Periphyton-macroinvertebrate interactions in light and fish manipulatedenclosures in a clear and a turbid shallow lake

Lone Liboriussen1,2,*, Erik Jeppesen1,2, Mette E. Bramm1 and Majbritt F. Lassen3

1National Environmental Research Institute, Department of Freshwater Ecology, P.O. Box 314, DK8600Silkeborg, Denmark; 2Department of Plant Biology, Institute of Biological Sciences, University of Aarhus,Nordlandsvej 68, DK8240 Risskov, Denmark; 3Department of Marine Ecology, Institute of Biological Sciences,University of Aarhus, Finlandsgade 14, DK8200 Aarhus N, Denmark; *Author for correspondence (e-mail:lol@dmu.dk)

Received 7 July 2003; accepted in revised form 30 June 2004

Key words: Benthic algae, Benthos, Bottom-up, Benthic-pelagic coupling, Grazing, Top-down

Abstract

In a clear and a turbid freshwater lake the biomasses of phytoplankton, periphytic algae and periphytonassoci-ated macrograzers were followed in enclosures with and without fish �Rutilus rutilus� and four light levels �100%,55%, 7% and � 1% of incoming light�, respectively. Fish and light affected the biomass of primary producersand the benthic grazers in both lakes. The biomass of primary producers was generally higher in the turbid thanthe clear lake, and in both lakes fish positively affected the biomass, while shading reduced it. Total biomass ofbenthic grazing invertebrates was higher in the clear than in the turbid lake and the lakes were dominated bysnails and chironomids � ostracods, respectively. While light had no effect on the biomass of grazers in the clearlake, snail breeding was delayed in the most shaded enclosures and presence of fish reduced the number of snailsand the total biomass of grazers. In the turbid lake ostracod abundance was not influenced by light, but washigher in fish-free enclosures. Density of chironomids correlated positively with periphyton biomass in summer,while fish had no effect. Generally, light-mediated regulation of primary producers was stronger in the turbidthan in the clear lake, but the regulation did not unambiguously influence the primary consumers. However,regulation by fish of the benthic grazer community was stronger in the clear than in the turbid lake, and in bothlakes strong top-down effects on periphyton were seen. The results indicate that if present-day climate in Den-mark in the future is found in coastal areas at higher latitudes, the effect of lower light during winter in suchareas will be highest in clear lakes, with typically lower fish biomass and higher invertebrate grazer density.

Introduction

Aquatic communities and food webs are structuredboth by the available resources �bottom-up forces�and by predation �top-down forces� �Carpenter et al.1987; Power 1992; Carpenter and Kitchell 1993;Rosemond et al. 1993�. It is generally recognised thatthe cascading effects of top-down versus bottom-upforces on biomass and community structure will varywith lake nutrient state �Downing et al. 1990�, waterdepth �Jeppesen et al. 1997� and among trophic lev-

els within the food web �McQueen et al. 1986; Pace1993�. However, the relative effects of these structur-ing forces, their interactions, persistence and the con-ditions under which they generally operate, are notfully understood.

In studies of consumer and resource control of mi-croalgal production in freshwater lakes, the pelagiccommunity has by tradition received considerablymore attention than the benthic community �Carpen-ter et al. 1987; Carpenter et al. 2001; Vadeboncoeuret al. 2002�. Yet, the importance of the littoral zone

Aquatic Ecology �2005� 39: 23–39 © Springer 2005

and periphyton for the structure and function of lakecommunities has been emphasised repeatedly �Wetzel1964; Jónasson and Adalsteinsson 1979; Loeb et al.1983; Hecky and Hesslein 1995; Vadeboncoeur et al.2002, Liboriussen and Jeppesen 2003�, and severalstudies have concluded that both benthic and pelagicfood webs may rely strongly on periphyton produc-tion �Burkholder and Wetzel 1989; Wetzel 1990;Vander Zanden and Vadeboncoeur 2002�. Several ex-perimental studies have shown positive effects of nu-trient enrichment on periphytic algal production andthe associated invertebrate herbivores �Cuker 1983;Hill et al. 1992; Rosemond et al. 1993�, others thatfish indirectly stimulate periphytic algae growth byeither removing grazers �Mazumder et al. 1989;Power 1990; Brönmark et al. 1992� or by affectinggrazer foraging activity or life history traits �McCol-lum et al. 1998�. Yet, experiments simultaneously fo-cusing on fish and resource control in streams havefound periphyton communities to be regulated byboth factors, but the degree of resource limitationvaries with predation pressure �Biggs et al. 2000;Flecker et al. 2002�.

Within the context of decades with eutrophication,lake research has focussed on nutrients as the limit-ing resource of aquatic primary production. However,light is the ultimate energy source for primary pro-duction, and the quantity of light reaching submergedsurfaces can be an important factor in structuring theperiphytic algal community, and thus the foodresources available to the benthic grazer community.Thus, the top-down regulation by fish may differalong a latitudinal gradient. How light influences suchinteractions is of importance when evaluating the ef-fects of global warming on lake ecosystems, as com-munities occurring today at a given latitude in theNorth temperature zone presumably will appear athigher latitudes in the future, leaving them exposedto other irradiance conditions than those prevailing atpresent.

We investigate how periphyton and the associatedgrazing macroinvertebrates quantitatively and season-ally respond to long-term experimental manipulationsof light and fish predation in a shallow turbid andclear lake, respectively. Fish, light availability andlake type are expected to effect the relative impor-tance of top-down and bottom-up regulation of theperiphyton community differently. We anticipate thatdespite lower irradiance, access to a larger pelagicnutrient pool results in a higher periphyton produc-tion in the shallow turbid lake if substrates for growth

are available. This higher periphyton production cas-cades to the consumer level resulting in a larger bio-mass of the grazer community. We also expect thethree trophic level ecosystems �fish-invertebrates-pe-riphyton� to have higher periphyton biomass andlower biomass of benthic grazers than the two trophiclevel ecosystems �invertebrates-periphyton�, becausefish indirectly stimulate periphyton growth by remov-ing herbivores and by translocating nutrients to thewater. Higher grazing pressures in the two trophiclevel ecosystems will restrict the ability of periphy-ton to respond to light changes. Thus, periphyton inthe three trophic level systems is expected to respondmore strongly to the light reduction than in the twolevel systems, not least during the low irradianceconditions during winter.

Materials and methods

Study site

Two shallow freshwater lakes, turbid Lake Søbygårdand clear Lake Stigsholm, were chosen as sites for theexperiment. Lake Søbygård is nutrient-rich and hasfor decades remained in a turbid state where emergentand floating-leaved macrophytes have been sparselydeveloped and submerged vegetation totally absent�Jeppesen et al. 1998�. The fish stock is dominated byroach �Rutilus rutilus� and perch �Perca fluviatilis�� � 15 cm� which comprise 61% and 17% of the totalcatch by weight in multi-mesh sized gill nets �CPUE�respectively �Jacobsen et al. 2004�. Lake Stigsholmhas less nutrients than Lake Søbygård. Within the lastdecades the lake has shifted several times between aclear state with substantial submerged vegetation anda turbid state with no vegetation �Søndergaard et al.1997�. Roach �79% of CPUE by weight� and perch�18%� are the most abundant fish species in the lake�Schriver et al. 1995�. Table 1 summarises informa-tion on lake morphology, water chemistry and chlo-rophyll a concentrations for the two lakes.

