H +Fish –Fish

0

20

40

60

80

100

Dis

trib

utio

n of

zoo

plan

kton

bio

mas

s (%

)

Rotifers Cladocerans Calanoids Cyclopoids

Lake Søbygård – turbid

Lake Stigsholm – clear

Fig. 5 Relative contribution (%) of different zooplankton groups to total zooplankton biomass in the presence (+) and absence ()) of

fish at the different light intensities in turbid Lake Søbygard (top) and clear Lake Stigsholm (bottom). Months showing similar

patterns, i.e. November–December and January–February, are averaged. Abbreviations for the treatments are as in Fig. 2.

Start November–December

January–February

January–February

March

SLMH SLMH SLMH SLMH

+Fish

Start November–December

March

SLMH SLMH SLMH SLMH

–Fish

0

20

40

60

80

100

Cal

anoi

d : c

opep

od r

atio

(%

)

Fig. 6 Calanoid : copepod ratios (±1 SE) by number in clear Lake Stigsholm. Months showing similar patterns, i.e.

November–December and January–February, are averaged. Abbreviations for treatments are as in Fig. 2.



whereas egg-bearing individuals were observed in the

fish-free enclosures, though mainly at the high and

medium light treatments. In the enclosures with fish

more nauplii were also recorded in both lakes

(LSMEANS, P < 0.01). In both lakes, higher propor-

tions of cyclopoid males (i.e. male : female ratios

between 0.8 and 1.0) were found in enclosures with

fish than in those without fish. In the latter, the ratio

was <0.5 in Lake Stigsholm and 0.5–0.7 in Lake

Søbygard.

The impact of light and fish on the life history of

E. gracilis was not as clear as for C. vicinus. However,

in the fish-free enclosures, the biomass of adult

calanoid copepods tended to increase as light inten-

sities decreased, whereas the share of nauplii

decreased with decreasing light intensity (Fig. 7).

Adult calanoid copepods constituted large propor-

tions of the calanoid biomass in the presence of fish at

all light levels. The male : female ratio among cala-

noid copepods ranged between 0.4 and 0.6, regardless

of the level of fish predation.

Discussion

We observed a strong effect of fish and light on the

winter zooplankton community. A shift occurred

from dominance of cyclopoid copepods in the absence

of fish in both lakes to dominance of small-sized

Dis

trib

utio

n of

cop

epod

s (%

)

Lake Søbygård – cyclopoid

Lake Stigsholm – cyclopoid

Lake Stigsholm – calanoid

Copepodites Nauplii

Male Female + eggs Female – eggs

0

20

40

60

80

100

Start November– December

January– February

March Start November– December

January– February

March

S L M H S L M H S L M H S L M H S L M H S L M H S L M H S L M H +Fish –Fish

0

20

40

60

80

100

0

20

40

60

80

100

Fig. 7 Relative contribution (%) of different development stages to total cyclopoid copepod biomass and total calanoid copepod

biomass in turbid Lake Søbygard and clear Lake Stigsholm. The cyclopoid copepods were mainly dominated by Cyclops vicinus

in both lakes and the calanoid copepods by Eudiaptomus gracilis in Lake Stigsholm. No calanoids were present in Lake Søbygard.

Months showing similar patterns, i.e. November–December and January–February, are averaged. Abbreviations for treatments are

as in Fig. 2.



rotifers in turbid Lake Søbygard and dominance of

rotifers and calanoid copepods in clear Lake Stigs-

holm when fish were present. High sex ratios in the

presence of fish also indicated a strong size-selective

predation pressure on cyclopoids (Hairston, Walton &

Li, 1983; Hansen & Jeppesen, 1992a). In contrast, sex

ratios for calanoid copepods were not related to the

fish treatment.

