The Role of Zooplankton in Littoral Communities: Diversity and Food Web Interactions in the Baltic Sea

Faculty of Biological and Environmental Sciences Department of Environmental Sciences University of Helsinki Finland

THE ROLE OF ZOOPLANKTON IN LITTORAL COMMUNITIES: DIVERSITY AND FOOD WEB INTERACTIONS IN THE BALTIC SEA

Laura Helenius

ACADEMIC DISSERTATION

To be presented, with the permission of the Faculty of Biological and Environmental Sciences of the University of Helsinki, for public examination in

Lecture hall 5, B-building Latokartanonkaari 7 on December 11th 2015, at 12 noon

Helsinki 2015

1 Supervisors:

Docent Leena Nurminen Docent Marko Reinikainen Department of Environmental Sciences Tvärminne Zoological Station University of Helsinki, Finland University of Helsinki, Finland

Docent Elina Leskinen Professor Hannu Lehtonen Department of Environmental Sciences Department of Environmental Sciences University of Helsinki, Finland University of Helsinki, Finland

Advisory committee:

Docent Maiju Lehtiniemi Docent Jaanika Blomster Finnish Environment Institute Department of Environmental Sciences Helsinki, Finland University of Helsinki, Finland

Reviewers:

Docent Maiju Lehtiniemi Professor Mariana Meerhoff Finnish Environment Institute Faculty of Sciences Helsinki, Finland University of the Republic, Uruguay

Examiner:

Professor Jonathan Shurin Section of Ecology, Behavior and Evolution University of California- San Diego, USA

Custos:

Professor Jukka Horppila Department of Environmental Sciences University of Helsinki, Finland

2 ABSTRACT

Zooplankton are considered an important link between the zooplanktivores that consume them and the lower trophic levels, yet their specific ecological role in littoral brackish ecosystems is still relatively unstudied. In general, ecological interest in zooplankton derives from their roles as grazers or as a food source. As grazers, their role is coupled with predicting future densities and composition of the algal community, while alternatively as prey they provide information on fish stocks in terms of the zooplankton production available to fish. This thesis aimed to unravel aspects related to these roles in the littoral zones of the Baltic Sea, by shedding light on the themes of zooplankton composition and diversity, the interactions between zooplankton and their predators, and the general feeding ecology of components of zooplankton.

The first objective of the thesis was to gain baseline information on zooplankton community composition and diversity in the littoral Baltic Sea via field sampling on a salinity gradient. The thesis also aimed to investigate how salinity and other abiotic factors, such as turbidity, temperature and wave exposure, affect zooplankton communities and the predation that structures them. Predation via two types of feeding by zooplanktivorous fish was studied experimentally as a regulator of zooplankton communities. Finally, the thesis investigated the role of copepod nauplii as grazers in laboratory conditions.

Salinity was found to be the most significant abiotic driver of spatial patterns of composition and diversity of zooplankton. Turbidity/chl a also influenced community structure to a lesser extent. The spatial patterns of species heterogeneity remained relatively constant regardless of temporal turnover, and there was an abrupt change in species composition at an intermediate salinity of 4 (on the Practical Salinity Scale) on the salinity gradient. Functional diversity of zooplankton was found to be related to salinity, but also to factors related to productivity after a certain threshold. Zooplankton diversity was also affected by predation, but this effect was regulated by the initial composition of the zooplankton community, which was in turn directly related to seasonality. Predation itself was found to structure the community through direct removal of crustacean zooplankton, as well as cascading effects on microzooplankton. These effects, as well as the extent of the disturbance generated by turbidity on zooplanktivorous feeding, were all closely related to predator type.

In the final section of the thesis, which concentrated on zooplankton as consumers, the functional responses of stage NII nauplii of the calanoid copepod Paracartia grani to various microalgae were found to be either Holling type II or III responses. Highest maximum clearance rates were found on a diatom and a dinoflagellate of a

3 size of ~12 µm, indicating an optimal prey:predator size ratio of 0.08. In plurialgal mixtures, feeding patterns were largely dependent on prey type.

Zooplankton are irrevocably linked to phytoplankton and fish through food web interactions. Changes in the abiotic environment inevitably lead to a response in the biotic environment as well, and a bottom-up resource level response reflects on top predators, in this case the littoral fish. Therefore, understanding the abiotic and biotic factors determining zooplankton diversity and density is a precondition to understanding the links between phytoplankton, zooplankton, and coastal zooplanktivores.

4 Abstract 3 Contents 5 List of Original Publications 6 Author Contribution 7 Abbreviations 8 1 Introduction 9 1.1 Linking food webs and diversity 9 1.2 The Baltic Sea as a study system: zooplankton and beyond 10 1.3 The importance of zooplankton: aspects of species composition and distribution 12 1.4 Zooplankton as prey: predation and its effects 13 1.5 Zooplankton as consumers: the functional response 17 2 Thesis Objectives 19 3 Materials and Methods 21 3.1 Study area and field sampling I( ) 21 3.2 Experimental work (II, III, IV) 22 3.2.1 Experimental fish and zooplankton 22 3.2.2 Aquarium experiments (II) 22 3.2.3 Mesocosm experiments (III) 25 3.2.4 Nauplius feeding experiments (IV) 25 3.3 Laboratory analyses and microscopy 26 3.4 Data analysis 27 3.4.1 Measures of zooplanktivore prey selectivity, zooplankton size, biomass and diversity 27 3.4.2 Ingestion and clearance rates 31 3.4.3 Statistical methods 31 4 Main Results 33 4.1 Environmental description of field site I( ) 33 4.2 Littoral community composition and diversity (I) 36 4.3 Predation by zooplanktivorous fish 41 4.3.1 Effects of turbidity on consumption and selection of zooplankton prey (II) 41 4.3.2 Zooplanktivorous predation and effects on prey community: zooplankton size, species composition and diversity (III) 43 4.4 Zooplankton grazing: feeding and selectivity of copepod nauplii (IV) 48 5 Discussion 52 5.1 Zooplankton in the littoral Baltic Sea (I) 52 5.1.1 Aspects of distribution 52 5.1.2 Aspects of diversity 54 5.2 Predation by zooplanktivorous fish: Is selection impaired by turbidity? II( ) 55 5.3 Predation by zooplanktivorous fish: effects on zooplankton community (III) 58 5.3.1 Community size structure and total abundance 58 5.3.2 Species composition: target prey 58 5.3.3 Species composition: cascading effects 60 5.3.4 Community diversity 61 5.4 Zooplankton as consumers: copepod nauplius feeding (IV) 62 6 Conclusions and Future Studies 65 Acknowledgements 67 References 70

5 ORIGINAL PUBLICATIONS

I Helenius LK, Lehtonen H, Leskinen E & Nurminen L. Spatial patterns of littoral zooplankton assemblages along a salinity gradient in a brackish sea: a functional diversity perspective. (Submitted manuscript)

II Helenius LK, Borg JP, Nurminen L, Leskinen E & Lehtonen H (2013). The effects of turbidity on prey consumption and selection of zooplanktivorous Gasterosteus aculeatus L. Aquatic Ecology 47(3): 349 – 356.

III Helenius LK, Aymà Padrós A, Lehtonen H, Leskinen E & Nurminen L (2015). Strategies of zooplanktivory shape the dynamics and diversity of littoral plankton communities: a mesocosm approach. Ecology and Evolution 5(10): 2021 – 2035.

IV Helenius LK & Saiz E. Feeding ecology of early stage nauplii of the calanoid copepod Paracartia grani: feeding rates, prey size spectrum and selectivity. (Manuscript)

Data not included in publications are presented in addition.

The original publications included in this thesis are reproduced with the permission of © Springer Science and Business Media and © John Wiley & Sons.

6 AUTHOR CONTRIBUTION

I II III IV

Original idea EL, HL, JB LN LN, LH ES, LH Study design LH, JB, LN LH, JB, LN LN, LH ES, LH Data collection LH, JB, LN LH, JB LH, AAP LH Data analysis LH LH, JB, LN LH, AAP LH, ES Manuscript LH, LN, LH, JB, LN, LH, AAP, LN, LH, ES preparation EL, HL EL, HL EL, HL

LH – Laura Helenius a), b) AAP – Anna Aymà Padrós c), d) EL – Elina Leskinen a) ES – Enric Saiz c) HL – Hannu Lehtonen a) JB – Janica Borg e) LN – Leena Nurminen a)

a) Department of Environmental Sciences, University of Helsinki, P.O. Box 65, 00014 Helsinki, Finland b) Tvärminne Zoological Station, University of Helsinki, J. A. Palménin tie 260, 10900 Hanko, Finland c) Institute of Marine Sciences, (ICM-CSIC), Passeig Marítim de la Barceloneta 37-49, 08003 Barcelona, Spain d) GRC Marine Geosciences, Department of Marine Stratigraphy, Paleontology and Geosciences, University of Barcelona, Carrer Martí i Franquès s/n, 08028 Barcelona, Spain e) Helcom Secretariat, Baltic Marine Environment Protection Commission, Katajanokanlaituri 6B, FI-00160 Helsinki, Finland

7 ABBREVIATIONS

ANOSIM Analysis of similarities ANOVA Analysis of variance Chl a Chlorophyll a (proxy for algal biomass) DistLM Distance based linear modelling ESD Equivalent spherical diameter FD Functional diversity Fmax Maximum clearance rate FSW Filtered seawater GAM Generalized additive model H´ Shannon-Weaver diversity index ICM Institut de Ciències del Mar Imax Maximum ingestion rate Km Half-saturation food concentration Kt Food concentration at Fmax MWS Mean weighted size nMDS Non-metric multidimensional scaling NTU Nephelometric turbidity units PCA Principal component analysis PCO Principal coordinate ordination PERMANOVA Permutational multivariate ANOVA PSS Practical Salinity Scale RMA Repeated measures ANOVA SIMPER Similarity percentages procedure SIMPROF Similarity profile TN Total nitrogen TP Total phosphorus TZS Tvärminne Zoological Station

8 1 INTRODUCTION Biodiversity can be defined, in its simplest form, as the way the total 1.1 THE LINK BETWEEN FOOD biomass of a community or assemblage WEBS AND DIVERSITY is partitioned among species. Species diversity is regulated by variation in the intensity of predation, competition and/ Food webs are essentially networks or disturbance (Paine 1966; Connell which record the dynamic interactions, 1978). Species richness is often used or simply the flow of energy and as a measure of diversity, but in fact resources, between species or functional the functional characteristics and groups inside ecosystems. The basic ecological roles of organisms, rather architectural characteristics of a food than their taxonomic identity, may be web depend on its connectance (the more relevant in examining effects on proportion of possible links that are ecosystem level processes (Walker 1991; realized), how the links are distributed, Hooper & Vitousek 1997; Walker et al. and the interaction strengths between 1999; Symstad et al. 2000). Functional species (Winemiller & Layman 2005). diversity is therefore based on the Recent studies indicate that most food functional traits of all the species in a webs are rife with omnivory, and community. The functional classification interspecies links are mostly inactive of organisms has become more common at any specific point in time, due to a in studies on biodiversity-ecosystem high proportion of generalist predators functioning relationships in terrestrial (Dunne et al. 2004). This complexity (e.g. Walker & Langridge 2002) and increases with species richness and level aquatic systems (e.g. Bady et al. 2005). of connectance, and in turn, both species In determining functional groups, traits richness (Tilman et al. 1996; McGrady- can be defined by the specific process of Steed et al. 1997; Naeem & Li 1997; interest, such as resource use in the case Cardinale et al. 2002) as well as species of zooplankton grazing (e.g. Barnett et al. composition contribute to biodiversity– 2007). Functional traits also describe how ecosystem functioning relationships species may respond to the environment (Hooper & Vitousek 1997; Symstad and perturbations in it, and knowing the et al. 1998). It follows that food webs traits present in a community increases and species diversity are highly linked the power of models that predict how a concepts, and many central studies in community will shift in the incident of aquatic ecology deal with the relationship environmental change (Norberg 2004). between the two, as diversity in the form of relative species abundance ultimately determines functional responses, adaptive foraging and prey switching in food webs (e.g. Paine 1966; Leibold 1996; Worm et al. 2002).

9 1.2 THE BALTIC SEA AS the Baltic Sea generally vulnerable to A STUDY SYSTEM: ZOO - a variety of human activities, including PLANKTON AND BEYOND maritime shipping, fisheries and nutrient supply via riverine runoff (HELCOM The Baltic Sea is a shallow but large 2009). In particular, the coastal areas in brackish sea, characterized by a the Gulf of Finland suffer from increasing temporally stable salinity gradient, eutrophication caused by excessive reaching from ˃ 20 on the Practical nutrient release, and subsequently, the Salinity Scale (PSS) in the opening area resulting turbidity and deterioration of towards the North Sea to approximately visual and light conditions in the water 2 in the Bothnian Bay (Kullenberg column (Cederwall & Elmgren 1990; 1981). The fauna and flora are of both Pitkänen et al. 2001; Schiewer 2008). marine and freshwater origin, in addition to brackish water species, and their large- Mesozooplankton communities are scale distribution is directly related to the generally dominated by copepods in existing salinity gradient (Hällfors et al. marine areas, while cladocerans are 1981; Snoeijs 1999). Due to the fact that considered a primarily freshwater both marine and freshwater species live group (Rudstam et al. 1994; Forró et al. at their physiological limits in the Baltic 2008). The unique brackish elements of Sea, it supports fewer species than true the Baltic Sea render the zooplankton marine or freshwater areas generally community in this area an intriguing do, and therefore its food webs are less mixture of both marine and freshwater complex (Elmgren 1984; Ojaveer et al. species (Koski et al 1999a). Historically, 2010). Because of its young age and the overall diversity of zooplankton recent rapid evolution from limnic to fully in the Baltic Sea has been presumed to marine to brackish conditions, as well as be decidedly low (e.g. Ackefors 1981). the ongoing niche occupation illustrated The general consensus has been that the by the numerous species invasions, variable environmental conditions and the Baltic Sea is also characterized by resulting instability of estuaries and other high instability and variability of both transitional aquatic areas limits species abiotic and biotic conditions (Menge & occurrence, and results in species-poor Sutherland 1987; Alenius et al. 1998). communities in brackish areas (McLusky The field sampling area of this thesis & Elliott 2004). The Artenminimum is located in the Gulf of Finland in the (‘species minimum’) concept of Remane northeastern corner of the Baltic, where (1934) stated that taxonomic diversity there is a permanent halocline caused is at its lowest at the horohalinicum, by the continuous freshwater discharge at a salinity of 5 – 8. However, the from rivers and the irregular saline notion of low zooplankton diversity has pulses from the North Sea (Kullenberg recently been challenged as outdated, 1981). This limited water exchange having resulted purely from previous with the North Sea, combined with a underestimation of microzooplanktonic large catchment area, inevitably leaves species and general limitations in

10 taxonomic knowledge (Ojaveer et al. Because monitoring of coastal plankton 2010; Telesh et al. 2011). Nearly 400 is generally conducted in areas with species of planktonic ciliates, rotifers vertical depths of over 20 meters, the and crustaceans are currently known studies characterizing zooplankton from estuarine and coastal ecosystems distribution and ecology in the Baltic of the Baltic Sea, with the most species- Sea have been conducted in adequately rich component being microzooplankton deep coastal waters or further pelagic (ciliates and rotifers) (Telesh & Heerkloss areas (e.g. Viitasalo et al. 1995; Uitto 2002; 2004). Of ciliates, the aloricate et al. 1997; Vuorinen et al. 1998; Koski oligotrichs (e.g. genera Strombidium, et al. 1999a; Telesh 2004). Until recent Strobilidium and Lohmaniella) and the attention on their diversity and dynamics tintinnids are abundant (Garstecki et (e.g. Scheinin & Mattila 2010), littoral al. 2000), while rotifers of the families zooplankton communities of shallow Synchaetidae and Brachionidae Baltic Sea waters (˂ 2 m depth) have contribute to total zooplankton biomass remained relatively unstudied, despite throughout the Baltic Sea (Witek 1995; the strong interaction potential between Telesh & Heerkloss 2002). Up to 95% zooplankton and fish juveniles and larvae of zooplankton biomass in Baltic coastal in these shallow zones. ecosystems is made up of rotifers, but their influence in terms of diversity and Zooplanktivorous fish in the littoral abundance decreases with increasing zones of the Baltic Sea consist of juvenile water salinity (Telesh 2004). Excluding cyprinids and percids, and small, rotifers, which are often included commercially unimportant species as mesozooplankton in Baltic Sea of both freshwater and marine origin monitoring data, the dominant coastal (Rajasilta et al. 1999). The three-spined mesozooplankton in the Gulf of Finland stickleback (Gasterosteus aculeatus are the calanoid copepod genera Acartia L.) is a small euryhaline fish, and the and Eurytemora, some species of which most common littoral fish species in tolerate wide salinity ranges (Ojaveer the northern Baltic Sea (Lemmetyinen et al. 2010). Accordingly, these two & Mankki 1975; Rajasilta et al. 1999; copepod genera and their interactions Ljunggren et al. 2010). The stickleback feature in much of the literature on has been established as a central link zooplankton distribution and food web in the Baltic Sea food web, and a key processes in the northern Baltic Sea consumer of zooplankton (Lemmetyinen (e.g. Hansson et al. 1990; Viitasalo et al. & Mankki 1975; Peltonen et al. 2004). 1994; Engström et al. 2000; Viitasalo et Increases in stickleback populations al. 2001; Sopanen et al. 2006). Neritic and other mesopredatory fish in the cladocerans in the general area include Baltic Sea have been credited to the podonids (genera Podon, Evadne) and fishery-induced decrease in offshore bosminids (Eubosmina) (Ojaveer et al. piscivorous predators, combined with 1998; Vuorinen et al. 1998). the continuous decline in the densities of dominant nearshore predators such

11 as European perch (Perca fluviatilis) differing feeding strategies on littoral and northern pike (Esox lucius), which zooplankton communities are of central have generated a mesopredator release interest in this thesis. in coastal areas (Eriksson et al. 2011). An increase in mesopredatory fish has been associated with community-wide 1.3 THE IMPORTANCE OF cascading effects on lower trophic levels, ZOOPLANKTON: ASPECTS including shifts in plankton biomass OF COMPOSITION AND (e.g. Casini et al. 2008; Eriksson et al. DISTRIBUTION 2009; Sieben et al. 2011). Zooplankton can be considered a Zooplanktivores utilize a range of significant trophic link between primary feeding strategies, which reflect on their producers and higher consumers, and physical capacities and target prey. The therefore they play a major role in aquatic stickleback is a vision-oriented selective food webs. As a grazing component, they particulate feeder, which seeks out and can shape phytoplankton communities, attacks individual prey items (Wootton and limit or enhance productivity 1984; Lazzaro 1987). An alternate, (Redfield 1980; Sterner 1989; Brett et non-selective filter-feeding strategy al. 1994; Jeppesen et al. 1990; Sommer is used by cyprinids, such as the roach et al. 2001; Muylaert et al. 2006). As (Rutilus rutilus L.), which is an efficient mediators of energy to higher trophic particulate feeder in clear water but may levels they are a significant prey item for switch to filter feeding to maximize invertebrates (Albertsson & Leonardson prey intake in compromised visibility 2001; Viherluoto & Viitasalo 2001) (Lammens et al. 1987; Diehl 1988). and fish and their larvae (Turner 1984; The roach is also common in littoral Gliwicz & Pijanowska 1989; Mehner zones of the Baltic Sea, and stocks & Thiel 1999; Elliott & Hemingway have increased considerably in the last 2002). Zooplankton species differ 20 years, with trends similar to other in their nutritional content and their cyprinid fish stocks (Lappalainen et al. importance as prey items, and substantial 2001; Lehtonen & Rask 2004). The roach changes in zooplankton composition population increase is largely attributed can quickly reflect on their predators to coastal eutrophication, which causes (e.g. Vuori & Nikinmaa 2007). Because low visibility conditions that favor of their position as intermediaries filter-feeding strategies (Lappalainen in the food web, zooplankton are et al. 2001; Nurminen et al. 2010). fundamentally involved in a multitude of Because of their ecological parallels ecosystem processes, and understanding and potential resource competition, as the distribution and composition of well as the increasing strength of the zooplankton communities in a system is trophic presence of the roach due to paramount to unraveling the mechanisms environmental conditions, these two key that shape abiotic and biotic processes in zooplanktivores and the effect of their that system.