Experimental design

Irradiance input �in the following termed ‘light’� andplanktivorous fish abundance were manipulated in 24transparent cylindrical PVC enclosures �diameter1.2 m� in each of the two lakes. Each enclosure waskept open to the atmosphere and fixed by analuminium ring penetrating 0.3–0.4-m into the sedi-

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ment, while a hard plastic ring and several rubberbands mounted to poles secured the top above thewater surface. All enclosures were aligned along agangway from which samplings could be conductedwithout major disturbance. The water level within theenclosures varied between 0.8 m and 1.0 m during thecourse of the experiment, thus approximating a totalwater volume of 1000 litres. Prior to the establish-ment of the enclosures all natural vegetation wascarefully removed from the area. All fish were pre-vented from entering the enclosures during construc-tion by filtering the inflowing water through a 1 mmnylon net. The enclosures were established in Octo-ber �2000� and the light intensity was reduced withindays after their establishment, while the first measure-ment of water chemistry and phytoplankton biomasswas conducted within the first week.

A 2�4 factorial stratified random design with threereplicate enclosures per treatment was set up addingplanktivorous fish ��� versus no fish �–� and regulat-ing the light intensity in the enclosure to one of fourlevels; high, medium, low and minimum light, corre-sponding to 100%, 55%, 7% and � 1% of theincoming irradiance, respectively. Light was con-trolled by covering the enclosures with black or greycotton material or a polyethylene net. The coverswere fixed just above the enclosure using poles andextended minimum 0.5 m into the water on all sides.The high light enclosures were covered by thin non-shading nylon nets to prevent bird access. Fish wereadded approximately a week after the enclosure es-tablishment. Seven underyearling �0�� roach werestocked to each enclosure, corresponding to a plank-tivorous fish biomass of approximately 15.5 g WWm–2. Fish were caught from the native population inthe lakes by electrofishing and to secure a high sur-vival rate they were left in a keepnet for at least 10days before stocking. The fish density in the enclo-sures was checked several times during the experi-ment by visual inspection using water binoculars.

New fishes were supplied to the enclosures when re-quired.

Sampling

The cover was removed from the enclosures duringsampling. However, since sampling was only con-ducted fortnightly in winter and monthly in summer,this light exposure was considered unimportant. Pe-riphyton from the enclosure walls was collected at2–4 weeks intervals with a 180 ml chamber covering38 cm2 from 0.05–0.20 cm below the water surface.A moveable brush operated from outside the chamberwas used to scrape off the periphyton. While remov-ing the periphyton, the chamber was fixed to the in-side wall of the enclosure by a large magnet placedon the outside. Before detaching the chamber, a lidwas pushed between the chamber and the wall clos-ing the chamber completely and preventing materialloss during handling. From each enclosure five ran-domly distributed samplings were pooled and ho-mogenised by vigorous shaking before subsamplesfor measurements of periphytic algae biomass weretaken. To account for the systematic overestimationinduced by suspending the periphyton in water fromthe enclosure, we subtracted the water column chlo-rophyll a concentration from the total chlorophyll aconcentration in the chamber.

Benthic macroinvertebrates associated with the en-closure walls were sampled by pressing and pulling asemiclosed plastic funnel vertically up the walls ofthe enclosure collecting periphytic algae and associ-ated invertebrates. The funnel had a 9 cm scrapingdiameter and ended up in a 500 �m mesh where thedetached material was collected. To avoid both dis-turbing the sediment and losing sampled material,scraping started 3-5 cm above the sediment and ex-tended to above the surface. Three randomly chosentransects, altogether covering a surface area from0.21–0.23 m2 �depending on the water level�, werepooled from each enclosure. The pooled sample in-

Table 1. Morphometric characteristics, annual and summer mean �1997–2001� concentrations of pelagic chlorophyll a, total phosphorus �TP�and total nitrogen �TN� for clear Lake Stigsholm and turbid Lake Søbygård.

Area �ha� Maximumdepth �m�

Mean depth�m�

Mean chl a ��g l–1� Mean TP ��g l–1� Mean TN ��g l–1�

annual summer annual summer annual summer

Stigsholm 20.7 1.2 0.8 36 � 10 38 � 15 96 � 29 102 � 39 2.65 � 0.2 1.95 � 0.2Søbygård 38.9 1.9 1.0 112 � 27 126 � 18 275 � 68 421 � 13 1.78 � 0.1 1.52 � 0.1

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cluding periphytic algae and macroinvertebrates wasrinsed on a filter �500 �m� and stored in 96% etha-nol. Macroinvertebrates were isolated from the algalfraction under a dissecting microscope, counted andidentified, where possible, to species level �Dall et al.1995; Fitter and Manual 1995�. Length-weight equa-tions were used to estimate the total macroinverte-brate biomass from body lengths measured using anocular micrometer. For the most abundant species thelength-weight relationship was estimated on at least30 frozen individuals by drying them at 105 °C for 6hours before weighing. Length-weight relationshipsfrom the literature �Smock 1980; Benke et al. 1999�were used for some of the smaller and less abundantspecies. For snails and mussels, shellfree weightswere used in the biomass calculations, whereas esti-mates for other groups covered intact individuals.Only benthic invertebrates feeding at least partiallyon periphytic algae were included in the biomass cal-culations. Left out were leeches, water mites, planar-ians and Hydra sp., which were sometimes presentbut never abundant.

Temperature and water turbidity �Secchi depth�were measured at each sampling event �Oct-Aug�.From October-March, turbidity was additionally de-termined as the water column light attenuation, bylogging the relative irradiance profile at 0.1 m inter-vals vertically through the water column. Relativelight was obtained by simultaneous measurements ontwo PAR sensors, one in the air �Li190SA� and onein the water �Li192SA�. From three replicate lightprofiles, the vertical light attenuation coefficient �Kd�was calculated from the slope of the log-transformedlight measurement. The relative irradiance at 1.0 mwater depth was estimated directly from Kd in winter,whereas Secchi depth transformed by the relation be-tween Secchi depth and Kd established from Octoberto March was used in summer. However, because allminimum light enclosures and many of the plant in-fested high and medium light enclosures were clearin summer, an exact Secchi depth could not be deter-mined. In these clear enclosures, Kd was estimatedfrom the pelagic chlorophyll a concentration usingestablished relationships from other enclosures anddates �Søbygård: r2�0.37, n�238; Stigsholm:r2�0.16, n�234�.

Coverage of submerged vegetation and duckweed�Lemna minor �L.�� was estimated monthly in eachenclosure and assigned to one of five categories: 0%,1–5%, 5–25%, 50–75% and 75–100%. In order tocalculate the percent volume infested �PVI� of the

macrophytes �Canfield et al. 1984�, vegetation heightand water depth were determined for each enclosure.

Analysis

Variable chemical parameters were determined onwater collected from the centre of the enclosures us-ing a core sampler �diameter 7.2 cm� and thus inte-grating the water column except the lower 5 cm.Initial concentrations refer to samples taken a weekafter the enclosures were established, i.e., after a fewdays with shade covers but before introduction offish. Concentrations of total phosphorus �TP� and to-tal nitrogen �TN� were determined monthly accord-ing to Koroleff �1976�. Pelagic and periphytic algaebiomasses were assayed as the concentration of totalextractable chlorophyll a. Water samples and subsam-ples of the periphyton suspension were filtered ontoWhatmann GF/C filters and frozen prior to extraction.Chlorophyll a was determined spectrophotometricallyafter ethanol extraction at room temperature accord-ing to Jepersen and Christoffersen �1987�.