Our results indicate strong resource control of

zooplankton during winter. First, the total zooplank-

ton biomass decreased with light, both in the presence

and absence of fish, which probably can be attributed

to a light-mediated reduction in the availability of

phytoplankton (Fig. 1a). Secondly, the consistent

absence of egg-bearing copepods and the constantly

low nauplii density at low and scarce light compared

to the high and medium light treatments strongly

suggest low food availability during winter at

reduced light levels. Santer & van den Bosch (1994)

observed that continuous egg production of C. vicinus

required food concentrations above 0.5 mg C L)1,

which is well above the actual food concentrations

at low and scarce light in our study. Thus, egg

production probably ceased and this led to low

recruitment during winter. The zooplankton commu-

nity structure was apparently also affected by the

availability of food. The increase in the relative

contribution of E. gracilis to the zooplankton commu-

nity with a reduction in light may be due to its

tolerance to starvation and higher energetic efficiency

at lower food concentrations compared to rotifers and

cyclopoid copepods (Santer, 1994). In addition, the

dominance of more polyphagous and detrivorous

rotifer species (such as Keratella quadrata (Muller,

1786), K. cochlearis (Gosse, 1851), species of Brachionus

and Filinia terminalis (Plate, 1886)) at low and scarce

light compared to the flagellate-eating Polyarthra at

high and medium light is a likely consequence of

reduced food availability.

Lake Stigsholm had a consistently higher zooplank-

ton biomass than Lake Søbygard for both fish treat-

ments and for almost all light conditions (Fig. 4a). In

contrast, phytoplankton biomass was not significantly

different between the two lakes (Fig. 1a). In a parallel

study Liboriussen & Jeppesen (2003) found that Lake

Stigsholm had a significantly higher benthic produc-

tion than Lake Søbygard due to higher light penetra-

tion in the water, however this was not reflected in the

periphyton biomass in the enclosures (Liboriussen

et al., 2005). Therefore, the higher zooplankton

biomass in Lake Stigsholm might be explained by a

partial consumption of benthic algae by zooplankton.

We found interaction effects of fish and light on the

zooplankton biomass. The strength of the fish effect

decreased with a reduction in light. Several mecha-

nisms may be involved here. First, the effect of

predation depends on the density of prey (Holling,

1966; Werner & Hall, 1974). Prey density may have

been too low at low and scarce light to be attractive to

predators. Secondly, fish predation may exert less

influence on the zooplankton community when the

larger zooplankton species are eliminated and the

community composition has shifted towards domi-

nance of small species and small-bodied individuals

(Vanni, 1987). Thirdly, the zooplankton at high and

medium light may have been able to better compen-

sate for predation than at low and scarce light because

of the higher food availability. Finally, the reduced

light conditions in the low and scarce light enclosures

may have influenced the number of prey in the fish’s

field of vision (Mills, Confer & Kretchmer, 1986;

O’Brien, 1987; Pekcan-Hekim & Horppila, 2007).

The light-induced changes in the structure and size

distribution of the phytoplankton community were

most pronounced in the clear lake and the light effect

was much stronger than the effect of fish. Neverthe-

less, the increase in the relative importance of nano-

plankton groups and, thus, the edible algal fraction at

reduced light was not large enough to overcome the

concurrent reduction of the total phytoplankton bio-

mass. In addition to changing the food quantity, light

and nutrients have also been found to affect phyto-

plankton stoichiometry (Sterner et al., 1997; Urabe

et al., 2002; Elser et al., 2003; Dickman, Vanni &

Horgan, 2006) and consequently the food quality for

grazers. Accordingly, Dickman et al. (2006) found that

the phytoplankton C : N and C : P ratios increased

with light, and slopes of the stoichiometric ratio

versus irradiance relationships were steeper with

ambient nutrients than with nutrients added. How-

ever, the effects of light and nutrients on phytoplank-

ton stoichiometry were often interactive and varied

considerably between lakes, but some of this variation

may be related to phytoplankton species diversity.

Changes in the elemental content of food, particularly

with respect to phosphorus, have been shown to be

important for grazer growth (Hessen, 1992). In addi-

tion, the effect of decreasing light on increasing



nutrient ratios has been shown to result in increased

herbivore production (Urabe et al., 2002).

We found an overall decrease in zooplankton

biomass with decreasing light and this may appear

contradictory to the results of Urabe et al. (2002).