12 Traditional niche-based theory assumes Telesh 2004). The characteristically that deterministic factors, including spatially and temporally heterogeneous species traits, interspecies interactions conditions in these environments can and environmental conditions, control produce significant spatial variability local community composition (Chesson in the distribution of species, whereas 2000). In theory, the resulting local extreme and/or long-term variations in communities then should have little salinity can define the species richness variation in species composition between of associated communities (de Jonge sites (i.e. exhibit low β-diversity) 1974; Michaelis et al. 1992; Li et al. if the environmental conditions are 2006). Indeed, in terms of zooplankton similar, and random stochastic factors specifically, salinity, water temperature discounted (Chase et al. 2009). and active chl a are considered crucial Community composition of organisms factors in controlling their distribution is then generally shaped by both internal in brackish and estuarine conditions processes, such as predation and (Gaughan & Potter 1995; Viitasalo et al. competition, as well as external processes 1995; Froneman 2001; 2004). related to the environment (Menge & Olson 1990). The surrounding physical While species-specific tolerances to environment acts as a physiological physical parameters determine the filter, by limiting species distribution species that have the potential to according to tolerance limits (Remmert occur in a habitat, biotic interactions 1983). Environmental conditions have a can determine the actual community primary role in shaping species patterns, composition. Negative interactions, and their fluctuations can both facilitate through competition or predation, can as well as exclude species, through restrict the distribution of a species turnover or migration (Hillebrand & (Black & Hairston 1988; Brooks & Shurin 2005; Shurin et al. 2010). Dodson 1965) or limit its population density (Thorp 1986). Therefore, In marine coastal areas, some of the the relative strengths of the biotic main environmental parameters that interactions, in the setting of the physical can affect community composition of constraints, shape community structure organisms are salinity, wave exposure on an environmental gradient. and temperature (Magill & Sayer 2002; Bonsdorff et al. 2003; Boström et al. 2006). In addition, aquatic environments 1.4 ZOOPLANKTON AS PREY: with steep horizontal gradients of salinity PREDATION AND ITS EFFECTS and nutrients, such as the Baltic Sea, usually support communities that are Predation is defined as a series of discrete generally controlled by interactions events occurring between predator and between abiotic and biotic characteristics, prey: the location of prey, followed as well as meteorological conditions by pursuit, attack, capture, handling (Li et al. 2000; Froneman 2001; 2004; and ingestion (Holling 1959; O’Brien

13 1979). In predator-prey interactions, the prey types, implying that prey are intake rate of an individual predator is ingested at different rates, and therefore, determined by attack rate and handling feeding is selective. Selective feeding time (Holling 1959). Inevitably, the is directly related to prey switching, as effects of predation depend on predator predators are known to alter their prey efficiency, and ultimately can vary and choice in the face of changing prey change with environmental conditions, abundance (e.g. Oaten & Murdoch which can influence either of these 1975). Prey selection and switching play components (O’Brien 1987). For an important role in maximizing foraging example, aquatic predators that use success in aquatic predators, and visual cues are highly influenced by the disparate feeding strategies have been light level and clarity of the surrounding shown to target different prey species water, and accordingly, elevated turbidity (Reiriz et al. 1998; Estlander et al. 2010). has been found to be deleterious to the Yet in the incidence of an environmental feeding of vision-oriented fish (Vinyard change, there may be a shift in the type & O’Brien 1976; Gardner 1981; Hayes of prey captured (Rowe 1984; Gregory & & Rutledge 1991; Benfield & Minello Northcoate 1993; Salonen & Engström- 1996; Rowe & Dean 1998; Nurminen & Öst 2010) or an impediment to size Horppila 2006). selective feeding (Rowe et al. 2003).

Prey selection is another aspect of In terms of zooplanktivory, plankton predation that can potentially be body size correlates with susceptibility influenced by environmental conditions to predation by fish, and hence prey and feeding strategy. The rates, durations species differ in their vulnerability to and efficiencies of the components of predation (Brooks & Dodson 1965). the predation process, as well as their Attack rates of fish are also generally dependencies on food availability, define higher on slow cladocerans than fast the functional response (Holling 1959). A and evasive copepods, resulting in an key concept in theories on predator-prey increased intake of the former prey type interaction is the functional response, in relation to the latter (Drenner et al. which defines the relationship between 1978; Persson 1987a). In zooplankton prey density and predator consumption communities, prey selection generally rate (Solomon 1949; Holling 1959). results in the direct depletion of selected Conventionally, three functional response crustacean prey, and the effects can types are described, deemed Holling cascade through other non-target type I (a linear increase in ingestion rate zooplankton species, and on through as a function of prey density), type II phytoplankton to influence ecosystem (curvilinear decelerating increase), and processes (Carpenter et al. 1985; Chang type III (sigmoidal increase) responses et al. 2004; Hansson et al. 2007). (Holling 1959) (Fig. 1a). Yet for any specific predator, parameters related to the functional response vary for different

14 a Type I b Type I e e t t a a r r n e c o i t n s a r e a g e n l I C

Type II Type II e e t t a a r r e n c o i n t a s r e a g e l n I C

Type III Type III e e t t a a r r e n c o i n t a s r e a g e l n I C

Fig 1. Three functional response types according to Holling (1959), plotted as (a) ingestion rate and (b) clearance rate as a function of prey concentration.

Strong community-wide predation from predation pressure (Carpenter et al. effects, such as trophic cascades, are 1996). For example, zooplanktivorous presumed to be especially common in predators have the potential to increase aquatic ecosystems (Carpenter et al. primary productivity by simply reducing 1985; Strong 1992; Shurin et al. 2002). the amount of herbivorous zooplankton Predators are able to control prey (Brett & Goldman 1996; Shurin et populations by changing their relative al. 2002). Therefore, predation by and absolute abundances, species zooplanktivores is considered a major composition and population structure driving force in shaping plankton (Carpenter et al. 1985; Hansson et al. communities, and hence a determinant 1990; Uitto et al. 1995), but also species of their structure (Holt 1984; Sommer et beyond their target prey by releasing al. 1986). the prey population of their target prey

15 The plankton ecology group (PEG) prey. Even in a single study system, they model (Sommer et al. 1986) has been can have positive or negative effects used to explain patterns in the seasonal on community diversity, depending succession of zooplankton in marine as on circumstances related to either the well as freshwater systems. It describes predator-prey interaction itself or to the the biotic interactions which unfold abiotic/biotic factors in the surrounding over a growing season, including habitat (Shurin 2001; Hillebrand 2003). species replacement. The unequivocal For example, the degree of prey dispersal role of fish predation in structuring can determine whether predators decrease zooplankton communities by the size- prey community diversity significantly selective removal of mesozooplankton or not (Shurin 2001). is emphasized in the PEG model. It has been suggested, that predation by fish Predation can have a major impact on has the potential to drive zooplankton interspecific competitive interactions, succession in some aquatic systems and the extent of the impact depends on (Cryer et al. 1986; Gliwicz & Pijanowska factors such as the scale of measurement 1989), and recent data emphasize the (individual vs. population), the intensity importance of predation in shaping of predation and the degree of prey zooplankton communities (Hansson et al. selectivity (reviewed by Chase et al. 2007). With sufficiently high predation 2002). Selective predation on dominant pressure, zooplankton populations can competitors can increase prey diversity even collapse irrespective of resource when the other competitors are capable availability (Nicolle et al. 2011). of coexistence: Predators promote prey Nonetheless, the complete removal diversity when they consume dominant of prey species, resulting in local prey species, and actively selecting extinction and hence reduction of total predators potentially switch to consuming prey diversity, is not the imminent the most abundant prey, acting as a consequence of all predation. stabilizing factor in maintaining prey diversity (Chesson 2002; Kondoh 2003). In general, the effects of predators on prey Therefore, different predators with diversity come across via two conflicting distinct feeding strategies are expected to mechanisms: 1) predators either reduce have different effects on the composition prey biomass by increasing prey and diversity of their prey communities, mortality or reducing prey reproduction, depending on the degree of selectivity or alternatively 2) predators prevent and adaptive foraging switches of the competitive exclusion of prey species predator. and apparent competition, and thus maintain diversity (Hillebrand & Shurin 2005). In the latter case, predators can generate resources, increase resource diversity or add limiting factors, therefore promoting the coexistence of competing

16 1.5 ZOOPLANKTON AS are dictated by the types and amounts of CONSUMERS phytoplankton consumed by grazers.

Zooplankton are important prey to higher In terms of zooplankton feeding on trophic levels, but also act as grazers, as algae, the functional response can also be well as predators of other zooplankton. In plotted as clearance rate (volume swept aquatic food webs, zooplankton biomass clear individual-1 time-1) as a function is not always directly derived from that of prey density (Fig. 1b). This allows of phytoplankton, because the quality for better separation between type II and and availability of phytoplankton as a type III responses, which can appear food source differs according to species similar at high prey densities. Increasing (Ahlgren et al. 1990; Sterner et al. 1993). the predictive power of aquatic food web Phytoplankton can affect its consumers models requires detailed knowledge of through several different factors: i) the such prey-specific functional responses size and shape of the food particles, of organisms. In shallow littoral habitats, food selectivity and ingestion rates, ii) grazing zooplankton even have the possible morphological defences against potential to regulate regime shifts in digestion, iii) nutritional paucity in terms terms of macrophyte and phytoplankton of P, N and fatty acids, and/or iv) toxicity domination (Jeppesen et al. 1998; (reviewed by Gulati & DeMott 1997). Scheffer 1998; Perrow et al. 1999). Survival, growth and egg production of Consequently, in the case of zooplankton, zooplankton can be severely weakened details on these responses are crucial, by low-quality or toxic phytoplankton particularly when attempting to predict (Uye 1996; Turner & Tester 1997; the outcome of grazing control of algae Koski et al. 1999b; Sopanen et al. in eutrophic systems, such as the Baltic 2006), thereby limiting the biomass of Sea (Fussman & Blasius 2005). zooplankton prey available to higher trophic levels. Phytoplankton nutritional Zooplankton functional responses have quality is not a straightforward concept, been investigated and quantified for but can be defined by its content of a large array of copepods (Lampitt & highly unsaturated fatty acids (HUFAs), Gamble 1982; Krylov 1988; Kiørboe which are essential in survival, growth et al. 1996; Saage et al. 2009; Zamora- and reproduction of marine and Terol & Saiz 2013), cladocerans (Horton freshwater zooplankton (Brett & Müller- et al. 1979; Porter et al. 1983; Chow- Navarra 1997). Zooplanktivorous fish Fraser & Spules 1992) and rotifers (Iyer in turn depend on zooplankton for & Rao 1996; Mohr & Adrian 2000). HUFAs, which are also important to Larval stages of planktonic crustaceans their growth (Desvilettes et al. 1997) are less studied. Yet nauplii of copepods, and larval development (Sargent et al. for example, make up large proportions 1995). Hence the amount of energy and of copepod biomasses in nature and essential fatty acids that are transferred therefore presumably have a high impact from zooplankton to higher trophic levels on grazing processes (Fryer 1986;

17 Castellani et al. 2007), as well as act as a major food source for fish larvae (e.g. Dalpadado et al. 2000; Gaard & Reinert 2002). Notably, nauplii of the calanoid copepod family Acartiidae are widespread and often numerically dominant in coastal areas around the globe, as the group prevails in a multitude of salinity conditions and has a high degree of tolerance for environmental change (Mauchline 1998).

Food type and availability are some of the major factors driving copepod feeding in natural systems (Saiz & Calbet 2011). It has long been known that zooplankton in general respond differently to potential food items (Gliwicz 1970). Additionally, the rate of intake of one prey type may be affected by the presence of alternative prey choices. Copepods are known to be size-selective omnivores, feeding on protozoans and large phytoplankton (Katechakis et al. 2002; Kleppel 1993; Sell et al. 2001; Sommer & Stibor 2002), and they have been shown to actively select or reject food particles (Paffenhöfer et al. 1982; Schultz & Kiørboe 2009). Complex feeding behaviors have been described for copepods, in which selection depends not only on size, but on the interplay between cell size and abundance (e.g. Wilson 1973; Kiørboe et al. 1996). Yet relatively little is known about the feeding rates and selectivity of naupliar stages. Even though early experimental work on nauplii feeding selectivity was conducted by Fernández (1979), empirical observations on feeding in controlled plurialgal suspensions are still scarce.

18 2. THESIS OBJECTIVES

Gaps remain in the knowledge surrounding coastal zooplankton distribution, diversity and interactions with other trophic levels. The main objective of this thesis was to present a comprehensive account of the composition, distribution, and diversity of littoral zooplankton communities in the Baltic Sea, and to examine their role as prey and consumers in the surrounding ecosystem (Fig. 2). This thesis is composed of four studies (numbered I – IV), which discuss the following themes with their respective specific aims:

I. What abiotic factors determine zooplankton distribution and Abiotic factors diversity in the littoral Baltic Sea? Zooplanktivorous fish II. How does increasing turbidity affect the efficiency and II. selectivity of zooplanktivory by two littoral predators with Zooplankton III. varying feeding strategies? I. III. How do these two zooplanktivores shape the IV. diversity and dynamics of Phytoplankton littoral zooplankton communities?

IV. How do the functional responses of a common copepod nauplius to different microalgal prey types vary?

Fig 2. A conceptual model of components of the littoral food web and the main questions of the thesis. Red arrows indicate conceptual effect links, black arrows indicate trophic links

19 1) Zooplankton diversity and distribution: To give a detailed description of the species composition and structure of littoral zooplankton communities, including fractions of the often overlooked microzooplankton component, in a representative area of the northern Baltic Sea. To examine spatial patterns and diversity of the community over a subtle coastal salinity gradient, and investigate locally variable environmental factors (temperature, wave exposure, degree of eutrophication) as possible drivers of spatial heterogeneity in diversity and species occurrence (I).

2) Zooplankton as prey and zooplanktivory as a process: To examine the influence of environmental change, in the form of increasing turbidity, on predation by zooplanktivorous fish with different feeding strategies. In effect, to determine whether zooplankton prey types have different vulnerabilities to selective predation under turbid conditions (II). Moreover, to examine the effects of predation by the same zooplanktivores on the structure and diversity of littoral zooplankton communities, and to compare the extent to which top-down control by the different predators mediates varying responses in interactions within their prey communities (III).

3) Zooplankton as consumers: To experimentally investigate the feeding ecology of a larval life stage of a ubiquitous calanoid copepod (Paracartia grani Sars), and determine its prey size spectrum and functional responses to different microalgal prey types (IV).

20 3 MATERIALS AND Tvärminne Archipelago, the sampling METHODS sites in study I geographically belonged to either the outer archipelago zone 3.1 STUDY AREA AND FIELD (hereafter referred to as OZ, sites 1 – 18), SAMPLING (I) the inner archipelago zone (IZ, sites 19 – 25) or the mainland zone (MZ, sites 26 – 31). Salinity measured on the sampling The Gulf of Finland is a eutrophic, highly gradient ranged from 6 to 2.6 from the seasonal sub-estuary of the Baltic Sea. outer archipelago to the mainland zone, The fragmented Tvärminne Archipelago respectively, with consistently higher in Hanko, Finland, is a well-studied area, salinities recorded later in the summer where the Tvärminne Zoological Station season. (University of Helsinki; hereafter referred to as TZS) is located. Sampling took The sites represented shallow beaches place at 31 shallow coastal bays along with a fine, sandy bottom substrate, a 40 km salinity and exposure gradient and were sampled in June/July 2009 from the outer archipelago to just outside and in August in 2010, outside of the semi-enclosed fjord-like Pojo Bay rotifer abundance peaks estimated from in the north (Fig. 3). The Pojo Bay is previous sampling in the area. Sampling separated from the outer archipelago by was conducted in the near vicinity of a 7 m deep sill that prevents the renewal the shore at a depth of 0.8 – 1.2 meters. of deep water in the bay, and there is Zooplankton samples were collected a high inflow of freshwater from the with 1 meter horizontal hauls using a Mustionjoki River at the north end of the modified plankton net with a buoy, with bay. Saline Baltic water moves landward a mesh size of 25 µm, and with 0.8 – 1 periodically from the open sea. Primary meter vertical hauls using a standard production in the archipelago and the plankton net with a mesh size of 50 µm. open sea areas is mainly limited by the The water volume filtered was estimated availability of nitrogen (Kivi et al. 1993), (without a flowmeter) as approximately and in the bay area by that of phosphorus 13 L and 40.2 L for the horizontal and (Lignell et al. 1992). Similar to other vertical tows respectively. Samples shores of the northern Baltic Proper, the were immediately fixed with 5% acid coast is divided into zones, which are Lugol’s solution. Water samples were characterized by distinct morphological, taken for measurements of nutrients, hydrographical and biological features: algal biomass, salinity and turbidity. a Pojo Bay zone, a mainland zone, Other environmental variables measured inner and outer archipelago zones and included temperature and wave exposure. an open-sea zone (Halme 1944; Niemi Estimations of wave exposure were made 1973; Munsterhjelm 2005), representing according to the Baardseth index, which an estuarine salinity surface water resulted in a value between 0 (indicating gradient of 2 – 7. According to these absolute shelter) and 40 (indicating traditional zonation classes of the maximal exposure) (Baardseth 1970).

21 Macrophyte coverage at each site Zooplankton for the aquarium and was estimated by diving in 2009. In mesocosm experiments (II, III) were 2010 all environmental variables were collected from the vicinity of the TZS additionally recorded with a YSI-6600 from depths of 1.5 to 15 meters using sonde (YSI Corp.). plankton nets of 100 to 200 µm mesh size. Prey items for use in the aquarium experiments, including two genera of 3.2 EXPERIMENTAL WORK (II, copepods (Acartia and Eurytemora) III, IV) and a cladoceran species (Daphnia longispina), were individually picked Experimental work consisted of into FSW using pipettes. aquarium experiments, in situ mesocosm experiments, and laboratory feeding For the nauplii feeding experiments experiments. Aquarium and mesocosm (IV), the naupliar stages of the calanoid experiments were conducted at copepod Paracartia grani Sars were TZS, while copepod nauplii feeding obtained from the continuous culture of experiments were conducted at the the ICM. Copepods were grown in 20 Institut de Ciències del Mar (ICM, L methacrylate cylinders at 18°C with a Barcelona, Spain). 12:12 light:dark cycle and fed with the cryptophyte Rhodomonas salina. Cohorts of stage NII nauplii were obtained by 3.2.1 EXPERIMENTAL FISH AND first collecting eggs using a vacuuming ZOOPLANKTON procedure with several filters to separate eggs from copepods. After cleaning with Two common brackish water littoral FSW, approximately 500,000 eggs were zooplanktivorous fish of a similar size transferred to a new cylinder to hatch but with varying feeding strategies were and grow in a suspension of R. salina. used for experimental work concerning Eggs that were unhatched after 24 hours predation on zooplankton (II, III): the were cleaned out of the cylinder. 50 vision-oriented particulate feeding hours after the original egg collection three-spined stickleback (Gasterosteus the nauplii were determined to be at the aculeatus L.) and the filter feeding desired developmental stage according juvenile roach (Rutilus rutilus L.). All to morphological characteristics (total fish were caught with a beach seine length, caudal armature setae) observed from the vicinity of the TZS and kept in via microscopy, and used for experiments. aerated housing tanks at a temperature of 18 – 19°C and an indoor 16:8 light:dark regime. For the aquarium experiments (II) 3.2.2 AQUARIUM EXPERIMENTS (II) fish were acclimated in their experimental tanks in the respective experimental Aquarium experiments were conducted turbidity conditions for at least 12 hours to determine the effects of turbidity on the before being used for experiments. feeding of zooplanktivorous sticklebacks

22 and roach. All experiments were carried Biosciences; www.licor.com/). Turbidity out in a temperature-controlled indoor was achieved in the experimental units by chamber in 10 L polypropylene tanks, adding sieved natural clayish sediment filled with 10 µm filtered sea water collected with an Ekman grab sampler and covered laterally to avoid visual from a nearby littoral area. In addition to distraction (Fig. 4). Light was provided the clear water control (< 1 NTU), two from above by fluorescent tubes and turbidity treatments were created based mean light intensity was measured using on preliminary experiments: medium a LI-1400 data logger equipped with (45-50 NTU, mean 47.16 ± 0.36 SE) and a LI-192SA quantum sensor (Li-Cor high (75-80 NTU, mean 77.38 ± 0.35 SE)

Fig 3. Map of the Tvärminne Archipelago on the southwest coast of Finland, northern Baltic Sea showing the location of the Tvärminne Zoological Station and littoral field sites (I). Sites are numbered 1 – 31 from the outer to the inner archipelago respectively. The traditional zonation of the archipelago is depicted with the abbreviations OZ (outer archipelago zone), IZ (inner archipelago zone), MZ (mainland zone) and SZ (sea zone).

