ROLE OF MACROPHYTES IN A CLAY-TURBID LAKE

IMPLICATION OF DIFFERENT LIFE FORMS ON WATER QUALITY

Leena Nurminen

Department of Limnology and Environmental Protection,P. O. Box 65, FIN-00014, University of Helsinki, Finland

Academic dissertation in Limnology.

To be presented, with the permission of the Faculty of Agriculture and Forestry of theUniversity of Helsinki, for public criticism in Auditorium (2041), Biocenter,

Viikinkaari 5, Helsinki 29th October, at 12 noon.

Helsinki 2003

Author`s address: Department of Limnology and Environmental ProtectionP. O. Box 65, FIN-00014 University of Helsinki, FinlandE-mail: leena.nurminen@helsinki.fi

Supervisors: Jukka Horppila, Dr.Department of Limnology and Environmental ProtectionUniversity of Helsinki, FinlandE-mail: jukka.horppila@helsinki.fi

Pertti Eloranta, Prof.Department of Limnology and Environmental ProtectionUniversity of Helsinki, FinlandE-mail: pertti.eloranta@helsinki.fi

Reviewers: Heikki Toivonen, Dr.Finnish Environment InstituteFinlandE-mail: heikki.toivonen@ymparisto.fi

Anne Ojala, Dr.Lammi Biological StationFinlandE-mail: anne.ojala@helsinki.fi

Opponent: Timo Kairesalo, Prof.Department of Ecological and Environmental SciencesUniversity of Helsinki, FinlandE-mail: timo.kairesalo@helsinki.fi

Copyright

I © Finnish Zoological and Botanical Publishing BoardII © E. Schweizerbart`sche VerlagsbuchhandlungIII © EAWAGIV © Blackwell Sciences Ltd.V © Elsevier Sciences Ltd.VI © Kluwer Academic Publishers

© Leena NurminenISBN 952-91-6368-1 (nid.)ISBN 952-10-1391-5 (PDF)http://ethesis.helsinki.fiYliopistopainoHelsinki 2003

Cover pictures: Erika Alajärvi, Leena Nurminen, Mika Vinni

ABSTRACT

The littoral zone is a very important component taking part in forming the food web structure and theprevailing ecology of a lake. Especially in shallow lakes, continuous biotic and abiotic interactions inthe littoral also reflect to the pelagic zone, having a bearing on the whole ecosystem. An importantstructuring force in the littoral is macrovegetation. The role of macrophytes is linked to their spatialdistribution and biomass, which in turn is a result of various environmental factors (e.g. trophic status,light, substrate character, competition). Submerged macrophytes have been shown in various studies tobe important in lake restorational aspects as they decrease sediment resuspension and remobilisation ofnutrients, as well as provide refuge for zooplankton, resulting in decreased turbidity and increasedwater quality.

Hitherto, investigations on the role of macrophytes have been mostly focused on submerged species asthey most promptly respond to eutrophication through light limitation and provide profitable refuge forzooplankton due to structural complexity. But in lakes with inherently low submerged vegetation, otherfunctional groups, e.g. emergent and floating-leaved species, may play an important role in determiningthe ecological status of a lake. In this thesis, the role of the emergent life form was studied in the twoimportant functions of macrophytes: 1) refuge for zooplankton and 2) effect on resuspension. Also,importance of fish herbivory on the restricted submerged flora of a turbid lake was evaluated.

This thesis shows that in clay-turbid eutrophicated lakes, emergent vegetation may play an importantrole in seasonal and diurnal regulation of zooplankton by providing refuge, especially for freeswimming cladocerans. In addition, in eutrophic and turbid conditions, lacking submergent flora,emergent and also floating-leaved vegetation may harbour considerable densities of plant-attachedcladocerans. These plankters in turn hold considerable phytoplankton filtering capacities, which mayresult in positive water quality effects through algal control.

The results also underline the importance of emergent vegetation in regulating turbidity caused byresuspended sediment. The results demonstrate that during the growing season, sediment resuspensionand consequently the increase in inorganic turbidity and internal P-loading may be substantiallyreduced by emergent, as well as submerged, vegetation. Due to a longer growing season, emergentvegetation may therefore have considerable water quality effects in a shallow lake.

This study also revealed that in turbid and eutrophicated conditions with low submerged biomass andfew dominating species, herbivory by fish may have an influence on the dominance proportions andspecies composition of the restricted submerged flora.

To conclude, in turbid lakes, other functional forms of macrophytes, besides submergents, should notbe overlooked. This thesis has highlighted the importance of emergent macrophytes in the ecosystem ofclay-turbid lakes. In the future, more detailed studies on the floating-leaved species, often abundant inturbid circumstances, have to be conducted. In all, more thorough investigations of interactions andprocesses linked with macrophytes related to phytoplankton-caused and inorganic turbidity should beperformed. The establishment of submerged macrophytes is traditionally considered essential in therestoration of eutrophicated lakes. This thesis underlines the importance of other life forms on waterquality. In this respect, emergent and floating-leaved species may be a more profitable tool inrestoration of lakes not only when removed- but also when retained. In general, the comprehensivefunction of macrophytes should be taken into more thorough account in lake restoration schemes:recreational expectations and water quality aspects should be weighed – and preferably combined.

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List of papers

This thesis is based on the following articles referred to in text by Roman numbers (I-VI).

I Nurminen, L. 2003: Macrophyte species composition reflecting water qualitychanges in adjacent water bodies of lake Hiidenvesi, SW Finland. - Ann. Bot.Fennici 40: 199-208.

II Nurminen, L., Horppila, J. & Tallberg, P. 2001: Seasonal development of thecladoceran assemblage in a turbid lake: the role of emergent macrophytes. - Arch.Hydrobiol. 151: 127-140.

III Nurminen, L. & Horppila, J. 2002: A diurnal study on the distribution of filterfeeding zooplankton: Effect of emergent macrophytes, pH and lake trophy. - Aquat.Sci. 64: 198-206.

IV Horppila, J. & Nurminen, L. 2001: The effect of an emergent macrophyte (Typhaangustifolia L.) on sediment resuspension in a shallow north temperate lake. -Freshwat. Biol. 46: 1447-1455.

V Horppila, J. & Nurminen, L. 2003: Effects of submerged macrophytes on sedimentresuspension and internal phosphorus loading in Lake Hiidenvesi (southernFinland). -Wat. Res. 37: 4468-4474.

VI Nurminen, L., Horppila, J., Lappalainen, J. & Malinen, T. 2003: Implications ofrudd (Scardinius erythophthalmus) herbivory on submerged macrophytes in ashallow eutrophic lake. -Hydrobiologia (in press).

Author`s contribution

I LN planned and conducted the study and wrote the paper.

II LN and JH planned the study and conducted the sampling jointly, PT helped in dataanalysis. LN conducted the microscope work, data analysis and wrote the paper.

III Both authors (LN, JH) designed the study and conducted the sampling. LNanalysed the data, conducted the laboratory work and wrote the paper.

IV Both authors designed the study and conducted the fieldwork jointly. LN did thelaboratory analyses and JH wrote the paper.

V Both authors designed the study and conducted the fieldwork. LN did the laboratoryanalyses and JH wrote the paper.

VI LN and JH designed the study and collected the fish data. JL and TM helpedinterpret the data. LN analysed the data and wrote the paper.

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CONTENTS

ABSTRACTLIST OF PAPERSAUTHOR´S CONTRIBUTION

1. INTRODUCTION .........................................................................................................71.1 Littoral zone – a link to the pelagic ........................................................................71.2 Theoretical background .........................................................................................71.3 Abiotic factors connected with macrophytes .........................................................9

1.3.1 Light climate ......................................................................................................91.3.2 Sediment resuspension .......................................................................................91.3.3 Nutrient dynamics ..............................................................................................9

1.4 Biological components interlinked to macrophytes .............................................101.4.1 Phytoplankton ..................................................................................................101.4.3 Zooplankton .....................................................................................................111.4.4 Fish..................................................................................................................12

1.5 Macrophytes in turbid water – diverse causal connection ..................................122. OBJECTIVES OF THE STUDY ...............................................................................133. STUDY AREA AND METHODS ..............................................................................15

3.1 Study lake..............................................................................................................153.2 Sampling and analyses..........................................................................................16

3.2.1 Macrophytes ....................................................................................................163.2.2 Seasonal and diurnal zooplankton distribution .................................................163.2.3 Sediment resuspension .....................................................................................163.2.4 Fish diet...........................................................................................................17

4. RESULTS AND DISCUSSION.................................................................................184.1 Macrophyte species composition ..........................................................................184.2 Role of emergent macrophytes as zooplankton refugia.......................................19

4.2.1 Influence on seasonality of zooplankton community .........................................194.2.2 Importance of lake trophy in diurnal distribution of zooplankton .....................214.2.3 Effect of a phytoplankton bloom on zooplankton assemblage............................22

4.3 Role of emergent and submerged species in sediment dynamics ........................234.3.1 Impact on sediment resuspension .....................................................................234.3.2 Importance in phosphorus reduction ................................................................25

4.4 Implications of fish herbivory ..............................................................................255. CONCLUSIONS ........................................................................................................276. FUTURE STUDY OUTLOOKS – Resonance of floating-leaved species ............287. FINAL WORDS..........................................................................................................298. REFERENCES ..........................................................................................................30

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1. INTRODUCTION

1.1 Littoral zone – a link to the pelagic

The littoral zone of the lake can be regardedas a very complex area with multipleinteractions between zooplankton-fish,predator-prey, biotic and abiotic factorsforming a continuous cycle, changing intime and space, that influences the entirelake ecosystem. Food web interactionswithin littoral habitats and links betweenlittoral and pelagic areas are inadequatelyunderstood. Animal movements (e.g.migration of fish and zooplankton) link thelittoral and pelagic habitats both in terms ofpredator-prey interaction and translocationof nutrients (Carpenter et al. 1992,Schindler et al. 1996). In this puzzle,vegetation is an important component inregulating the biological structure of a lakevia the littoral zone, especially in shalloweutrophic lakes (Timms & Moss 1984). Inaddition, abiotic factors, e.g. turbidity,bottom texture and light, reflect particularlyon submerged vegetation.

The quantitative role of macrophytes in lakeecology is closely linked to their spatialdistribution and biomass, which in turn is aresult of various environmental factors

(Duarte et al. 1986, Middelboe & Markager1997). Besides lake trophic status, otherimportant factors impinging on macrophyteoccurrence are light transmission,temperature, pH, substrate characteristics,lake morphology, intra- and interspecificcompetition, herbivory and epiphyte loading(Dale 1986, Duarte et al. 1986, Vant et al.1986, Lodge 1991). Different macrophytelife forms require nutrients from differentsources and vary in exposure tolerance(Toivonen & Huttunen 1995). Therefore,macrophyte species richness and proportionsof various growth forms closely reflect thetrophic state of lakes (Schulthorpe 1967,Toivonen & Huttunen 1995). The role ofmacrophytes as stabilizing and structuringcomponents in lakes of differing trophy havebeen emphasized in the stable state theoryby Scheffer et al. (1993) and in thecascading hypothesis by Jeppesen et al.(1998).

1.2 Theoretical background

The alternative stable state theory byScheffer et al. (1993), underlining thestabilizing effect of vegetation, is based onthe interaction between submergedmacrophytes and phytoplankton-inducedturbidity in a shallow lake (Fig. 1). This

Figure 1. Stable-state theory by Scheffer et al. (1993) (modified) based on alternativeequilibrium turbidities caused by disappearance of submerged vegetation.

TU

RB

IDIT

Y

NUTRIENTS

WITHOUT VEGETATION

WITH VEGETATION

CRITICAL TURBIDITY

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theory is grounded on assumptions thatturbidity increases concomitantly withnutrient level, increase of vegetation resultsin reduced turbidity, and vegetationvanishes when a critical level of turbidity isexceeded. Existence of submergedvegetation stabilizes the water quality of ashallow lake to a certain threshold. Even arather considerable rise in nutrient loadingcannot affect the turbidity level due tostabilizing effects of vegetation. Thus, thecritical level of nutrient loading, causingphytoplankton turbidity, is lifted. However,in a vice versa situation of a high turbiditylevel and scanty vegetation, a much lowernutrient status should be attained in order toreach the same desired turbidity level.Thus, according to this theory, submergedvegetation performs as both positive (highbiomass) and negative (low biomass) bufferin the altering stable states of shallow lakeecosystems.

The other background assumption related tothe structuring role of vegetation in lakes isthe hypothesis by Jeppesen et al. (1998)which is based on the cascading effect ofsubmerged vegetation in lakes of differingtrophy (Fig. 2). The theory emphasizes theimportance of structural complexity ofsubmerged plants in providing refuge forzooplankton against fish predation. Thebiomass and seasonality of zooplankton isconnected to lake trophy, in turn reflectingthe vegetation density. In eutrophic lakeswith high macrophyte density, thezooplankton peak follows plant biomass,coinciding in late summer. On the contrary,in hypertrophic and oligotrophic waterswith more scanty vegetation, thezooplankton biomass peak takes place inthe beginning of summer or autumn, as noadequate refuge by vegetation is present.

Figure 2. Conceptual model by Jeppesen et al. (1998) (modified) illustrating the change in zooplanktonseasonality and biomass in various nutrient levels and the relationship with submerged vegetation.