However, in our study, the TP concentration and the

gradient in light conditions (TP ranged

0.2–0.3 mg P L)1 and light from 100% to <1% of the

incoming light) were much higher and stronger than

those studied by Urabe et al. (TP range: <0.0015–

0.012 mg P L)1, light treatments: 100% and 7%). No

relationship could be traced between Chl-a and the TP

concentration. Thus, it would appear that in lakes

with a high phosphorus content, such as those in our

study, the relative effects of changing stoichiometric

composition at variable light conditions may be of

much less importance than those of food availability.

In clear lake Stigsholm, the calanoid : copepod ratio

was higher in the presence than in the absence of fish.

This result disagrees with the findings of most studies

that generally show a lower calanoid : cyclopoid ratio

in the presence of planktivorous fish (Soto & Hurlbert,

1991b; summarised in Hurlbert & Mulla, 1981).

Cyclopoid copepods are usually found to dominate

in the presence of fish, both in experimental studies

(Lynch, 1979; Horppila & Kairesalo, 1990) and in lakes

(Brooks & Dodson, 1965; Hansen & Jeppesen, 1992b),

and they are, therefore, generally considered to be less

susceptible to fish predation than calanoid copepods

(Cryer, Pierson & Townsend, 1986). However, in

accordance with our results, Brooks (1968) observed

higher calanoid : cyclopoid ratios in the presence of

fish and suggested that it is the irregular, jerky motion

of cyclopoid copepods that attracts the attention of a

searching fish more readily than the typically gliding

motion of calanoid copepods. In support of this

interpretation, studies have shown that the biomass

(Nilssen, 1977; Papinska, 1988), life cycles (Nilssen,

1978; Maier, 1989) and even behaviour of cyclopoid

copepods (George, 1973; Gliwicz & Rowan, 1984) are

affected by the predation of planktivorous fish. In our

study, the lack of large cladocerans in winter may

have played a significant role in the outcome of the

calanoid–cyclopoid interactions. This hypothesis is

supported by Hurlbert & Mulla (1981) who suggested

that, when Daphnia are absent, fish select for cyclopoid

over calanoid copepods. This, in turn, decreases

cyclopoid predation on the calanoid copepods, there-

by favouring the calanoids. That cyclopoid adults and

advanced stages of copepodites can exert a consider-

able impact on the population dynamics of calanoid

copepods has been demonstrated in several studies

(Brandl & Fernando, 1978; Zankai, 1984; Kawabata,

1991). Conversely, calanoid biomass tended to be

higher in the absence of fish at low and scarce light,

which indicates that the impact of fish can exceed that

of cyclopoids when these copepods are controlled by

fish predation.

In our study, differences in body size are not

considered to be important for the preference by fish

of C. vicinus over E. gracilis, as females of both species

did not differ in body size (mean difference in length:

0.05 mm), whereas male E. gracilis were, on average,

0.2 mm larger than male C. vicinus (data not shown).

Spatial niche separation might have influenced the

susceptibility of the two copepod species to predation.

C. vicinus inhabits the lower depths during daytime,

whereas E. gracilis is more pelagically oriented (Maier,

1996). Moreover, fish mainly relied on benthic food in

the enclosures (J. Takken, NERI, pers. comm.), thereby

exposing the cyclopoid copepods to fish predators.

Calanoid copepods were not observed in the turbid

lake. This may reflect the high biomass of cyprinids in

this lake. Other long-term studies verify the absence

of calanoid copepods from the lake (Hansen &

Jeppesen, 1992a; Jeppesen et al., 1998).