23 Fig 4. Photographs of the setup of the aquarium experiments (II) and the in situ mesocosms (III).

24 turbidity. Turbidity levels can be as high periods lasting 16 days. The plankton as 45 NTU in the Baltic Sea archipelago community in each enclosure consisted (Granqvist & Mattila 2004). The highest of a mixture of the natural surrounding treatment represented a level not seawater community and additional currently recorded in the area, although zooplankton acquired from the nearby higher turbidities have been recorded in area, to maximize both density and subtropical and temperate estuaries (e.g. diversity of the experimental community. Cyrus & Blaber 1987; Maes et al. 1998). The mixture created was calculated to be equivalent to ten times the current In each experiment, 40 plankters of natural density of zooplankton. This was respective prey types were released into to enable the detection of changes in an experimental tank containing one diversity and prevent complete depletion individual fish. The adjusted density of any particular prey type, since of zooplankton corresponds to the zooplankton were not replaced during composition and density of the natural the experiments. Equal aliquots of the zooplankton populations in littoral areas plankton mixture were added to each of the surrounding archipelago. The pre- enclosure and allowed to settle for five determined feeding time was 30 minutes, hours before fish were released into the after which fish were dissected. Eight enclosures. replicates of each zooplanktivore group (male stickleback, female stickleback, Three fish were released into each of juvenile roach) were conducted in the six enclosures, so that three enclosures control (clear) and in each turbidity contained sticklebacks and three treatment (medium, high) giving a total contained roach, which was equivalent to of 72 experiments. Roach data were not approximate fish densities in local natural included in paper II. conditions, determined from previous surveys. An additional three fishless enclosures served as controls, giving a 3.2.3 MESOCOSM EXPERIMENTS total of three treatments. Zooplankton in (III) the enclosures was sampled using a 2.85 L Limnos water sampler before releasing Mesocosms were used to investigate the the fish (day 1), and on days 4, 10 and 16 differential effects of zooplanktivorous of the 16-day experiment. sticklebacks and roach on a natural zooplankton community. The experiments were carried out in nine 3.2.4 NAUPLIUS FEEDING UV- resistant 2225 L polyethylene EXPERIMENTS enclosures, placed at a depth of 0.9 – 1.1 m in a shallow bay in the vicinity A series of functional response of the TZS (Fig. 4). The two study experiments was carried out on periods took place in June (spring) and Paracartia grani nauplii using the August (summer) with experimental following algae: the haptophyte

25 Isochrysis galbana, the dinoflagellates were combinations of 1) I. galbana Heterocapsa sp., Gymnodinium and G. litoralis and 2) I. galbana and litoralis and Akashiwo sanguinea, the Heterocapsa sp. In the mixed suspensions, diatom Thalassiosira weissflogii, the five mid-level cell concentrations cryptophyte Rhodomonas salina, and established from the functional response the heterokontophyte Nannochloropsis experiments, of I. galbana were used, oculata. Three to seven concentrations and a steady concentration of a secondary of each suspension were prepared, and alga (Heterocapsa sp. or G. litoralis) was the range of algal concentrations was added. Incubations were conducted as obtained by successive dilution of stock above. cultures. The suspensions were adjusted using a Coulter Multisizer particle counter. Three initial, three control 3.3 LABORATORY ANALYSES (algae only) and three experimental AND MICROSCOPY (algae and nauplii) bottles were filled with prey suspension. Nauplius densities Turbidity (in nephelometric turbidity were adjusted according to algae type units, NTU) was determined using a and concentration, and ranged from standard turbidity meter (Hach 2100P; ~12 – 390 individuals per bottle. The Hach Co., Loveland, CO, USA) (I, control and experimental bottles were II). Temperature and salinity (VWR sealed with plastic foil to prevent bubble EC300 Portable conductivity, salinity formation, capped, and mounted on a and temperature instrument) were plankton wheel (0.2 rpm), while initial measured from separate water samples bottles were sampled immediately to in mesocosm and field samples (I, III). determine initial prey concentrations. Salinity is reported using the Practical Incubation took place for approximately Salinity Scale. Nutrient concentrations 24 hours, at 18°C with a 12:12 light:dark (total nitrogen [TN], total phosphorus cycle. After incubation, nauplii were [TP]) were determined according to removed from the bottles, preserved methods by Koroleff (1979) (I, III). To using acidic Lugol’s solution, counted determine algal biomass (expressed and measured. Cell concentrations in as chl a), 200 ml of sample water was the algal suspensions were immediately filtered (GF/F filter, 25 mm) and the determined using a Coulter Multisizer filters frozen until further analysis. particle counter, or alternatively counted Chlorophyll was extracted from the under an inverted microscope from filters using 5 ml of ethanol, and the preserved samples. N. oculata cell solutions read with a spectrophotometer concentrations were estimated using (I, III). Carbon content of algae and spectrophotometric determination of chl nauplii were estimated at TZS using a and pheo-pigments. Experiments using mass spectrometry (Europa Scientific plurialgal mixtures were also conducted ANCA-MS 20-20 C/N analyzer) from to determine possible interference and samples which had been filtered onto selectivity patterns in feeding. These pre-combusted 25mm GF/C filters, dried

26 and packed into cryovials with vanadium 3.4 DATA ANALYSIS pentoxide (IV). 3.4.1 MEASURES OF ZOO - Zooplanktivore stomach content analyses PLANKTIVORE PREY SELECTIVITY, were carried out under a binocular ZOOPLANKTON SIZE, BIOMASS microscope (II). Sticklebacks were AND DIVERSITY dissected, their gender determined and the stomach contents were identified and counted under a binocular microscope. Prey selectivity (II) was determined by The buccal cavity and esophagus were calculating Chesson’s α (Chesson 1978) flushed with water to ensure that all as a selectivity index: consumed zooplankters were accounted for. For cross-referencing with stomach contents, water from the experimental tanks was filtered through a 50 µm net and the remaining zooplankters were counted. Water samples were used to quantify roach consumption data, due to the cyprinid pharyngeal teeth, which macerated prey items and made quantification from the gut content less accurate. (where ni0 is the number of prey items i present at the beginning of The identification and quantification (ind foraging, ri is the number of items L-1) of zooplankton from multispecies of food type i in the consumer’s samples was conducted using an diet, m is the number of food inverted microscope (I, III). Zooplankton categories available). Values samples were divided into appropriate above and below 1/m (in this subsamples using a Folsom plankton case 0.33) indicate positive and splitter (either ½, ¼ or 1/8 divisions) negative selection respectively. due to high zooplankton densities. Individuals were identified to the lowest possible taxonomical level and life stages of copepods were documented as calanoid/cyclopoid nauplii, calanoid/ cyclopoid copepodites or adults, where only adults were identified to the species or genus level.

27 Mean weighted size (MWS, III) was used as a measure of zooplankton community size changes, and calculated for crustaceans and dominant rotifer species as follows:

where Pi is the proportion of individuals belonging to the ith species.

Functional diversity (FD) values were where Li is the mean length of calculated from trait data. Zooplankton species i in a sample and Di is the traits were chosen to reflect potential density of species i in that sample. effects on ecosystem function, and in this case, traits that describe resource use were selected. Traits included: 1) trophic group based on prey type (herbivore, Species/group abundances (I, III) omni-herbivore, herbi-detritivore, omni- were calculated as individuals L-1 and carnivore and carnivore, where preying converted to biomasses (µg L-1 wet on heterotrophic protists was considered weight) (I) according to unpublished herbivory since direct ingestion of ciliates calculations from the Finnish Institute was ambiguous for some cladoceran of Marine Research based on length groups) 2) feeding type (suspension, measurements. suspension/surface, suspension/ambush, B/D/C/S filtration [DeMott and Kerfoot The Shannon-Weaver diversity index 1982] and raptorial) and 3) prey size and FD (sensu Petchey and Gaston 2002) range. Trait information and values were used as measures of taxonomic and were taken from literature, so that functional diversity, respectively (I, III). only crustaceans and rotifers for which The Shannon-Weaver index accounts for sufficient information exists were used the abundance and evenness of species for the analysis. Qualitative measures present, and is calculated as follows: were entered as rank categories (from herbivore to carnivore and from passive forms of feeding [suspension] to more active ones [raptorial]). Trait values

28 were standardized, to represent a starting point situation where the biological variation within each trait was equally important.

A dendrogram depicting the between- group functional relationships was generated using hierarchical clustering analysis (standardized Euclidean distances and average linkage), resulting in groups of functional effect types. In this case, the groups were of zooplankton genera with similar effects on trophic transfer. A functional dendrogram of resource use of common Baltic Sea littoral crustaceans is shown in Fig. 5. FD values were calculated as the total branch length needed to join all groups in an assemblage, and were standardized to range between 0 (assemblages composed of 1 species) and 1.

29 Zooplankton group Diaphanosoma brachyurum Diaphanosoma Ceriodaphnia quadrangula Ceriodaphnia Pleopsis polyphemoides Pleopsis Eurytemora hirundoides Eurytemora Ceriodaphnia pulchella Ceriodaphnia Chydorus sphaericus Chydorus Thermocyclops spp Thermocyclops Temora longicornis Temora Cercopagis pengoi Cercopagis Evadne nordmanni Evadne Eurytemora affinis Eurytemora Acartia longiremis Acartia Daphnia cucullata Daphnia Mesocyclops spp spp Megacyclops Daphnia cristata Daphnia Podon leuckarti Evadne anonyx Evadne Eubosmina spp Eubosmina Acartia bifilosa Acartia Harpacticoida Acartia tonsa Acartia Cyclops spp Alona spp Alona 0 0.5 1.0 Distance 2 1 1.5 4 3 2.0 2.5 3.0

Fig 5. A dendrogram produced by hierarchical clustering analysis of typical Baltic Sea coastal zooplankton, showing four functional groups of planktonic crustaceans according to resource use. Data from study I.

30 3.4.2 INGESTION AND CLEARANCE analyses (II). Differences between sexes RATES in each prey item consumed were tested using a one-way ANOVA; differences Nauplius ingestion and clearance rates in selectivity were tested for each prey in feeding experiments were determined type with a two-way ANOVA with according to equations from Frost (1972) Tukey’s HSD post-hoc analyses (II). (IV). Feeding parameters (maximum Repeated measures ANOVA (RMA) filtration rate Fmax, maximum ingestion was used to compare experimental rate Imax and half saturation constant Km) patterns of zooplankton abundance in were derived from Holling functional mesocosms (III). One-way ANOVA and response fits. Cell counts were converted RMA were used to compare differences into carbon and nitrogen amounts using in mean weighted zooplankton size and conversion factors derived from mass the temporal patterns of size change, spectrometry measurements, and daily respectively (III). RMA and one-way ration (% body carbon/nitrogen ingested ANOVA were used to compare patterns d-1 nauplius-1) was calculated from these. in zooplankton diversity measures in the field and in mesocosmsI, ( III). General linear modeling and generalized additive 3.4.3 STATISTICAL METHODS modeling (GAM) were used to model diversity values against environmental Univariate methods were employed to variables of the field sites (I). Nonlinear test for differences in zooplanktivore prey least-squares regression was used to fit consumption and selectivity, patterns in functional response curves for nauplius zooplankton abundance and size, and feeding experiments (IV). differences in diversity measures. The effects of turbidity treatment and species Multivariate methods were used to on total prey consumption were assessed examine zooplankton community using a two-way ANOVA on square root structure in the field and in mesocosms, transformed data (√(x +5)), with Tukey’s and to visualize relationships between HSD post-hoc analyses (II). The effects environment and biota. The Bray-Curtis of turbidity on total prey consumption of similarity coefficient was applied to stickleback and roach were tested using create species similarity matrices from one-way ANOVA with Tukey’s HSD zooplankton abundance data. Non- post-hoc analysis and Kruskal-Wallis metric multidimensional scaling (nMDS) with pairwise comparisons respectively (I, III) and principal coordinate ordination (II). Prey selectivity was examined with (PCO) were used to visualize differences the Chi-square goodness-of-fit test (χ2 = in overall zooplankton community 2 ∑ (Oi – Ei) /Ei) (II). Differences between structure (III). Analysis of similarities the sexes of stickleback in total prey (ANOSIM) was used to test whether the a consumption in response to turbidity priori defined archipelago zones formed changes were tested using a two-way distinct zooplankton communities that ANOVA with Tukey’s HSD post-hoc differed from each other (I). Hierarchical

31 clustering and the SIMPROF procedure were used to identify deviating field sites in terms of community composition (I). The Similarity Percentages (SIMPER) procedure analyzed the contribution of taxa to the mean dissimilarity between samples (I, III). Principal component analyses (PCA) were carried out to portray environmental parameters of field sites (I). To assess the relationship between the plankton assemblage and the environmental parameters PRIMER v6 routines were used. The RELATE routine using the Spearman rank correlation coefficient was used to quantify the relationship, and the BEST procedure was applied to determine which environmental factors best correlate with the species matrix (I). Distance-based linear modeling (DistLM) was used to describe the biota using environmental variables (I). A partly nested permutational MANOVA (PERMANOVA) was run to test for differences in overall community structure between mesocosms (III). SPSS v 21 (2012 IBM), R v 2.10.1 (R Development Core Team 2013) and PRIMER v 6 (PRIMER-E Ltd., Plymouth, UK) were used to analyze the data.

32 4 MAIN RESULTS high algal biomass. However, in terms of zooplankton composition (section 4.1 ENVIRONMENTAL 4.2) neither site differed significantly DESCRIPTION OF FIELD SITE from other sites in the zone (site 13) or in the immediate geographic proximity (site 16) regardless of sampling time. When all environmental data from field This was presumably related to the fact sampling sites (1 – 31) were combined that communities were to a great extent from both years (2009 and 2010), a determined by salinity. Environmental cluster analysis identified five general data for all sites and combined for 2009 littoral habitat groups (Table 1). Sites and 2010 are summarized in Fig. 6 and 13 and 16 were not found to fit into depicted in detail in paper I. any of the environmentally determined groups of habitats. Site 13 was a shallow, extremely sheltered lagoon, which grouped most closely with the similar sites in the MZ, with the exception of its high salinity. Site 16 was a long, relatively exposed beach with high salinity and

Table 1. Field site environmental data combined from years 2009 and 2010. Habitat groups (I-V, shown with the associated sites) were determined by cluster analysis of environmental characteristics of sites in the Tvärminne Archipelago.

Habitat group

I II III IV V Overall Overall Overall Overall (1-12, (20- (17, 18, (27- (15, 19, mean S.D. Min Max 14) 23) 25, 26) 30) 24, 31) Salinity (PSS) 5.40 5.46 4.06 3.26 4.40 4.80 0.86 2.55 6.0 Water 18.6 21.2 21.6 20.4 22.4 20.2 2.03 15.8 24.4 temperature (°C) Exposure 4.30 3.31 3.61 3.81 3.73 3.88 0.53 2.47 4.86 index Chl a (µg L-1) 6.91 11.04 13.56 5.65 25.63 10.9 7.18 3.20 34 TN (µg L-1) 1065 839 929 893 1323 1031 189 808 1650 TP (µg L-1) 24.8 29.6 25.0 22.2 36.6 26.15 6.89 17.15 44.6 Turbidity 1.99 3.30 2.39 2.33 4.34 2.56 0.92 1.43 5.45 (NTU)

33 Salinity Turbidity 7 7

6 6 e l 5 5 a c S y t i 4 4 n i U l a T S N l

a 3 3 c i t c a r 2 2 P

1 1

0 0 0 1 2 3 4 5 6 7 8 9 10111213141516171819202122232425262728293031 0 1 2 3 4 5 6 7 8 9 10111213141516171819202122232425262728293031 Sampling site from outer to inner archipelago Sampling site from outer to inner archipelago

Temperature Macrophyte coverage 30 90

80 25 70

20 60 s u x

i 50 e s l 15 d e n I C 40 °

10 30

20 5 10

Wave exposure Algal biomass 6 40

35 5 30

x 4 e

d 25 L n / i g h µ t ,

e 3 20 a s l d r h c a

a 15

B 2 10 1 5

0 0 0 1 2 3 4 5 6 7 8 9 10111213141516171819202122232425262728293031 0 1 2 3 4 5 6 7 8 9 10111213141516171819202122232425262728293031 Sampling site from outer to innter archipelago Sampling site from outer to inner archipelago

Total nitrogen (TN) Total phosphorus (TP) 1800 50

1600 45

1400 40 35 1200 30 1000 L L / /

g g 25 µ 800 µ 20 600 15

400 10

200 5

34 Salinity Turbidity 7 7

6 6 e l 5 5 a c S y t i 4 4 n i U l a T S N l

a 3 3 c i t c a r 2 2 P

1 1

Temperature Macrophyte coverage 30 90

80 25 70

20 60 s u x i 50 e s l 15 d e n I C 40 °

10 30

20 5 10

Wave exposure Algal biomass 6 40

35 5 30

x 4 e

d 25 L n / i g h µ t , e 3 20 a s l d r h c a

a 15

B 2 10 1 5

Total nitrogen (TN) Total phosphorus (TP) 1800 50

1600 45

1400 40 35 1200 30 1000 L L / /

g g 25 µ 800 µ 20 600 15

400 10

200 5

Fig 6. Environmental variables from all field sites, with mean values ± SE from 2009 and 2010 where possible. Macrophyte coverage (2009), algal biomass (2010), and nutrient data (2010) are from a single year. Wave exposure indices do not differ yearly. Data from study I.

35 4.2 Littoral community species per zone differed between composition and diversity (I) sampling periods and are summarized in Table 2. Cluster analyses without a priori Altogether 64 zooplankton taxa grouping for the zooplankton community (including species, genera and distinguished only two primary clusters: crustacean life stages, recorded as the brackish area (with salinity ˃ 4) nauplii/copepodites for copepods and the freshwater area (with salinity ˂ and juveniles for cladocerans) were 4) (Fig. 8). The SIMPROF procedure identified in both time periods, although consistently identified two sites (20 and the groups were not concurrent between 31) which differed in composition from years. Total abundance was higher in the other sites in their respective zones. earlier 2009 sampling period compared There was generally low correlation to the later sampling period in 2010. between the abiotic and biotic High abundance was associated with resemblance matrices. Main results from high densities of calanoid nauplii or the multivariate routines are summarized rotifers in both years, and additionally in Table 3. The species matrices of in the 2010 sampling the dominant the different sampling periods were calanoid copepods. Highest biomasses similar, indicating approximate temporal were associated with calanoid nauplii, consistency in spatial patterns (ρ = 0.52, dominant rotifers (Synchaeta, Keratella) p = 0.001). or dominant crustaceans (cladocerans Pleopsis polyphemoides and Eubosmina, copepods Acartia, Eurytemora, and calanoid/cyclopoid copepodites). Combined abundance and biomass values from both sampling periods for all field sites are shown in Fig. 7.

The nMDS ordinations consistently grouped OZ and IZ sites together according to their zooplankton composition, with a transitional zone at sites 24 – 25, and the low salinity MZ sites clearly separated from the archipelago zones. The ANOSIM did not show differences between IZ and OZ in 2009 (R = 0.069, p = 0.25), but distinguished MZ from the two archipelago zones (IZ and MZ R = 0.644, p = 0.006 and OZ and MZ R = 0.835, p = 0.001), and conversely all the zones from each other in 2010 (R = 0.623, p = 0.001). Typical

36 Fig. 7. Mean density (a) and biomass (b) of zooplankton in field sites from combined 2009 and 2010 sampling. Sites 16 and 30 are based on data from 2009 and 2010 only, respectively. ‘Copepods’ include adults and copepodites; ‘others’ include copepod nauplii and meroplanktonic larvae. Data from study I.