Statistics

Due to damage to some of the enclosures the facto-rial three block design was not complete throughoutthe experiment. In turbid Lake Søbygård, one enclo-sure �medium light with fish� was left out from April,while two enclosures �low light no fish and high lightwith fish� were left out from July. In clear Lake Stig-sholm, one low light no fish enclosure was left outfrom March. Correlations between water turbidity andphytoplankton biomass were analysed by calculatingPearson’s correlation coefficient. Effects of light, fish,date and lake on water chemistry and turbidity, per-iphytic algal biomass, total grazer biomass and abun-dances of different grazer groups were tested usingANOVA with repeated measures �GLM procedure inthe Statistical analysis System, SAS version 8.2� andBonferroni corrections for multiple comparison�Sokal and Rohlf 1995�. When significant effectswere identified multiple comparison �Tukey’s HSDtest� was used to elucidate the differences �Sokal andRohlf 1995�. To meet assumptions of a normal distri-bution and to assure homogeneity of variances, datawere transformed by log10, log10�x�1� or arcsinewhen necessary.

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Results

Pelagic parameters

Initially, significantly higher TP concentration�ANOVA; p � 0.001 �n�48�� and lower TN concen-trations �ANOVA; p � 0.001 �n�48�� were found inthe turbid Lake Søbygård �0.170 � 0.043 mg TP l–1;0.93 � 0.26 mg TN l–1� than in the clear Lake Stigs-holm �0.075 � 0.016 mg TP l–1; 1.39 � 0.21 mgTN l–1�. Yet, throughout the rest of the experiment thenutrient concentrations did not differ between the twolakes. Light significantly affected both the TP and TNconcentrations in the lakes �Table 2� and low andminimum light enclosures generally had higher nutri-ent concentrations than the high and medium lightenclosures �Figure 1�. Fish had no overall effect onthe pelagic nutrient concentrations �Table 2�, but inthe clear lake the TP concentration was significantlyhigher in enclosures with fish than in those withoutfish �ANOVA; fish: p � 0.001 �n�261��.

The pelagic chlorophyll a concentration �in thefollowing termed phytoplankton biomass� was ini-tially higher in the turbid lake �range: 28–96 �g l–1�than in the clear lake �range: 8–51 �g l–1� �ANOVA;p � 0.001 �n�48�� and this inter-lake differenceremained significant throughout the experiment.Shading significantly reduced the phytoplankton bio-mass and this was evident already at the initial sam-pling 6 days after the enclosures were covered �Figure1�. The phytoplankton biomass was significantlyhigher in the enclosures with fish than in the fish-freeenclosures, but no interactions were of significance�Table 2�. Distinct seasonal patterns in phytoplanktonbiomass were seen in the two lakes. In the clear lakephytoplankton biomass peaked from late January toApril at high and medium light, and the biomass wasgenerally higher in winter-spring than in summer. By

contrast, the turbid lake had the highest phytoplank-ton concentrations from late January to August at highand medium light �Figure 1�. Water turbidity in termsof both Kd �October-March� and Secchi depth �Octo-ber-August� correlated to chlorophyll a �Kd: Pearson;r�0.52 p � 0.001, �n�480�; Secchi: Pearson; r�0.50p � 0.001, �n�493��. Lake Søbygård was signifi-cantly more turbid than Lake Stigsholm and turbiditywas highest in the presence of fish �Table 2�. Turbid-ity did, however, not differ significantly betweenthe two lakes during winter �October to March��p�0.266�. Water temperature varied little betweenthe lakes, and during the coldest period �January toMarch� both lakes were frequently covered with ice�Figure 1�. Mean maximum daily irradiance in thearea ranged from 132 �mol PAR m–2 s–1 in Decem-ber to 1317 �mol PAR m–2 s–1 in July �Figure 2�.

Periphytic algal biomass

Light, fish and season significantly affected theperiphytic algal biomass on the enclosure walls inboth lakes �Table 3�, and seasonal variation was largeramong light treatments within the lakes than betweenthe lakes at similar light treatments. The periphyticalgal biomass increased from the first to the secondsampling and the accumulation rate increased withlight availability �Figure 3�. At high light, the peri-phytic algal biomass was higher in winter �NovemberJanuary� and midsummer �June-August� than in latewinter and spring �late January-May�. Medium lightconditions, however, had a less distinct seasonal pat-tern, which furthermore differed between the lakes. Inwinter and spring, a relatively constant periphytonbiomass was seen in the clear lake, while a unimodalrelationship was found in the turbid lake. In earlysummer, the periphyton biomass declined in bothlakes and high accumulation rates subsequently fol-

Table 2. Summary of ANOVA tests analysing if total phosphorus �TP�, total nitrogen �TN� and phytoplankton biomass �Chl a� in 24 enclo-sures in clear Lake Stigsholm and turbid Lake Søbygård were affected by fish and light �October-April�. The 24 enclosures in each lake wereeither with fish or without fish and exposed to one of four light levels �high, medium, low or minimum light�. Due to repeated measurementsBonferroni correction was applied. *p � 0.05, **p � 0.01, ***p � 0.001, ns � non significant. �TP and TN: n�11; Chl a: n�16�.

Date Fish Light Fish*Date Light*Date Light*Fish Light*Fish*Date

TP Søbygård *** ns *** * * *** nsStigsholm *** *** *** ns *** ** ns

TN Søbygård *** ns *** ns *** *** nsStigsholm *** ns *** ns ns ns ns

Chl a Søbygård *** *** *** ** *** ns nsStigsholm *** *** *** *** *** ns ns

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lowed before a maximum biomass was attained inJuly-August �Figure 3�. Low light treatments had lowand constant periphyton densities in winter, but fromMarch to August a relatively constant biomass accu-mulation was observed. Periphytic algal biomass didnot vary according to season at the minimum lightconditions. The temporal variation in periphyton bio-mass at high light corresponds inversely with changesin the phytoplankton biomass, however in May in theclear lake both communities occurred at low densi-ties �Figure 1, Figure 3�. Lower light treatments didnot have such an inverse relationship. At high light

and in the presence of fish the turbid lake supportedhigher biomass of periphytic algae than did the clearlake �p�0.042, n�68� �Figure 4�. Mean periphytonalgal biomass from October to August did not differbetween the high and medium light treatments, but atmore shaded treatments the biomass decreased withthe light availability �Figure 4�. Irrespective of sea-son, periphytic algal biomass correlated positivelywith the total sum of light received during the 2-weekperiod before sampling, and this relationship did notdiffer between the lakes �Figure 5�.

Figure 1. Seasonal variation in total nitrogen �TN�, total phosphorus �TP�, water temperature �°C� and pelagic chlorophyll a concentrations�mean � SE� within light and fish manipulated enclosures located in clear Lake Stigsholm and turbid Lake Søbygård. Concentrations fromhigh light �H� enclosures were pooled with those of medium light �M� enclosures �open symbols�, while concentrations from low light �L�and minimum light �O� enclosures were pooled �closed symbols�. Fish �0� roach� were either present in �� fish; solid line� or absent from�– fish; dotted line� the enclosures �n�4–6�.