Considering the importance of light for visual

predation, it was expected that a reduction in light

would provide, in part, a predation refuge for larger

crustaceans as attenuation of contrast between prey

items and their environment makes them less visible

to fish (Lythgoe, 1966). However, a refuge effect of

large-bodied cladocerans at low and scarce light may

have been difficult to detect because of the strong

light-mediated suppression of zooplankton biomass

in general, which may have counteracted the light

refuge effect of large-bodied cladocerans. It may be

argued that the absence of large cladocerans during

autumn and winter was due to low fecundity med-

iated by food shortage and low temperatures or,

possibly, low winter hatching of resting eggs (Jeppe-

sen et al., 2004). In addition, the possibility that

cyclopoids controlled the large cladocerans by prey-

ing upon their juveniles and eggs at the beginning of

the experiment and, thus, kept the populations at low

levels is a likely contributory explanation for the low

abundance of cladocerans (Gliwicz & Stibor, 1993;

Adrian & Deneke, 1996).



We found the effect of light reduction to be

marginal at 55% light, while strong effects were seen

when the light was reduced to 7% or below. When an

IPCC (1996) climate A2 scenario is employed, we can

predict that the current winter temperatures in Den-

mark (54–55�N) in the future probably will occur in

coastal areas at latitudes between 60 and 65�N where

the global irradiance is, on average, 40–50% lower

than in Denmark during the period November to

February. Therefore, when the temperate shallow lake

plankton communities expand further northward due

to the global temperature increase, results from this

study indicate that light will likely be of only modest

importance for their development in winter in these

new areas, at least for the rest of this century.

However, some reservations regarding this conclu-

sion exist: (i) our results are derived from eutrophic

shallow lakes, the typical lake type in the cultivated

landscape of Denmark (Søndergaard, Jeppesen &

Jensen, 2005). Different results may be obtained in

more oligotrophic lakes where the benthic production

is of higher importance (Liboriussen & Jeppesen, 2003;

Vadeboncoeur et al., 2003) and light limitation of

primary production possibly more severe. However,

in lowland coastal areas further north we can expect

more intensive agriculture in a future warmer climate;

therefore, the present-day oligotrophic lakes in these

areas may become more eutrophic in the future and

thereby approach the conditions in today’s Danish

shallow lakes; (ii) As the expected light reduction is

close to our 55% treatment we cannot exclude the

possibility of a larger effect if the response from 55%

to 7% shows a sharp nonlinear threshold response

close to the 55%. Moreover, the IPCC predictions are

themselves uncertain and (iii) in deep lakes, the effect

may likely be stronger as phytoplankton can be

expected to be more light limited than in shallow

lakes due to deep mixing in winter. Clearly, more

studies are needed to fully elucidate the role of light

for the winter plankton dynamics in lakes seen in a

global warming perspective.

Acknowledgments

We wish to thank the owners of the lakes, Kirsten Ove

Henriksen (Lake Stigsholm) and Wefri a ⁄s Frijsenborg

and Wedellsborg (Lake Søbygard), for permission to

set up the experiments. The technical staff at the

National Environmental Research Institute, Silkeborg,

are gratefully acknowledged for their assistance. We

are also grateful to Anne Mette Poulsen for skilful

editorial assistance. This study was supported by the

EU EUROLIMPACS project (GOCE-CT-2003-505540)

and CLEAR (A Villum Kann Rasmussen Centre of

Excellence project). MV was supported by a Marie

Curie post-doctoral grant (MEIF-CT-18 2005-010554)

and a Juan de la Cierva grant (Spanish Ministry of

Education and Science).

References

Adrian R. & Deneke R. (1996) Possible impact of mild

winters on zooplankton succession in eutrophic lakes

of the Atlantic European area. Freshwater Biology, 36,

757–770.

Bottrell H.H., Duncan A., Gliwicz Z.M., Grygierek E.,

Herzig A., Hillbricht-Ilkowska A., Kurasawa H., Lars-

son P. & Weglenska T. (1976) A review of some

problems in zooplankton production studies. Norwe-

gian Journal Zoology, 24, 419–456.

Brandl Z. & Fernando C.H. (1978) Prey selection by the

cyclopoid copepods Mesocyclops edax and Cyclops

vicinus. Verhandlungen der Internationale Vereinigung

der Limnologie, 20, 2505–2510.

Brooks J.L. (1968) The effects of prey size selection by

lake planktivores. Systematic Zoology, 17, 273–291.