37 Table 2. Main groups of zooplankton typifying the salinity zones of a coastal Baltic Sea area according to SIMPER analysis during two sampling years (OZ = outer archipelago zone, IZ = inner archipelago zone, MZ = mainland zone)

Zone 2009 2010 OZ Synchaeta, Keratella spp., bivalve Keratella spp., Acartia spp., larvae, Acartia spp., Pleopsis polyphemoides IZ Synchaeta, Keratella spp., bivalve Calanoid nauplii, Eubosmina spp., larvae, Eurytemora spp., Evadne spp., Keratella spp. calanoid copepodites MZ Keratella spp., Mesocyclops spp., Tintinnopsis beroidea, Vorticella spp., Thermocyclops spp., Eurytemora spp., cyclopoid copepodites, Eurytemora spp. cyclopoid copepodites, Acartia spp., P.polyphemoides, Eubosmina spp.

Table 3. Showing results from multivariate routines performed on a zooplankton species matrix and associated environmental variables of the 2009 – 2010 field sites. Results from the RELATE (correlation between the zooplankton species matrix and the environmental variables) and BEST (environmental factors which best correlate with the species matrix) routines are shown, as well as the variables included in and the associated R2 value for the best model determined by distance-based linear modeling.

RELATE BEST BEST DistLM R2 correlation variables correlation variables 2009 0.361 Salinity, 0.707/0.661 Salinity, 0.395 turbidity/ turbidity, Salinity temperature 2010 0.258 Salinity/ 0.686/0.582 Salinity 0.267 Salinity, chl a

38 a 50

70 t y i r a l i m i S 80

100 0 0 8 6 7 1 3 2 5 2 9 3 1 4 1 5 6 4 7 8 9 8 1 2 7 3 4 5 6 9 1 2 1 1 1 2 1 1 1 2 1 2 1 1 3 2 2 2 2 2 2 Site

MZ IZ/OZ

b 50

70 y t i r a l i m i S 80

100 0 9 5 7 8 4 5 2 1 3 1 2 0 4 3 1 6 7 8 9 0 4 9 7 8 1 2 3 5 6 2 1 1 1 1 2 2 2 2 2 1 1 1 1 1 3 2 2 2 2 3 Site

MZ IZ/OZ

Fig. 8. Results of a hierarchical cluster analysis of Tvärminne Archipelago coastal field sites 1 – 31 based on zooplankton communities in (a) 2009 and (b) 2010, showing the two main clusters of the brackish area (IZ/OZ) and the freshwater area (MZ). Data from study I.

39 The functional dendrogram resulted in 4.3 PREDATION BY four functional groups of planktonic ZOOPLANKTIVOROUS FISH crustaceans (Fig. 5). Using the a priori defined zones, crustacean FD was 4.3.1 EFFECTS OF TURBIDITY ON significantly higher in the MZ compared CONSUMPTION AND SELECTION to the other two zones (one way ANOVA OF ZOOPLANKTON PREY (II) F2,58 = 13.478, p ˂ 0.001). General linear models were fitted to the data with FD Total prey consumption in response as the response variable and salinity, to increasing turbidity was found to temperature, turbidity, and exposure as differ between sticklebacks and roach predictors. For the 2009 data the model (two-way ANOVA, species*turbidity included only salinity as significant, with treatment, F2,72 = 52.5, p < 0.001) an inverse relationship between FD and (Fig. 9). Consumption by sticklebacks salinity (R2 = 0.56, 28 df, p ˂ 0.001). In declined with increasing turbidity (one- 2010 FD decreased non-linearly with way ANOVA, F2,21 = 44.430, p < 0.001), salinity and a smoothing function was rendering it lower in the high turbidity applied. Salinity (p = 0.002), temperature treatment than in the control and the (p = 0.002) and turbidity (p = 0.001) were medium treatment (p < 0.001 in both). all significant in the model R( 2 = 0.73). Conversely, consumption by roach increased in high turbidity (Kruskal- All zooplankton groups were considered Wallis, H = 15.521, p < 0.001). in measuring taxonomic diversity (H´). A GAM (Generalized Additive Model) was fitted to the data, with H´ as response variable and salinity, turbidity and exposure as well as total zooplankton biomass as predictors. Only salinity was significant. Incorporating nonlinear effects improved the model significantly, and it explained 26.9% of the deviance (p = 0.004). H´ increased with salinity until 5, at which point it decreased. The pattern in total biomass was similar, and there was a weak correlation between taxonomic diversity and biomass (Pearson’s correlation r(58) = 0.317, p = 0.01).

40 80 ------

70 ------

60 d e

m 50 u s n o c

s 40 l a u d i v i 30 d n I 20

0 Clear Medium High Turbidity treatment

Fig. 9. Differences in total zooplankton consumed by stickleback (■) and roach (□) in different turbidity treatments. Dashed lines connect treatments in which total amounts did not differ significantly within planktivore species. Values are mean ± S.E, n = 16 (stickleback) and n = 8 (roach). Total amount of zooplankters available in each treatment was 120. Data for sticklebacks from paper II.

In sticklebacks, consumption of both positive selection for the daphnid in the 2 the daphnid (one-way ANOVA F2,45 = clear water control (chi-square test, χ 10.298, p = < 0.01) and the copepods = 10.11, p < 0.01), but in the turbidity (one-way ANOVA, F2,45 = 8.827, p treatments no significant selection for < 0.05) were significantly lower in any prey species was found (p ˃ 0.05) high turbidity. Sticklebacks showed a (Fig. 10). When only copepods were high selectivity for the daphnid in all considered, roach appeared to display no treatments, which increased in elevated significant selection for either group (all turbidity (Fig. 10). Selectivity for the p > 0.5). smaller copepod species proved negative in the control and the negative selection intensified with increasing turbidity (Fig. 10). When the two copepod groups were considered, sticklebacks selected Acartia or alternatively rejected Eurytemora in the clear water control (chi-square test, χ2 = 17.36, p < 0.001). Roach showed

41 0.8 a 0.7

0.6 x e

d 0.5 n i y t i

v 0.4 i t

c ------e l 0.3 e S 0.2

0.1

0 Clear Medium High

0.8 b 0.7

0.6 x e

d 0.5 n i y t i

v 0.4 i t c

e ------l 0.3 e S 0.2

0.1

0 Clear Medium High Turbidity treatment

Fig. 10. Mean Chesson’s α index (Chesson, 1978) for consumption of Daphnia longispina (white), Acartia sp. (striped) and Eurytemora sp. (black bars) for (a) stickleback and (b) roach in different turbidity treatments. The dashed line shows the value of 1/n, where values above the line indicate positive selection and values below the line indicate negative selection. Data for (a) from paper II.

42 4.3.2 ZOOPLANKTIVOROUS seasonal variation). Overall, community PREDATION AND EFFECTS size structure was clearly shifted towards ON PREY COMMUNITY: larger species in the absence of predation. ZOOPLANKTON SIZE, SPECIES An nMDS of the combined community COMPOSITION AND DIVERSITY (III) data showed the successional differences in zooplankton community between In the mesocosm experiments, control and predator treatments, and community effects of predation were notably the development of the spring found to be dependent on predator type as control community towards a large- well as initial community structure (i.e. bodied summer community (Fig. 11).

Synchaeta, T. lobiancoi, P. polyphemoides, Vorticella, Trichocerca, bivalve larvae, K. cruciformis

2D Stress: 0.11 Sampling 1R Spring Summer Similarity 10C 1C 60 1C 10C 1S 1R1R1C 4C 80 1S1S 1R 1S 1R 10C 4C 1R4R4S4R 1C 16C 4C 1C 4S 4R 16C 4S1S 1S 4R 1C 16C 4C4S 4C4R4R 4S 16C 10C 4S 10C 10C 4C 16C

16S 10S 16R 16C 10R 10R 10R 10R 10R 16S 16R 10R 16S16R 10S 10S 16R 10S 16S 10S 10S 16R 16S 16R 16S

K. quadrata, Eubosmina, Acartia, Lohmaniella, K. cochlearis, calanoid nauplius

Fig. 11. NMDS ordination of zooplankton communities (square root transformed data) combined for spring and summer mesocosm experiments. Numbers represent sampling days 1, 4, 10 and 16. Letters represent control (C), stickleback (S) and roach (R) treatments. Superimposed clusters are based on Bray-Curtis similarities at levels of 60% (solid line) and 80% (dashed line). Arrows indicate direction of increasing abundances of zooplankton groups which contributed most to differences between communities. Data modified from paper III.

43 In the spring, initial total abundance of the control (p ˂ 0.01 and p ˂ 0.005 individuals was high due to representation respectively). Patterns in cladoceran by numerous small-sized taxa (Fig. 12). and copepod abundance varied between High total abundance was reflected in high treatments, as shown by the significant densities of small-bodied zooplankton time*treatment interactions (Table groups, such as microzooplankton and 4). Crustacean abundance in predator rotifers, while low total abundance was enclosures was significantly lower than associated with high densities of larger in the control towards the end of the crustaceans (Fig. 12). Microzooplankton experiment (one-way ANOVA, day 10 and rotifer abundances were determined F2,8 = 23.033, p ˂ 0.005, and day 16 F2,8 by time and treatment (Table 4), and = 9.124, p ˂ 0.05 for cladocerans; day 10 stickleback enclosures had a significantly F2,8 = 19.423, p ˂ 0.005, and day 16 F2,8 higher abundance of these groups than = 136.416, p ˂ 0.001 for copepods).

Spring Summer 1000 450

900 400

800 350 700 300 1 1 - -

L 600 L s s l l 250 a a u Control u Control

d 500 d v i v i i i 200 d Stickleback d Stickleback n n

I 400 I Roach Roach 150 300 100 200

100 50

0 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 Experiment day Experiment day

Spring Summer 1000 450

900 400

800 350 700 300 1 1 - -

L 600 L s s l l 250 a a u Control u Control

d 500 d v i v i i i 200 d Stickleback d Stickleback n n

I 400 I Roach Roach 150 300 100 200

100 50

0 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 Experiment day Experiment day

Fig. 12. Total zooplankton abundance in mesocosm experiments with zooplanktivore treatments (including microzooplankton). Abundances are plotted over the four sampling dates to show the time*treatment interaction from the repeated-measures ANOVA. Note distinct axis scales. Data from paper III.

44 Table 4. Summary of the results of a two-factor ANOVA with repeated measures (RMA) for the analysis of differences in weighted size, total abundance, group abundances, and two measures of diversity (the Shannon–Weaver diversity index, H´, and functional diversity, FD) across time and predator treatment in the spring and summer periods of a mesocosm experiment.

Spring Summer Source of df F p df F P variation Weighted size Time 3 67.761 ˂0.001 3 11.313 ˂0.001 Treatment 2 81.558 ˂0.001 2 2.036 0.211 Time*treatment 6 57.005 ˂0.001 6 5.702 0.002

Total abundance Time 3 5.654 0.007 3 27.771 ˂0.001 Treatment 2 27.282 0.001 2 5.141 0.05 Time*treatment 6 0.905 0.513 6 3.376 0.021

Microzoopl. Time 3 11.871 0.01 3 3.257 0.121 abundance Treatment 2 12.107 0.008 2 0.316 0.740 Time*treatment 6 4.592 0.051 6 0.372 0.706

Rotifer Time 3 20.282 ˂0.001 3 40.424 ˂0.001 abundance Treatment 2 5.90 0.038 2 7.393 0.024 Time*treatment 6 1.098 0.401 6 7.495 0.015

Cladoceran Time 1.7 1.864 0.206 3 2.214 0.122 abundance Treatment 2 13.377 0.006 2 4.576 0.062 Time*treatment 3.4 6.078 0.01 6 2.676 0.049

Copepod Time 3 23.236 ˂0.001 1.4 8.556 0.014 abundance Treatment 2 29.157 0.001 2 2.383 0.173 Time*treatment 6 18.383 ˂0.001 2.8 4.409 0.041 Taxonomic Time 3 6.363 0.004 3 28.988 ˂0.001 diversity (H´) Treatment 2 48.561 ˂0.001 2 0.303 0.750 Time*treatment 6 5.188 0.003 6 1.510 0.231 Functional Time 3 1.580 0.229 3 0.458 0.715 diversity (FD) Treatment 2 1.350 0.328 2 0.029 0.972 Time*treatment 6 3.197 0.026 6 0.966 0.475

Throughout the duration of the spring from the control (pairwise comparisons experiment there were clear differences stickleback t = 5.36, p(MC) = 0.001 and in zooplankton successional dynamics roach t = 4.29, p(MC) ˂ 0.005). The between treatments, as indicated by the main results of the SIMPER analyses significant time*treatment interaction show the zooplankton groups which of the partly-nested PERMANOVA contributed most to the dissimilarities (F = 6.60, p = 0.001). Segregation of between enclosures, notably the stickleback enclosures from the control Eurytemora and Acartia abundances as early as the fourth experimental day differentiating the predator enclosures was apparent (pairwise comparisons (Table 5). A difference between the t = 2.52, p(MC) ˂ 0.05). By day 10 predator enclosures was detectable, as predator enclosures clearly differed roach and stickleback enclosures were

45 segregated into their own distinct groups life stages. Both predator enclosures (pairwise comparisons t = 1.93, p(MC) ˂ remained significantly segregated from 0.05). On the last sampling day (day 16) the control (pairwise comparisons of the spring experiment, both predator stickleback t = 6.03, p = 0.001, roach t enclosures were characterized by = 3.63, p(MC) ˂ 0.005), in which typical rotifers and ciliates. Roach enclosures groups were the dominant calanoid were more diverse, and additionally copepods and nauplii. characterized by calanoid copepod

Table 5. Dissimilarities between treatments on days 10 and 16 of the experiments (spring and summer) displaying species/genera which cumulatively contribute to over 50% of the dissimilarity determined from the SIMPER analysis. Species/genera are grouped as microzooplankton (micro), rotifers (rot), cladocerans (clad) and copepods (cop). Direction of difference describes whether the group abundance is higher (+) or lower (-) in the second treatment of the treatment pair compared to the first.

Period/ Treatment Dissimilarity Species/group Percentage Direction of Day pair percentage contribution difference

Spring Control – 58.56% Tintinnopsis lobiancoi (micro) 41.57% + 10 Stickleback Synchaeta spp. (rot) 10.14% +

Spring Control – 47.58% Tintinnopsis lobiancoi (micro) 33.04% + 10 Roach Synchaeta spp. (rot) 12.36% + Pleopsis polyphemoides 10.02% - (clad) Spring Stickleback 22.30% Tintinnopsis lobiancoi (micro) 37.75% - 10 – Roach Vorticella spp. (micro) 5.25% - Eurytemora spp. (cop) 4.84% + cyclopoid nauplius (micro) 4.70% + Spring Control – 71.57% Tintinnopsis lobiancoi (micro) 33.66% + 16 Stickleback Synchaeta spp. (rot) 14.13% + Keratella cruficormis (rot) 7.83% + Spring Control – 54.54% Tintinnopsis lobiancoi (micro) 34.98% + 16 Roach Synchaeta spp. (rot) 10.63% + Keratella cruciformis (rot) 9.24% + Spring Stickleback 29.05% Tintinnopsis lobiancoi (micro) 24.07% - 16 – Roach Synchaeta spp. (rot) 10.98% - calanoid nauplius (micro) 6.65% + Lohmaniella spp. (micro) 6.23% + Notholca spp. (rot) 5.75% + Summer Control – 34.52% Calanoid nauplius (micro) 16.55% + 10 Stickleback Synchaeta spp. (rot) 15.92% + 46 Calanoid copepodite (cop) 9.37% + Eubosmina spp. (clad) 8.79% - Summer Control – 34.48% Synchaeta spp. (rot) 15.30% + 10 Roach Keratella quadrata (rot) 15.10% + Calanoid nauplius (micro) 10.82% + Period/ Treatment Dissimilarity Species/group Percentage Direction of Day pair percentage contribution difference

Spring Control – 58.56% Tintinnopsis lobiancoi (micro) 41.57% + 10 Stickleback Synchaeta spp. (rot) 10.14% +

Spring Control – 47.58% Tintinnopsis lobiancoi (micro) 33.04% + 10 Roach Synchaeta spp. (rot) 12.36% + Pleopsis polyphemoides 10.02% - (clad) Spring Stickleback 22.30% Tintinnopsis lobiancoi (micro) 37.75% - 10 – Roach Vorticella spp. (micro) 5.25% - Eurytemora spp. (cop) 4.84% + cyclopoid nauplius (micro) 4.70% + Spring Control – 71.57% Tintinnopsis lobiancoi (micro) 33.66% + 16 Stickleback Synchaeta spp. (rot) 14.13% + Keratella cruficormis (rot) 7.83% + Spring Control – 54.54% Tintinnopsis lobiancoi (micro) 34.98% + 16 Roach Synchaeta spp. (rot) 10.63% + Keratella cruciformis (rot) 9.24% + Spring Stickleback 29.05% Tintinnopsis lobiancoi (micro) 24.07% - 16 – Roach Synchaeta spp. (rot) 10.98% - calanoid nauplius (micro) 6.65% + Lohmaniella spp. (micro) 6.23% + Notholca spp. (rot) 5.75% + Summer Control – 34.52% Calanoid nauplius (micro) 16.55% + 10 Stickleback Synchaeta spp. (rot) 15.92% + Calanoid copepodite (cop) 9.37% + Eubosmina spp. (clad) 8.79% - Summer Control – 34.48% Synchaeta spp. (rot) 15.30% + 10 Roach Keratella quadrata (rot) 15.10% + Calanoid nauplius (micro) 10.82% + Acartia spp. (cop) 9.02% -

Summer Stickleback 22.21% Calanoid nauplius (micro) 11.94% - 10 – Roach Keratella quadrata (rot) 10.70% + Calanoid copepodite (cop) 10.22% - Synchaeta spp. (rot) 9.73% + Eubosmina spp. (clad) 6.61% - Pleopsis polyphemoides 5.46% + (clad) Summer Control – 41.27% Keratella quadrata (rot) 16.05% + 16 Stickleback Calanoid nauplius (micro) 11.70% + Eubosmina spp. (clad) 11.01% - Keratella cochlearis (rot) 8.48% + Calanoid copepodite (cop) 7.46% + Summer Control – 47.12% Keratella quadrata (rot) 17.03% + 16 Roach Calanoid nauplius (micro) 11.58% + Keratella cochlearis (rot) 11.49% + Eubosmina spp. (clad) 11.43% - Summer Stickleback 23.85% Acartia spp. (cop) 14.26% - 16 – Roach Keratella quadrata (rot) 12.01% + Keratella cochlearis (rot) 8.98% + Eubosmina spp. (clad) 7.81% - Synchaeta spp. (rot) 6.46% + Euchlanis dilatata (rot) 5.48% +

47 Initial group abundances in the summer Diversity values differed throughout reflected the large-bodied community, the spring experiment depending on with lower densities of microzooplankton treatment (Table 4). Taxonomic diversity and rotifers and higher densities of decreased in stickleback enclosures, crustaceans compared to the spring and on the last sampling days was period. Total zooplankton abundance significantly lower than in the other increased in all enclosures with time, treatments (one-way ANOVA, day as opposed to the decreasing trend in 10 F2,6 = 231.893, p ˂ 0.001 and day the spring, but the response pattern 16 F2,6 = 6.455, p ˂ 0.05). Functional differed with treatment, as indicated by diversity was also significantly lower in the significant time*treatment interaction the stickleback than control enclosures (Fig. 12, Table 4). Correspondingly to on day 16, in direct opposition of the the spring experiment, the significant initial sampling (one-way ANOVA, F2,6 time*treatment interaction revealed that = 7.011, p ˂ 0.05). Predation had no the succession of cladocerans and adult effect on either diversity measure in the copepods differed between treatments summer experiment. (Table 4). Adult copepods were slightly more abundant in stickleback enclosures throughout the experiment, except on day 4.4 ZOOPLANKTON GRAZING: 10, when abundance was significantly FEEDING AND SELECTIVITY OF higher in the control (one-way ANOVA COPEPOD NAUPLII (IV) F2,8 = 13.862, p ˂ 0.01). All data from unialgal experiments The significant time*treatment interaction were fitted to Holling type II or type III indicated differences in zooplankton equations. depending on the pattern of succession between treatments (partly- clearance rates at low prey concentrations nested PERMANOVA, F = 2.30, p (Fig. 13). The functions used were as = 0.001). Communities in predator follows: enclosures differed from the control from day 10 onwards (pairwise comparisons Holling type II: I = (C* Imax) / (C+ Km) stickleback t = 2.32, p(MC) ˂ 0.05 and F = a / (C+b) 2 2 and roach t = 2.74, p(MC) ˂ 0.01). On Holling type III: I = (Imax*C ) / (C + 2 2 2 day 16 roach enclosures were very Km ) and F = Imax* C / (C + Kt ) homogenous and least similar to the control (pairwise comparisons, t = 3.32, where I is the ingestion rate and Imax the p(MC) ˂ 0.05), which also significantly maximum ingestion rate (cells ind-1 d-1), differed from stickleback enclosures F is the clearance rate (ml ind-1 d-1), C is (pairwise comparisons, t = 2.25, p(MC) the concentration of prey (cells ml-1), a ˂ 0.05) (Table 5). The cladoceran Podon and b are prey specific constants, Km is leuckartii was unique to the control. the half saturation constant, and Kt is the food concentration at which maximum clearance rate is reached. Maximum

48 clearance rates (Fmax) were highest for T. weissflogii and lowest for I. galbana, indicating that the prey size spectrum peaked at an approximate prey:predator size ratio of 0.08. The daily rations (in % body carbon and nitrogen ingested day-1 nauplius-1) were highest for ingestion of the dinoflagellate Heterocapsa sp. (up to 335% and 276% for C and N respectively) and lowest for R. salina (92% and 65% for C and N respectively). In the plurialgal mixtures using I. galbana as a baseline prey, maximum clearance rate for I. galbana was up to 32% lower than in unialgal suspensions, and clearance rate of the secondary alga depended on prey type, rendering lower (Heterocapsa sp.) or higher (G. litoralis) values than estimated from the Holling fits.