HYPERTROPHIC

EUTROPHIC- high macrophyte density

MESOTROPHIC OLIGOTROPHIC

EUTROPHIC- low macrophyte density

APRIL NOVEMBER

MACROPHYTE

ZOOPLANKTON

BIO

MA

SS

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1.3 Abiotic factors connected withmacrophytes

1.3.1 Light climate

The biological nature of each lake,reflecting also on macrophyte diversity andbiomass, is strongly ruled by the euphoticdepth, beyond which light level falls below1% of surface irradiation (the critical levelfor photosynthesis) (Wetzel 1983). Thelight photon can either absorb or scatter –the proportions of which differ according towater quality and are very lake-specific.Scattering is caused by inorganic suspendedparticles and does not remove light fromthe water as absorption does, but changesdirection (Kirk 1994). On the contrary,dissolved organic substances absorb lightand phytoplankton both scatter and absorb.Also different wavelengths (blue, green,red) absorb in variable depths in differenttypes of lakes (Kirk 1985). Understandingthe differences between absorption,scattering and light attenuation isfundamental since different relativeconcentrations of phytoplankton, suspendedsolids and detritus effect the entity of lightunder water. Since algae and submergedvegetation depend on light availability,these causal links in the light climate arevery important.

1.3.2 Sediment resuspension

In lakes, water movement leading toresuspension of sediment depends on wavevelocity, sediment properties, lake shape,and depth profile (Håkanson & Jansson1983). In lakes with variable depth profile,sediment in exposed shallow areas areresuspended and concentrated to deeperparts. But in shallow lakes, resuspensioncan be continuous due to lack of deeperareas acting as sediment traps (Evans1994). In addition to lake profile, the typeof sediment is fundamental to resuspensionfrequency; organic substances and clayhave low settling rates, whereas coarsermaterial such as sand is not easilyresuspended (Håkanson & Jansson 1983).

In addition to wave action, sediment canalso be resuspended by animals (Anderssonet al. 1988). Especially in shallow lakes,large part of the fish community feed oninvertebrates dwelling on the bottom. As awhole, resuspension by benthivores can bequite substantial, e.g. bream (Abramisbrama (L.)) can suspend 5 times its bodyweight per day (Breukelaar et al. 1994).Generally, main causes for turbidity inshallow lakes are suspended solids andalgae, which tend to sink in lack ofresuspension (Barko & James 1998).Aquatic macrophytes have been observedto reduce sediment resuspension bydepressing wave velocity and hindering fishtampering (Dieter 1990, Madsen et al.2001). The effect of aquatic vegetationappears to correlate with the vegetationstructure and density.

1.3.3 Nutrient dynamics

In shallow lakes, mostly due to the intensesediment-water contact nutrient dynamics isa continuous process (Evans 1994). One ofthe most important nutrients is phosphorusthat correlates positively witheutrophication. The sediment-waterinteraction is very important, as a great dealof usable phosphorus can be stored in thesediment to be readily released. In general,sediment acts as a phosphorus buffer, butsome mechanisms such as oxygen and iron,turbulence, decomposition andresuspension may enhance phosphorusrelease (Scheffer 1998).

Many biotic components have a significantrole in nutrient cycling. Fixation ofatmospheric nitrogen by e.g. cyanobacteriamay cause influx of nitrogen to water. Ingeneral, phytoplankton obtain much of therequired nutrients from the water column(Barko & Smart 1980). Aquatic animalshave their own input in the ongoing nutrientcirculation. Zooplankton and fish uptakenutrients in feeding and release nutrientsback to water column by excretion (Taylor1984, Kraft 1992). Also, benthivorous

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invertebrates excrete mineral nutrients andenhance mixing of sediment surface, andphosphorus release tends to increase inconcert with increasing invertebratebiomass (Wiśniewski & Planter 1985). Therole of benthivorous fish is two-sided asthey on one hand, may reduce the release ofphosphorus from sediment by decreasingthe invertebrate densities, but on the otherhand act as nutrient pumps, causingresuspension while foraging and excretenutrients into water column.

Effect of macrophytes on the phosphoruscycle is ambiguous (Granéli & Solander1988). Vegetation beds reduce turbulence,which enhances possible anaerobicconditions at sediment surface but at thesame time prohibits resuspension and limitsphosphorus release from sediment.Macrophytes mobilize nutrients fromsediment directly through root uptake anddecayal and indirectly by causingfluctuations in pH and oxygen throughmetabolic activities (Barko & Smart 1980,Barko & James 1998). In general, aquaticvegetation can be considered as aphosphorus sink during growth and as apotential source during senescence(Carpenter & Lodge 1986). The emphasisof vegetation on phosphorus availabilitydepends on both macrophyte species anddensity (Van Donk et al. 1993, Christensen& Andersen 1996). In shallow waterbodies, potential negative effects bymacrophytes on water quality (i.e.enhanced nutrient cycling) may beovershadowed by the ability of plant bedsto moderate wave velocity (i.e. turbidityand suspended particle concentrations inthe water) (Barko & James 1998).

1.4 Biological components interlinked tomacrophytes

1.4.1 Phytoplankton

Phytoplankton is an important indicator ofwater quality (e.g. algal biomass, speciesformation, nutrient uptake) and coincidingwith nutrient loading often has a dominant

role as the main primary producer inshallow lakes. Macrophytes and theirsymbiotic epiphytes, which especially inshallow eutrophic lakes may play aconsiderable role in nutrient dynamics,compete for the same available nutrients(Kufel & Ozimek 1994). Nevertheless,phytoplankton, in addition to epiphyton,has been proven to be instrumental (directlyor indirectly) in many processes takingplace in the littoral zone related tomacrophytes. The volume of sedimentationand resuspension (in turn modified bymacrophyte beds), influencesphytoplankton communities, as mostspecies tend to sink in still water (Barko &James 1998). Macrophytes also have ashading effect on phytoplankton leading toreduced intensity (Ozimek et al. 1990). Thetotal shading effect depends on the biomassand surface area of plant species (Sher-Kaulet al. 1995).

Very crucial linkage having a substantialbearing on the water quality isphytoplankton grazing by zooplankton, towhich macrophytes provide refuge frompredators. Therefore, plant beds enableincreased grazing, influencing thechlorophyll a concentrations(phytoplankton-caused turbidity) of thelake. Macrophytes apparently have a certainthreshold after which they have asubstantial effect on phytoplanktonbiomass. Plant threshold levels suggested tobe adequate vary between 20-50% PVI(percent volume infested) (Canfield et al.1984, Schriver et al. 1995). On the whole,studies on the relative importance of top-down control of phytoplankton byzooplankton or bottom-up control throughnutrients in macrophyte beds are scarce.Fish modify the influence of macrophyteson phytoplankton through zooplanktonpredation in different plant densities.Therefore, phytoplankton variables maychange along nutrient, macrophyte and fishgradients.

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1.4.3 Zooplankton

Zooplankton grazing has been recognizedto be an indisputable factor regulatingphytoplankton in lakes (e.g. Kerfoot et al.1988). Particularly Daphnia, aspredominant cladoceran, can play a majorrole in the seasonality and biomass ofphytoplankton. Biomass, average individualsize and structure of the zooplanktoncommunity are largely determined bypredation pressure. In shallow eutrophiclakes, fish predation can induce a shift fromDaphnia-domination to a zooplanktoncommunity with smaller cladocerans, e.g.Bosmina, coinciding with rotifers andcyclopoid copepods (Jeppesen et al. 1992).Predation pressure increases in concert withlake trophy due to shift to a higherproportion of zooplanktivores and changein age composition towards younger fish,predating more selectively on zooplankton(Cryer et al. 1986).

Zooplankton seek refuge against predation,and in shallow lakes, where shelterprovided by a depth gradient is absent,zooplankton resort to horizontal migrationamong macrophytes for refuge (Walls et al.1990). Horizontal distribution ofzooplankton varies diurnally andseasonally, mostly due to the spatial andtemporal variation of predation by e.g.young-of-the-year fish (YOY) andinvertebrate predators (Cryer & Townsend1988). Reverse migration caused bypredation of YOY fish or plant-associatedpredators such as odonates has also beenreported, although diurnal horizontalmigration (DHM) induced by invertebratepredators is probably most important inlakes with low fish densities (Lauridsen etal. 1996). Also diurnal microverticalmigration, e.g. pH-induced, is reported inmany studies (e.g. Hansen et al. 1991).According to Ivanova and Klekowski(1972), high lake pH may impair thesurvival of grazing zooplankton,influencing the respiration and filtrationrate of cladocerans. Large cyanobacteriamay, in addition of elevating pH, affect the

filtration capacity of zooplankton byinterference and be less edible and eventoxic (Dawidowicz 1990, Gliwicz 1990).

Migration by zooplankton into vegetation isa trade off between predation risk andoptimal feeding conditions sincemacrophytes (e.g. Myriophyllum) producerepellants suppressing zooplankton(Lauridsen et al. 1997). Additionally,filtration among plants and macrophyteshading, causing a lower phytoplanktonbiomass, result in smaller littoralzooplankters, such as Ceriodaphnia andDiaphanosoma (Lauridsen et al. 1996).Despite unfavourable conditions, especiallylarge zooplankton aggregate within thevegetation beds during daytime (Timms &Moss 1984, Davies 1985, Lauridsen &Buenk 1996). Refuge effect and relativezooplankton composition and abundanceamong vegetation depends on plant density(Schriver et al. 1995) and fish composition(Persson 1991). In larger stands, especiallyfree-swimming, often pelagic, cladoceransare more scarce (Lauridsen et al. 1996), butplant-associated species may be veryabundant (Paterson 1994). Cladoceransfixed to plants (e.g. Sida crystallina (O.F.Müller)) may be crucially underestimated,and they may possess a considerablefiltration capacity (Irvine et al. 1990,Jeppesen et al. 1997). Plant density affectsthe predation capability of fish, the denserthe bed the better the refuge (Schriver et al.1995, Jeppesen et al. 1997), although, highfish predation have been shown to suppresszooplankton communities even in densevegetation (Kairesalo et al. 1998). Ingeneral, sparse plant beds allow efficientforaging for some juvenile fish (poorprotection for pelagic zooplankton) butplant-associated cladocerans appear toescape predation and can be abundant evenat high fish densities.

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1.4.4 Fish

Fish in a shallow lake play an indispensablerole in structuring the lake community. Inaddition to direct predation, fish mayinfluence both bottom-up and top-downcontrol via their search for food at thebottom. While searching for food, fish stirup sediment, causing a rise inconcentrations of suspended solids(Breukelaar et al. 1994). Increase inturbidity reduces hunting by visualpredators (e.g. perch; Perca fluviatilis L.),which in turn increases the number ofplanktivorous prey fish, resulting in anegative impact on large zooplankton(Jeppesen et al. 1997).

Many factors influence the structure of fishcommunity. High pH has a negativeinfluence on fish recruitment and frysurvival (Timmermann 1987). Increase inlake trophy leads to a change in fishcommunity structure where vegetationplays a significant role; in turbid waterslacking vegetation, dominating species arecyprinids and pikeperch (Stizostedionlucioperca (L.)) (Lammens 1989), whereasin vegetated water, percids and small pikes(Esox lucius L.) prevail (Grimms 1983).Predator efficiency declines in concordwith macrophyte structural complexity(Heck & Crowder 1991), but reversely preydensity and diversity increases, therefore,fish presumably grow best in intermediatevegetation density (Crowder & Cooper1982). The structuring role of vegetation onthe fish community is based on foodavailability and predation risk leading tomacrophyte density mediating predator-prey interactions. Foraging efficiencyamong vegetation is discovered to bespecies-specific; zooplankton consumptionby juvenile roach (Rutilus rutilus (L.))decreased with vegetation density, whereascapture rates of rudd (Scardiniuserythrophthalmus (L.)) and perch can beenhanced by vegetation when not too dense(Winfield 1987, Persson et al. 1993).Vegetation does not influence fishcommunities only by predator-prey

interactions; herbivory of macrophytes bycyprinids (rudd and roach) has beenobserved to play an important role instructuring macrophyte species compositionin lakes (Van Donk 1998).

The protective importance of macrophytesagainst predation from larger piscivores iscrucial for juvenile fish (Venugopal &Winfield 1993, Persson & Eklöv 1995).This results in higher densities of juvenilefish in macrophyte rich lakes (Carpenter &Lodge 1986). Importance of YOY fish isfar more prominent in lake ecosystems thanexpected (e.g. Cryer et al. 1986; Whiteside1988). In meso-eutrophic lakes, juvenilefish may be responsible for the mid summerzooplankton biomass decline (Fig. 2)(Luecke et al. 1990).

1.5 Macrophytes in turbid water –diverse causal connection

The formation and existence ofmacrophytes has a duplex causalconnection with turbidity (Fig. 1; Schefferet al. 1993). Vegetated lakes are moretransparent as vegetation has a decreasingeffect on turbidity. The cascading powerover phytoplankton-induced turbidity isclearly seen in temperate lakes where themacrophyte biomass peak is in mid summerand the chlorophyll peak appears in springand fall. In Dutch lakes, wintergreensubmerged plant, Elodea, keptphytoplankton biomass generally low,whereas Ceratophyllum and Potamogetonoming shorter growing seasons, allowedphytoplankton blooms in spring andautumn (Van Donk & Gulati 1995). Aspreviously discussed, in addition toinfluencing algal growth and seasonality,macrophytes may buffer sedimentresuspension by wave action (inorganicturbidity), affect nutrient availability andharbour filter feeding cladocerans.However, the weighting of these variousmechanisms on water quality variesconsiderably in different lakes.