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Fish had a significant effect on the periphytic algalbiomass �Table 3� and less periphyton was generallyfound in fish-free enclosures relative to that in enclo-sures with fish. Yet, at medium light treatments in theturbid lake and at high light treatments in the clearlake fish did not significantly affect the biomass. Therelative effect of fish on the periphytic algal biomassdid not differ significantly between the lakes, but thedifference decreased with increasing light conditionsand thus with increasing periphytic algal biomass�ANOVA; light: p � 0.001; fish: p�0.251, light*fish:p�0.214, n�96� �Figure 6�.

Macroinvertebrate communities

Total mean biomass of periphyton feeding macroin-vertebrates �grazers� associated with the enclosurewalls was higher and included more species in theclear lake than in the turbid lake. Lower biomasseswere generally found in winter than in summer, and

accumulation of grazer biomass commenced inMarch-April in the clear lake and in June in the tur-bid lake �Figure 7�. In the clear lake, most light treat-ments attained a constant grazer biomass from Mayto August and light had no overall effect on the grazerbiomass, while fish significantly lowered it �Table 3�.In the turbid lake, light and fish significantly affectedthe grazer biomass; increased light generally stimu-lated the biomass while the presence of fish reducedit. Yet, because of significant interactions betweenlight, fish and date it is difficult to draw general con-clusions as to the overall relation between the treat-ments and biomass of grazing invertebrates �Table 3�.The grazer communities in the clear lake, both innumber and biomass, were dominated by Asellusaquaticus and several species of snails �mainly Lym-nea peregra, Physa fontinalis, Valvata sp. andBithynia sp.�. Snails accounted for almost 90% of to-tal invertebrate biomass in the clear lake, whereasoligochaetes, chironomids, ostracods etc. were of mi-

Figure 2. Maximum daily irradiance during the experimental period registered approximately 30 and 55 km from Lake Søbygård and LakeStigsholm, respectively. �Source: The Danish Institute of Agricultural Sciences, Denmark�.

Table 3. Summary of ANOVA tests analysing if periphytic algal biomass �mg chl a m–2� and the invertebrate biomass �mg DW m–2� asso-ciated to enclosure walls in clear Lake Stigsholm and turbid Lake Søbygård were affected by the presence versus absence of planktivorousfish, the available light conditions and the sampling date. The 24 enclosures in each lake were either with planktivorous fish or without fishand exposed to one of four light levels �high, medium, low or minimum light�. Due to repeated measurements Bonferroni correction wasapplied. *p � 0.05, **p � 0.01, ***p � 0.001, ns � non significant.

Lake n Date Fish Light Date*Fish Date*Light Fish*Light Date*Fish* Light

Periphytic algal biomassStigsholm �clear� 284 *** *** *** ns *** ns nsSøbygård �turbid� 274 *** *** *** ns *** *** ns

Invertebrate biomassStigsholm �clear� 166 *** *** ns ns ns ns nsSøbygård �turbid� 160 *** *** ** * * * *

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nor importance. During winter, P. fontinalis and largeindividuals of L. peregra dominated the snailcommunity, and low densities ranging from 0 � 0 to14 � 10 individuals per m–2 were observed at alllight and fish treatments �Table 4�. In April Bithyniasp. and Valvata sp. started to emerge and the total sumof snails increased in the enclosures �Table 4�. Themaximum snail density was observed in the high lightfish-free enclosures in June, small-sized species be-ing dominant �Table 5�. Small snails were particularlyabundant in June where 50% of the snails had a shellheight lower than 2.1 mm, whereas the equivalentsize in January-March was 7.0–7.1 mm �Table 5�.Snail size differed significantly among light treat-ments at most sampling dates, but the effect differedbetween winter and summer �Table 5�. The largest

snails were generally found at the highest light levelsin winter and at the lowest light levels in summer.Fish, however, only had a significant effect on snailsize in March when larger snails were found in thefish-free enclosures than in the enclosures with fish�Table 5�.

Ostracods dominated the grazer community in theturbid lake during winter, while chironomid larvaewere most abundant in June-August. Significantlyhigher abundances of ostracods were found in thefish-free enclosures than in those with fish, while lighthad no effect on the ostracod abundance �Table 6��ANOVA; light: p�0.160, fish: p � 0.001, light*fish:p�0.039 �n�168��. During the major part of the ex-periment, the minimum light fish-free enclosurescontained many ostracods, but the highest densities

Figure 3. Seasonal variation in periphytic algal biomass �mean � SE� in enclosures located in clear Lake Stigsholm and turbid Lake Søbygårdand exposed to one of four light treatments �high, medium, low and minimum light levels� and either fishfree �– fish� or stocked with plank-tivorous fish �� fish�. Periphyton was sampled 0.05–0.20 cm below the surface �n�2–3�.

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were observed in the high light enclosures in March� � 1400 individuals per m–2�. In the turbid lake chi-ronomid larvae were found in very low densities dur-ing winter and spring �Table 7�. However, in June andAugust they became abundant mainly in the high andmedium light enclosures �Table 7�. In June-August,light had a significant stimulated effect on their abun-dance, while fish had no overall effect �ANOVA;light: p � 0.025, fish: p�0.234, light*fish: p�0.140�n�36��. The high abundances of chironomids inJune and August were strongly correlated to theperiphytic algal biomass on the enclosure walls�Pearson; r�0.70 p � 0.001, �n�36��.

Macrophytes

Most of the high light and medium light enclosuresin the clear lake became massively infested by mac-rophytes �Elodea canadensis, Potamogeton crispus�in summer �Figure 8�, whereas only few macrophytesoccurred at low and minimum light conditions or inany of the enclosures in the turbid lake. Duckweed�Lemna minor�, however, occasionally developed in

the low light enclosures and at higher light levels.Ultimately it covered the entire water surface in someof the enclosures in the clear lake, while it was onlyfound in three enclosures in the turbid lake �Figure8�.

Discussion

Fish and light availability affected the biomass of pe-riphyton and the associated benthic macroinvertebrategrazers in both the turbid and the clear lake. A reduc-tion of light reduced the biomass of pelagic and peri-phytic primary producers substantially, but thisreduction had no overall effect on the biomass ofbenthic macroinvertebrate grazers. Further the pres-ence of fish had directly or indirectly a positive effecton the periphyton biomass in both lakes, although fishonly significantly reduced the total biomass of thebenthic grazer community in the clear lake.

Whereas a light reduction to 7% and � 1% of theincident irradiance strongly reduced the periphytic al-gal biomass throughout the experiment, a 45% light

Figure 4. Mean � � SE� biomass of periphytic algae �November-August� and phytoplankton �October-August� from light �high, medium,low and minimum light levels� and fish �� fish and fish� manipulated enclosures in clear Lake Stigsholm and turbid Lake Søbygård.

31

reduction only affected the biomass in winter�November–January� when irradiance was low. Stron-ger light control in winter than in summer was alsoindicated by the seasonality of microalgal communi-ties in the low light enclosures in which algal biomassaccumulation was low until March, when incomingirradiance started to increase substantially. A seasonalchange in the relative importance of light inconstraining the periphyton biomass was also re-ported by Rosemond et al. �2000�, who found lightconstraints of stream periphyton in summer and fall,but not in spring. Like in our study, they observed theproportionally greatest reduction of periphyton bio-mass in light reduction experiments when ambientlight attained its lowest levels.