49 I. galbana I. galbana 10000 Type III 0.25 F = 8238 * C / (C^2 + 18 841^2)

y ) response

y ) R sq = 0.67 a a

d 8000 0.20 / d / d

I. galbana I. galbanad n i n i / s / l

l 10000 0.25

6000 Type III ( m l 0.15 ( c e

e F = 8238 * C / (C^2 + 18 841^2) t e t y ) response r a

y ) R sq = 0.67 a r a a

d 8000 I = (9453 x C^2) / (C^2 + 22 830^2) 0.20 / d c e n / d n o

4000 d 0.10

i R sq = 0.99

I. galbanan I. galbana i n r a i s t / a s / e l e l 10000 0.25 l g ( m l n

6000 C 0.15 I Type III ( c e e

2000 t 0.05 F = 8238 * C / (C^2 + 18 841^2) e t y )

response r a

y ) R sq = 0.67 a r a a

d 8000 I = (9453 x C^2) / (C^2 + 22 830^2) 0.20 c e / d n / n d o 4000 0.10

i R sq = 0.99 d n i r a n s t 0 i 0.00 a / s / e l 0 20000 40000 60000 80000 100000 120000 e 0 20000 40000 60000 80000 100000 120000 l l g n ( m l C

I 6000 0.15 ( c e

Prey concentration (cells/ml) e Prey concentration (cells/ml)

2000 t 0.05 e t r a

R. r a salina I = (9453 x C^2) / (C^2 + 22 830^2) R. salina c e n n

o 4000 0.10

i R sq = 0.99 0.40 r a

s t 0 0.00 a e 0 20000 40000 60000 80000 100000 120000 0 20000 40000 60000 80000 100000 120000 e

Type III l g F = 1168 x C / (C^2 +1711^2)

n 1250 C I

y ) Prey concentration (cells/ml) Prey concentration (cells/ml) response y ) R sq = 0.94 a 2000 0.05 a d d / /

d 0.30 R. salina R. d salina n i

1000 n i / s /

l 0.40 l 0 0.00 ( m l

c e 0 20000 40000 60000 80000 100000 120000 0 20000 40000 60000 80000 100000 120000

( Type III e F = 1168 x C / (C^2 +1711^2) 1250 t

e 750 t y ) r a

responsePrey concentration (cells/ml) y ) 0.20 Prey concentrationR sq =(cells/ml) 0.94 a r a a d d / c e n / d n 0.30 o d i

R. n salina R. salina I = (1232 x C^2) / (C^2 +1840^2) a i

1000 n r

500 i s t / a s / e l R sq = 0.97 e l 0.40 l g ( m l n C

c e 0.10 I (

Type III e

t F = 1168 x C / (C^2 +1711^2) e 1250250750 t y ) r a 0.20 response y ) R sq = 0.94 a r a a d c e d / n / n d o 0.30 d i a

n I = (1232 x C^2) / (C^2 +1840^2) i r 1000500 n i s t 0 0.00 a / s / e R sq = 0.97 l 0 2000 4000 6000 8000 10000 12000 e 0 2000 4000 6000 8000 10000 12000 l l g ( m l n C 0.10 I c e (

Prey concentration (cells/ml) e Prey concentration (cells/ml) t

e 250750 t r a 0.20 Heterocapsar a sp. Heterocapsa sp. c e n n o i

I = (1232 x C^2) / (C^2 +1840^2) a 10005000 r 0.001.00 s t a

e 0 2000 4000 R6000 sq = 0.978000 10000 12000 0 2000 4000 6000 8000 10000 12000 Type II e l g F = 479 / (C + 524) n C 0.10 I y ) responsePrey concentration (cells/ml) Prey concentration (cells/ml) y ) a R sq = 0.74 250 a d 800 .80 / d / d

Heterocapsa sp. Heterocapsad sp. n i n i / s / l

l 1000 1.00 0 0.00 600 0 Type2000 II 4000 6000 8000 10000 12000 ( m l .60 0 2000 4000 6000 8000 10000 12000 ( c e e F = 479 / (C + 524) t e t y )

response r a

Prey concentration (cells/ml) y ) Prey concentration (cells/ml) a

r a R sq = 0.74 a

d 800 .80 / d c e n / d n o

400 d .40 i

Heterocapsan sp. Heterocapsa sp. i n r a i s t / a s / e l e l 1000 1.00 l g ( m l n

600 I = (1043 x C) / (C + 2561) C .60 I

( c e Type II e

200 t .20 F = 479 / (C + 524) e

t R sq = 0.81 y ) response r a y ) a r a R sq = 0.74 a

d 800 .80 c e / d n / n d o 400 .40 i d n i r a n s t 0 i .00 a / s / e l 0 2000 4000 6000 8000 10000 e 0 2000 4000 6000 8000 10000 l l g n ( m l

I = (1043 x C) / (C + 2561) C I 600 .60 ( c e

Prey concentration (cells/ml) e Prey concentration (cells/ml)

200 t .20

e R sq = 0.81 t r a

T. r a weissflogii T. weissflogii c e n n

o 400 .40 i 500 r a

s t 0 .00 a e 0 Type2000 II response4000 6000 8000 10000 0 2000 4000 6000 8000 10000 e l g F = 167 / (C + 54)

n 1.25

I = (1043 x C) / (C + 2561) C I

y ) Prey concentration (cells/ml) Prey concentration (cells/ml) y ) R sq = 0.75 a 200 .20 a

d 400 R sq = 0.81 d / / d

T. weissflogii T. d weissflogii n i

n 1.00 i / s /

l 500 l 0 .00 300 0 Type2000 II response4000 6000 8000 10000 ( m l 0 2000 4000 6000 8000 10000 ( c e e F = 167 / (C + 54) t 1.25

e .75 t y ) r a Prey concentration (cells/ml) y ) Prey concentrationR sq (cells/ml) = 0.75 a r a a

d 400 d / c e n / d n o

200 d i

T. n weissflogii T. weissflogii i

n 1.00 r a

i .50 s t / a s / e l e l 500 l g ( m l n

300 C I Type II response ( c e e

I = (402 x C) / (C + 572) t 100 1.25 F = 167 / (C + 54) e .25.75 t y ) r a

y ) R sq = 0.75 a R sq = 0.78 r a a

d 400 c e d / n / n d o 200 i d n i r a n 1.00.50 s t 0 i .00 a / s / e l 0 2000 4000 6000 8000 e 0 2000 4000 6000 8000 l l g n ( m l C

I 300 ( c e Prey concentrationI = (402 (cells/ml) x C) / (C + 572) e Prey concentration (cells/ml)

100 t

e .25.75 t R sq = 0.78 r a r a G. litoralis c e

G.n litoralis

50 n o 200 i

r a 0.60.50

s t 0 .00

150 a e 0 2000 4000 Type 6000III 8000 0 2000 4000 6000 8000 e l g F = 174 x C / (C^2 +254^2) n C I Prey concentrationresponse (cells/ml) Prey concentration (cells/ml) y ) y ) 100 I = (402 x C) / (C + 572) 0.50 R sq = 0.47 a a .25 d d / / R sq = 0.78 d d G. litoralis n G.n litoralis i i / 0.40 s / 0.60 l 100 l 1500 .00 0 2000 4000 Type 6000III 8000 ( m l 0 2000 4000 6000 8000 e

( c e F = 174 x C / (C^2 +254^2) t

e response r a t y ) y ) Prey concentration (cells/ml) 0.500.30 Prey concentrationR sq =(cells/ml) 0.47 a a a r d d c e / / n n d d

o G. litoralis i n n r a i

G.i litoralis / a s t 50 0.400.20 s / e e l 100 0.60 l l g

150 I = (117 x C^2) / (C^2 + 142^2) ( m l C

n Type III I e ( c e R sq = 0.68 t F = 174 x C / (C^2 +254^2) e

response r a 0.10 t

y ) 0.30 y ) 0.50 R sq = 0.47 a a a r c e d d / / n n d d o i r a n n i i 0 0.00 a / s t 0.20 50 0.40 e s / e 0 500 1000 1500 2000 0 500 1000 1500 2000 l l 100 l g I = (117 x C^2) / (C^2 + 142^2) ( m l C n I

Prey concentration (cells/ml) e Prey concentration (cells/ml)

( c e R sq = 0.68 t

e 0.10 r a t 0.30 a r c e n n o i 0 r a 0.00 a s t 0.20 50 0 500 1000 1500 2000

0 500 1000 1500 2000 e e l

g I = (117 x C^2) / (C^2 + 142^2) C n I Prey concentrationR sq = 0.68 (cells/ml) Prey concentration (cells/ml) 0.10

0 0.00 0 500 1000 1500 2000 0 500 1000 1500 2000 Prey concentration (cells/ml) Prey concentration (cells/ml) I. galbana I. galbana 10000 Type III 0.25 F = 8238 * C / (C^2 + 18 841^2)

y ) response

y ) R sq = 0.67 a a

d 8000 0.20 / d / d d

I. galbanan I. galbana i n i / s / l l 10000 0.25 6000 Type III ( m l 0.15 ( c e e

t F = 8238 * C / (C^2 + 18 841^2) e t r a

y ) response

y ) R sq = 0.67 a r a

I = (9453 x C^2) / (C^2 + 22 830^2) a d

8000 c e 0.20 / n d / n o d 4000 0.10

i R sq = 0.99 d n r a i n s t i a / e s / e l l l g n C ( m l I 6000 0.15 ( c e 2000 e 0.05 t e t r a

r a I = (9453 x C^2) / (C^2 + 22 830^2) c e n n

o 4000 0.10

i R sq = 0.99

0 r a 0.00 s t a

e 0 20000 40000 60000 80000 100000 120000 0 20000 40000 60000 80000 100000 120000 e l g n C I Prey concentration (cells/ml) Prey concentration (cells/ml) 2000 0.05 R. salina R. salina

0.40 0 0.00 0 Type20000 III40000 60000 80000 100000 120000 0 20000 40000 60000 80000 100000 120000 1250 F = 1168 x C / (C^2 +1711^2) y )

responsePrey concentration (cells/ml) y ) Prey concentrationR sq =(cells/ml) 0.94 a a d d / /

d 0.30 d

R. n salina R. salina i

1000 n i / s / l l 0.40 ( m l c e (

Type III e t F = 1168 x C / (C^2 +1711^2) e 1250750 t r a y ) 0.20

response y ) R sq = 0.94 a r a a d c e d / n / n o d

i 0.30 d I = (1232 x C^2) / (C^2 +1840^2) a n r i

1000500 n s t i a / e

s / R sq = 0.97 e l l l g n C ( m l 0.10 I c e ( e t

e 750250 t r a 0.20 r a c e n n o i

I = (1232 x C^2) / (C^2 +1840^2) a 5000 r 0.00 s t a

e 0 2000 4000 R6000 sq = 0.978000 10000 12000 0 2000 4000 6000 8000 10000 12000 e l g n C 0.10 I Prey concentration (cells/ml) Prey concentration (cells/ml) 250 Heterocapsa sp. Heterocapsa sp.

1000 1.00 0 Type II 0.00 0 2000 4000 6000 8000 10000 12000 0 2000 4000 6000 F = 8000479 / (C 10000+ 524) 12000

y ) response Prey concentration (cells/ml) y ) Prey concentration (cells/ml) a R sq = 0.74 a

d 800 .80 / d / d d

Heterocapsan sp. Heterocapsa sp. i n i / s / l l 1000 1.00

600 ( m l .60

( c e Type II e

t F = 479 / (C + 524) e t r a y ) response y ) a r a R sq = 0.74 a d

800 c e .80 / n d / n o d 400 .40 i d n r a i n s t i a / e s / e l l l g n C I = (1043 x C) / (C + 2561) ( m l I 600 .60 ( c e 200 e .20 t

e R sq = 0.81 t r a r a c e n n

o 400 .40 i

0 r a .00 s t a

e 0 2000 4000 6000 8000 10000 0 2000 4000 6000 8000 10000 e l g n

I = (1043 x C) / (C + 2561) C I Prey concentration (cells/ml) Prey concentration (cells/ml) 200 R sq = 0.81 .20 T. weissflogii T. weissflogii

500 0 .00 0 Type2000 II response4000 6000 8000 10000 0 2000 4000 6000 8000 10000 1.25 F = 167 / (C + 54) y )

Prey concentration (cells/ml) y ) Prey concentrationR sq (cells/ml) = 0.75 a a

d 400 d / / d d

T. n weissflogii T. weissflogii i

n 1.00 i / s / l l 500

300 ( m l

( c e Type II response e

t F = 167 / (C + 54)

e 1.25.75 t r a y )

y ) R sq = 0.75 a r a a d

400 c e n d / / n o

d 200 i d n r a i

n .50

s t 1.00 i a / e s / e l l g l n C ( m l I 300 ( c e 100 I = (402 x C) / (C + 572) e t

e .75.25 t R sq = 0.78 r a r a c e n n

o 200 i

0 r a .50.00 s t a

e 0 2000 4000 6000 8000 0 2000 4000 6000 8000 e l g n C I Prey concentration (cells/ml) Prey concentration (cells/ml) 100 I = (402 x C) / (C + 572) .25 R sq = 0.78 G. litoralis G. litoralis 0.60 1500 Type III .00 0 2000 4000 6000 8000 0 2000 4000 6000 8000 response F = 174 x C / (C^2 +254^2) y ) y ) Prey concentration (cells/ml) 0.50 Prey concentrationR sq =(cells/ml) 0.47 a a d d / / d d G. litoralis n n i G.i litoralis / 0.40 s /

l 100 0.60 l 150 Type III ( m l e ( c e t F = 174 x C / (C^2 +254^2) e r a t response 0.30 y ) y ) R sq = 0.47 a 0.50 a a r c e d d / n / n o d d i r a n n i i a s t 0.20 50 / e e 0.40 s / l

l 100 g l I = (117 x C^2) / (C^2 + 142^2) C ( m l n I

R sq = 0.68 e ( c e t 0.10 e r a t 0.30 a r c e n n o i

0 r a 0.00 a s t 50 0 500 1000 1500 2000 0.20 0 500 1000 1500 2000 e e l

g I = (117 x C^2) / (C^2 + 142^2) C n I Prey concentrationR sq = 0.68 (cells/ml) Prey concentration (cells/ml) 0.10

0 0.00 0 500 1000 1500 2000 0 500 1000 1500 2000 Prey concentration (cells/ml) Prey concentration (cells/ml)

Fig. 13. Showing functional responses (ingestion rate and clearance rate as functions of prey density) of the Paracartia grani nauplius to various microalgal prey: P. grani vs. Isochrysis galbana, Thalassiosira weissflogii, Rhodomonas salina, Heterocapsa sp. and Gymnodinium litoralis. Maximum ingestion rate values (Imax) estimated from the Holling fits are indicated with a dashed circle. Data from paper IV.

51 5 DISCUSSION component. The same phenomenon has been found in other studies in estuaries 5.1 ZOOPLANKTON IN THE and lagoons associated with the Baltic LITTORAL BALTIC SEA Sea, whereas succession on a spatial scale has generally been found to be 5.1.1 ASPECTS OF DISTRIBUTION comparatively uniform (Gasiūnaitė & Razinkovas 2004; Scheinin & Mattila 2010 but see Koski et al. 1999a). In this Zooplankton species were not evenly study, the extent and patterns of spatial distributed across the salinity gradient heterogeneity in species composition (I), as is the general case with estuarine on a larger scale remained relatively organisms (Segerstråle 1959; Remane & constant regardless of sampling period, Schlieper 1971). A salinity of 4 was found so that the interannual between-site to be an unambiguous boundary value, relationships remained similar, even which segregated freshwater communities though the respective assemblages from more marine ones. A corresponding differed. Therefore, successional range, from freshwater values up to a dynamics were clearly portrayed salinity of 4, has also been found to define throughout the gradient. Rotifers were a low salinity estuarine zone in terms particularly pervasive throughout the of fish and invertebrates (Bulger et al. sampling area, with dominant Keratella 1993). Predictably, salinity was the most species abundant in the MZ in 2009 significant abiotic structuring force on and in the OZ in 2010. This reflected zooplankton composition. Correlations the general patterns in rotifer spatial between the abiotic variables and the succession, which developed from the biota involved either salinity alone warmer, sheltered sites in the early (2010) or salinity and turbidity/chl a sampling to the outer archipelago in the (2009). Salinity limits and preferences of later sampling. zooplankton are known to regulate their long-term distribution patterns in the In terms of zooplankton composition, pelagic, and expectedly this appeared to the transition region was at sites 24 and be the case in the littoral as well (Ojaveer 25, which belonged to either the MZ or et al. 1998; Vuorinen et al. 1998). Factors the IZ depending on sampling year. Both related to productivity (temperature, sites were located at the entrance to the trophic state and phytoplankton biomass) geographical bottleneck between the IZ have also previously been found to and the MZ, and had much lower salinity determine zooplankton composition in values than the offshore high salinity the Baltic Sea (Johansson 1992; Scheinin sites (19 – 23) in the IZ. In general, the & Mattila 2010). zones were differentiated by distinct zone-related taxa (e.g. bivalve larvae in The temporal differences in species the IZ/OZ, cyclopoids in the MZ), or composition were considerable, especially alternatively by varying densities of the concerning the microzooplankton most abundant taxa (e.g. the copepod