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As vegetation has a major function incontrolling turbidity, also turbidity amongother factors regulates macrophyte growth(Scheffer 1998). Maximum depth for plantgrowth is inversely related to attenuation oflight (Chambers & Kalff 1985). Moreimportant than the light that reaches thebottom is the amount of light reaching theplant canopy. Therefore, the effect ofturbidity on submerged vegetation dependson the growth form as canopy-formingspecies prevail when nutrient levelincreases (Chambers 1987, Moss 1998). Inturbid waters, also species overwintering invegetative form have a competitiveadvantage, since they hold the energy tostart spring growth and do not requirebottom-reaching light (Scheffer et al.1992). Periphyton growth together withnutrient loading increases turbidityaffecting plant growth. Periphyton canreduce light by 80%, limit diffusion ofcarbon and other nutrients and alsomechanically suppress plants (Sand-Jensen& Borum 1984). Other important factorseffecting formation of vegetation is waveaction and herbivory. Water movementenhances nutrient uptake but can alsoincrease uprooting and turbidity, due toresuspension, resulting in inhibition of plantsettlement (Van Donk & Otte 1996,Scheffer 1998). Herbivory, via grazing anduprooting of plants, can be very substantialleading up to over 50% reduction invegetation (Lodge 1991). Herbivorous fishin temperate lakes (e.g. rudd and roach)have not been witnessed to reduce plantbiomass but may have a potential effect onplant species composition through selectivegrazing (Van Donk et al. 1998). As anindirect effect, bottom foraging of thesegrazers stir up sediment, leading toinhibition of plant growth.

2. OBJECTIVES OF THE STUDY

The discussion on the manifold causal roleof macrophytes in littoral ecosystems andtheir stabilizing effect on water quality aremostly confined to submerged species (e.g.Hanson and Butler 1994, Jacobsen et al.1997, Stansfield et al. 1997). This is due totheir alert response to eutrophicationthrough changing light climate, and abilityto provide profitable refuges forzooplankton due to structural complexity(Dionne & Folt 1989). The stable statetheory by Scheffer et al. (1993) as well asthe refuge hypothesis by Jeppesen et al.(1998) are both founded on submergedspecies. However, the role of othermacrophyte life forms needs to bespecified, especially in lakes, where thewater quality is not solely regulated by thedevelopment of phytoplankton biomass, butalso by inorganic suspended solids. Suchlakes may be inherently quite turbid andhave scanty submerged vegetation.Therefore, the role of emergent andfloating-leaved species should be takenunder more careful scrutiny.

The study area of this thesis, LakeHiidenvesi, resembles an inherently clay-turbid eutrophicated lake with relativelyscarce submerged vegetation. In thesesettings, I aimed to clarify the role of theemergent life form on the two importantfunctions of macrophytes: 1) refuge forzooplankton and 2) effect on sedimentresuspension. In addition, the importance offish herbivory on the restricted submergedvegetation was investigated. This thesistherefore hypothesizes that in clay-turbidcircumstances, in the absence ofsubmergents, other life forms e.g. emergentand floating-leaved, play a significant rolein the important structural and stabilizingfunctions of vegetation stated.

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The thesis is composed of six studies ofwhich paper I is a vegetation mapping andlife form structure study in the differentbasins of Lake Hiidenvesi with divergentwater quality. In paper II, the role ofemergent vegetation on the seasonaldistribution of littoral zooplankton (refugeeffect) in turbid water is evaluated. Thisstudy aimed to clarify whether the seasonaldevelopment of zooplankton follows thehypothesis by Jeppesen et al. (1998) inclay-turbid circumstances where emergentmacrophytes dominate instead ofsubmerged species. The same theme iscontinued in paper III where diurnalhorizontal migrations of zooplanktersamong emergents in basins of differingwater quality (eutrophic and mesotrophic)is studied. In addition, in this paper (III) theeffects of mass occurrence ofphytoplankton, common in eutrophicconditions, on littoral zooplanktoncomposition and diurnal distribution arediscussed.

The importance of different macrophyte lifeforms, in this study emergent (IV) andsubmerged (V) macrophyte stands, onsediment resuspension and phosphorusdynamics is investigated and compared.Finally, the effect of fish, in this case rudd,herbivory on the species composition andabundance of inherently scanty submergedvegetation is studied in paper VI.

However, as discussed in previous sectionsthe littoral ecosystem is a linkage of abioticand biotic factors jointly affecting theprocesses. Therefore, in addition to thesemain research subjects, this thesis also aimsto discuss some of the causal links andprocesses in the manifold field of researchrelated to macrophytes in clay-turbid lakes(Fig. 3).

Figure 3. Schematic illustration of the different abiotic and biotic links related to macrophytes discussed directly andundirectly in this thesis (bold Roman numbers indicate articles) (solid line -positive effect; broken line - negative effect).

PHYTOPLANKTON

ZOOPLANKTON

NUTRIENTS

FISH

LIGHT

PREDATION

GRAZINGpH

TROPHYINCREASE

BIOTURBATION

pH

SPECIESCOMPOSITION

IV

III

III

III II

I

II, III

II, III

II, III

IV, VIV, V

IV

I, II, III

II, IIII

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III

II, III

II, IIIPREDATION

REFUGE

REFUGE

REFUGE

II, III

SHADING

HERBIVORY

RESUSPENSION

RESUSPENSION

RESUSPENSION

SPECIESCOMPOSITION

15

3. STUDY AREA AND METHODS

3.1 Study lake

Isontalonselkä

Nummelanselkä

Kirkkojärvi

River Vihtijoki

River Vanjoki

Kiihkelyksenselkä

Retlahti

Vaanilanlahti

Figure 4. Map of Lake Hiidenvesi; study areas(indicated as basins) are shown. Main characteristicsand water quality variables of basins are indicated inTable 1.

Lake Hiidenvesi is the second largest lake(30.3 km2) on the southwestern coast ofFinland (60º 24´ N, 24º 18´E).

Due to heavy point and non-point loading,the lake has a long eutrophication historywith severe cyanophyte blooms occurringsince 1960s (Tallberg et al. 1999). Almost90% of the annual external phosphorusloading (0.5-1 g m2 P) to the lake comesfrom the two rivers Vihtijoki (51%) andVanjoki (38%) (Ranta & Jokinen 1998).

Altogether, Lake Hiidenvesi is inherentlyconsiderably turbid, due to the compositionand resuspension of the bottom material(inorganic matter e.g. clay). The lake is aflow-through system, consisting of severalseparate basins quite different in theirmorphology and trophic status (Table 1),the basins being as follows: Kirkkojärvi(northeastern part), Nummelanselkä,Kiihkelyksenselkä, Retlahti, Isontalonselkäand Vaanilanlahti (southwestern part) (Fig.4).

Due to high turbidity, the biomass ofsubmerged macrophytes is relatively lowand restricted to shallow sheltered bays.Emergent vegetation in the lake is relativelyabundant especially in shallow Kirkkojärviand Vaanilanlahti basins. Floating-leavedlife form is common throughout the lakewith wide zones of Nuphar lutea (L.)prevailing in every basin.

Table 1. Main characteristics and environmental variables of the interconnectedbasins of Lake Hiidenvesi (measured 8th August) (I). (bottom type; 1 *semi-hard, 2*semi-soft, 3 *soft)

BasinsTot-N(µg l-1)

Tot-P(µg l-1)

Secchi(cm)

Turbidity(NTU)

Conductivity(mS m-1)

Mean depth(m)

Bottom type

Kirkkojärvi 1400 100 30 58 10.1 1.9 3Nummelanselkä 1100 50 60 25 8.7 2.6 2Kiihkelyksenselkä 1100 40 100 16 8.2 11.2 1Retlahti 850 30 120 8 8.1 7.9 1Isontalonselkä 730 30 110 11 8.2 3.3 1Vaanilanlahti 890 140 110 6 10.3 1.3 2

16

3.2 Sampling and analyses

3.2.1 Macrophytes

The aquatic vegetation mapping (I) wasconducted with an aquascope and samplingrakes (modified garden rake and Luther-rake; Luther 1951). Simultaneously withmapping, macrophyte abundance (modified3-degree Norrlin scale method; Luther1951, Munsterhjelm 1997) and growingdepths were charted. Chemical waterquality samples (total P, total N) wereanalysed according to the standards ofFinnish Environment Institute. Turbidityand conductivity were analysed with YSI6600 sonde. The mappings were roughlycompared to earlier vegetation mappingsfrom the 1950´s (K. Aura, pers. comm). Toevaluate the weighing of eachenvironmental variable on the speciesoccurrence, each measured parameter wasindependently tested with the macrophytelife forms using Mantel-test (McCune &Mefford 1999). The ordinations for speciesdata of different life forms in the basinswere performed with the program PC-ORD,using detrended correspondence analysis(DCA) (McCune & Mefford 1999).

3.2.2 Seasonal and diurnal zooplanktondistribution

The sampling for zooplankton wasconducted with a tube sampler (h = 1 m, V= 7.5 l); fortnightly during the summer(seasonally) from three different zones ofemergent vegetation (5 m inside andoutside the stand and at the edge) (II) anddiurnally (5 samples in total; 3 times atnoon and 2 at midnight) from threedifferent zones (same as above) ofemergent stands in two basins (Typhaangustifolia in Kirkkojärvi basin;Phragmites australis in Isontalonselkäbasin) of differing water clarity and quality(III). The cladoceran samples (5 replicates,II; 3 replicates consisting 3 pooledsubsamples, III) were enumerated using aninverted microscope and identified to genusor species level. Dense samples were

subsampled and 30 individuals from eachspecies were measured (Daphnia spp. usingeye-length) and individual numbers wereconverted to carbon biomass, using length-carbon- regressions (e.g. Luokkanen 1995).Cladoceran biomasses and densities in thedifferent vegetation zones were comparedusing analysis of variance for repeatedmeasurements and the mean lengths ofdifferent cladocerans with analysis ofvariance (II). Paired comparisons wereconducted with Bonferroni t-tests (II).Cladoceran biomass, densities andindividual lengths during day and night inthe different zones were compared usingthe Mann-Whitney U-test (III).

The daily phytoplankton consumption rateof zooplankton (II) was calculated usingthe equation of Lampert (1988), accordingto which the daily amount of carboneliminated = 83 mg g-1 d-1 DW, and bymethod of Jeppesen et al. (1994), accordingto which cladocerans ingest an amount ofphytoplankton equivalent to 100% of theirown biomass per day. Consumption rateswere compared with phytoplanktonbiomass, taken from the epilimnion (0-2 m)with tube sampler.

Physical and chemical water characteristics(e.g. temperature, pH) (II, III) were takenduring every sampling and the density ofstands was measured with a 0.25 m2 frame.The photosynthetic photon flux density at400-700 nm from 10 cm below the watersurface and 10 cm above the bottom in eachzone was measured by a LI-COR quantummeter. Phosphorus, nitrogen andchlorophyll a were measured in thebeginning of the study (III).

3.2.3 Sediment resuspension

The sediment resuspension studies relatedto macrophytes were conducted in threedifferent zones (5 m inside and outside andat the edge) of emergent (IV) macrophytesand two zones (30 m inside and outside)related to submerged (V) vegetation. The

17

stem densities of emergents and PVI(percent volume infested) of submergedvegetation were measured during everysampling. The rate of sedimentresuspension was estimated using themethod by Gasith (1975), applicableespecially to shallow water bodies, basedon the assumption that the organic mattercontent of the bottom sediment is differentfrom that of suspended seston. The methoduses the equation

)(

)(

TR

TS

ff

ffSR

−−= (Gasith 1975, Bloesch

1994), whereR= resuspended bottom sediment (dry mass)S= entrapped settling flux (dry mass)fS = organic fraction of SfR= organic fraction of R (surface sediment)fT= organic fraction of seston (T)suspended in the water

Gross sedimentation rate was determinedby placing sedimentation traps (5replicates) in each zone. The traps (height :width ratio of 6 : 1) were lifted at 14-dayintervals. The content of traps was driedand the organic fraction (fS) wasdetermined by ignition at 550 °C. Sestonsamples from each zone were taken with atube sampler, filtered through a GF/C filterand, following filtration, analyzed forsuspended solids (SS) and loss on ignition(fT), total P and SRP (soluble reactivephosphorus). In addition, three replicatesurface sediment samples were also liftedfrom each zone with a corer and analyzedfor loss on ignition (fR). The rate of Presuspension in each zone was estimatedusing the calculated resuspension rates andthe P content of surface sediment,determined on each date from the surfacesediment samples. Following therecommendations of Gasith (1975), thevalues of gross sedimentation rate (S) werecorrected by subtracting the dry mass ofsuspended matter, contained by the watervolume in each trap, from the gross drymass per trap. Between-zone differences inthe values of fS, fR, fT, as well as in the

sedimentation rate, were tested usinganalysis of variance for repeatedmeasurements (IV,V). Paired comparisonswere conducted with Bonferroni t-tests(IV,V).