The community structure of macroinvertebrategrazers differed substantially between the two lakes.Irrespective of fish densities, snails completely domi-nated the biomass in the clear lake, and chironomidsand ostracods dominated in the turbid lake. Lowerbiomass of plankti-benthivorous fish, higher benthic

primary production �Liboriussen and Jeppesen 2003�and a generally higher habitat diversity due to the oc-casional occurrence of high densities of macrophytes�Søndergaard et al. 1997� may explain the higherabundance of snails in the experiment in the clear lakerelative to the turbid lake, where submerged plantswere absent and the fish density high �Jeppesen et al.1998�.

In the experiment in the clear lake, light had nooverall effect on the total biomass of benthic macro-invertebrate grazers though it tended to increase withirradiance in winter. However, it apparently affectedthe timing of reproduction and hence the size distri-bution of the snail community in summer. Snailsstarted breeding earlier in the high and medium lightenclosures than in the more shaded enclosures. In theformer, snail reproduction and abundance peaked inJune, while the density at lower light conditions in-creased more slowly from April to August. Snailsmay respond to low food availability by increasingtheir foraging effort �James et al. 2000�, often at theexpense of growth or fecundity. Accordingly, im-proved food conditions resulted in increased growthrates and higher number of breeding bouts both for L.peregra populations from different locations �Lamand Calow 1989� and for P. fontinalis kept at differ-ent nutrient levels �Jones et al. 1999�. The large dif-ference in average snail size also reflects a reductionin the number of adults. In an enclosure experimentVermaat �1994� observed that a considerable fractionof adult B. tentaculata and V. piscinalis returned tothe sediment after oviposition on macrophytes andenclosure walls in late spring. Moreover, high mor-tality of adult L. peregra after spring oviposition isgenerally reported �Dussart 1979�. Variation in thereproductive timing of snail communities at differentlight conditions may therefore explain why moreadult snails were found later in the season at low thanhigh irradiance. Although such food-mediated differ-ences in snail life history traits may at least partly ex-plain the lack of light-mediated control of the totalgrazer biomass in the clear lake, other mechanismsand conditions may be important as well. Many snailspecies are found to be active both on enclosurewalls, vegetation surfaces and in the sediment, andtheir abundance and distribution within and amonghabitats may change with season �Vermaat 1994�.Accordingly, relating benthic grazer communitiesfrom the entire enclosure wall with periphyton densi-ties only in the upper part of the wall may have af-fected the results on the grazer-periphyton interac-

Figure 5. Relationship between the total sum of light 2 weeks priorto sampling and mean periphytic algal biomass on the enclosurewalls in clear Lake Stigsholm and turbid Lake Søbygård. Lines de-note significant relationships: Lake Stigsholm; log y � 0.016 �0.483 log x, r2 � 0.73, p � 0.001, Lake Søbygård; log y � 0.105� 0.534 log x, r2 � 0.75, p � 0.001, �n�96�. Test of; same slopes:p � 0.308, same intercept: p � 0.735.

32

tions. Furthermore, the development of high densitiesof macrophytes in the high and medium light enclo-sures in June-August provided extra surfaces onwhich the benthic grazers could dwell, forage andhide from predators. It is therefore likely that totalgrazer biomass in the macrophyte-colonised enclo-sures is underestimated relative to those withoutmacrophytes. The strong positive correlation betweenlight availability, periphytic algal biomass and an ex-cessive and early snail reproduction suggests that al-though we found no overall effect of light on the totalbiomass of grazers, resource limitation may affect thestructure and life history of the grazer community.

The presence of fish strongly reduced the total bio-mass of benthic macroinvertebrate grazers andincreased periphytic algal biomass, while it had littleeffect on the size distribution of the snail communi-ties. Likewise, Brönmark et al. �1992� found a higherbiomass of periphytic algae in enclosures with natu-ral densities of pumpkinseed sunfish �Lepomis gibbo-sus� relative to fish-free control enclosures, becausethe snail biomass was significantly reduced in enclo-sures with sunfish. An equivalent top-down regulationfrom roach to periphytic algae may operate in our en-closures and hence control the overall fish-inverte-brate-periphyton interactions. McCollum et al. �1998�showed that although fish had only visual and olfac-

tory contact with snails, their presence either inhib-ited snail reproduction or increased the mortality ofsmall snails so that twice as many snails were pro-duced in the absence of fish. Whether fish in our studycontrolled benthic grazers directly by predation or in-directly by inducing a shift in habitat is debatable.The 0� roach added to the enclosures in October hadan average length of approximately 5 cm, and assum-ing a growth rate of 0.45 �Cryer et al. 1986� theywould be approximately 6.8 cm by June in enclosuresof fair food availability. Roach of this size have beenfound to include large proportions of benthic inverte-brates in their diet �Persson and Hansson 1999� andpredation on small, newly hatched snails couldaccordingly be expected. However, because fish didnot significantly change the size distribution of thesnail communities after hatching of a new generation,it seems plausible that fish did not reduce the snailpopulation by direct consumption. Nevertheless, ourresults suggest indirect effects, because snails weretypically more numerous in fish-free enclosuresalready in April, when Valvata sp. and Bithynia sp.started to emerge from the sediment and before snailbreeding and protective macrophyte beds wereobserved. Direct consumption of these hard-shelledand relatively large individuals �mean size in April:Valvata sp. 3.7 mm and Bithynia sp. 7.5 mm� by our

Figure 6. Relative response of the periphytic algal biomass to the addition of fish at high, medium, low and minimum light conditions inclear Lake Stigsholm and turbid Lake Søbygård. The line through the middle of the box shows the median, and the dots show the mean ofthe distribution. The outer edges of the box correspond to the 25th and 75th percentiles, and the whiskers to the 10th and 90th percentile.

33

size class of roach is not plausible. Fish cues mayhave encouraged the snails to remain in the sedimentor induced a preference for vegetation rather than the

exposed surfaces on the enclosure walls, the latter,however, only being possible in the high and mediumlight enclosures.

Figure 7. Seasonal variation in the biomass of periphyton associated macroinvertebrates �mean � SE� in light and fish manipulated enclo-sures in clear Lake Stigsholm and turbid Lake Søbygård. The enclosures were exposed to one of four light treatments �high, medium, lowand minimum light� and were either fish-free �– fish� or stocked with planktivorous fish �� fish�.

Table 4. Mean � � SE� number of snails �individuals per m–2� associated to the inner walls of light and fish manipulated enclosures in clearLake Stigsholm from January to August. The enclosures were exposed to one of the four light levels: high, medium, low or minimum light,and either contained planktivorous fish ��� or were without fish �-� �n � 2–3�.