52 Acartia, cladoceran Eubosmina and However, this trend was not evident in Keratella rotifers). Cyclopoids and the other highly eutrophic sites. Chemical onychopods are generally limited by pollution, such as pesticides and oil, salinity (e.g. Jennings et al. 1994; Onbé & were other possible segregating factors. Ikeda 1995), but the salinity differences Estuarine zooplankton abundance and on this gradient were too subtle to community structure have been found to directly restrict the distribution of the be altered by pollution, mainly exhibited planktonic crustaceans through strict as a decrease in copepod density, and tolerance limits. This was depicted by the specifically in the Gulf of Finland with sporadic occurrence of cyclopoids in the a reduction in the dominant calanoids OZ and podonid cladocerans in the MZ Eurytemora and Acartia. (Ojaveer et in salinities ˃ and ˂ 4, respectively. The al. 1998; Uriarte & Villate 2004). This low between-site variation south of the corresponds to the significantly lower ecotone supports traditional niche-based calanoid nauplius abundances (2009 and theory, by which deterministic factors, 2010) and lower Eurytemora abundance including environmental conditions, (2009) at site 31 compared to other control local community composition. MZ sites, and the complete absence of Deterministic processes are expected to Acartia (2010). However, it is also worth be of higher influence than stochastic considering that a general decline in processes (e.g. random extinctions mesozooplankton abundance, including or colonizations) in just such harsh abundances of Acartia and Eurytemora, fluctuating environmental conditions has been observed in the Gulf of Finland (Chase 2007; Lepori & Malmqvist 2009). in long-term data, which has been attributed to increasing temperature However, temporally consistent (Suikkanen et al. 2013). differences were found between sites 20 and 31 and other sites in their respective Site 20 was distinct from the other zones. Site 31 differed from the other OZ/IZ sites due to high densities of sites of the MZ due to its extremely high harpacticoids and small cladocerans, densities of all life stages and species and a diverse rotifer population that of cyclopoids and the omnivorous consisted of species not found in other cladoceran Pleopsis polyphemoides, OZ/IZ sites. Site 20 is classified as a which was absent from other MZ semi-enclosed flad, a brackish lagoon in sites. Moreover, a high density and a geomorphometric evolutionary stage in diversity of rotifers, and a distinct lack which it is still in continuous contact with of calanoid copepods differentiated it the sea, but with the natural land-uplift from surrounding sites. Compared to process it is in the process of gradually other sites in its geographical vicinity, becoming isolated from the sea, with the site had extremely high chl a, and slower sea water influx compared to accordingly, eutrophication has been more open bays (Munsterhjelm 2005). found to strengthen the role of rotifers Macrophytes, macroinvertebrate in estuarine communities (Telesh 2004). fauna, and fish assemblages have been

53 found to differ between morphometric 20. Predation may indirectly facilitate developmental stages of bays in the invasion by species at lower trophic northern Baltic, and zooplankton levels, which are otherwise excluded by communities in such shallow bays have interactions with the target prey (Holt et been found to be particularly diverse al. 1994; Leibold 1996). Ceriodaphnia and abundant compared to pelagic was uncommon at other sites but may areas (Appelgren & Mattila 2005; gain a foothold in areas where larger Hansen et al. 2007; Snickars et al. and more actively grazing crustaceans 2009; Scheinin & Mattila 2010). The are removed by predation. Similarly, discrepancy between this site and the we found fish predation to increase other bays suggests that isolation-related rotifer abundance and prevent intense water exchange is also a significant domination by any particular species in a factor in molding coastal zooplankton small-bodied prey community (III). Prey- composition. Preliminary data on fish predator relationships could be a factor biomasses, species composition and in distinguishing this flad site from the stomach contents indicate that three- others. spined sticklebacks occur at the site and readily consume zooplankton (Borg et al. unpublished). The linkages between 5.1.2 ASPECTS OF DIVERSITY zooplankton and environmental variables may be less evident in such stable semi- Functional diversity was inversely enclosed, isolated areas, where predation related to salinity in the field. This is by zooplanktivorous fish can result in to be expected, because competition the efficient top-down control of large structures communities more intensely crustaceans. Biotic interactions, such as in these physically less harsh habitats. predation and competition, are expected to High functional diversity results from be more important in shaping community competitive exclusion characterizing structure in the absence of environmental interactions among species: Organisms stress, and accordingly, species need to feed at different trophic levels, adaptations that promote environmental using different temporal patterns tolerance often trade off with adaptations and feeding strategies to be able to that promote fitness under conditions of coexist (Armstrong & McGehee 1976). intense biotic interactions (Wellborn et However, site 20 was repeatedly al. 1996). A flad resembles a relatively anomalous regarding the salinity- small, ‘closed’ system, where biotic FD relationship, portraying lower relationships play a significant role in diversity than predicted by salinity structuring assemblages because of alone. This is again concurrent with high interaction potential. This is in line intense fish predation, which potentially with the low copepod abundance and decreases prey diversity (Paine 1966). the high diversity of rotifers, as well as Additionally, in the later sampling a high abundance of the small grazing period, turbidity and temperature cladoceran Ceriodaphnia found at site complicated the salinity-FD relationship,

54 with low salinity sites exhibiting lower after which diversity decreased. The FD values than predicted. These sites relationship is similar to that found for had high temperatures towards the crustacean zooplankton in the Baltic Sea end of the summer, which presumably (Telesh et al. 2011). This intermediate would begin to either directly limit the salinity may represent a distinct physico- occurrence of thermophobic crustacean chemical barrier between marine and taxa or indirectly decrease longevity freshwater faunas due to changes in the (e.g. Altshuler 2011), and hence decrease ionic composition of the water, which within-site diversity. This suggests then decreases the diversity of metazoan that at a certain temperature threshold, plankton (Khlebovich 1968). the FD-salinity relationship does not hold. Additionally, FD was higher than predicted by salinity alone at sites with 5.2 PREDATION BY high algal biomass, suggesting that ZOOPLANKTIVOROUS FISH: increased resources result in higher FD IS SELECTION IMPAIRED BY regardless of salinity. In equally shallow TURBIDITY? (II) lake systems, productivity was generally negatively related to zooplankton In the aquarium experiments investigating functional diversity, but the type of turbidity as an environmental deterrent phytoplankton resource was found to of selective predation, the total prey be indicative of the response (Barnett & consumption of sticklebacks decreased in Beisner 2007). elevated turbidity, consistent with other studies on vision-oriented particulate The lowest taxonomic diversity was found feeders (e.g. Nurminen et al. 2010, in the transition zone from freshwater to Estlander et al. 2012). In contrast, several brackish water, at sites 24, 25 and 26 in earlier studies on sticklebacks feeding on 2009. These sites had high densities of larger benthic prey have indicated trivial particular rotifer taxa. The dominance of or even nonexistent decreases in foraging eurytopic species is a common feature success in higher turbidities, suggesting in Baltic estuaries (Telesh 2004), and that sticklebacks may compensate for accordingly, all sites with low diversity visual impairment by chemical cues were dominated by high densities (Quesenberry et al. 2007; Webster et al. of either Keratella cochlearis or K. 2007). However, our result emphasizes quadrata, regardless of zone or sampling the view that zooplanktivory is more period. In agreement with previous vulnerable to decreasing visibility than studies in brackish waters and estuaries benthic feeding on larger and/or sessile (Gasiūnaité 2000; Telesh 2004), our prey (Horppila et al. 2010; Estlander et study did not find a linear relationship al. 2012). between salinity and taxonomic diversity of zooplankton. Instead we found Conversely, increased total prey similar evidence of high diversity at consumption by roach in elevated an intermediate salinity, in this case 5, turbidity was in line with a presumed

55 switch in feeding strategy, from zooplankton body size is known to particulate feeding to filter feeding, correlate with susceptibility to predation specifically to compensate for reduced by zooplanktivorous fish due to factors visibility in turbid water (Lammens related to preference or accessibility et al. 1987). This switch in feeding (Brooks & Dodson 1965; Kohler & Ney strategy has been observed in roach in 1982). Cladocerans are more vulnerable reduced light conditions (Van den Berg than copepods because of inferior escape et al. 1993). The significant increase ability (e.g. Wong 1996; O’Keefe et al. in feeding in turbid water found in our 1998; Kiørboe et al. 1999). The positive experiments indeed implies a switch selection for the daphnid by sticklebacks to an efficient filter feeding mode was consistent throughout the treatments, to maintain, or in this case increase, even though total prey consumption consumption. Similar conclusions have as well as specific consumption of been drawn in a study by Nurminen et al. daphnids decreased in highly turbid 2010. However, low total consumption water. A similar pattern of increased by roach in the clear water control was or unaffected predation on larger prey problematic, as it may have been due to types in diminished visual conditions has uncontrolled factors, such as predation been detected in other vision-oriented risk or schooling behavior. It has been feeders (Mikheev et al. 2004; Salonen & suggested that turbid environments may Engström-Öst 2010). actually offer protection to juvenile fish from their predators (Gradall & Swenson Out of the copepods Acartia was 1982; Gregory & Northcote 1993; consumed at higher rates than Lehtiniemi et al. 2005). An important Eurytemora by sticklebacks in clear factor affecting feeding motivation is water. Higher capture success rates per predation risk (Reiriz et al. 1998), and predator encounter have been recorded juveniles used here may have found it for Acartia, compared to Eurytemora too risky to feed actively in the clear (Viitasalo et al. 2001). In the turbid water control. The decreased foraging treatments this difference in consumption activity subsequently resulted in reduced rates was imperceptible. An early escape encounter rate with prey. Furthermore, response by Acartia may prevent the roach is a facultative schooling encounters with predators in conditions species which aggregates when foraging where visual constraints impair prey (Haberlehner 1988) and could be too detection, dampening the difference intimidated to feed individually. Due to caused by genus-specific capture success these uncertainties, the roach data were rates (Viitasalo et al. 2001). not included in paper II. As expected, roach did not display Selectivity patterns were similar for similar strong selection for Daphnia. both predators in clear water, where Notwithstanding the clear water control the most highly consumed prey type where Daphnia was positively selected, was expectedly the large daphnid, as there was no statistically significant

56 selection for the different prey types. This of the topical interest in eutrophication has also been documented in previous (e.g. Lehtiniemi et al. 2005; Engström- studies on cyprinids (Mikheev et al. 2004; Öst & Mattila 2008; Salonen et al. 2009; Estlander et al. 2010). The aggregating Ajemian et al. 2015). Yet inorganic clay behavior and moderate swimming is also considered a main component velocity of daphnids is expected to render of turbidity in coastal areas (Mobley them prey by default, and vulnerable 1994), which is why our experiments to predation in large clusters by filter were conducted using natural clayish feeding. As previous studies using other sediment to simulate turbidity caused by filter-feeding fish have documented, the resuspension of bottom sediments. these fish tend to be escape-selective Climate change models predict that rather than size-selective zooplankton extreme weather phenomena in Europe predators, with a higher tendency to will become more common during consume zooplankton with poor motility the course of this century (Beniston and inferior swimming ability regardless et al. 2007), which could lead to storm of size, and lower “preferences” for surges and coastal erosion increasing fast-swimming copepods (Drenner et the amounts of inorganic suspended al. 1982; Gophen et al. 1983; Persson solids in the water column. Compared 1987b). In terms of copepod selection, to algal turbidity, which can affect the higher consumption of Eurytemora zooplanktivorous feeding at relatively compared to Acartia in the clear water low levels of ca. 5 – 7 NTU (Salonen control is consistent with escape-selective & Engström-Öst 2010; Salonen & predation. Acartia is more stationary and Engström-Öst 2013), inorganic turbidity ‘alert’, and theoretically more sensitive was not found to affect feeding at to the hydrodynamic disturbance created correspondingly low levels. Both the size by cruising predators that approach at and the shape of the suspended particles high speed (e.g. Viitasalo et al. 1998; influence the scattering and absorption Viitasalo et al. 2001). We did not quantify of light in the water column (Kirk 1981), or record predator swimming behavior, and identifying the source of turbidity is but studies have shown that differential key in assessing effects on feeding. Our feeding behavior in selective and filter results confirm that inorganic turbidity, feeding fish (discontinuous searching, at the extreme levels that can occur in vigorous attacks and repeated strikes vs. estuaries, can be detrimental to visually continuous swimming and schooling) feeding zooplanktivorous fish, but the results in differences in prey capture effects are not directly comparable efficiency, especially when foraging on to those caused by algal turbidity of evasive copepods (Peterka and Matěna equivalent NTU. 2011).

Many of the studies on the effects of turbidity on Baltic zooplanktivores have centered around algal turbidity, because

57 5.3 PREDATION BY (Synchaeta, Keratella and nauplii). ZOOPLANKTIVOROUS FISH: Therefore, smaller zooplankton groups EFFECTS ON ZOOPLANKTON benefited from the presence of fish. Our COMMUNITY (III) results corroborated previous ones, which suggest that total zooplankton abundance 5.3.1 COMMUNITY SIZE STRUCTURE is related to mere predator presence, AND TOTAL ABUNDANCE whereas community composition is more affected by predator type (Des Roches et Zooplankton community size al. 2013). structure can reflect the abundance of zooplanktivorous fish, the intensity of zooplanktivory, or both (Brooks 5.3.2 COMMUNITY COMPOSITION: & Dodson 1965). In our mesocosms, TARGET PREY the structural development of a spring community initially dominated by Predator assemblages can be the defining rotifers was efficiently controlled by the factor of zooplankton community predatory removal of large crustaceans. structure, with even more extensive The differences observed in the two effects than environmental factors, such predators in aquarium experiments as temperature (Meerhoff et al. 2007). were emulated in the community-wide The most obvious predation-related size structure: The intense predation by structuring mechanism is direct removal sticklebacks clearly decreased mean by consumption. In our mesocosms, weighted size of the target prey population, predation effects that were apparently while roach predation merely kept size caused by direct prey removal included from increasing. Large crustaceans were the low densities of the cladocerans presumably the individually sought Pleopsis polyphemoides in the spring target prey of sticklebacks, whereas the and Eubosmina in the summer in overall low crustacean density was likely predator enclosures. These expectedly to encourage feeding on smaller prey inflicted a large part of the dissimilarity by cruising roach. Prey availability and found between the predator enclosures escape ability were more important than and the control, since large crustacean size in shaping the community in roach zooplankton (e.g. Acartia and P. enclosures, and so average zooplankter polyphemoides) are strongly top-down size did not decrease. In the crustacean- controlled (Horsted et al. 1988). Both dominated summer community overall roach and sticklebacks can target large predation effects were more obvious cladocerans according to our aquarium than in the spring. Instead of merely experiments, hence the effect was not suppressing the development of the dependent on predator type. In addition, community towards larger body size, the replacement of Pleopsis with the predation by both predator types actively larger Podon leuckartii was observed decreased mean prey size, and resulted in only in the control. The interactive clear abundance peaks of small species effects of predation and resource

58 competition are generally thought to between the copepods and decreased cause species replacement in seasonal food web persistence by causing the near succession. However, intense predation extinction of Eurytemora (McCann et is considered to keep populations at al. 1998). Eurytemora is expected to be densities where exploitative competition the preferred prey for particulate feeders is not significant enough to cause such because of its larger size, and egg- species replacement (Gliwicz and carrying females are often targeted by Pijanowska 1989). In an extensive study visual predators (Rajasilta & Vuorinen of zooplankton in a littoral area similar 1983), while Acartia is less conspicuous to that surrounding our mesocosms, because of its smaller size and the females’ Scheinin & Mattila (2010) also found egg depositing behavior (Viitasalo et P. leuckartii to be unique to a specific al. 2001). The stickleback-induced mesotrophic site, suggesting that it Eurytemora extinction was in line with may require biotic conditions that are the recent observation of high predation rarely met, for example low levels of pressure eliminating the relevance of zooplanktivory. resource competition as a community- structuring factor, leaving predation alone The effects of predation on copepods to control the prey population (Nicolle were less straightforward, and more et al. 2011). In the roach enclosures dependent on predator type. Established Acartia also became the more abundant copepod populations appeared to even copepod by the final sampling, but benefit from selective visual predation, without Eurytemora extinction. This was with intense nauplii production resulting consistent with results from the aquarium in substantial cohorts of copepodites experiments (II): Predation by cruising and adults in the summer experiments. feeders does not target Eurytemora Zooplanktivory targeted cladocerans as such, but the ‘alertness’ of Acartia over copepods (II), and was more (Viitasalo et al. 2001) may result in efficient at controlling population lower predator encounter rate, rendering increases of cladocerans when copepod it less vulnerable to filter-feeding roach. populations were well-established. In general, predators are expected to The main compositional difference promote diversity when their impact in copepod densities between the two is greater, but not eliminative, on the predators was observed as a change in dominant competing prey. Through this the competitive interaction between mechanism, roach predation maintained the calanoid copepods Eurytemora and prey diversity, which was depicted by the Acartia. Eurytemora benefits from its relatively stable FD values. higher food ingestion rates and probable higher growth efficiency when food However, in the summer experiments resources are adequate (Adrian et al. the interaction was altered due to the 1999), and it clearly dominated the initial community structure and lower spring control. However, stickleback phytoplankton availability. In direct foraging influenced the interplay reversal to the spring experiment,

59 Acartia was clearly more abundant than the result of the aquarium experiments, Eurytemora in the control enclosures. where Acartia was positively selected by The lower phytoplankton availability of sticklebacks, predation appeared to affect the summer period conceivably favored Eurytemora more severely than Acartia Acartia, which has a wider food niche in the mesocosms. This could be due to resulting from its unique capacity for complicated indirect effects of resource raptorial as well as suspension feeding competition induced by predation, or (Gyllenberg 1980; Tiselius 1990; Adrian alternatively the lack of spatial constraints et al. 1999). It is reasonable to assume in comparatively natural surroundings, that increased resources in the form of allowing the evasive strategy of Acartia rotifers and nauplii buffered predation to prevent it from being detected and effects on Acartia. consumed. The specific preference for Acartia by selective zooplanktivory Stickleback predation enhanced could be construed as an artefact of the the difference in relative calanoid experimental setup, although we cannot abundances, since Eurytemora is more be sure of the exact mechanism (direct susceptible to selective predation. removal vs indirect effects) causing the Predation efficiency on Acartia Eurytemora population decline in the was presumably higher in the roach mesocosms. enclosures, resulting in a lower abundance of Acartia compared to the stickleback enclosures. This could be evidence of 5.3.3 COMMUNITY COMPOSITION: a switch in the roach feeding strategy CASCADING EFFECTS in the summer period. Theoretically, large body size of the average prey Predation does not merely affect target encourages particulate feeding in a prey, but can have community-wide zooplanktivore that is capable of both effects due to trophic cascades, changes strategies (Lammens 1985; Lammens in competitive inter-species interactions et al.. 1987). This was supported by the and anti-predator behavior in prey altogether minimal differences between organisms (Eklöv & VanKooten 2001; the predator enclosures in the summer Englund 2005). Much of the variation period, as well as the effective decline in induced by predation in our mesocosm size structure in roach enclosures, which experiments was credited to a few key was a conceivable indication of size- taxa, some of which were components selective feeding. of microzooplankton, and not direct target prey of either predator. Several Clearly, the Acartia/Eurytemora microzooplankton groups (T. lobiancoi interaction indicates that predation in the spring and calanoid nauplii in the experiments in confined aquarium areas summer) underwent a rapid population may not be directly applicable to more surge in the predator enclosures, while natural full-community circumstances. rotifers followed enhanced succession, Contrary to what would be expected from undergoing either a crash (Synchaeta