Brooks J.L. & Dodson S.I. (1965) Predation, body size,

and composition of plankton. Science, 150, 28–35.

Carpenter S.R. & Kitchell J.F. (Eds) (1993) The Trophic

Cascade in Lakes. Cambridge University Press, Cam-

bridge.

Christoffersen K., Riemann B., Klysner A. & Søndergaard

M. (1993) Potential role of fish predation and natural

populations of zooplankton in structuring a plankton

community in eutrophic lake water. Limnology and

Oceanography, 38, 561–573.

Cryer M., Pierson G. & Townsend C.R. (1986) Reciprocal

interactions between roach, Rutilus rutilus, and zoo-

plankton in a small lake: prey dynamics and fish

growth and recruitment. Limnology and Oceanography,

31, 1022–1038.

Culver D.A., Boucherle M.M., Bean D.J. & Fletcher J.W.

(1985) Biomass of freshwater crustacean zooplankton

from length–weight regressions. Canadian Journal of

Fisheries and Aquatic Sciences, 42, 1380–1390.

Dickman E.M., Vanni M.I. & Horgan M.J. (2006) Inter-

active effects of light and nutrients on phytoplankton

stoichiometry. Oecologia, 149, 676–689.

DS 2201 (1986) Vandundersøgelse: Klorofyl a, spektrofoto-

metrisk maling i ethanolekstrakt. Dansk Standard-

iseringsrad, København. [Water Investigation: Chlorophyll



a, Spectrophotometrical Measurement in Ethanol Extract].

The Danish Standardisation Council, Copenhagen. (In

Danish).

Dumont H.J., Van de Velde I. & Dumont S. (1975) The

dry weight estimate of biomass in a selection of

Cladocera, Copepoda and Rotifera from the plankton,

periphyton and benthos of continental waters. Oecolo-

gia, 19, 75–97.

Elser J.J., Kyle M., Makino W., Yoshida T. & Urabe J.

(2003) Ecological stoichiometry in the microbial food

web: a test of the light:nutrient hypothesis. Aquatic

Microbial Ecology, 31, 49–65.

George D.G. (1973) Diapause in Cyclops vicinus. Oikos, 24,

136–142.

Gliwicz Z.M. (1969) The food resources of lake zoo-

plankton. Ekologia Polska, 15, 205–223.

Gliwicz Z.M. (2003) Between hazards of starvation and

risk of predation: ecology of offshore animals. In:

Excellence of Ecology, Book 12 (Ed. O. Kinne), 379 pp.

International Ecology Institute, Oldendorf ⁄Luhe.

Gliwicz Z.M. & Rowan M.G. (1984) Survival of Cyclops

abyssorum tatricus (Copepoda, Crustacea) in alpine

lakes stocked with planktivorous fish. Limnology and

Oceanography, 29, 1290–1299.

Gliwicz Z.M. & Stibor H. (1993) Egg predation by

copepods in Daphnia brood cavities. Oecologia, 95,

295–298.

Hairston N.G. Jr, Walton W.E. & Li K.T. (1983) The

causes and consequences of sex-specific mortality in a

freshwater copepod. Limnology and Oceanography, 28,

935–947.

Hansen A.-M. & Jeppesen E. (1992a) Life cycle of Cyclops

vicinus in relation to food availability, predation,

diapause and temperature. Journal of Plankton Research,

14, 591–605.

Hansen A.-M. & Jeppesen E. (1992b) Changes in the

abundance and composition of cyclopoid copepods

following fish manipulations in eutrophic Lake Væng,

Denmark. Freshwater Biology, 28, 183–193.

Hansen A.-M., Jeppesen E., Bosselmann S. & Andersen P.

(1992) Zooplankton i søer – metoder og artsliste. Miljøpro-

jekt nr. 205. Miljøministeriet, Miljøstyrelsen. (In Dan-

ish).

Hansson L.-A., Nicolle A., Brodersen J., Romare P.,

Nilsson P.A., Bronmark C. & Skov C. (2007) Conse-

quences of fish predation, migration, and juvenile

ontogeny on zooplankton spring dynamics. Limnology

and Oceanography, 52, 696–706.