Light Fish Jan Feb Mar Apr May Jun Aug

High � 9 � 9 11 � 6 13 � 13 9 � 5 25 � 14 255 � 121 37 � 16– 6 � 3 8 � 4 10 � 5 39 � 8 59 � 15 788 � 289 296 � 155

Medium � 9 � 5 2 � 2 14 � 10 40 � 20 36 � 16 607 � 149 80 � 36– 9 � 4 5 � 5 8 � 4 46 � 35 35 � 16 311 � 90 81 � 42

Low � 0 � 0 2 � 2 5 � 4 9 � 4 51 � 18 224 � 84 40 � 26– 7 � 1 3 � 3 5 � 3 34 � 4 94 � 26 189 � 96 235 � 47

Minimum � 0 � 0 0 � 0 0 � 0 6 � 1 24 � 7 25 � 13 9 � 3– 9 � 4 11 � 11 2 � 2 22 � 9 94 � 39 136 � 46 142 � 61

34

In the turbid lake, ostracods were more abundantthan chironomids from January to May, and in con-trast to the latter their abundance was significantlylower in enclosures with fish. Yet, our data do notclarify if fish reduced the ostracods by consumptionor if the risk of predation by fish induced a habitatdisplacement to the sediment, as described by Uibleinet al. �1996� or, less likely, that densities by changewere lower at the start of the experiment in the fish-

free enclosures. Higher densities of ostracods in thefish-free enclosure and thus higher grazing on the pe-riphyton might explain the lower periphyton densitiesgenerally seen in these enclosures. Ostracod abun-dance was not affected by light, but at low and mini-mum light the densities appeared to be more constantand the reproductive output lower than at high andmedium light. Low chironomid larvae densities dur-ing autumn-spring may reflect a low pool of potential

Table 5. Seasonal changes in snail shell height �mm� and a summary of ANOVA tests analysing if the shell height was affected by light andfish manipulation of enclosures in clear Lake Stigsholm. The 24 enclosures were either with fish ��� or without fish �-� and exposed to oneof four light levels �high �H�, medium �M�, low �L� or minimum �0� light�. Significant treatment effects are summarised in parentheses belowthe test result. Due to repeated measurements Bonferroni correction was applied. * p � 0.05, ** p � 0.01, *** p � 0.001, ns � non signifi-cant.

Jan Feb Mar Apr May Jun Aug

Summary snail shell heightMean 7.9 8.1 8.0 6.0 5.8 2.7 4.2Median 7.0 7.0 7.1 5.0 4.9 2.1 3.0Range 2.0-20.1 2.0-15.0 2.0-18.9 1.0-30.5 1.2-17.1 0.5-22.0 0.6-20.9n 39 26 34 170 217 1429 558

ANOVALight * ns * ** ns *** ***

�H � MLO� �H � MLO� �HM � LO� �O � HML� �OL � HM�Fish ns ns * ns ns ns ns

�- � ��Light*Fish ns ns ns ns ns ns ns

Table 6. Mean � � SE� number of ostracods �individuals per m–2� associated to the inner walls of light and fish manipulated enclosures inturbid Lake Søbygård from January to August. The enclosures were exposed to one of the four light levels: high, medium, low or minimumlight, and either contained planktovorous fish ��� or were without fish �-� �n�2-3�.

Light Fish Jan Feb Mar Apr May Jun Aug

High � 3 � 1 2 � 2 2 � 2 4 � 3 0 � 0 24 � 9 124 � 94– 13 � 11 33 � 19 797 � 420 12 � 6 2 � 2 0 � 0 69 � 56

Medium � 1 � 1 3 � 3 5 � 4 0 � 0 2 � 2 0 � 0 24 � 20– 34 � 17 102 � 11 8 � 3 39 � 18 11 � 3 2 � 2 529 � 428

Low � 0 � 0 0 � 0 0 � 0 18 � 16 5 � 5 43 � 43 4 � 4– 0 � 0 27 � 11 3 � 3 7 � 1 2 � 2 2 � 2 2 � 2

Minimum � 0 � 0 2 � 2 0 � 0 1 � 1 0 � 0 1 � 1 10 � 10– 68 � 28 6 � 3 16 � 3 98 � 51 79 � 43 9 � 9 6 � 4

Table 7. Mean � � SE� number of chironomid larvae �individuals per m–2� associated to the inner walls of light and fish manipulated en-closures in turbid Lake Søbygård from January to August. Data for the fish ��� and the fish-free �-� treatments were pooled for the high light�H� and medium light �M� enclosures and for the low light �L� and minimum light �O� enclosures �n � 5-6�.

Light Fish Jan Feb Mar Apr May Jun Aug

High � Medium � 3 � 1 2 � 2 2 � 1 4 � 1 8 � 1 309 � 217 633 � 340– 5 � 4 1 � 1 0 � 0 4 � 2 2 � 2 147 � 60 519 � 207

Low � Minimum � 4 � 3 0 � 0 2 � 1 1 � 1 6 � 4 143 � 93 37 � 13– 1 � 1 0 � 0 1 � 1 1 � 1 1 � 1 2 � 2 28 � 15

35

colonists at the start of the experiment determined byhigh fish predation in the lake where the experimentwas run rather than unfavourable food and habitatconditions in the enclosures. Yet, the positive corre-lation between chironomid density and the periphyticalgal biomass in June-August following the appear-ance of the new generation suggests that periphytonis an important resource for the chironomids,presumably both as a habitat and as a food source.However, the positive correlation even in enclosureswithout fish implies that the chironomid larvae didnot exert a strong top-down control on the biomassof the periphyton mat they inhabited. This is in ac-cordance with Forrester et al. �1999�, who found thatalthough fish directly consumed chironomids, higherdensities occurred in enclosures with fish than infishless enclosures, because fish simultaneously stim-ulated periphyton growth. Low vulnerability to fishpredation because of their embedment in the periphy-ton mat �Biggs et al. 2000� and predation by inverte-brate predators on chironomids �Diehl 1992� haveadditionally been suggested as explanations of thelack of fish-mediated regulation of chironomids. Top-down regulation of chironomids by fish has, however,been reported in other studies �Mazumder et al. 1989;Williams et al. 2002� and is plausible also in fieldstudies.

Because of the basic structural inter-lake differencein the composition and total biomass of the grazercommunities among the two lakes, regulation of pe-

riphyton and the general fish-grazer-periphyton inter-actions differed as well. Under shaded conditions therelative effect of fish on the periphytic algal biomasswas higher in the clear lake than in the turbid lake.This interlake difference is most likely due to theconsistently higher grazer biomass in the clear lake,which allows fish to have a higher impact on thegrazer community and thus induces a larger fish-me-diated stimulation of periphyton. In addition, grazerbody size might be of importance. In an empiricalanalysis of the removal rate of periphyton by grazers,Cattaneo and Mousseau �1995� found grazer bodysize to be the main controlling factor, whereas thetaxon of the grazer and the algal composition of theperiphyton were of comparatively minor importance.Likewise, a comparative study of four of the snailspecies found in the clear lake �L. peregra, P.fontinalis, V. piscinalis and B. tentaculata� revealedthat most of the variation in periphyton removalamong species could be explained by snail size �Ver-maat and Hootsmans 1994; Brönmark and Vermaat1997�. The combination of dominance of the largerindividuals and the higher biomass of benthic grazersin the clear lake may therefore explain the higher re-duction of periphyton biomass here than in the turbidlake dominated by small individuals and with low to-tal biomass. Yet, light mediated differences in foodquality may also influence the grazing pressure andhence the periphyton biomass, since benthic macro-grazers may feed selectively on high-energy food

Figure 8. Percentage of total enclosure volume infested by macrophytes �PVI� and of total enclosure surface covered by Lemna minor inJune-August at high, medium, low and minimum light exposed enclosures in clear Lake Stigsholm �mean � SE� �n�5–6�.

36

�Cruz-Rivera and Hay 2000�. Unfortunately, we haveno information on the periphyton composition to elu-cidate the role of food quality in our experiment.

Our results may be of importance for the currentdebate on the effects of changes in climate on lakeecosystems �Straile and Adrian 2000�. Global warm-ing models predict that the winter temperature inNorthern Europe may increase by 2.5–4.5°C duringthe next century �IPCC 1996�. Higher temperatureswill accordingly occur at latitudes with lower ambi-ent irradiance than that at latitudes where these tem-peratures are found today. Our results indicate that inshallow lakes these differences in light intensity willnot only impact periphyton biomass during winter butalso the relative impact of fish on periphyton, beingproportionally higher at low light intensity.