60 in the spring) or an abrupt rise (K. absence of large cladocerans and other quadrata in the summer). In control crustaceans, such as the large omnivorous enclosures in the absence of predation, copepods, which readily ingest rotifers. microzooplankton densities were much Since fish predation removed larger lower, and presumably limited by either competitors and potential predators, resource competition or direct grazing rotifers rapidly populated the newly by mesozooplankton (Kivi et al. 1993). produced vacant niches due to their fast Heterotrophic protists, such as ciliates, reproductive rates (Likens 2010). The are subject to the same grazing pressure appearance of Keratella cruciformis in by mesozooplankton as similarly sized the spring and the shift from Synchaeta to and shaped phytoplankton, and in the case Keratella in the summer were indications of copepods, they are often the preferred of rapid rotifer succession, as Keratella prey item (Paffenhöfer et al. 2005; Vargas tends to succeed the more aggressively et al. 2006). Therefore, heterotrophic feeding raptorial Synchaeta in Baltic protists and other organisms at the base Sea coastal systems (e.g. Scheinin & of the food web, with the exception Mattila 2010). Meanwhile abundances of relatively impervious armored of Synchaeta and Keratella remained dinoflagellates, are usually kept in check low in control enclosures, where they by grazing, unless fish predation in turn were presumably kept in check by large impedes mesozooplankton, as was the crustaceans. case in the predator enclosures (Sanders & Wickham 1993; Jürgens et al. 1996; Johansson et al. 2004). Microzooplankton 5.3.4 COMMUNITY DIVERSITY can contribute largely to total grazing, often consuming more than 50% of The initial composition of zooplankton primary production (Calbet & Landry community (i.e. seasonal variation) 2004), which could explain why the determined the degree of predation effects predatory removal of mesozooplankton on diversity (III). In an initially diverse grazers was not reflected in significantly summer community the predation effect higher phytoplankton biomass compared was not significant, whereas in a species- to control enclosures. poor spring community, predation by sticklebacks significantly depleted Predator enclosures generally had higher diversity. In the spring, the stickleback rotifer densities than the control during enclosures became dominated by rotifers both experimental periods. Herbivorous and the tintinnid T. lobiancoi, which cladocerans are known to suppress indicated high predation pressure on rotifers through mechanical interference mesozooplankton. Both taxonomic and or exploitative competition, especially functional diversity decreased in the species of Synchaeta, Keratella and stickleback enclosures in the spring Trichocerca (Gilbert 1989). As expected, period, and increased (H´) or remained the rotifers in the predator enclosures same (FD) in the roach enclosures. Initial underwent enhanced succession in the diversity in the spring community was

61 low, and stickleback predation merely either predator. Diversity itself is a removed species and further depleted predation-regulating factor, because diversity. The collapse of functional non-target prey cause weakened diversity in stickleback enclosures in the predator-prey interactions by masking spring reflects diversity on direct target prey, diluting prey concentrations, and/ prey. The collapse resulted from the or confusing predators (Kratina et al. loss of entire functional groups through 2007). In addition, predation on a diverse predation, including groups consisting of cladoceran community likely weakened cyclopoids, cladocerans and herbivorous the link between predators and the copepods. The disappearance of these less vulnerable copepods, which were groups have strong implications on allowed to stabilize their populations. grazing processes, as well as the control Large and diverse cladoceran prey of rotifer populations through direct populations are less likely to be severely consumption (cyclopoids) and resource affected by moderate predation, because competition (cladocerans) (Gilbert of their fast reproductive rates. Overall, 1989; Nagata & Hanazato 2006). The the predation effect was coupled with decrease in taxonomic diversity reflected temporal patterns of seasonality, so that community-wide diversity, including high zooplankton diversity in the summer non-target lower trophic levels, and was mitigated zooplanktivore control of the apparent before any significant decline prey community, regardless of predator in functional diversity. Typically species type. Similarly, high prey diversity has can be removed without obvious decline been shown to moderate the effects of top- in ecosystem functioning due to a degree down control of grazers on phytoplankton of functional redundancy, but once an (Hillebrand & Cardinale 2004). entire functionally similar group expires, the collapse can be dramatic (Woodward 2009). However, in our mesocosms this 5.4 ZOOPLANKTON AS removal of grazers was not reflected in CONSUMERS: COPEPOD a significant increase in phytoplankton NAUPLIUS FEEDING ECOLOGY biomass, possibly due to compensatory (IV) grazing by microzooplankton. Conversely to stickleback effects, The type, quality and amount of predation by the cruising roach did phytoplankton consumed by grazing not cause near extinctions of large zooplankton have immense consequences crustaceans or intense domination by on the survival and reproduction of small plankters, so even with prey grazers in both freshwater (Ahlgren depletion, the functional composition of 1993; Müller-Navarra 1995; Repka the prey community remained similar to 1997) and marine systems (Jonasdottir the control. 1995; Turner & Tester 1997; Sopanen et al. 2006; Vargas et al. 2006). High- In the more diverse summer community quality food sources are critical in there were no effects on diversity by maintaining growth and reproduction in

62 both zooplankton and their predators. mechanism, as it reduces prey mortality It follows that the trophic transfer of when prey populations are low in density, food quality indicators, such as essential and therefore potentially vulnerable to fatty acids, from primary producers to extinction (Murdoch 1969; Roughgarden consumers, is the focus of a myriad of & Feldman 1975). studies (e.g. Müller-Navarra et al. 2000; Brett et al. 2006; Persson & Vrede 2006). As expected for nauplii of the size of Copepod nauplii are a part of aquatic Paracartia grani, the dinoflagellate food webs as important prey for fish Heterocapsa sp. and the diatom T. larvae (Siefert 1972; Munk & Kiørboe weissflogii represented optimum prey in 1985); therefore understanding their terms of size (Berggreen et al. 1988). The feeding ecology is a crucial aspect of daily rations obtained from different prey unraveling aquatic food web processes. types varied to a great extent, suggesting that factors of palatability and prey In this study, the functional responses of morphology result in satiation levels Paracartia grani for various microalgae at differing levels of energy input. For represented either a type II or type III example, prey types can vary in the extent response, depending on prey type. The to which they fill the nauplius gut due to responses were relatively similar in terms different shapes and outer structures. In of ingestion rate, but in terms of clearance general, satiation was achieved at a prey rate, type III responses indicated a concentration of 200 – 500 ng C ml-1. feeding threshold prey concentration, This could be regarded as the energy under which feeding decreased or ceased requirement for P. grani nauplii in non- completely, in order to conserve energy limiting prey conditions. (Price & Paffenhöffer 1985). When the prey concentration and subsequent energy In grazers, the concept of switches in prey gain was not high enough to compensate preference with prey availability may have for energy loss through the predation powerful implications for phytoplankton process, P. grani nauplii demonstrated succession and competition. However, very low clearance rates. This was found in this study nauplius clearance rates in all prey except the optimal prey types remained relatively constant in the Heterocapsa sp. and Thalassiosira plurialgal mixtures, regardless of the weissflogii. Type III responses have concentrations of prey types, with high recently been identified in copepod clearance rates for dinoflagellates. nauplii (e.g. Almeda et al. 2010), and The only exception to this was the low may be more common than previously clearance of Heterocapsa sp. in the thought in zooplankton (Sarnelle & presence of low concentrations of I. Wilson 2008). They have generally not galbana. Further experimentation and been taken into consideration because of actual microscopic observation of feeding a lack of empirical observations at low behavior may reveal the mechanism food levels. Yet the type III response may behind this result, but it may be related be a significant ecosystem stabilizing to complicated interactions between the

63 prey types themselves, which potentially The prevalence of calanoid nauplii in increase encounter rate between predator the field sampling of this study (I), as and prey (Heterocapsa sp.) at higher well as their significance as a resource concentrations of a less targeted prey (I. component in the interactions between galbana). This study emphasizes the need zooplankton and zooplanktivorous for more experimentation on plurialgal predators (III), indicate that their trophic mixtures, which resemble natural role in the coastal Baltic Sea may be more systems. The presence of several prey extensive than previously conceived. types undoubtedly complicates feeding Moreover, the population-age structure relationships because of prey selectivity hypothesis predicts that warming waters, and the added interactions between such as those of the coastal Baltic, present prey, and may result in paradoxical a competitive advantage to younger and observations. smaller age classes by increasing their metabolism (Daufresne et al. 2008; Although P. grani does not occur in the Ohlberger et al. 2011), thereby potentially Baltic Sea, the closely related Acartia is a changing population structure. This could cosmopolitan genus, and results obtained emphasize the role of nauplii as grazers in this study can be incorporated to model in the Baltic Sea ecosystem. In essence, Baltic ecosystem functioning as well. functional response experiments can be a Acartia is often the dominant calanoid useful way to quantify nauplius feeding copepod in Baltic coastal waters, and requirements and subsequent grazing in the central Baltic Sea it has been potential, especially in response to thought to have benefited from the recent phytoplankton dynamics. The resulting trend of increasing water temperature data can be used as direct inputs in food and decreasing salinity (Möllmann et web models. al. 2005). However, a recent long-term study has indicated the exact opposite pattern in the open sea areas of the Gulf of Finland, where increasing temperature was related to Acartia population decline (Suikkanen et al. 2013). A simultaneous shift in phytoplankton community composition from Cryptophyceae, which is considered high-quality food for zooplankton (Lehman & Sandgren 1985), to phytoplankton classes that are an inferior food source, may also partially explain the decrease in Acartia abundance (Ljunggren et al. 2010; Suikkanen et al. 2013).

64 6. CONCLUSIONS AND as phytoplankton control by grazing. FURTHER STUDIES This study emphasized the subtle cascading effects of zooplanktivorous fish on microzooplankton components of Total zooplankton abundance was the food web (III). Moreover, interesting consistently found to be related to temporal implications arise from our experiments variation (I, III), and it directly reflected on the deleterious effects of turbidity the size structure of the community in the on zooplanktivory (II). Three-spined natural ecosystem and in the mesocosms. sticklebacks in the Baltic Sea have been Salinity was a major regulating force of presumed to benefit from climate change, zooplankton community composition, because of higher feeding rates related as it is to communities of other Baltic to increasing temperature (Lefébure et Sea organisms (Ojaveer et al. 2010), al. 2014), coupled with a simultaneous so drastic changes in salinity can be decline in coastal piscivores (Ljunggren expected to have major consequences et al. 2010). However, even if for coastal zooplankton biodiversity. The zooplankton resource levels remain high, experimental results seemed to parallel significant increases in turbidity caused observations in the field, confirming the by climate change-related phenomena, relevance of the predation experiments. such as eutrophication and erosion, could Zooplankton abundance was found to affect stickleback populations if feeding be relatively similar in nature and the efficiency decreases to the extent detected experimental mesocosm communities in our feeding experiments. Nevertheless, in the presence of predation, and despite reportedly high turbidity values additionally comparable with a recent in coastal zones, the turbidity levels study conducted in ecologically similar measured in littoral sampling sites in this areas in the Baltic Sea (Scheinin & study (I) were not currently high enough Mattila 2010). The late summer rotifer to impede feeding to the extent that was abundance peak that occurred in predator observed in the aquarium experiments enclosures in mesocosm experiments is (II). Whether these results can be also observed in the natural Baltic Sea applied to community-wide effects is system (I), suggesting that predation ambiguous without further large-scale effects in the experimental mesocosms experimentation in turbid conditions, as were at least partially comparable to well as experiments combining multiple those in real ecosystems. environmental stressors. However, there is an implication that an environmental Zooplanktivores consume prey change affecting only specific predators according to their physiological needs has the potential to mitigate top-down and capabilities, and control community control, while the role of unaffected structure of zooplankton through their predators may become accentuated. feeding behavior. By doing so, they can eventually have significant impacts on Inspecting zooplankton using trait- ecosystem effects through factors such based approaches is becoming more

65 commonplace, because groupings based on function, rather than taxonomy, are especially useful for studies on food web processes. This study utilized traits that are a direct indicator of interaction through equivalent diets. Nevertheless, functional classification was based largely on the degree of omnivory, rather than specific feeding patterns. To enable a more detailed functional classification of zooplankton based on resource use traits, further species-specific feeding experiments quantifying functional responses are necessary. Future studies should also include functional response types using traits such as generation time, reproductive rate, body size, escape ability and swimming velocity. These could provide indications of community stability and resilience, by quantifying the recovery potential of zooplankton as prey populations.

This thesis adds details to knowledge of the trophic ecology of littoral zooplankton. The main focus has been the abiotic and biotic factors that affect zooplankton community composition and diversity. Because of the strong community-structuring roles of abiotic factors such as salinity and turbidity, as well as biotic factors such as predation, littoral zooplankton communities will undoubtedly be significantly altered along with the changes associated with the forthcoming regime shifts occurring with climate change.

66 ACKNOWLEDGEMENTS I have also had ideal surroundings to conduct field work at: the Tvärminne Zoological Station is such a beautiful I would like to express my gratitude to and special place, where I’ve gotten to my thesis reviewers Dr Maiju Lehtiniemi begin my career as a scientist. There and Professor Mariana Meerhoff for their I’ve experienced both the epiphanies and valuable comments and suggestions, highs of success, as well as the struggles which greatly improved this thesis. I and the downtrodden exhaustion. I want would also like to thank my opponent to thank all the staff at Tvärminne for Professor Jonathan Shurin, as well as providing such a great place to work, but Professor Jukka Horppila for acting as especially Veijo Kinnunen, Dr Joanna the custos at the public examination and Norkko, Professor Alf Norkko, Dr Jaana for all the practical help leading to the Koistinen, Antti Nevalainen and Mariella publication of this thesis. Holstein-Myllyoja, who always took an interest in my work and went out of their This PhD project, like many before it, way to help with all kinds of practical began by chance: Plankton samples hitches. Also zooplankton experts Dr without a purpose transformed into Matias Scheinin and Dr Jonna Engström- an ambitious adventure, and what an Öst are acknowledged for providing amazing ride it has been, involving so advice and expertise. many people I need to thank. Firstly, Dr Leena Nurminen, my primary I had the opportunity to spend three supervisor, has been a huge influence months working at the Institut de Ciències and driving force of this project, and she del Mar in Barcelona, and would like to literally taught me how to write all over thank all the brilliant people of the Marine again. I have so much respect for you and Zooplankton Ecology Group for making your academic achievements, as well as me feel so welcome: Dr Albert Calbet, gratitude for all that you have done for Professor Guilherme Bersano, Dr Miguel me and this project over the years. Thank Alcaraz, Dr Stamatina Isari, Kaiene you for this opportunity! My supervisors Griffell, and most of all my supervisor Professor Hannu Lehtonen, Dr Elina Dr Enric Saiz. I had an incredibly Leskinen and Dr Marko Reinikainen educational (and enjoyable) time at ICM have provided major support during this and learned so much. The admirable project, dedicated a substantial amount proficiency, enthusiasm and passion of time to manuscripts and to help me I got to experience in the lab were so progress, and offered their expertise infectious, and really confirmed my own whenever needed. I would also like to interest in zooplankton ecophysiology. thank my thesis advisory committee Dr Lehtiniemi and Dr Jaanika Blomster, for Moreover I would like to thank all the their support and advice. I have had a people I worked with on a daily basis at great expert team to work with. the Aquatic Sciences section in Viikki, especially the brilliant ladies I had

67 the honor to share 4713 with: Jenni K, Anna I, Sandra L, Julia S, Alex B and Laura V, Zeynep PH, Sanna L and Satu Emma T: all inspiring, intelligent people. E. It was truly a pleasure! Thanks for And of course my teaching colleagues the laughs, conversations and advice, and my students – I learned so much and thanks for being there. I could not from them, hopefully taught them a thing have wished for better colleagues, who or two, and even inspired a few future turned into friends. I would also like marine biologists! to acknowledge our technicians Raija Mastonen and Jouko Sarén for their On a personal level, I want to thank my vital presence and help in the lab, and mom and dad, Tarja and Matti, who have the doctoral program coordinator Anni always supported me unconditionally, Tonteri for her advice and assistance with but rationally. You’ve always pushed me travel grants and postgrad courses. Much to be the best that I can be. Every single credit goes to Nica B, my co-author and thing you’ve done, I’m grateful for, and original partner in crime, who taught this I doubt I will ever be able to repay you plankton ecologist everything she needed for everything or express my gratitude as to know about fishing – it all started with much as you deserve it. I’m just lucky to you! Zeynep PH and Nica B are both have been brought up by such intelligent, also acknowledged for taking the time to brave and loving parents. My siblings read and provide essential insights on an Katja, the original Dr Helenius, and earlier version of this thesis. I’d like to Janne, the multitalent: you’re my idols. thank Anna AP for being my colleague, Thanks for the awesome conversations, co-author and more importantly, friend. the laughs, the support and for just We made a great team, and Titanic, being you. Also for always being ready Goliath and co finally triumphed – the to drive to Tvärminne with me to pack next cheap beers are on me! I also owe up hundreds of plankton samples, build huge thanks to all our field and lab crew mesocosms or collect mud. Janne you’re throughout the years, including the practically a marine biologist yourself, ‘French guys’ Yoan, Romain, Yohann after all the field work you’ve helped and Damien, as well as Roosa and Elina. me with. You deserve special thanks None of this work would have been for making Helsinki home for me, possible without all your efforts. Irene unwinding with Trivial Pursuit nights Virtanen is acknowledged for doing an and dinners at Umeshu. I’m generally in excellent job with the layout of the thesis. awe of how great my family is! Thank you for all of it. I’d also like to thank all the wonderful people I have met on courses and in I want to thank my friends around the meetings in Helsinki, Greenland, USA, world, always supporting me from afar Scotland, Sweden and England, and the and having me escape Helsinki to visit other places I’ve had the chance to visit you, especially Karla K, Lieve dP, Nick during these years. Special thanks to S, Shelley R, Donna H, Giulia C and Sofia F, Anna T, Teresa C, Florence D, Vicky M. Thank you to those that suffered

68 through some pretty dire Helsinki winters with me and survived: Suvi R, Alex G, Maria L, and also my precious oldest friends in Finland, whose support and company I appreciate immensely: Kristiina M, Camilla H and Anne K.

And of course to Zack, across the ocean, for everything.

I am extremely grateful for all the funding that has made this thesis possible. This PhD project was financially supported by the University of Helsinki Research Foundation and the Walter and Andrée de Nottbeck Foundation. The DENVI doctoral program, University of Helsinki Department of Environmental Sciences, the Finnish Concordia Fund, Societas Pro Fauna et Flora Fennica and Maa- ja vesitekniikan tuki ry have also provided funding with project and travel grants.

It’s been amazing. On to new adventures.

69 REFERENCES

Ackefors H (1981) Zooplankton. In: Voipio A (ed) The Baltic Sea. Amsterdam Elsevier. pp 238 – 255.

Adrian R, Hansson S, Sandin B, De Stasio B & Larsson U (1999) Effects of food availability and predation on a marine zooplankton community: A study on copepods in the Baltic Sea. International Review of Hydrobiology 84(6): 609 – 626.

Ahlgren G (1993) Seasonal variation of fatty acid content in natural phytoplankton in two eutrophic lakes. A factor controlling zooplankton species? Verhandlungen der Internationale Vereinigung für theoretische und angewandte Limnologie 25: 144 – 144.

Ahlgren G, Lundstedt L, Brett M & Forsberg C (1990) Lipid composition and food quality of some freshwater phytoplankton for cladoceran zooplankters. Journal of Plankton Research 12(4): 809 – 818.

Ajemian MJ, Sohel S & Mattila J (2015) Effects of turbidity and habitat complexity on antipredator behavior of three-spined sticklebacks (Gasterosteus aculeatus). Environmental Biology of Fishes 98(1): 45 – 55.

Albertsson J & Leonardsson K (2001) Deposit-feeding amphipods (Monoporeia affinis) reduce the recruitment of copepod nauplii from benthic resting eggs in the northern Baltic Sea. Marine Biology 138(4): 793 – 801.

Alenius P, Myrberg K & Nekrasov A (1998) The physical oceanography of the Gulf of Finland: a review. Boreal Environment Research 3(2): 97 – 125.

Almeda R, Augustin CB, Alcaraz M, Calbet A & Saiz E (2010) Feeding rates and gross growth efficiencies of larval developmental stages of Oithona davisae (Copepoda, Cyclopoida). Journal of Experimental Marine Biology and Ecology 387: 24 – 35.

Altshuler I, Demiri B, Xu S, Constantin A, Yan ND & Cristescu ME (2011) An integrated multi-disciplinary approach for studying multiple stressors in freshwater ecosystems: Daphnia as a model organism. Integrative and Comparative Biology 10.1093/icb/icr103.

Appelgren K & Mattila J (2005) Variation in vegetation communities in shallow bays of the northern Baltic Sea. Aquatic Botany 83: 1 – 13.

Armstrong RA & McGehee R (1976) Coexistence of species competing for shared resources. Theoretical Population Biology 9(3): 317 – 328.

Baardseth E (1970) A square-scanning,two stage sampling method of estimating seaweed quantities. Reports of the Norwegian Institute of Seaweed Research 33:1–41.

Bady P, Dolédec S, Fesl C, Gayraud S, Bacchi M & Schöll F (2005) Use of invertebrate traits for the biomonitoring of European large rivers: the effects of sampling effort on genus richness and functional diversity. Freshwater Biology 50(1): 159 – 173.