Hessen D.O. (1992) Nutrient element limitation of zoo-

plankton production. American Naturalist, 140, 799–814.

Holling C.S. (1966) The functional response of inverte-

brate predators to prey density. Memoirs of the Ento-

mology Society of Canada, 48, 1–86.

Horppila J. & Kairesalo T. (1990) A fading recovery: the

role of roach (Rutilus rutilus L.) in maintaining high

phytoplankton productivity and biomass in Lake Ves-

ijarvi, southern Finland. Hydrobiologia, 200 ⁄201, 153–165.

Hurlbert S.H. & Mulla M.S. (1981) Impacts of mosquito-

fish (Gambusia affinis) predation on plankton commu-

nities. Hydrobiologia, 83, 125–151.

IPCC (1996) Climate change 1995. The science of climate

change. In: Contribution of Working Group I to the Second

Assessment Report of the Intergovernmental Panel on

Climate Change (Eds J.T. Houghton, L.G. Meiro Filho,

B.A. Callander, N. Harris, A. Kattenberg & K. Maskell),

pp. 572. Cambridge University Press, Cambridge and

New York.

Jacobsen L., Berg S., Broberg M., Jepsen N. & Skov C.

(2002) Activity and food choice of piscivorous perch

(Perca fluviatilis) in a eutrophic shallow lake: a radio-

telemetry study. Freshwater Biology, 47, 2370–2379.

Jacobsen L., Berg S., Jepsen N. & Skov C. (2004) Does

roach behaviour differ between shallow lakes of

different environmental state? Journal of Fish Biology,

65, 135–147.

Jeppesen E., Jensen J.P., Søndergaard M., Lauridsen T.,

Pedersen L.J. & Jensen L. (1997) Top-down control in

freshwater lakes: the role of nutrient state, submerged

macrophytes and water depth. Hydrobiologia, 242 ⁄ 343,

151–164.

Jeppesen E., Søndergaard M., Jensen J.P., Mortensen E.,

Hansen A. & Jørgensen T. (1998) Cascading trophic

interactions from fish to bacteria and nutrients after

reduced sewage loading: an 18-year study of a shallow

hypertrophic lake. Ecosystems, 1, 250–267.

Jeppesen E., Jensen J.P., Søndergaard M., Lauridsen T. &

Landkildehus F. (2000) Trophic structure, species

richness and diversity in Danish lakes: changes along

a phosphorus gradient. Freshwater Biology, 45, 201–218.

Jeppesen E., Jensen J.P., Jensen C., Faafeng B., Hessen

D.O., Søndergaard M., Lauridsen T.L., Brettum P. &

Christoffersen K. (2003) The impact of nutrient state

and lake depth on top-down control in lakes: study of

466 lakes from the temperate zone to the Arctic.

Ecosystems, 6, 315–325.

Jeppesen E., Jensen J.P., Søndergaard M., Fenger-Grøn

M., Sandby K., Møller P.H. & Rasmussen H.U. (2004)

Does fish predation influence zooplankton community

structure and grazing during winter in north temper-

ate lakes? Freshwater Biology, 49, 432–447.

Jepsen N. & Berg S. (2002) The use of winter refuges by

roach tagged with miniature radio transmitters. Hydro-

biologia, 483, 167–173.

Kawabata K. (1991) Ontogenetic changes in copepod

behaviour – an ambush cyclopoid predator and a

calanoid prey. Journal of Plankton Research, 13, 27–34.



Keast A. (1968) Feeding of some Great Lakes fishes at low

temperatures. Journal of the Fisheries Research Board of

Canada, 25, 1199–1218.

Kniesly K. & Geller W. (1986) Selective feeding of four

zooplankton species on natural lake phytoplankton.

Oecologia, 69, 86–94.

Koroleff F. (1975a) Determination of total phosphorus. In:

Methods of Seawater (Ed. K. Grasshoff), pp. 168–172.