3.2.4 Fish diet

Rudd (Scardinius erythrophthalmus) datafor diet analysis were collected amongmacrophyte vegetation with gillnets (meshsizes 10-45 mm from knot to knot) placedin water depths of 1-1.5 m (VI).Gillnettings were conducted during the daywith nets held in the water for 1-2 h. Thegut content (anterior third) was analysed forvolume proportions of different food items(Rask 1989). The fish (n = 516) weremeasured to nearest mm and weighted tonearest g. The age was determined usingboth scales and cleithra (Horppila &Nyberg 1999). The growth rate was back-calculated using Fraser-Lee method(Bagenal & Tesch 1978).

Food consumption of rudd (age groups 3-7)was estimated using bioenergetics model(Kitchell et al. 1977, Hewett & Johnson1992). Existing roach parameters (Horppila& Peltonen 1997) were applied to rudd. Thecalorimetric values were obtained fromliterature (Cummins & Wuycheck 1971,Horppila & Peltonen 1997). Back-calculated yearly growth rates were used incalculating macrophyte consumption ofeach age group. Back-calculated lengthswere converted to weight using the length-weight equation w = 0.00003 L 3.305 (r2 =0.99). Total macrophyte consumption byrudd was estimated using a scenario ofdifferent combinations of biomass and agegroup distributions.

18

4. RESULTS AND DISCUSSION

4.1 Macrophyte species composition

The macrophyte vegetation in LakeHiidenvesi (I) was different in the divergentareas of the lake, conceivably due to thedisparity of water chemistry, substratumand morphological features of theconnected basins (Smith & Wallsten 1986,Bailey 1988). The overall rather low lightpenetration constrains the flora to turbiditytolerant species and life forms. Themacrophyte vegetation is biased towardseurycoic (wide amplitude) emergent andfloating-leaved species, with a fairly smallbiomass of truly submerged plants, and e.g.rosette types (isoetids), demandingrelatively good light conditions, arepractically absent (I) (Toivonen &Huttunen 1995).

The diversity of helophytes in LakeHiidenvesi is engrossing, as the speciesrichness, (increasing with lake trophy)resembles local variation of trophic state,substratum characters and exposuregradients (I) (Table 2), which areconcomitantly the most important featuresdetermining the formation of emergentvegetation (Bailey 1988, Toivonen &Huttunen 1995). Eutraphent species such asTypha latifolia L., Typha angustifolia L.,

Sparganium erectum Rehman, Glyceriamaxima (Hartm.) Holmberg and Acoruscalamus L., tolerating loose loam substrata(Toivonen & Bäck 1989), thrive in theshallow waters of the northern andnorthwestern basins of Lake Hiidenvesi (I).

Indifferent Phragmites australis (Cav.)Trin. Ex Steudel and Equisetum fluviatile L.requiring more exposed sites with coarsersubstrata, dominate the less eutrophicatedwestern and southern basins (I). Floating-leaved species, e.g. nymphaeids, andPolygonum amphibium L. are wellrepresented in Lake Hiidenvesi (I), due toan allegedly advantageous life form inturbid waters.

As light attenuation and depth are mostimportant factors explaining submergedvegetation abundance, the speciesabundance and overall biomass ofsubmerged flora in turbid Lake Hiidenvesiis mainly restricted to rather few low light-tolerant species (I). However, thesomewhat differing species composition ofthe basins reflects the changing lightconditions and nutrient status (Table 2).Prevailing “turbidity tolerant“ flora, inaddition to Potamogeton obtusifolius Mert.& Koch, are pleustophytes, which arerootless byonants, (Ceratophyllumdemersum L., Ranunculus circinatus Sibth.)and canopy-forming submerged plants(Myriophyllum verticillatum L.) (I).

Table 2. The statistically significant (p< 0.05) environmental variables (rows) influencing thedistribution of different macrophyte life forms (columns) in the basins of Lake Hiidenvesi(Mantel-test) (I).

Emergent Submerged Floating-leaved Pleustophyte All formsTurbidity 0.05 - - - -Conductivity 0.01 0.04 0.02 0.03 0.03Bottom type 0.03 - - 0.04 0.03Phosphorus 0.05 0.02 0.03 0.03 0.03

19

The species assemblage in Lake Hiidenvesiindicated a clear eutrophication process,leading to transition toward a moreeutraphent vegetation. It seems that duringthe past 50 years, the contrast between theinterconnected basins has broadened andculminated with the northernmost basins,Kirkkojärvi and Nummelanselkä, becomingmanifestly more eutrophic (I). Tall reedyhelophytes and nymphaeids, favoringeutrophication (Toivonen & Bäck 1989),are the life forms thriving in LakeHiidenvesi, many of which have expandedtheir distribution in the lake (I). Likewisethe emergent vegetation, the main cause forchange in the naturally low-light resistantsubmerged flora is the rise of nutrient leveland softening of bottom material. Byonantpleustophytes, such as Ceratophyllumdemersum and Ranunculus circinatus,thriving from sheltered soft habitats andhaving a high tolerance for low lightconditions (Uotila 1971, Meriläinen &Toivonen 1979), have plagued parts of theshallow northern basins, especiallyKirkkojärvi basin (I). In addition, nutrientlevel increase induces macrophytecompetition with phytoplankton, as well asshading by phytoplankton blooms andperiphyton (Sand-Jensen & Søndergaard1981). Sand-Jensen & Borum (1991) foundperiphyton coverage to be the majorproblem for diminishing of submergedplants in eutrophic lakes, reducing the lightlevel at the leaf surface up to 80%. Thus,heavy periphyton vegetation, plaguing thesubmerged flora, especially in shallowKirkkojärvi and Vaanilanlahti basins,cannot be overlooked as a cause, if notreducing, at least partly regulatingespecially the rooted submerged vegetation.

4.2 Role of emergent macrophytes aszooplankton refugia

4.2.1 Influence on seasonality ofzooplankton community

In north temperate lakes, the mostfrequently observed seasonal pattern oflittoral zooplankton includes a spring peakfollowed by a steep decline in mid summer,being usually explained by increasedpredation of underyearling fish (Cryer et al.1986, Whiteside 1988). This is trueespecially in lakes with low submergedmacrophyte density and consequently lowrefuge availability for zooplankton(Jeppesen et al. 1998). In eutrophic lakeswith high submerged macrophyte coverage,the refuge effect is high and zooplanktonbiomass follows the macrophyte biomass,peaking in mid summer (Fig. 2; Jeppesen etal. 1998). In this study related to emergentspecies (Typha angustifolia) (II), althoughthe zooplankton biomass was quite low, theseasonal pattern followed the oneresembling high macrophyte biomass lakes,zooplankton peak taking place in midsummer, even though coinciding with thehighest consumption rate of fish. In thebeginning of summer as no refuge forcladocerans was found (II), predationprobably suppressed zooplankton biomass.Through the summer as emergent standsdeveloped, the cladoceran abundanceincreased accordingly (II) (Fig. 5). Amongthe vegetation, the biomass of especiallyfree-swimming filter feeders(Diaphanosoma brachyurum (Lieven),Bosmina longirostris (O. F. Müller),Ceriodaphnia quadrangula (O. F. Müller)and chydorids) increased, while at the edgeand outside the stands, the free-swimmingcladoceran biomass remained low (II) (Fig.5). This seasonal succession resembled thetrend observed by e.g. Lehtovaara &Sarvala (1984).

The pattern observed was concievably aconsequence of concomitant changes inpredation pressure and refuge availability

20

provided by emergents, as predationpressure in the studied Kirkkojärvi basin ishigh, indicated by high catches of smallcyprinids as well as perch and smallaverage size of cladocerans with high shareof cyclopoid copepods and cladocerans inthe crustacean assemblage (Tallberg et al.1999, Olin et al. 2002). The fishassemblage of the Kirkkojärvi basin isdominated by cyprinids, different speciesspawning in sequence in spring. The YOYfish inhabit the vegetation, feeding at firston algae and rotifers and switching tocladocerans (Hammer 1985). Thus,predation pressure provided by small fish isconsiderable.

Figure 5. Total cladoceran carbon biomass (top),biomass of filter feeding cladocerans (middle) andbiomass of free-swimming filter feeding cladocerans(bottom) in the different zones of the Typhaangustifolia stands (vertical bars indicate SD values)(II).

The effects of emergent macrophytes on thegrazing pressure of cladocerans can beconsiderable (II). Even though low at theedge and outside the stands, the grazingpressure of free-swimming filter feederswithin the vegetation (II) (Fig. 6) reachedthe 80% daily grazing considered to besufficient to balance growth rates of algae(Reynolds 1984). In the outer zone of theemergent stand, the grazing pressure of therather large-sized plant-associatedcladoceran, Sida crystallina (O. F. Müller),was higher than of the free-swimmingspecies together (II) (Fig. 6). In oursampling, due to methodology, the densityof Sida crystallina (mostly fixed to plantse.g. floating-leaved) was allegedlyunderestimated.

Figure 6. Consumption rate (as percentage ofphytoplankton biomass) by Sida crystallina and bylittoral and pelagic free-swimming filter feeders inthe different zones of the Typha angustifolia stand(II). The calculations follow the method introducedby Jeppesen et al. 1994.

Another clear effect on zooplanktonprovided by emergent macrophytes inturbid conditions is reduced concentrationsof suspended solids, indicated by theenhanced light conditions among thevegetation (II). Emergent macrophytes can

Free-swimming filter feeders

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August SeptemberJune July

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21

reduce resuspension to one fifth comparedto unvegetated areas (IV). This isremarkable since high concentrations ofsuspended solids can reduce fecundity andsurvivorship of cladocerans via reducedingestion rates of phytoplankton cells(Gliwicz & Rybak 1976).

4.2.2 Importance of lake trophy in diurnaldistribution of zooplankton

To avoid predators, many cladocerans seekrefuge during the day, i.e. performhorizontal migration within macrophytebeds (Walls et al. 1990). As previousstudies showed clear refuge providance ofemergent vegetation in turbid conditions(II), the effect of lake trophy (turbidhypertrophic and less turbid, mesotrophic)(Table 1) on diel migration patterns ofzooplankton (III) was further studied. Thetwo areas studied, Kirkkojärvi basin andIsontalonselkä basin, had differentcladoceran assemblages, both in respect ofspecies composition and diel communitystructure. In the turbid Kirkkojärvi basin,diel changes in cladoceran assemblageswere observed in the form of nocturnalpeaks both in density (III) (Fig. 7) andbiomass (Fig. 8).

Kirkkojärvi basin

Cladocera

0

10

20

30

Inner Edge Outer

Ind.

l-1

Isontalonselkä basin

Cladocera

0

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Day Night

Figure 7. Mean total cladoceran densities during theday and night sampling in the three zones of theemergent vegetation stands of Kirkkojärvi andIsontalonselkä basins (vertical bars indicate SDvalues) (III).

These day-night differences were primarilydue to the prevailing cladocerans,Limnosida frontosa (Sars), Diaphanosoma

brachyurum, Sida crystallina, and mostlyplant-associated chydorids (III). InIsontalonselkä basin, with distinctivelyclearer water, the emergent stand seemedinsufficient to provide refugia forzooplankton or induce diel migration,indicated by highest cladoceran densitiesduring the day (III) (Fig. 7). This beingmostly due to the daytime peak in free-swimming filterers (Fig. 8), namely,Daphnia spp. (III).

Figure 8. Total cladoceran carbon biomass (top) andbiomass of free-swimming filter feeders (bottom) inthe three zones of the emergent stands ofKirkkojärvi and Isontalonselkä basins (vertical barsindicate SD values) during three sequential days(III).

According to the study by Smiley andTessier (1998), YOY fish, congregatingwithin the vegetation during the day, mayresult in opposite diurnal migration, i.e.cladocerans moving into open water duringthe day and into vegetation during night.The reverse horizontal migration (nocturnalaggregation among vegetation) among thelarge-sized cladocerans, Limnosida frontosaand Sida crystallina, in Kirkkojärvi basin(III) (Fig. 9) suggested that even in turbidlakes fish may have a significant role inregulating zooplankton communities(Gliwicz 1986).

Since in Kirkkojärvi basin dense schools ofsmall fish seek refugia within thevegetation from piscivores during the day

Kirkkojärvi basinCladocera

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µg

Cl-1

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µgC

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Inner Edge Outer

22

(unpublished), large-sized zooplankton mayreciprocally concentrate into the pelagic(Walls et al. 1990). Sida crystallina was theonly cladoceran in which night-time densitypeaks were observed in both Kirkkojärviand Isontalonselkä basins (III). Thesecoinciding peaks, with highest densities atthe edge zone (III), support previousfindings that Sida crystallina actively usesthe edge of macrophyte beds, stayingattached to plants during the day, but isfree-swimming at night, performing dielhorizontal movement (Fairchild 1981,Vuille 1991). In Kirkkojärvi basin,Limnosida frontosa, on the contrary to Sidacrystallina, migrated from the inner zoneout into the pelagic (III) (Fig. 9), this beingin harmony with the more limnetic natureof the species.

Figure 9. Percentage of the (a) Limnosida frontosaand (b) Sida crystallina populations during day-night sampling in the three zones of the emergentvegetation stand of Kirkkojärvi basin during threesequential days (III).