Conclusions

The light-mediated bottom-up regulation of primaryproducers was generally stronger in the turbid than inthe clear lake, but the light regulation was not unam-biguously reflected at the primary consumer level.Top-down regulation of the benthic grazer commu-nity was stronger in the clear lake than in the turbidlake, and in both lakes strong effects on periphytonwere seen. Both light-mediated bottom-up and fish-mediated top-down forces affected the biomass of pe-riphyton in our experiment, while the reductiveimpact of the two factors on the benthic grazer com-munity was highly dependent on the structural com-position of the community. Our results indicate that ifthe present-day climate in Denmark in the future willbe found at higher latitudes �e.g., coastal lakes inNorway�, the effect of lower light during winter inthese areas will be strongest in clear shallow lakes,with typically lower fish biomass and higher inverte-brate grazer density.

Acknowledgements

We greatly appreciate assistance with identification ofinvertebrates by Marie Koenig. This study was sup-ported by the Danish Research Agency, the DanishNatural Science Research Council �grant 9901385�,the Danish research programme ‘The role of fish inecosystems 1999–2001’ funded by the Ministry ofAgriculture, Fisheries and Food and the researchproject’ �Consequences of weather and climate

changes for marine and freshwater ecosystems. Weacknowledge The Danish Institute of AgriculturalSciences in Foulum, Denmark, for kindly providingus the data on daily irradiance. Thanks to Anne MettePoulsen for linguistic improvements.

References

Benke A.C., Huryn A.D., Smock L.A. and Wallace J.B. 1999.Length-mass relationships for freshwater macroinvertebrates inNorth America with particular reference to the southeasternUnited States. Journal of the North American Benthological So-ciety 18�3�: 308–343.

Biggs B.J.F., Francoeur S.N., Huryn A.D., Young R., Arbuckle C.J.and Townsend C.R. 2000. Trophic cascades in streams: effectsof nutrient enrichment on autotrophic and consumer benthiccommunities under two different fish predation regimes. Cana-dian Journal of Fisheries and Aquatic Sciences 67�7�: 1380–1394.

Brönmark C. and Vermaat J.E. 1997. Complex fish-snail-epiphy-ton interactions and their effects on submerged freshwater mac-rophytes.. In: Jeppesen E., Søndergaard M., Søndergaard M. andChristoffersen K. �eds�, The Structuring Role of SubmergedMacrophytes in Lakes. Springer-Verlag Inc., New York, USA.

Brönmark C., Klosiewski S.P. and Roy A.S. 1992. Indirect effectsof predation in a freshwater benthic food chain. Ecology 73:1662–1674.

Burkholder J.M. and Wetzel R.G. 1989. Epiphytic microalgae onnatural substrata in a hardwater lake: Seasonal dynamics ofcommunity structure, biomass and ATP content. Archiv für Hy-drobiologie, Suppl. 83: 1–56.

Canfield D.E., Shireman J.V., Colle D.E., Haller W.T., WatkinsC.E. and Maceina M.J. 1984. Prediction of chlorophyll a con-centrations in Florida lakes: Importance of aquatic macrophytes.Canadian Journal of Fisheries and Aquatic Sciences 41:497–501.

Carpenter S.R., Kitchell J.F., Hodgson J.R., Cochran P.A., ElserJ.J., Elser M.M., Lodge D.M., Kretchmer D., He X. and VonendeC.N. 1987. Regulation of lake primary productivity by food webstructure. Ecology 68�6�: 1863–1876.

Carpenter S.R., Cole J.J., Hodgson J.R., Kitchell J.F., Pace M.L.,Blade D., Cottingham K.L., Essington T.E., Houser J.N. andSchlindler D.E. 2001. Trophic cascades, nutrients, and lake pro-ductivity: whole-lake experiments. Ecological Monographs71�2�: 163–186.

Cattaneo A. and Mousseau B. 1995. Empirical analysis of the re-moval rate of periphyton by grazers. Oecologia 103: 249–254.

Cruz-Rivera E. and Hay M.E. 2000. Can quantity replace quality?Food choice, compensatory feeding, and fitness of marine me-sograzers. Ecology 81�1�: 201–219.

Cryer M., Peirson G. and Townsend C.R. 1986. Reciprocal inter-actions between roach, Rutilus rutilus, and zooplankton in asmall lake: Prey dynamics and fish growth and recruitment.Limnology and Oceanography 31�5�: 1022–1038.

Cuker B.E. 1983. Competition and coexistence among the grazingsnail Lymnaea, chironomidae, and microcrustacea in an arcticepilithic lacustrine community. Ecology 64�1�: 10–15.

37

Dall P.C., Iversen T.M., Kirkegaard J., Kristensen S., LindegaardC. and Thorup J. 1995. En oversigt over danske ferskvandsin-vertebrater til brug ved bedømmelse at forurening i søer ogvandløb. Ferskvandsbiologisk Laboratorium, Helsingørgade 51,DK-3400 Hillerød.

Diehl S. 1992. Fish predation and benthic community structure -the role of omnivory and habitat complexity. Ecology 73 �5�:1646–1661.

Downing J.A., Plante C. and Lalonde S. 1990. Fish productioncorrelated with primary productivity, not the morphoedaphic in-dex. Canadian Journal of Fisheries and Aquatic Sciences 47:1929–1936.

Dussart G.B.J. 1979. Life cycles and distribution of the aquaticgastropod molluscs Bithynia tentaculata �L�, Gyraulusalbus�Muller�, Planorbis planorbis �L� and Lymnaea peregra �Muller�in relation to water chemistry. Hydrobiologia 67 �3�: 223–239.

Fitter R. and Manual R. 1995. Lakes, Rivers, Streams and Pondsof Britain and North-West Europe. Harper Collins Publishers,London, UK.

Flecker A.S., Taylor B.W., Bernhardt E.S., Hood J.M., CornwellW.K., Cassatt S.R., Vanni M.J. and Altman N.S. 2002. Interac-tions between herbivorous fishes and limiting nutrients in atropical stream ecosystem. Ecology 83�7�: 1831–1844.

Forrester G.E., Dudley T.L. and Grimm N.B. 1999. Trophic inter-actions in open systems: Effects of predators and nutrients onstream food chains. Limnology and Oceanography 44�5�: 1187–1197.

Hecky R.E. and Hesslein R.H. 1995. Contribution of benthic algaeto lake food webs as revealed by stable isotope analysis. Journalof the North American Benthological Society 14�4�: 631–653.

Hill W.R., Boston H.L. and Steinman A.D. 1992. Grazers and nu-trients simultaneously limits lotic primary productivity. Cana-dian Journal of Fisheries and Aquatic Sciences 49: 504–512.

IPCC 1996. Climate Change 1995. The science of climate change:contribution of WGI to the second assessment report of the In-tergovernmental Panel on Climate Change. Houghton J.T., MeiroFilho L.G., Callender B.A., Harris N., Kattenberg A. andMaskell K. �eds.� Cambridge University Press, UK, p. 572.

Jacobsen L., Berg S., Jepsen N. and Skov C. 2004. Does roach be-haviour differ between lakes of different environmental state?Journal of Fish Biology 65�1�: 135–147.