Verlag Chemie, Weinheim.

Koroleff F. (1975b) Determination of total nitrogen. In:

Methods of Seawater (Ed. K. Grasshoff), pp. 123–125.

Verlag Chemie, Weinheim.

Lambert W. & Muck P. (1985) Multiple aspects of food

limitation in zooplankton communities: the Daphnia–

Eudiaptomus example. Archiv fur Hydrobiologie

Ergebnisse der Limnologie, 21, 311–322.

Liboriussen L. & Jeppesen E. (2003) Temporal dynamics

in epipelic, pelagic and epiphytic algal production in a

clear and a turbid shallow lake. Freshwater Biology, 48,

418–431.

Liboriussen L., Jeppesen E., Bramm M.E. & Lassen

M.F. (2005) Periphyton–macroinvertebrate interac-

tions in light and fish manipulated enclosures in a

clear and a turbid shallow lake. Aquatic Ecology, 39,

23–39.

Lynch M. (1979) Predation, competition, and zooplank-

ton community structure: an experimental study.

Limnology and Oceanography, 24, 253–272.

Lythgoe J.N. (1966) Visual pigments and underwater

vision. In: Light as an Ecological Factor (Eds R. Bain-

bridge, G.C. Evans & O. Rackham), pp. 375–391.

Blackwell Scientific Publications, Oxford.

Maier G. (1989) Variable life cycles in the freshwater

copepod Cyclops vicinus (Uljanin 1875): support for the

predator avoidance hypothesis? Archiv fur Hydrobiolo-

gie, 115, 203–219.

Maier G. (1996) Variable mating durations in cyclopoid

copepods: an adaptation to changing predation risks?

Archiv fur Hydrobiologie, 137, 349–361.

McCauley E. (1984) The estimation of the abundance and

biomass of zooplankton in samples. In: A Manual on

Methods for the Assessment of Secondary Productivity

in Fresh Waters, 2nd edn (Eds J.A. Downing &

F.H. Rigler), pp. 228–265. Blackwell Scientific Publish-

ers, Oxford.

Mills E.L., Confer J.L. & Kretchmer D.W. (1986) Zoo-

plankton selection by young yellow perch: the influ-

ence of light, prey density, and predator size.

Transactions of the American Fisheries Society, 115, 716–

725.

Nilssen J.P. (1977) Cryptic predation and the demo-

graphic strategy of two limnetic cyclopoid copepods.

Memorie dell’Istituto Italiano di Idrobiologia, 34, 187–196.

Nilssen J.P. (1978) On the evolution of life histories of

limnetic cyclopoid copepods. Memorie dell’Istituto Ital-

iano di Idrobiologia, 36, 193–214.

O’Brien W.J. (1987) Planktivory by freshwater fish: thrust

and parry in the pelagial. In: Predation – Direct and

Indirect Impacts on Aquatic Communities (Eds W.C.

Kerfoot & A. Sih), pp. 3–16. University Press of New

England, Hanover, NH.

Olrik K. (1991) Planteplanktonmetoder – prøvetagning, bear-

bejdning og rapportering ved undersøgelser af plante-

plankton i søer og marine omrader. [Phytoplankton

Methods – Sampling, Analyses and Reports When

Analysing Phytoplankton in Lake and Marine Waters].

Environmental Project No. 187. Ministry of the Envi-

ronment, Danish Environment Protection Agency,

Copenhagen, pp. 108. Denmark. (In Danish).

Papinska K. (1988) The effect of fish predation on Cyclops

life cycle. Hydrobiologia, 167 ⁄ 168, 449–453.

Pekcan-Hekim Z. & Horppila J. (2007) Feeding effi-

ciency of white bream at different inorganic turbid-

ities and light climates. Journal of Fish Biology, 70,

474–482.

Pourriot R. (1977) Food and feeding habits in Rotifera.

Archiv fur Hydrobiologie Ergebnisse der Limnologie, 8,

243–260.

Reynolds C.F. (1984) The Ecology of Freshwater Phytoplank-

ton. Cambridge University Press, Cambridge.