In Isontalonselkä basin, the clearlypredominating cladoceran was Daphnia sp.,showing ´shore avoidance` (Hutchinson1967) by aggregating in the open waterboth night and day (III). This behaviour of

cladocerans may be induced by severaldifferent mechanisms. Macrophytes serveas a habitat for invertebrate predators(Kornijów & Kairesalo 1994) and severalfish species (Boikova 1986, Lauridsen et al.1999) that constitute a predation risk tolarge-bodied zooplankton, inducingconcentration in open water. Furthermore,YOY fish, feeding primarily onzooplankton, may be aggregated withinmacrophyte stands either on a diel(Gauthier & Boisclair 1997) or a seasonalbasis (Whiteside 1988, Hall & Rudstam1999). The daytime cladoceran densitypeak, observed in the outer zone ofIsontalonselkä basin (III) (Fig. 8), is incontrast with findings in the Kirkkojärvibasin and other shallow eutrophic lakes(Lauridsen & Buenk 1996, Lauridsen et al.1996, Jeppesen et al. 1997), wherecladocerans aggregate near macrophytestands during day and are pelagic duringnight, but again in harmony withobservations by Lauridsen et al. (1999)from mesotrophic lakes. According toJeppesen et al. (1997) and Stansfield et al.(1997), macrophyte density is a criticalfactor for the efficiency of the beds aszooplankton refuge. Since there was nonotable difference in the macrophytedensities between the two basins (III), thedistinctively more transparent water inIsontalonselkä basin may abate thesufficiency of emergent macrophytes asrefugia for zooplankton.

4.2.3 Effect of a phytoplankton bloom onzooplankton assemblage

Contradictory to preceding observations inKirkkojärvi basin (II), no clear refugeeffect, i.e. aggregation within the emergentstand was detected in the diurnaldistribution study (III), conceivably due tothe ongoing cyanobacterial bloom. Thesuppressing impact of phytoplankton,leading to cladocerans avoidingunpropitious conditions clearly overruledthe refuge effect. In Kirkkojärvi basin,typical small-sized “midsummer”

Limnosida

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%

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23

cladocerans Diaphanosoma brachyurum,Ceriodaphnia quadrangula and Chydorussphaericus (O.F. Müller) (Manuljova1964), benefiting together with Bosminalongirostris from high concentrations ofsmall-sized suspended material in the water(Gliwicz 1977), normally compose most ofthe biomass of the free-swimming filterfeeders (II). High concentrations offilamentous phytoplankton can largelyexplain the scarcity of cladocerans, e.g.Daphnia spp. is known to decline duringalgal blooms as filamentous algaemechanically inhibit the filtration processes(Gliwicz 1990).

In addition, the low density of filter feedingzooplankton (III) can be the consequenceof elevated pH (Fig. 10) (Jeppesen et al.1990), since most, particularly smallcladocerans, i.e. Bosmina longirostris(Hansen et al. 1991) and Ceriodaphniaquadrangula (O`Brien & De Noyelles1972), are noted to suffer from pH valuesapproaching 10. Furthermore, a typicallittoral predator, Polyphemus pediculus(L.), normally abundant among theemergent stands in Kirkkojärvi basin (II),was absent during the study (III), beingconcomitant with the species vulnerabilityto high pH (Beklioglu & Moss 1995). Therole of a dominant cladoceran incyanophyte-plagued Kirkkojärvi basin (III)indicates that Diaphanosoma brachyurum,besides being better adapted to mineralturbidity than other crustacean zooplankters(Hart 1988, Koening et al. 1990) and ableto utilize organically enriched, suspendedclay as food resource (Cuker & Hudson1992) is comparatively tolerant to themechanical inhibition by filamentous algae.On the other hand, stressed increase in thefree-swimming filter feeder densities,coinciding with the decreased pH (III),suggests sensibility to high pH. A smallerdifference in the two nocturnal densitypeaks in differing pH environments,compared with other filtrating cladocerans(III), suggests that Sida crystallina, isconceivably not as sensitive to elevated pH.

However, due to widespread nymphaeidstands, Sida crystallina is one of thedominating cladocerans in Kirkkojärvibasin, and the notably smaller densitiescompared to previous studies (II) thereforestress the overall suppressing effect of thephytoplankton bloom (III), as large filterfeeders are noted to be most vulnerable tofilamentous algae (Dawidowicz 1990). Inaddition, pH values above 9.5 or 10 mayimpair fish activity whilst the activity oflarge filter feeding cladocerans maycontinue up to pH values about one unithigher (Beklioglu & Moss 1995).Underlined reverse movement byLimnosida frontosa and Sida crystallinaduring our study when pH dropped to 6(III) supports the argument ofsimultaneously increased predation bysmall fish.

Figure 10. Effect of increased pH on cladocerandensity in Kirkkojärvi basin, during a cyanophytebloom (III).

4.3 Role of emergent and submergedspecies in sediment dynamics

4.3.1 Impact on sediment resuspension

The importance of macrophytes in sedimentresuspension of a shallow turbid lake wasstudied by investigating submerged andemergent life forms and comparing theobtained resuspension results. Theresuspension values in Kirkkojärvi (5 - 37 gm-2 d-1) fell within the limits reported fromother lakes (Evans 1994). In our studies, onaverage, the submerged vegetation (mixed

0

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doce

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nsity

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.l-1

)

24

stand of Ranunculus circinatus,Ceratophyllum demersum and Potamogetonobtusifolius; PVI max. 30%) (V) reducedresuspension rate by 10.9 g m-2 DM and thenearby stand of the emergent Typhaangustifolia (IV) (10-22 stems m-2) wasestimated to be on the same level (9.7 -16.4 g m-2 DM).

The resuspension rate measured during thestudy conducted among the submergedmacrophytes (V) (83 d) constituted to 1701g m-2 DM of sediment in the outer zone and793 g m-2 DM in the inner zone. Thedifference between the two zones increasedin the course of the summer together withthe growing macrophyte density. DuringJune, the resuspension rate in the inner zonewas >60% and in August <20% of that inthe outer zone (V) (Fig. 11). Corroboratingthe conclusions by Dieter (1990), theresults from Kirkkojärvi demonstrated thatthe rate of resuspension can also besubstantially reduced by emergentmacrophytes (IV). During 12-26 May, theresuspension rates in the inner zone and atthe edge were 76% and 93% of that in theouter zone, respectively. In the course ofthe summer, the differences increased and,during 21 July - 3 August, thecorresponding numbers were 18% (IV)(Fig. 11) and 51%.

Figure 11. Percentage of resuspension (g m-2 d-1

DM) in the inner zone from the resuspension of theouter zone of both submerged and emergentvegetation stands.

During 9 - 23 June, the resuspension rate inthe inner zone was temporarily elevated.This was due to a peak in the effects ofwaves originating from wind blowingexceptionally from the north-east, adirection having the highest effective fetch.During the study period, 2210 g m-2 DM ofsediment was resuspended in the outer zoneof emergent macrophytes, whereas at theedge and in the inner zone, thecorresponding numbers were 1414 and 858g m-2 DM (IV), respectively.

Both macrophyte life forms, submerged (V)and emergent (IV), remarkably reduced theconcentration of suspended solids withinthe vegetations. The close agreement ofresuspension values and suspended solidconcentrations suggests that in Kirkkojärviresuspension was a continuous process, asis common in shallow water areas, exceptfor periods of ice cover (Evans 1994). Noclear dependence of resuspension rate onwind speed or wave height was observed,suggesting that moderate wave heightswere enough to cause resuspension(Bengtsson et al. 1990) and thatresuspension was caused by multiplefactors including benthivorous fish(Breukelaar et al. 1994) and wavesgenerated by boat traffic (Yousef et al.1980). In Kirkkojärvi, boat traffic isfrequent and benthivorous fish speciesmake up 65% of the catches ofexperimental nettings (Vinni et al. 2000).

Measurement of sediment resuspension isdifficult even at favorable conditions(Bloesch 1994, Evans 1994). In the littoralzone of Kirkkojärvi, the organic content ofseston and surface sediment differedsignificantly, facilitating the use of themethod by Gasith (1975). The closeagreement with the resuspension ratesobtained in emergent (IV) and submerged(V) studies also emphasize the goodrepeatability of the measurements. Becauseof the decreased water turbulence withinthe traps, studies with sediment trapsusually result in higher sedimentation

0

20

40

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%

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Submerged

JUNE AUGUST

25

compared with mass balance calculations(Kozerski 1994). Traps measure the upperlimit of the average resuspension rateduring the exposure time of the trap(Kozerski 1994). Thus, the present resultsprobably represent maximum values ofsedimentation and resuspension inKirkkojärvi. The exposure time of the trapswas within the limits recommended forexperiments on settling fluxes for organicmaterial (Bloesch & Burns 1980).

4.3.2 Importance in phosphorus reduction

From the resuspension study conductedamong submerged and emergentvegetation, calculations for phosphorusresuspension and retention were alsoperformed. In the study conducted amongsubmerged vegetation (V), with theresuspended sediment, 2.0 g m-2 P wasbrought into the water column in the outerzone and 0.98 g m-2 P in the inner zone.Submerged plants thus reduced the internalloading of total P by 12 mg m-2 per day. Inthe emergent vegetation investigation (IV),3.3 g m-2 P was brought to the watercolumn in the outer zone, 1.9 g m-2 P at theedge and 1.1 g m-2 P in the inner zone.Thus, compared with open water areas, thestem density at the edge reduced theinternal loading of total P by 16.7 mg m-2 d-

1 and the density in the inner zone by 26.2mg m-2 d-1.

In Kirkkojärvi, the present area ofsubmerged stands is ca. 15 ha and ofemergent macrophytes (mainly T.angustifolia and T. latifolia) approximatelythe same ca. 16.6 ha (unpublished). Thus,during the study period submergedvegetation retained approximately 150 kg(V) and emergent macrophytes 232 kg(edge) -365 kg (inner zone) (IV) ofphosphorus, adding up to a total of ca. 747kg phosphorus, which would otherwisehave been transported into the watercolumn. The helophytes do not senesceuntil late September. By applying theobserved average daily P resuspensionvalues in each emergent zone for a six-

month open-water season, the emergentstands in Kirkkojärvi can be estimated toannually retain 510-800 kg P, whichcorresponds to 6-10 % of the currentexternal P loading (Tallberg et al. 1999).

The inverse relationship between suspendedsolids and SRP in the inner zone ofsubmerged macrophytes (V) suggested thatresuspended particles adsorbed phosphorusfrom the water. In the outer zone, no sign ofsuch an effect was found. In all the zones ofthe emergent investigation (IV), the effectof SS on SRP was non-significant,corroborating the results by Søndergaard etal. (1992). Thus, SRP release fromresuspended sediment is not governed bythe amount of suspendoids in the water butrather by SRP concentration in the waterduring resuspension. Resuspended particlescan either adsorb phosphorus from thewater or release it, depending on their Psaturation level. The concentration of SRPin the pelagic zone of Kirkkojärvi increasedsteeply in late July (from below 10 µg l-1 toabove 40 µg l-1, unpublished), suggestingan increased availability of P towards latesummer. It can be concluded that when theconcentration of SRP in the water ofKirkkojärvi is low, resuspension releasesSRP from the sediment to the water, therelease rate being (due to higherresuspension rate) substantially higher inopen water areas than in areas covered bymacrophytes.

4.4 Implications of fish herbivory

The gut content of rudd during themacrophyte growing season was studied toinvestigate the volume of plant grazing.The diet of all studied rudd (VI) containedanimal remains, plant material and detritus(Fig. 12), being congruent with the speciesomnivorous feeding habits (Niederholzer &Hofer 1980). The highest macrophyteconsumption in the beginning and end ofsummer (VI) was related to the biomasspeak of macrophytes in late summer, butalso to the absence of animal food. Rudd is

26

not very active in selecting food, and on thecontrary, utilizes majority of the suitable-sized submerged species, occurring inadequately high densities (Prejs &Jackowska 1978). In Kirkkojärvi, thesubmerged macrophyte community iscompounded of a mixed vegetation of e.g.Potamogeton obtusifolius, Sparganiumemersum, Ranunculus circinatus,bryophytes and also occasional massoccurrences of filamentous algae (I), allbeing well represented in the rudd diet (VI)(Fig. 12). Some species, such as submergedMyriophyllum verticillatum, pleustophyticCeratophyllum demersum, and nymphaeids,forming high biomasses in the littoral ofKirkkojärvi (I), were nevertheless absent inrudd guts (VI).

Figure 12. Volume percentage composition of thediet of different rudd age groups. Total number ofanalysed fish in each time period is shown inparentheses. On the left hand side, rudd diet dividedinto plant material, detritus and animal material(zoo). On the right, plant material divided into morespecific categories (VI).

Also, Prejs & Jackowska (1978) and vanDonk & Otte (1996) found a highpreference of rudd for Elodea andPotamogeton but avoidance of, chemicallyand mechanically inconvenient,Myriophyllum and Ceratophyllum. Thefeeding habits observed were, therefore,rather due to the distribution and densitiesof edible macrophytes.