James M.R., Hawes I. and Weatherhead M. 2000. Removal ofsettled sediments and periphyton from macrophytes by grazinginvertegbrates in the littoral zone of a large oligotrophic lake.Freshwater Biology 44�2�: 311–326.

Jeppesen E., Søndergaard M., Jensen J.P., Kanstrup E. and PetersenB. 1997. Macrophytes and turbidity in brackish lakes with spe-cial emphasis on the role of top-down control. In: Jeppesen E.,Søndergaard M., Søndergaard M. and Christoffersen K. �eds�,The Structuring Role of Submerged Macrophytes in Lakes.Springer-Verlag Inc., New York, USA, pp. 369–377.

Jeppesen E., Søndergaard M., Jensen J.P., Mortensen E., HansenA.M. and Jørgensen T. 1998. Cascading trophic interactionsfrom fish to bacteria and nutrients after reduces sewage loading:An 18-year study of a shallow hypertrophic lake. Ecosystems 1:250–267.

Jepersen A.M. and Christoffersen K. 1987. Measurements of chlo-rophyll a from phytoplankton using ethanol as extractionsolvent. Archiv für Hydrobiologie 109�3�: 445–454.

Jònasson P.M. and Adalsteinsson H. 1979. Phytoplankton produc-tion in shallow eutrophic Lake Mývatn, Iceland. Oikos 32: 113–138.

Jones J.I., Young J.O., Haynes G.M., Moss B., Eaton J.W. andHardwick K.J. 1999. Do submerged aquatic plants influencetheir periphyton to enhance the growth and reproduction of in-vertebrate mutualists? Oecologia 120: 463–474.

Koroleff F. 1976. Methods of Seawater Analysis. Verlag Chemie,Weinheim, Germany.

Lam P.K.S. and Calow P. 1989. Intraspecific life history variationin Lymnaea peregra �Gastropoda, Pulmonata�. 1. Fieldstudy.Journal of Animal Ecology 58�2�: 571–588.

Liboriussen L. and Jeppesen E. 2003. Temporal dynamics inepipelic, pelagic and epiphytic algal production in a clear and aturbid shallow lake. Freshwater Biology 48�3�: 418–431.

Loeb S.L., Reuter J.E. and Goldman C.R. 1983. Littoral zone pro-duction of oligo-throphic lakes: The contributions of phytoplank-ton and periphyton. In: Wetzel R.G. �ed.�, Periphyton ofFreshwater Ecosystems. Dr. W. Junk Publishers, The Hague, Thenetherlands, pp. 161-167.

Mazumder A., Taylor W.D. and McQueen D.J. 1989. Effects of nu-trient and grazers on periphyton phosphorus in lake enclosures.Freshwater Biology 22: 405–415.

McCollum E.W., Crowder L.B. and McCollum S.A. 1988. Com-plex interactions of fish, snails, and littoral zone periphyton.Ecology 79�6�: 1980–1994.

McQueen D.J., Post J.R. and Mills E.L. 1986. Trophic relationshipsin freshwater pelagic ecosystems. Canadian Journal of Fisheriesand Aquatic Sciences 43�8�: 1571–1581.

Mace M.L. 1993. Heterotrophic microbial process.. In: CarpenterS.R. and Kitchell J.F. �eds�, Cascading Trophic Interactions.Cambridge University Press, Cambridge, UK.

Persson A. and Hansson L.A. 1999. Diet shift in fish followingcompetitive release. Canadian Journal of Fisheries and AquaticSciences 56�1�: 70–78.

Power M. 1992. Top-down and bottom-up forces in food webs: Doplants have primacy? Ecology 73�3�: 733–746.

Power M.E. 1990. Effects of Fish in River Food Webs. Science250: 811–814.

Rosemond A.D., Mulholland P. and Elwood J.W. 1993. Top-downand bottom-up control of stream periphyton: Effects of nutrientsand herbivores. Ecology 74�4�: 1264–1280.

Rosemond A.D., Mulholland P.J. and Brawley S.H. 2000. Season-ally shifting limitation of stream periphyton: Response of algalpopulations and assamblage biomass and productivity to varia-tion in light, nutrients, and herbivores. Canadian Journal ofFisheries and Aquatic Sciences 57: 66–75.

Schriver P., Bøgestrand J., Jeppesen E. and Søndergaard M. 1995.Impact of Submerged Macrophytes on Fish-Zooplankton-Phytoplankton Interactions Large-Scale Enclosure Experimentsin a Shallow Eutrophic Lake. Freshwater Biology 33�2�: 255–270.

Smock L.A. 1980. Relationships between body size and biomassof aquatic insects. Freshwater Biology 10�4�: 375–383.

Sokal R.R. and Rohlf F.J. 1995. Biometry. W.H. Freeman andCompany, New York, USA.

Straile D., Livingstone D.M., Weyhenmeyer G.A. and George G.2003. The North Atlantic oscillation: climatic significance andenvironmental impact. Geophysical Monograph 134: 263–279.

Søndergaard M., Lauridsen T.L., Jeppesen E. and Bruun L. 1997.Macrophyte-waterfowl interactions: Tracking a variable resource

38

and the impact of herbivory on plant growth. In: Jeppesen E.,Søndergaard M., Søndergaard M. and Christoffersen K. �eds�,The Structuring role of Submerged Macrophytes in Lakes.Springer-Verlag Inc., New York, USA, pp. 298–306.

Uiblein F., Roca J.R., Baltanas A. and Danielopol D.L. 1996.Tradeoff between foraging and antipredator behaviour in a mac-rophyte dwelling ostracod. Archiv Fur Hydrobiologie 137�1�:119–133.

Vadeboncoeur Y., Vander Zanden M.J. and Lodge D.M. 2002. Put-ting the lake back together: reintegrating benthic pathways intofood web models. BioScience 52: 44–55.

Vander Zanden M.J. and Vadeboncoeur Y. 2002. Fishes as integra-tors of benthic and pelagic food webs in lakes. Ecology 83�8�:2152–2161.

Vermaat J.E. 1994. Periphyton removal by freshwater micrograz-ers.. In: van Vierssen W., Hootsmans M.J.M. and Vermaat J.E.�eds�, Lake Veluwe, a Macrophyte-dominated System underEutrophication Stress. Kluwer Academic Publishers, Dordrecht,The Netherlands, pp. 213–249.

Vermaat J.E. and Hootsmans M.J.M. 1994. Periphyton dynamicsin a temperature-light gradient.. In: van Vierssen W., HootsmansM.J.M. and Vermaat J.E. �eds�, Lake Veluwe, a Macrophyte-dominated System under Eutrophication Stress. Kluwer Aca-demic Publishers, Dordrecht, The Netherlands, pp. 193–212.

Wetzel R.G. 1964. A comparative study of the primary productiv-ity of higher aquatic plants, periphyton, and phytoplankton in alarge, shallow lake. Internationale Revue der gesamten Hydro-biologie 49�1�: 161.

Wetzel R.G. 1990. Land-water interfaces: Metabolic and limnolog-ical regulators. Verhandlungen der Internationalen Vereinigungfür theoretische und angewandte Limnologie 24: 6–24.

Williams A.E., Moss B. and Eaton J.W. 2002. Fish induced mac-rophyte loss in shallow lakes: top-down and bottom-up processesin mesocosm experiments. Freshwater Biology 47�11�:2216–2232.

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