Rudstam L.G., Lathrop R.C. & Carpenter S.R. (1993)

The rise and fall of a dominant planktivore: direct

and indirect effects on zooplankton. Ecology, 74, 303–

319.

Santer B. (1994) Influence of food type and concentration

on the development of Eudiaptomus gracilis and the

implications for the interactions between calanoid and

cyclopoid copepods. Archiv fur Hydrobiologie, 131, 141–

159.

Santer B. & van den Bosch F. (1994) Herbivorous

nutrition of Cyclops vicinus: the effect of a pure algal

diet on feeding, development, reproduction and life

cycle. Journal of Plankton Research, 16, 171–195.

SAS Institute Inc. (1990) SAS User’s Guide: Statistics,

Version 8.2. SAS Inst., Inc., Cary, NC.

Sokal R.R. & Rohlf F.J. (1995) Biometry – The Principles and

Practice of Statistics in Biological Research, 3rd edn. W. H.

Freeman and Company, New York.

Sommer U., Gliwicz Z.M., Lambert W. & Duncan A.

(1986) The PEG-model for seasonal succession of

planktonic events in fresh waters. Archiv fur Hydrobi-

ologie, 106, 433–471.

Søndergaard M., Jeppesen E. & Jensen J.P. (2005)

Water Framework Directive: ecological classification

of Danish lakes. Journal of Applied Ecology, 42, 616–

629.



Soto D. & Hurlbert S.H. (1991a) Short term experiments

on calanoid–cyclopoid–phytoplankton interactions.

Hydrobiologia, 215, 83–110.

Soto D. & Hurlbert S.H. (1991b) Long-term experiments

on calanoid–cyclopoid interactions. Ecological Mono-

graphs, 61, 245–265.

Sterner R.W., Elser J.J., Fee E.J., Guildford S.J. & Chrza-

nowski T.H. (1997) The light:nutrient ratio in lakes: the

balance of energy and materials affects ecosystem

structure and process. American Naturalist, 150, 663–684.

Toth L.G., Zankai N.P. & Messner O.M. (1987) Alga

consumption of four dominant planktonic crustaceans

in Lake Balaton (Hungary). Hydrobiologia, 145, 323–332.

Urabe J., Kyle M., Makino W., Yoshida T., Andersen T. &

Elser J.J. (2002) Reduced light increases herbivore

production due to stoichiometric effects of light:nutri-

ent balance. Ecology, 83, 619–627.

Utermohl H. (1958) Zur vervollkommnung der quantitativen

phytoplanktonmethodik. Mitteilungen 9. Internationale

Vereinigung fur Theoretische und Angewandte Lim-

nologie, Stuttgart.

Vadeboncoeur Y., Jeppesen E., Vander Zanden M.J.,

Schierup H.-H., Christoffersen K. & Lodge D. (2003)

From Greenland to green lakes: cultural eutrophication

and the loss of benthic pathways. Limnology & Ocean-

ography, 48, 1408–1418.

Vanni M.J. (1987) Effects of food availability and fish

predation on a zooplankton community. Ecological

Monographs, 57, 61–88.

Vanni M.J. & Findley D.L. (1990) Trophic cascades and

phytoplankton community structure. Ecology, 71, 921–

937.

Ventura M. & Catalan J. (2005) Reproduction as one of

the main causes of temporal variability in the elemen-

tal composition of zooplankton. Limnology and Ocean-

ography, 50, 2043–2056.

Werner E.E. & Hall D.J. (1974) Optimal foraging and the

size selection of prey by the bluegill sun fish (Lepomis

macrochirus). Ecology, 55, 1042–1052.

Zankai N.P. (1984) Predation of Cyclops vicinus (Cope-

poda: Cyclopoida) on small zooplankton animals in

Lake Balaton (Hungary). Archiv fur Hydrobiologie, 99,

360–378.

(Manuscript accepted 15 November 2008)



Documents

The role of light for fish–zooplankton–phytoplankton interactions during winter in shallow lakes–a climate change perspective