The ability to consume alternate low-energy food sources, such as detritus andplant material, is one of the characteristicsof cyprinids (Michelsen et al. 1994). Fishutilize the majority of animal tissue butconsiderably less of the plant materialingested, therefore, a relevant amount ofmacrophytes must be consumed (Prejs1976, Prejs & Jakowska 1978). Also,feeding rate of rudd has been established toincrease concurrently with vegetationdensity (Peirson et al. 1985). The biomassof rudd stock in the littoral area of theKirkkojärvi basin is not known, but fallsprobably within the range of 50-100 kg ha-

1. The annual plant consumption by thestock would thus be 45-115 kg ha -1 (VI).

Herbivorous fish, such as rudd, harvestplant biomass and may influence themacrophyte species formation (van Donk &Otte 1996), but also grazing of benthic foodremobilises nutrients stored in the sedimentand plant biomass, accelerating internalloading (Hansson et al. 1987, Horppila1999). In addition, the effect of a strongrudd population in a shallow lake may haveantagonistic effects; on the other hand,accelerating turbidity by bottom dwelling,but also enhancing macrophyte growth byconsumption of young shoots (Prejs 1984,van Donk & Otte 1996), which in turnreduce resuspension (V). In the studiedKirkkojärvi basin, partly selective grazingand partly upholding of turbidity and highnutrient levels by bottom dwelling,conceivably promotes the inedible andpleustophytic macrophyte growth form,which has increased in Kirkkojärvi duringthe past decades (I).

May-June(n=175)

0 %

20 %

40 %

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100 %

2 3 4 5 6 7 >7

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0 %

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2 3 4 5 6 7 >7

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2 3 4 5 6 7 >7

Age group (y)

Plant Detritus Zoo

2 3 4 5 6 7 >7

Plant detritusPlant seedRanunculus circinatusSparganium emersumPotamogeton obtusifoliusBryophytaFilamentous algae

2 3 4 5 6 7 >7

2 3 4 5 6 7 >7

27

5. CONCLUSIONS

In a clay-turbid water body, an inherentlyscarce submerged macrophyte compositionmay prevail, therefore drastic changes inthe species and life form composition dueto decrease in the trophic state of the lakeor increase of (phytoplankton-induced)water transparency are not necessary likely.In such lakes, the stabilizing and structuralrole of other life forms besides submergedvegetation, e.g. emergent and floating-leaved, may be seriously overlooked. Theenvironmental premiss provided by highbackground concentrations of suspendedinorganic particles may provide a newperspective for the function of vegetation inturbid lakes.

As detected in this thesis, in clay-turbideutrophic conditions emergent vegetationappears to play an important role in theseasonal regulation of zooplankton byproviding refuge for especially free-swimming cladocerans. The aggregationamong the vegetation resembles the trendobserved with submerged vegetation ineutrophic lakes. In addition, emergentvegetation appear to provide prominentrefuge also for large-sized plant-associatedspecies, such as Sida crystallina. Thesecladocerans, occurring in considerabledensities and holding remarkablephytoplankton filtering capacities, musthave considerable water quality effectsthrough algal control. In eutrophic andturbid lakes, with scarce submergedvegetation the refuge function of emergentand, also floating-leaved, life forms maytherefore be prominent. In such lakes, withhigh predation pressure by fish and thequite low total zooplankton biomass, theimportance of these life forms may beemphasized.

The differences in total cladoceran densityand behaviour, as well as dissimilar speciescomposition, in the study areas of differingtrophy suggest that emergent stands inmesotrophic conditions, in contrast to

eutrophic and more turbid circumstances,might not provide adequate refuge for filterfeeders to induce diurnal horizontalmigration among the vegetation.

Although the studies in this thesis detectedthat emergents encourage zooplanktonaggregation within vegetation in turbid andeutrophic conditions, it appears that heavyphytoplankton blooms overshadow thiseffect directly, through mechanicalenhancement, as well as indirectly, viaelevated pH, influencing the proportionalcomposition and diurnal distribution oflittoral zooplankton.

Wind-induced water movements maydetermine whether the littoral zone acts as asink or a source of nutrients for the pelagicsystem. The results in this thesisdemonstrated that sediment resuspensionand the consequent increase in inorganicwater turbidity and internal loading ofphosphorus may be substantially reducedby macrophytes, both submerged andemergent life forms. In clay-turbid lakeswith low submerged vegetation density,emergent macrophytes were discovered tobe substantial in reducing phosphoruscycling from the sediment. In addition,owing to a longer growing season thansubmerged species, emergent vegetationcontribute to considerable water qualityeffects.

In turbid and shallow eutrophicated lakeswith low submerged biomass and fewdominating species, herbivory by fish mayhave an influence on the speciescomposition of submerged vegetation. Fish,as rudd in this study, is a quite omnivorousfeeder, grazing on any edible and suitable-sized plants. A rudd population alone is notlikely able to consume adequate quantitiesto alter the proportions of different speciessince herbivory also enhances growth ofnew shoots. However, as this thesisindicates, partly selective grazing and partlyupholding of turbidity and high nutrientlevels by bottom dwelling, conceivably

28

promotes the inedible and pleustophyticmacrophyte growth form.

The establishment of submergedmacrophyte stands is often considered to becrucial for restoration of shallow lakes butthe effects of e.g. emergents are not sooften recognized. On the contrary,emergent and floating-leaved life forms areoften considered less important in the lakerestoration viewpoint, in fact they are oftenrecommended to be harvested, to removenutrients or to improve the recreationalpossibilities of the lake. This thesishowever, highlights the importance of theseundermined macrophytes to water quality.They are important in many aspects ofrestoration - not only when removed - butalso when retained. In this thesis, emergentvegetation has been shown to reducesediment-induced turbidity and nutrientcycling, as well as to provide refuge forphytoplankton grazing zooplankton(phytoplankton-induced turbidity). In thisrespect, emergent and presumably alsofloating-leaved stands are important factorsin terms of water quality, especially in clay-turbid lakes with inherently scantysubmerged vegetation. In general, thecomprehensive function of macrophytesshould be taken into more thorough accountin lake restoration schemes: recreationalexpectations and water quality aspectsshould be weighed – and preferablycombined.

6. FUTURE STUDY OUTLOOKS –Resonance of floating-leaved species

Hitherto, few studies on the food webeffects of floating-leaved species, that areoften very abundant in turbid lakecircumstances, have been conducted (e.g.Moss et al.1998). Preliminary studies inLake Hiidenvesi have demonstrated theimportance of floating-leaved Nuphar luteaas refugia for Sida crystallina, as the large-sized zooplankter are found fixed to theleaves in considerable densities, with

cladoceran abundance increasing inconcordance with leaf area (Fig. 13).

Figure 13. Relationship between leaf area offloating-leaved macrophytes (Nuphar lutea) anddensity of cladocerans (Sida crystallina) attached toleaves in Kirkkojärvi basin.

Therefore, our investigations underline theneed to study the potential refuge effect offloating-leaved macrophytes, especially forplant-associated cladocerans, in turbidconditions. According to our findings,diurnal migration on/off the leaves by Sida,is very pronounced and regular, suggestingpredator avoidance behaviour (Fig. 14).

Figure 14. Diurnal changes in the proportion ofplant-attached cladoceran, Sida crystallina, on theleaves of floating Nuphar lutea and adjacent openwater of Kirkkojärvi basin.

Floating-leaved stands are potentialharbours for prominent plant-associatedzooplankton communities (e.g. Sida),possessing considerable phytoplanktonconsumption rates as indicated also in thestudies of this thesis. In this light, floating-

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leaved stands may have considerablewhole-lake water quality effects. Thereforemore detailed investigation on the role offloating-leaved life form especially inturbid lakes should be conducted: both theimportance as refugia for zooplankton andimpact on resuspension should be clarified.In all, more thorough investigation ofinteractions and processes linked withmacrophytes related to phytoplankton-caused and inorganic turbidity should beconducted.

7. FINAL WORDS

I would like to express my gratitude to awide range of people as no woman is anisland.

The homey atmosphere of the Departmentof Limnology and EnvironmentalProtection enabled the start, process andcompletion of this work. A special andwarm debt of gratitude goes naturally to mysupervisors Pertti Eloranta and especiallyJukka Horppila, and co-authors JyrkiLappalainen, Tommi Malinen and PetraTallberg.

In addition, numerous interestingdiscussions, never-ending patience andguidance, as well as a helping hand wasalways available from a very broad field ofexpertise (not always only scientific) righthere in the department. Therefore, I want tothank my fellow citizens and companionsof destiny for these shared years: ErikaAlajärvi, Jukka Koski-Vähälä, KatriinaKönönen, Anne Liljendahl-Nurminen, JuhaNiemistö, Jaana Marttila, Zeynep Pekcan,Janne Soininen, Laura Uusitalo, AnuVäisänen and numerous anonymous. Andof coarse the “fish boys” regardless of rank:Kimmo Kahilainen, Hannu Lehtonen, KariNyberg, Heikki Peltonen, Mikko Olin,Mikko Salonen, Kari Saulamo, ArtoTolonen, Antti Tuomaala, Mika Vinni andthe rest of you Fish Folks! Jouko Sarén andRaija Mastonen were indispensable for

being responsible for laboratory work– andnot forgetting the Sirpas (Braunschweilerand Ranta-Haatanen) who – after all- keepthe world turning in our department. Ahumble Thank You to all of you.

An expression of gratitude also goes to myreviewers, Anne Ojala and HeikkiToivonen and the honourable opponent,Timo Kairesalo, who all undoubtedly put agreat deal of their time and expertise insubmerging (perhaps little emerging andfloating as well..) themselves in this thesis.

I would also like to mention my historicroots in the Department of Hydrobiology.From those times I have been enriched byespecially two valuable friendships. Thankyou for Maiju Lehtiniemi – for leading theway, and Eeva Huitu, for walking with me,and both of them for sharing numerousmoments of discussion in both scientificand not-so-scientific subject fields.

I also express my deepest gratitude to mydear family, especially my parents Ulla andKauko, and precious friends in my “civilianlife”. Thank you for making me what I amand sharing this fascinating journey calledlife with me. Your patience and presenceenabled this work –without dispute. I wouldalso like to mention my four-legged friendsthat come in all shapes and sizes: sincerejoy givers and stress killers of the best kind.

The studies in this thesis were funded bythe Academy of Finland, Alfred KordelinFoundation, Finnish Environment Instituteand the University of Helsinki. All theseinstances are greatly appreciated.

Lastly, I want to thank Nature itself forbeing such an intriguing horn of plenty forall little scientists to explore. After all - it’sthe small drops that mount up to a lake.

Finally- the final drop.

30

8. REFERENCES

Andersson, G., Granéli, W. & Stenson, J.,1988. The influence of animals onphosphorus cycling in lake ecosystems.Hydrobiologia, 170, 267-284.

Bagenal, T.B. & Tesch, F.W., 1978. Age andgrowth. In: W. Ricker (ed.), Methods forassessment of fish production in fresh waters,IPB Handbook 3 Blackwell, Oxford, 131-165.

Bailey, R. C., 1988. Correlations betweenspecies richness and exposure: freshwatermolluscs and macrophytes. Hydrobiologia, 162,183-191.

Barko, J.W. & Smart, R.M., 1980. Mobilizationof sediment phosphorus by submersedfreshwater macrophytes. Ecol. Monogr., 51,219-238.

Barko, J.W. & James, W.F., 1998. Effects ofsubmerged aquatic macrophytes on nutrientdynamics, sedimentation and resuspension. In:E. Jeppesen, Ma. Søndergaard, Mo.Søndergaard, & K. Christoffersen (eds.), Thestructuring role of submerged macrophytes inlakes, Ecological Studies, Springer Verlag, NewYork, 131, 197-214.

Beklioglu, M. & Moss, B., 1995. The impact ofpH on interactions among phytoplankton algae,zooplankton and perch (Perca fluviatilis) in ashallow, fertile lake. Freshw. Biol., 33, 497-509.

Bengtsson, L., Hellström, T. & Rakoczi, L.,1990. Redistribution of sediment in threeSwedish lakes. Hydrobiologia, 192, 167-181.

Bloesch, J., 1994. A review of methods used tomeasure sediment resuspension. Hydrobiologia,284, 13-18.

Bloesch, J. & Burns, N.M., 1980. A criticalreview of sediment trap technique. Schweiz.Hydrol., 42, 15-56.

Boikova, O.S., 1986. Horizontal distribution ofcrustaceans in Lake Glubokoe. Hydrobiologia,141, 113-123.

Breukelaar, A.W., Lammens, E.H.R.R. &Breteler, J.G.P.K., 1994. Effects of benthivorousbream (Abramis brama) and carp (Cyprinuscarpio) on sediment resusupension andconcentrations of nutrients and chlorophyll-a.Freshw. Biol., 32, 113-121.

Canfield, D.E. Jr., Shireman, J.W., Colle, D.E.,Haller, W.T., Watkins, C.E. & Maceina, M.J.,1984. Prediction of chlorophyll a concentrationsin Florida lakes: importance of aquaticmacrophytes. Can. J. Fish. Aquat. Sci., 41, 497-501.

Carpenter, S. & Lodge, D., 1986. Effects ofsubmersed macrophytes on ecosystemprocesses. Aquat. Bot., 26, 341-370.

Carpenter, S.R., Kraft, C.E., Wright, R.A., He,X., Soranno, P.A. & Hodgson, J.R., 1992.Resilience and resistance of a lake phosphoruscycle before and after food web manipulation.Am. Nat., 140, 781-798.

Chambers, P.A., 1987. Light and nutrients in thecontrol of aquatic plant community structure: II.In situ observations. J. Ecol., 75, 621-628.

Chambers, P.A. & Kalff, J., 1985. Depthdistribution and biomass of submerged aquaticmacrophyte communities in relation to Secchidepth. Can. J. Fish. Aquat. Sci., 42, 701-709.

Christensen, K.K. & Andersen, F.Ø., 1996.Influence of Littorella uniflora on phosphorusretention in sediment supplied with artificialporewater. Aquat. Bot., 55, 183-197.

Crowder, L.B. & Cooper, W.E., 1982. Habitatstructural complexity and their interactionbetween bluegills and their prey. Ecology, 63,1802-1813.

Cryer, M., Peirson, G. & Townsend, C.R., 1986.Resiprocal interactions between roach (Rutilusrutilus (L.)) and zooplankton in a small lake:

31

prey dynamics and fish growth and recruitment.Limnol. Oceanogr., 31, 1022-1038.

Cryer, M. & Townsend, C.R., 1988. Spatialdistribution of zooplankton in a shalloweutrophic lake, with a discussion of its relation tofish predation. J. Plankton Res., 10, 487-501.

Cuker, B.E. & Hudson, L. Jr., 1992. Type ofsuspended clay influences zooplankton responseto phosphorous loading. Limnol. Oceanogr.,37(3), 566-576.

Cummins, W.C. & Wuycheck, J.C., 1971.Caloric equivalents for investigations inecological energetics. Mitt. Int. Verein. Limnol.18. 318 pp.

Dale, H.M., 1986. Temperature and light: thedetermining factor in maximum depthdistribution of aquatic macrophytes in Ontario,Canada. Hydrobiologia, 133, 73-77.

Dawidowicz, P., 1990. Effectiveness ofphytoplankton control by large-bodied andsmall-bodied zooplankton. Hydrobiologia,200/201, 43-47.

Davies C. J., 1985. Evidence for a diurnalhorizontal migration in Daphnia hyalinalacustris. Hydrobiologia, 120, 103-106.

Dieter, C.D., 1990. The importance of emergentvegetation in reducing sediment resuspension inwetlands. J. Freshw. Ecol., 5, 467-474.

Dionne, M. & Folt, C.L., 1989. An experimentalanalysis of macrophytes growth forms as fishforaging habitats. Can. J. Fish. Aquat. Sci., 48,123-131.

Duarte, C.M., Kalff, J. & Peters, R.H., 1986.Pattern in biomass and cover of aquaticmacrophytes in lakes. Can. J. Fish. Aquat. Sci.43, 1900-1908.

Evans, R.D., 1994. Empirical evidence of theimportance of sediment resuspension in lakes.Hydrobiologia, 284, 5-12.

Fairchild, G.W., 1981. Movement andmicrodistribution of Sida crystallina and otherlittoral microcrustacea. Ecology, 62, 1341-1352.

Gasith, A., 1975. Tripton sedimentation ineutrophic lakes – simple correction for theresuspended matter. Verh. Int. Ver. Limnol., 19,116-122.

Gauthier, S. & Boisclair, D., 1997. The energeticimplications of diel onshore-offshore migrationby dace (Phoxinus eos × P. neogaetus) in a smalloligotrophic lake. Can. J. Fish. Aquat. Sci., 54,1996-2006.

Gliwicz, Z.M., 1977. Food size selection andseasonal succession of filter feeding zooplanktonin an eutrophic lake. Ekol. pol., 25, 179-225.

Gliwicz, Z.M., 1986. Predation and theevolution of vertical migration in zooplankton.Nature, 320, 746-748.

Gliwicz, Z.M., 1990. Why do cladocerans fail tocontrol algal blooms? Hydrobiologia, 200/201,83-97.

Gliwicz, Z.M. & Rybak, J. I., 1976.Zooplankton. In: E. Pieczynska (ed.), Selectedproblems of lake littoral ecology, Warsaw;University of Warsaw, 69-96.

Granéli, W. & Solander, D., 1988. Influence ofaquatic macrophytes on phosphorus cycling inlakes. Hydrobiologia, 170, 245-266.

Grimms, M.P., 1983. Regulation of biomassesof small (<41 cm) northern pike (Esox lucius L.)with special reference to the contribution ofindividuals stocked as fingerlings (4-6 cm). Fish.Manag., 14, 115-133.

Hall, S.R. & Rudstam, L.G., 1999. Habitat useand recruitment: a comparison of long-termrecruitment patterns among fish species in ashallow eutrophic lake, Oneida lake, NY. U.S.A.Hydrobiologia, 408/409, 101-113.

Hammer, C., 1985. Feeding behaviour of roach(Rutilus rutilus) larvae and the fry of perch

32

(Perca fluviatilis) in Lake Lankau. Arch.Hydrobiol., 103, 61-74.

Hansen, A.-M., Christensen, J.V. & Sortkjaer,O., 1991. Effect of high pH on zooplankton andnutrients in fish-free enclosures. Arch.Hydrobiol., 123, 143-164.

Hanson, M.A. & Butler, M.G., 1994. Responsesof plankton, turbidity and macrophytes tobiomanipulation in a shallow prarie lake. Can. J.Fish. Aquat. Sci., 51, 1180-1188.

Hansson, L.-A., Johansson, L. & Persson, L.,1987. Effect of fish grazing on nutrient releaseand succession of primary producers. Limnol.Oceanogr., 32, 723-729.

Hart, R.C., 1988. Zooplankton feeding rates inrelation to suspended sediment content: Potentialinfluences on community structure in a turbidreservoir. Freshw. Biol., 19, 123-139.

Heck, K.L. & Crowder, L.B., 1991. Habitatstructural complexity and predator-preyinteractions in vegetated aquatic systems. In: S.S.Bell, E.D. Mcoy & H.R. Mushinsky (eds.),Habitat structure: the physical arrangement ofobjects in space, Chapman & Hall, London,281-299.

Hewett, S.W. & Johnson, B.L., 1992. A fishbioenergetics model 2, an upgrade of ageneralized bioenergetics model for fish growthfor microcomputers. UW Sea Grant TechnicalReport No. WIS-SG-92-250.

Horppila, J., 1999. Diel changes in dietcomposition of an omnivorous cyprinid - apossible source of error in estimating foodconsumption. Hydrobiologia, 400, 33-39.

Horppila, J. & Nyberg, K., 1999. The validity ofdifferent methods in the back-calculation of thelengths of roach – a comparison between scalesand cleithra. J. Fish Biol., 54, 489-498.

Horppila, J. & Peltonen, H., 1997. Abioenergetics approach on food consumption of

roach (Rutilus rutilus (L.)) in a eutrophic lake.Arch. Hydrobiol., 139, 207-222.

Hutchinson, G.E., 1967. A treatise on limnology.II. Introduction to lake biology and thelimnoplankton. John Wiley & Sons Inc, NewYork, 1115 pp.

Håkanson, L. & Jansson, M., 1983. Principles ofLake Sedimentology. Springer-Verlag, Berlin,316 p.

Irvine, K., Moss, B. & Stansfield, J., 1990. Thepotential of artificial refugia for maintaining acommunity of large-bodied Cladocera againstfish predation in a shallow eutrophic lake.Hydrobiologia, 200-201, 379-390.

Ivanova, M.B. & Klekowski, R.Z., 1972.Respiratory and filtration rates in Simocephalusvetulus (O.F. Müller) (Cladocera) at differentpH. Pol. Arch. Hydrobiol., 19, 303-318.

Jacobsen, L., Perrow, M.R., Landhildehus, F.,Hjørne, M., Lauridsen, T.L. & Berg, S., 1997.Interactions between piscivores, zooplanktivoresand zooplankton in submerged macrophytes:preliminary observations from enclosures andpond experiments. Hydrobiologia, 342/343, 197-205.

Jeppesen, E., Jensen, J.P., Søndergaard, M.,Lauridsen, T., Pedersen, L.J. & Jensen, L., 1997.Top-down control in freshwater lakes: the role ofnutrient state, submerged macrophytes and waterdepth. Hydrobiologia, 342/343, 151-164.

Jeppesen, E., Lauridsen, T.L., Kairesalo, T. &Perrow, M., 1998. Impact of submergedmacrophytes on fish-zooplankton interactions inlakes. In: E. Jeppesen, Ma. Søndergaard, Mo.Søndergaard, & K. Christoffersen (eds.), Thestructuring role of submerged macrophytes inlakes, Ecological Studies, Springer Verlag, 131,91-114.

Jeppesen, E., Søndergaard, M., Kanstrup, E.,Petersen, B., Eriksen, R., Hammerstøh, M.,Mortensen, E., Sortkjaer, O. & Olrik, K., 1994.Does the impact of nutrients on the biological

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structure and function of brackish andfreshwater lakes differ? Hydrobiologia, 275/276,15-30.

Jeppesen, E., Søndergaard, M., Sortkjær, O.,Mortensen, E. & Kristensen, P., 1990.Interactions between phytoplankton,zooplankton and fish in a shallow, hypertrophiclake: A study on phytoplankton collapses inLake Søbygård, Denmark. Hydrobiologia, 191,149-164.

Jeppesen, E., Sortkjaer, O., Søndergaard, M. &Erlandsen, M., 1992. Impact of a trophic cascadeon heterotrophic bacterioplankton production intwo shallow fish-manipulated lakes. Arch.Hydrobiol. Beih. Ergebn. Limnol., 37, 219-231.

Kairesalo, T., Kornijów, R. & Luokkanen, E.,1998. Trophic cascade structuring a planktoncommunity in a strongly vegetated lake littoral.In: M. Scheffer (ed.), Ecology of shallow lakes.Population and community biology series 22,Chapman & Hall, London, 357.

Kerfoot, C.W., Levitan, C. & DeMott, W.R.,1988. Daphnia-phytoplankton interactions:density-dependent shifts in resource quality.Ecology, 69, 1806-1825.

Kirk, J.T.O. 1985. Effects of suspendoids(turbidity) on penetration of solar radiation inaquatic ecosystems. Hydrobiologia, 125, 195-208.

Kirk, J.T.O. 1994. Light and photosynthesis inaquatic ecosystems. Cambridge UniversityPress, Cambridge.

Kitchell, J.F., Stewart, D.J. & Weininger, D.,1977. Applications of a bioenergetics model toyellow perch (Perca flavescens) and walleye(Stizostedion vitreum vitreum). J. Fish. Res. Bd.Can., 34, 1922-1935.

Koening, J.P., Burkett R.D. & Edmundson,J.M., 1990. The exclusion of limnetic Cladocerafrom turbid glacier-meltwater lake. Ecology, 71,57-67.

Kornijów, R. & Kairesalo, T., 1994. Elodeacanadensis sustains rich environment formacroinvertebrates. Verh. Int. Ver. Limnol., 25,2270-2275.

Kozerski, H.-P., 1994. Possibilities andlimitations of sediment traps to measuresedimentation and resuspension. Hydrobiologia,284, 93-100.

Kraft, C.E., 1992. Estimates of phosphorusand nitrogen cycling by fish using abioenergetics model. Can. J. Fish. Aquat.Sci., 49, 2596-2604.

Kufel, L. & Ozimek, T., 1994. Can Characontrol phosphorus cycling in Lake Lukanjo(Poland)? Hydrobiologia, 275/276, 277-283.

Lammens, E.H.R.R., 1989. Causes andconsequences of the success of bream in Dutcheutrophic lakes. Hydrobiol. Bull., 23, 11-18.

Lampert, W., 1988. The relationship betweenzooplankton biomass and grazing: a review.Limnologica 19, 11-20.

Lauridsen, T.L. & Buenk, I., 1996. Diel changesin the horizontal distribution of zooplankton inthe littoral zone of two shallow eutrophic lakes.Arch. Hydrobiol., 137, 161-176.

Lauridsen, T., Jeppesen, E., Mitchell, S.T.,Lodge, D.M. & Burks, R.L., 1999. Diel variationin horizontal ditribution of Daphnia andCeriodaphnia in oligotrophic and mesotrophiclakes with contrasting fish densities.Hydrobiologia, 408/409, 241-250.

Lauridsen, T.L., Jeppesen, E., Søndergaard, M.& Lodge, D., 1997. Horizontal migration ofzooplankton: Predator-mediated use ofmacrophyte habitat. In: E. Jeppesen, Ma.Søndergaard, Mo. Søndergaard, & K.Christoffersen (eds.), The structuring role ofsubmerged macrophytes in lakes, EcologicalStudies, Springer Verlag, New York, 131, 233-239.

34

Lauridsen, T.L., Pedersen, J.L., Jeppesen, E. &Søndergaard, M., 1996. The importance ofmacrophyte bed size for cladoceran compositionand horizontal migration in a shallow lake. J.Plankton Res., 18, 2283-2294.

Lehtovaara, A. & Sarvala, J., 1984. Seasonaldynamics of total biomass and speciescomposition of zooplankton in the littoral of anoligotrophic lake. Verh. Int. Verein. Limnol., 22,805-810.

Lodge D.M., 1991. Herbivory of freshwatermacrophytes. Aquat. Bot., 41, 195-224.

Luecke, C., Vanni, M.J, Magnuson, J.J.,Kitchell, J.F. & Jacobson, P.J., 1990. Seasonalregulation of Daphnia populations byplanktivorous fish: Implications for theclearwater phase. Limnol. Oceanogr., 35, 1718-1733.

Luokkanen, E., 1995. Vesikirppuyhteisön lajisto,biomassa ja tuotanto, Vesijärven Enonselällä.Helsingin yliopiston Lahden tutkimus- jakoulutuskeskuksen raportteja ja selvityksiä. 25:1-53 (in Finnish with English summary).

Luther, H., 1951. Verbreitung und Ökologie derhöheren Wasserpflanzen im Brackwasser derEkenäs-gegend in Südfinnland. I, AllgemeinerTeil, Acta Bot. Fennica, 49, 1-231.

Madsen, J.D., Chambers, P.A., James, W.F.,Koch, E.W. & Westlake, D.F., 2001. Theinteraction between water movement, sedimentdynamics and submerged macrophytes.Hydrobiologia, 444, 71-84.

Manuljova, E. F., 1964. Vetvistousye rački(Cladocera) fauny SSSR. Izdatel`stvo Nauka,Moskva-Leningrad, 327 p.

McCune, B. & Mefford, M.J., 1999. PC-ORD.Multivariate analysis of ecological data, version4, MjM Software Design, Gleneden Beach,Oregon.

Meijer, M.-L., Jeppesen, E., Van Donk, E. &Moss, B., 1994. Long-term responses to fish-

stock reduction in small shallow lakes-Interpretation of five-year results of fourbiomanipulation cases in the Netherlands andDenmark. Hydrobiologia, 276, 457-466.

Meriläinen, J. & Toivonen, H., 1979. LakeKeskimmäinen, dynamics of vegetation in asmall shallow lake. Ann. Bot. Fennici, 16, 123-139.

Michelsen, K., Pedersen, J., Christoffersen, K. &Jensen, F., 1994. Ecological consequences offood portioning for the fish population structurein a eutrophic lake. Hydrobiologia, 291, 35-45.

Middelboe, A.L. & Markager, S., 1997. Depthlimits and minimum light requirements offreshwater macrophytes. Freshw. Biol., 37, 553-568.

Moss, B., 1998. Ecology of Fresh Waters 2nd Ed,Man and Medium, Blackwell Scientific, Oxford.

Moss, B., Kornijòw, R. & Measey, G. J., 1998.The effect of nymphaeid (Nuphar lutea) densityand predation by perch (Perca fluviatilis) on thezooplankton communities in a shallow lake.Freshw. Biol., 39, 689-697.

Munsterhjelm, R. 1997. The aquatic macrophytevegetation of flads and gloes, S coast of Finland.Acta Bot. Fennica, 157, 1-68.

Niederholzer, R. & Hofer, R., 1980. The feedingof roach (Rutilus rutilus L.) and rudd (Scardiniuserythrophthalmus L.,). I. Studies on naturalpopulations. Ekol. pol., 28, 45-59.

O`Brien, W.J. & De Noyelles, F., 1972.Photosynthetically elevated pH as a factor inzooplankton mortality in nutrient rich ponds.Ecology, 53, 605-614.

Olin, M., Rask, M., Ruuhijärvi, J., Kurkilahti,M., Ala-Opas, P. & Ylönen, O., 2002. Fishcommunity structure in meso- and eutrophiclakes of southern Finland: the relativeabundances of percids and cyprinids along atrophic gradient . J. Fish. Biol., 60, 593-612.

35

Ozimek, T., Van Donk, E. & Gulati, R.D., 1990.Can macrophytes be useful in thebiomanipulaton of lakes? The Lake Zwemlustexample. Hydrobiologia, 200/201, 399-409.

Paterson, M.J., 1994. Invertebrate predation andthe seasonal dynamics of microcrustacea in thelittoral zone of a fishless lake. Arch. Hydrobiol.Suppl.,99, 1-36.

Peirson, G., Cryer, M., Winfield, I.J. &Townsend, C.R., 1985. The impact of reducednutrient loading on the fish community of asmall isolated lake, Alderfen Broad. Proceedingsfrom the 4th British Freshwater Fish Conference,Liverpool University 1985.

Persson, L., 1991. Behavioural response topredators reverses the outcome of competitionbetween prey species. Behav. Ecol. Sociobiol.,28, 101-108.

Persson, L. & Eklöv, P., 1995. Prey refugesaffecting interactions between piscivorous perchand juvenile perch and roach. Ecology, 76, 70-81.

Persson, L., Johansson, L., Andersson, G., Diehl,S. & Hamrin, S.F., 1993. Density dependentinteractions in lake ecosystems whole lakeperturbation experiments. Oikos, 66, 193-208.

Prejs, A., 1976. Fishes and their feeding habits.1. Fish fauna. Ch. IX. In: E. Pieczynska, (ed.),Selected problems of lake littoral ecology,Warsaw University Press, Warsaw, Poland, 155-179.

Prejs, A., 1984. Herbivory by temperatefreshwater fishes and its consequences. Env.Biol. Fish., 10, 281-296.

Prejs, A. & H. Jackowska, 1978. Lakemacrophytes as the food of roach (Rutilusrutilus) and rudd (Scardinius erythrophthalmus)I. Species composition and dominance relationsin the lake and the food. Ekol. pol., 26, 429-438.

Ranta, E. & Jokinen, O. 1998. Hiidenveden jaeräiden siihen laskevien vesistönosien

yhteistarkkailun yhteenveto vuodelta 1997.Julkaisu 81, Länsi-Uudenmaan Vesi – jaYmpäristö Ry, (Monitoring report on LakeHiidenvesi and adjacent waterbodies in 1997, InFinnish).

Rask, M., 1989. A note on the diet of roachRutilus rutilus L. and other cyprinids atTvärminne, northern Baltic Sea. Aqua Fennica,19, 19-27.

Reynolds, C. S., 1984. The ecology offreshwater phytoplankton. Cambridge, 384 p.

Sand-Jensen, K. & Borum, J., 1984. Epiphyteshading and is effect on photosynthesis and dielmetabolism of Lobelia dortmanna during thespring bloom in a Danish lake. Aquat. Bot., 20,109-120.

Sand-Jensen, K. & Borum, J., 1991. Interactionamong phytoplankton, periphyton andmacrophytes in temperate freshwater andestuaries. Aquat. Bot., 41, 137-175.

Sand-Jensen, K. & Søndergaard, M., 1981.Phytoplankton and epiphyte development andtheir shading effect on submerged macrophytesin lakes of different nutrient status. Int. Rev. ges.Hydrob., 66, 529-554.

Scheffer, M., 1998. Ecology of shallow lakes.Population and community biology series 22,Chapman & Hall, London, 357 p.

Scheffer, M., Hosper, S. H., Meijer, M-L. &Moss, B., 1993. Alternative equilibria in shallowlakes. TREE, 8, 275-279.

Scheffer, M., de Redelijkheid, M. R. & Noppert,F., 1992. Distribution and dynamics ofsubmerged vegetation in a chain of shalloweutrophic lakes. Aquat. Bot., 42, 199-216.

Scher-Kaul, S., Oertli, B., Castella, A. &Lachavanne, J-P., 1995. Relationship betweenbiomass and surface area of six submergedaquatic plant species. Aquat. Bot., 51, 147-154.

36

Schindler, D.E., Carpenter, S.R., Cottingham,K.L., He, X., Hodgson, J.R., Kitchell, J.F. &Soranno, P.A., 1996. Food web structure andlittoral zone coupling to pelagic cascades. In:G.A. Polis & K.O. Winemiller (eds), Foodwebs: integration of pattern and dynamics, NewYork., Chapman & Hall, 96-108.

Schriver, P., Bøgestrand, J., Jeppesen, E. &Søndergaard, M., 1995. Impact of submergedmacrophytes on fish-zooplankton-phytoplanktoninteractions: Large-scale enclosure experimentsin shallow eutrophic lake. Freshw. Biol., 33,255-270.

Schulthorpe, C.D., 1967. The biology of aquaticvascular plants. St. Martin`s Press, New York.610 p.

Smiley, E.A. & Tessier, A.J., 1998.Environmental gradients and the horizontaldistribution of microcrustaceans in lakes.Freshw. Biol., 39, 397-409.

Smith, V.H. & Wallsten, M., 1986. Prediction ofemergent and floating-leaved macrophyte coverin Central Swedish lakes. Can. J. Fish. Aquat.Sci., 43, 2519-2523.

Søndergaard, M., Kristensen, P. & Jeppesen, E.,1992. Phosphorus release from resuspendedsediment in the shallow and wind-exposed LakeArresø, Denmark..Hydrobiologia, 228, 91-99.

Stansfield, J.H., Perrow, M.R., Tench, L.D.,Jowitt, A.J.D. & Taylor, A.A.L., 1997.Submerged macrophytes as refuges for grazingCladocera against fish predation: observation onseasonal changes in relation to macrophyte coverand predation pressure. Hydrobiologia, 342/343,229-240.

Tallberg, P., Horppila, J., Väisänen, A. &Nurminen, L., 1999. Seasonal succession ofphytoplankton and zooplankton along a trophicgradient in a eutrophic lake – implications forfood web management. Hydrobiologia, 412, 81-94.

Taylor, W.D., 1984. Phosphorus flux throughepilimnetic zooplankton from Lake Ontario:Relationship with body size and significance tophytoplankton. Can. J. Fish. Aquat. Sci., 41,1702-1712.

Timmermann, M., 1987. Manglendereproduction af skalle (Rutilus rutilus (L.)) ogrudskalle (Scardinius erythrophthalmus (L.)) ogskalle- (R. rutilus (L.)), brazen- (Abramis brama(L.)) og aborre- (Perca fluviatilis (L.)) yngelensdensitet og vaekst i Vaeng Sø. MSc- thesis,Miljøstyrelsens Ferskvands laboratorium ogFerksvandsbiologisk Laboratorium,Københavns Universitet, (in Danish).

Timms, R.M. & Moss, B., 1984. Prevention ofgrowth of potentially dense phytoplanktonpopulations by zooplankton grazing in thepresence of zooplanktivorous fish in a shallowwetland ecosytem. Limnol. Oceanogr., 29, 472-486.

Toivonen, H. & Bäck, S. 1989: Changes inaquatic vegetation of a small eutrophicated andlowered lake (southern Finland). Ann. Bot.Fennici, 26, 27-38.

Toivonen, H. & Huttunen, P. 1995: Aquaticmacrophytes and ecological gradients in 57small lakes in southern Finland. Aquat. Bot., 51,197-221.

Uotila, P. 1971: Distribution and ecologicalfeatures of hydrophytes in the polluted LakeVanajavesi, S. Finland. Ann. Bot. Fennici, 8,257-295.

Van Donk, E., 1998. Switches between clear andturbid water states in a biomanipulated lake(1986-1996): The role of herbivory onmacrophytes. In: E. Jeppesen, Ma. Søndergaard,Mo. Søndergaard, & K. Christoffersen (eds.),The structuring role of submerged macrophytesin lakes, Ecological Studies, Springer Verlag,New York, 131, 290-297.

Van Donk, E. & Gulati, R.D., 1995. Transitionof a lake to turbid state six years after

37

biomanipulation: Mechanisms and pathways.Wat. Sci.Technol., 32, 197-206.

Van Donk, E. & Otte, A., 1996. Effects ofgrazing by fish and waterfowl on thebiomass and species composition ofsubmerged macrophytes. Hydrobiologia,340, 285-290.

Van Donk, E., Gulati, R.D., Iedema, A. &Meulemans, J.T., 1993. Macrophyte-relatedshifts in the nitrogen and phosphorus contents ofthe different trophic levels in a biomanipulatedshallow lake. Hydrobiologia, 82, 19-26.

Vant, W.N., Davies-Colley, R.J., Clayton, J.S. &Coffey, B.T., 1986. Macrophyte depth limits innorth island New-Zealand lakes of differingclarity. Hydrobiologia, 137, 55-60.

Venugopal, M.N. & Winfield, I.J., 1993. Thedistribution of juvenile fishes in hypertrophicpond: can macrophytes potentially offer a refugefor zooplankton? J. Freshw. Ecol., 8, 389-396.

Vinni, M., Horppila, J., Olin, M., Ruuhijärvi, J.& Nyberg, K., 2000. The food, growth andabundance of five co-existing cyprinids in lakebasins of different morphometry and waterquality. Aquat. Ecol., 34, 421-431.

Vuille, T., 1991. Abundance, standing crop andproduction of microcrustacean populations(Cladocera, Copepoda) in the littoral zone ofLake Biel, Switzerland. Arch. Hydrobiol., 123,165-185.

Walls, M., Rajasilta, M., Sarvala, J. & Salo, J.,1990. Diel changes in horizontalmicrodistribution of littoral Cladocera.Limnologica, 20, 253-258.

Wetzel, R.G., 1983. Limnology. Second edition.Sanders College Publishing. USA.. 767 p.

Whiteside, M.C., 1988. 0+ fish as major factorsaffecting abundance patterns of littoralzooplankton. Verh. Int. Ver. Limnol., 23, 1710-1714.

Winfield, I.J., 1987. The influence of simulatedaquatic macrophytes on the zooplanktonconsumption rate of juvenile roach Rutilusrutilus, rudd Scardinius erythrophthalmus andperch Perca fluviatilis. J. Fish Biol., 29, 37-48.

Wiśniewski, R. & Planter, M., 1985. Exchangeof phosphorus across the sediment - waterinterface (with special attention to the influenceof biotic factors) in several lakes of differenttrophic status. Verh. Int. Ver. Limnol., 22, 3345-3349.

Yousef, Y.A., McLellon, W.M., Zebuth, H.H.,1980. Changes in phosphorus concentrationsdue to mixing by motorboats in shallow lakes.Wat. Res., 14, 841-852.