Barnett A & Beisner BE (2007) Zooplankton biodiversity and lake trophic state: explanations invoking resource abundance and distribution. Ecology 88(7): 1675 – 1686.

Barnett AJ, Finlay K & Beisner BE (2007) Functional diversity of crustacean zooplankton communities: towards a trait‐based classification.Freshwater Biology 52(5): 796 – 813.

Benfield MC & Minello TJ (1996) Relative effects of turbidity and light intensity on reactive distance and feeding of an estuarine fish.Environmental Biology of Fishes 46(2): 211 – 216.

Beniston M, Stephenson DB, Christensen OB, Ferro CA, Frei C, Goyette S, Halsnaes K, Holt T, Jylhä K, Koffi B, Palutikof J, Schöll R, Semmler T & Woth, K. (2007). Future extreme events in European climate: an exploration of regional climate model projections. Climatic Change 81(1): 71 – 95.

Black II RW & Hairston Jr NG (1988) Predator driven changes in community structure. Oecologia 77(4): 468 – 479.

Bonsdorff E, Laine O, Hänninen J, Vuorinen I & Norkko A (2003) Zoobenthos of the outer archipelago waters (N. Baltic Sea) – the importance of local conditions for spatial distribution patterns. Boreal Environment Research 8(2): 135 – 145.

Boström C, O’Brien K, Roos C & Ekebom J (2006) Environmental variables explaining the structural and functional diversity of seagrass macrofauna in an archipelago landscape. Journal of Experimental Marine Biology and Ecology 335(1): 52 – 73.

Brett MT, Wiackowski K, Lubnow FS, Mueller-Solger A, Elser JJ & Goldman CR (1994) Species-dependent effects of zooplankton on planktonic ecosystem processes in Castle Lake, California. Ecology 75(8): 2243 – 2254.

Brett MT & Goldman CR (1996) A meta-analysis of the freshwater trophic cascade. Proceedings of the National Academy of Sciences 93(15): 7723 – 7726.

Brett MT & Müller-Navarra DC (1997) The role of highly unsaturated fatty acids in aquatic foodweb processes. Freshwater Biology 38: 483 – 499.

70 Brett MT, Müller-Navarra DC, Ballantyne AP, Ravet JL & Goldman CR (2006) Daphnia fatty acid composition reflects that of their diet. Limnology and Oceanography 51(5): 2428 – 2437.

Brooks JL & Dodson SI (1965) Predation, body size and composition of plankton. Science 150(3692): 28 – 35.

Bulger AJ, Hayden BP, Monaco ME, Nelson DM & McCormick-Ray MG (1993) Biologically-based estuarine salinity zones derived from a multivariate analysis. Estuaries and Coasts 16(2): 311 – 322.

Calbet A & Landry MR (2004) Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems. Limnology and Oceanography 49(1): 51 – 57.

Cardinale BJ, Palmer MA & Collins SL (2002) Species diversity enhances ecosystem functioning through interspecific facilitation. Nature 415(6870): 426 – 429.

Carpenter SR, Kitchell JF & Hodgson JR (1985) Cascading trophic interactions and lake productivity. BioScience 35(10):634 – 639.

Carpenter SR & Kitchell JF (1996) The trophic cascade in lakes. Cambridge University Press. 400 pp.

Casini M, Lövgren J, Hjelm J, Cardinale M, Molinero JC & Kornilovs G (2008) Multi-level trophic cascades in a heavily exploited open marine ecosystem. Proceedings of the Royal Society of London B: Biological Sciences 275(1644): 1793 – 1801.

Castellani C, Irigoien X, Harris RP & Holliday NP (2007) Regional and temporal variation of Oithona spp. biomass, stage structure and productivity in the Irminger Sea, North Atlantic. Journal of Plankton Research 29(12):1051 – 1070.

Cederwall H & Elmgren R (1990) Biological effects of eutrophication in the Baltic Sea, particularly the coastal zone. Ambio: A Journal of the Human Environment 19(3): 109 – 112.

Chang KH, Nagata T & Hanazato T (2004) Direct and indirect impacts of predation by fish on the zooplankton community: an experimental analysis using tanks. Limnology 5(2): 121 – 124.

Chase JM (2007) Drought mediates the importance of stochastic community assembly. Proceedings of the National Academy of Sciences 104(44): 17430 – 17434.

Chase JM, Abrams PA, Grover JP, Diehl S, Chesson P, Holt RD, Richards SA, Nisbet RM & Case TJ (2002) The interaction between predation and competition: a review and synthesis. Ecology Letters 5(2): 302 – 315.

Chase JM, Biro EG, Ryberg WA & Smith KG (2009) Predators temper the relative importance of stochastic processes in the assembly of prey metacommunities. Ecology Letters 12(11): 1210 – 1218.

Chesson J (1978) Measuring preference in selective predation. Ecology 59(2): 211-215

Chesson P (2000) Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics 31:343 – 366.

Chow-Fraser P & Sprules WG (1992) Type-3 functional response in limnetic suspension-feeders, as demonstrated by in situ grazing rates. Hydrobiologia 232(3): 175 – 191.

Connell JH (1978) Diversity in tropical rain forests and coral reefs. Science 199(4335): 1302 – 1310.

Cryer M, Peirson G & Townsend CR (1986) Reciprocal interactions between roach, Rutilus rutilus, and zooplankton in a small lake: Prey dynamics and fish growth and recruitment.Limnology and Oceanography 31(5): 1022-1038.

Cyrus DP & Blaber SJM (1987) The influence of turbidity on juvenile marine fishes in estuaries. Part 1. Field studies at Lake St. Lucia on the southeastern coast of Africa. Journal of Experimental Marine Biology and Ecology 109(1): 53 – 70.

Dalpadado P, Ellertsen B, Melle W & Dommasnes A (2000) Food and feeding conditions of Norwegian spring-spawning herring (Clupea harengus) through its feeding migrations. ICES Journal of Marine Science 57(4): 843 – 857.

Daufresne M, Lengfellner K & Sommer U (2009) Global warming benefits the small in aquatic ecosystems.Proceedings of the National Academy of Sciences 106(31): 12788 – 12793. de Jonge VN (1974) Classification of brackish coastal inland waters.Hydrobiological Bulletin 8(1-2): 29 – 39.

DeMott WR & Kerfoot WC (1982) Competition among cladocerans: nature of the interaction between Bosmina and Daphnia. Ecology 63(6): 1949 – 1966.

Des Roches S, Shurin JB, Schluter D & Harmon LJ (2013) Ecological and evolutionary effects of stickleback on community structure. PloS One 8(4): e59644.

Desvilettes C, Bourdier G & Breton JC (1997) Changes in lipid class and fatty acid composition during development in pike (Esox lucius L) eggs and larvae. Fish Physiology and Biochemistry 16(5): 381 – 393.

Diehl S (1988) Foraging efficiency of three freshwater fishes: effects of structural complexity and light.Oikos 53(2): 207 – 214.

71 Drenner RW, Strickler JR & O’brien WJ (1978) Capture probability: the role of zooplankter escape in the selective feeding of planktivorous fish.Journal of the Fisheries Research Board of Canada 35(10): 1370 – 1373.

Drenner RW, deNoyelles Jr F & Kettle D (1982) Selective impact of filter-feeding gizzard shad on zooplankton community structure. Limnology and Oceanography 27(5): 965 – 968.

Dunne JA, Williams RJ & Martinez ND (2004) Network structure and robustness of marine food webs. Marine Ecology Progress Series 273: 291 – 302.

Eklöv P & VanKooten T (2001) Facilitation among piscivorous predators: effects of prey habitat use. Ecology 82(9): 2486 – 2494.

Elliott M & Hemingway KL (eds) (2002) Fishes in Estuaries. Blackwell. 636 p.

Elmgren R (1984) Trophic dynamics in the enclosed brackish Baltic Sea. Rapports et Procès-Verbaux des Réunions du Conseil International pour L’Exploration de la Mer 183: 152 – 169.

Englund G (2005) Scale dependent effects of predatory fish on stream benthos.Oikos 111(1): 19 – 30.

Engström J, Koski M, Viitasalo M, Reinikainen M, Repka S & Sivonen K (2000) Feeding interactions of the copepods Eurytemora affinis and Acartia bifilosa with the cyanobacteria Nodularia sp. Journal of Plankton Research 22(7): 1403 – 1409.

Engström-Öst J & Mattila J (2008) Foraging, growth and habitat choice in turbid water: an experimental study with fish larvae in the Baltic Sea. Marine Ecology Progress Series 359: 275 – 281.

Eriksson BK, Ljunggren L, Sandström A, Johansson G, Mattila J, Rubach A, Råberg S & Snickars M (2009) Declines in predatory fish promote bloom-forming macroalgae.Ecological Applications 19(8): 1975 – 1988.

Eriksson BK, Sieben K, Eklöf J, Ljunggren L, Olsson J, Casini M & Bergström U (2011) Effects of altered offshore food webs on coastal ecosystems emphasize the need for cross-ecosystem management. Ambio: A Journal of the Human Environment 40(7): 786 – 797.

Estlander S, Nurminen L, Olin M, Vinni M, Immonen S, Rask M, Ruuhijärvi J, Horppila J, Lehtonen H. (2010) Diet shifts and food selection of perch Perca fluviatilis and roach Rutilus rutilus in humic lakes of varying water colour. Journal of Fish Biology 77(1): 241 – 256.

Estlander S, Horppila J, Olin M, Vinni M, Lehtonen H, Rask M & Nurminen L (2012) Troubled by the humics – effects of water colour and interspecific competition on the feeding efficiency of planktivorous perch. Boreal Environment Research 17(3-4): 305 – 312.

Fernandéz F (1979) Particle selection in the nauplius of Calanus pacificus. Journal of Plankton Research 1(4): 313 – 328.

Forró L, Korovchinsky NM, Kotov AA & Petrusek A (2008) Global diversity of cladocerans (Cladocera; Crusteacea) in freshwater. Hydrobiologia 595: 177 – 184.

Froneman PW (2001) Seasonal changes in zooplankton biomass and grazing in a temperate estuary, South Africa. Estuarine, Coastal and Shelf Science 52(5): 543 – 553.

Froneman PW (2004) Zooplankton community structure and biomass in a southern African temporarily open/closed estuary. Estuarine, Coastal and Shelf Science 60(1):125 – 132.

Frost BW (1972) Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus. Limnology and Oceanography 17(6): 805 – 819.

Fryer G (1986) Structure, function and behaviour, and the elucidation of evolution in copepods and other crustaceans. Syllogeus 58: 150 – 157.

Fussmann GF & Blasius B (2005) Community response to enrichment is highly sensitive to model structure. Biology Letters 1(1): 9 – 12.

Gaard E & Reinert J (2002) Pelagic cod and haddock juveniles on the Faroe plateau: distribution, diets and feeding habitats, 1994 – 1996. Sarsia: North Atlantic Marine Science 87(3): 193 – 206.

Gardner MB (1981) Mechanisms of size selectivity by planktivorous fish: a test of hypotheses.Ecology 62(3): 571 – 578.

Garstecki T, Verhoeven R, Wickham S & Arndt H (2000) Benthic-pelagic coupling: A comparison of the community structure of benthic and planktonic heterotrophic protists in shallow inlets of the southern Baltic. Freshwater Biology 45(2): 147 – 167.

Gasiūnaitė ZR & Razinkovas A (2004) Temporal and spatial patterns of crustacean zooplankton dynamics in a transitional lagoon ecosystem. Hydrobiologia 514(1-3): 139 – 149.

Gaughan DJ & Potter IC (1995) Composition, distribution and seasonal abundance of zooplankton in a shallow, seasonally closed estuary in temperate Australia. Estuarine, Coastal and Shelf Science 41(2): 117 – 135.

72 Gilbert JJ (1989) The effect of Daphnia interference on a natural rotifer and ciliate community: Short-term bottle experiments. Limnology and Oceanography 34(3): 606 – 617.

Gliwicz ZM (1970) Calculation of food ration of zooplankton community as an example of using laboratory data for field conditions.Polskie Archiwum Hydrobiologii 17(30): 169 – 175.

Gliwicz ZM & Pijanowska J (1989) The role of predation in zooplankton succession. In: Plankton Ecology: Succession in Plankton Communities. Springer Berlin Heidelberg. pp. 253 – 296.

Gophen M, Drenner RW & Vinyard GL (1983) Cichlid stocking and the decline of the galilee saint peter’s fish Sarotherodon( galilaeus) in Lake Kinneret, Israel. Canadian Journal of Fisheries and Aquatic Sciences 40(7): 983 – 986.

Gradall KS & Swenson WA (1982) Responses of brook trout and creek chubs to turbidity. Transactions of the American Fisheries Society 111(3): 392 – 395.

Granqvist M & Mattila J (2004) The effects of turbidity and light intensity on the consumption of mysids by juvenile perch (Perca fluviatilis L.). Hydrobiologia 514: 93 – 101.

Gregory R & Northcote T (1993) Surface, planktonic, and benthic foraging by juvenile chinook salmon (Oncorhynchus tshawytscha) in turbid laboratory conditions. Canadian Journal of Fisheries and Aquatic Sciences 50(2): 233 – 240.

Gulati R & DeMott W (1997) The role of food quality for zooplankton: remarks on the state-of-the-art, perspectives and priorities. Freshwater Biology 38(3): 753 – 768.

Gyllenberg G (1980) Feeding of the copepod Eurytemora hirundoides (Crustacea) on different algal cultures. Annales Zoologici Fennici 17:181 – 184.

Haberlehner E (1988) Comparative analysis of feeding and schooling behaviour of the Cyprinidae Alburnus alburnus (L., 1758), Rutilus rutilus (L., 1758), and Scardinius erythrophthalmus (L., 1758) in a backwater of the Danube near Vienna. Internationale Revue der gesamten Hydrobiologie und Hydrographie 73(5): 537 – 546.

Halme E (1944) Planktologische Untersuchungen in der Pojo- Bucht und angrenzenden Gewässern. I. Milieu und Gesamtplankton. Annales Zoologici Societatis Zoologicae-Botanicae Fennicae ‘Vanamo’ 10(2): 1 – 180.

Hansen JP, Wikström S & Kautsky L (2007) Effects of water exchange and vegetation on the macroinvertebrate fauna composition of shallow land-uplift bays in the Baltic Sea. Estuarine, Coastal and Shelf Science 77(3): 535 – 547.

Hansson S, Larsson U & Johansson S (1990) Selective predation by herring and mysids, and zooplankton community structure in a Baltic Sea coastal area. Journal of Plankton Research 12(5): 1099-1116.

Hansson L, Nicolle A, Brodersen J, Romare P, Nilsson P & Brönmark C (2007) Consequences of fish predation, migration, and juvenile ontogeny on zooplankton spring dynamics. Limnology and Oceanography 52(2):696 – 706.

Hayes JW & Rutledge MJ (1991) Relationship between turbidity and fish diets in Lakes Waahi and Whangape, New Zealand. New Zealand Journal of Marine and Freshwater Research 25(3): 297 – 304.

HELCOM (2009) Eutrophication in the Baltic Sea – An integrated thematic assessment of the effects of nutrient enrichment and eutrophication in the Baltic Sea region. Baltic Sea Environment Proceedings No. 115B (Andersen JH & Laamanen M, Eds). 152 p.

Henriksen CI, Saiz E, Calbet A & Hansen BW (2007) Feeding activity and swimming patterns of Acartia grani and Oithona davisae nauplii in the presence of motile and non-motile prey. Marine Ecology Progress Series 331:119 – 129.

Hillebrand H (2003) Opposing effects of grazing and nutrients on diversity. Oikos, 100(3): 592 – 600.

Hillebrand H & Cardinale BJ (2004) Consumer effects decline with prey diversity. Ecology Letters 7(3): 192 – 201.

Hillebrand H & Shurin J (2005) Biodiversity and aquatic food webs. In: Belgrano A (ed) Aquatic food webs: an ecosystem approach. Oxford University Press pp. 184 – 197.

Holt RD (1984) Spatial heterogeneity, indirect interactions, and the coexistence of prey species. American Naturalist 124(3): 377 – 406.

Holt RD, Grover J & Tilman D (1994) Simple rules for interspecific dominance in systems with exploitative and apparent competition. American Naturalist 144(5): 741 – 771.

Hooper DU & Vitousek PM (1997) Effects of plant composition and diversity on ecosystem processes. Science 277(5330): 1302 – 1305.

Horppila J, Olin M, Vinni M, Estlander S, Nurminen L, Rask M, Ruuhijärvi J & Lehtonen H (2010) Perch production in forest lakes: the contribution of abiotic and biotic factors. Ecology of Freshwater Fish 19(2): 257 – 266.

Horsted SJ, Nielsen TG, Riemann B, Pock-Steen J & Bjørnsen PK (1988) Regulation of zooplankton by suspension-feeding

73 bivalves and fish in estuarine enclosures.Marine Ecology Progress Series 48(3): 217 – 224.

Horton PA, Rowan M, Webster KE & Peters RH (1979) Browsing and grazing by cladoceran filter feeders. Canadian Journal of Zoology 57(1): 206 – 212.

Hällfors G, Niemi Å, Ackefors H, Lassig J & Leppäkoski E (1981) Biological oceanography. In: The Baltic Sea, Elsevier Netherlands pp. 219 – 274.

Iyer N & Rao T (1996) Responses of the predatory rotifer Asplanchna intermedia to prey species differing in vulnerability: laboratory and field studies.Freshwater Biology 36(3): 521 – 533.

Jennings CD, Greenwood JG & Kay BH (1994) Response of Mesocyclops (Cyclopoida: Copepoda) to biological and physicochemical attributes of rainwater tanks. Environmental Entomology 23(2): 479 – 486.

Jeppesen E, Søndergaard M, Sortkjoær O, Mortensen E & Kristensen, P (1990) Interactions between phytoplankton, zooplankton and fish in a shallow, hypertrophic lake: a study of phytoplankton collapses in Lake Søbygård, Denmark. Hydrobiologia 191(1): 149 – 164.

Jeppesen E, Sondergaard M, Sondergaard M & Christofferson K (Eds) (2012) The structuring role of submerged macrophytes in lakes (Vol. 131). Springer Science & Business Media. 377 p.

Johansson S (1992) Regulating factors for coastal zooplankton community structure in the northern Baltic Proper. PhD thesis, Stockholm University.

Johansson M, Gorokhova E & Larsson U (2004) Annual variability in ciliate community structure, potential prey and predators in the open northern Baltic Sea proper. Journal of Plankton Research 26(1): 67 – 80.

Jonasdottir SH, Fields D & Pantoja S (1995) Copepod egg production in Long Island Sound, USA, as a function of the chemical composition of seston. Marine Ecology Progress Series 119(1): 87 – 98.

Jürgens K & DeMott WR (1995) Behavioral flexibility in prey selection by bacterivorous nanoflagellates.Limnology and Oceanography 40(8): 1503 – 1507.

Katechakis A, Stibor H, Sommer U & Hansen T (2002) Changes in the phytoplankton community and microbial food web of Blanes Bay (Catalan Sea, NW Mediterranean) under prolonged grazing pressure by doliolids (Tunicata), cladocerans or copepods (Crustacea). Marine Ecology Progress Series 234: 55 – 69.

Khlebovich VV (1968) Some peculiar features of the hydrochemical regime and the fauna of mesohaline waters. Marine Biology 2(1):47 – 49.

Kiørboe T, Saiz E & Visser A (1999) Hydrodynamic signal perception in the copepod Acartia tonsa. Marine Ecology Progress Series 179: 97 – 111.

Kiørboe T, Saiz E & Viitasalo M (1996). Prey switching behaviour in the planktonic copepod Acartia tonsa. Marine Ecology Progress Series 143(1-3): 65 – 75.

Kirk JTO (1981) Estimation of the scattering coefficient of natural waters using underwater irradiance measurements.Australian Journal of Marine and Freshwater Research 32: 533 – 539.

Kivi K, Kaitala S, Kuosa H, Kuparinen J, Leskinen E, Lignell R, Marcussen B & Tamminen T (1993) Nutrient limitation and grazing control of the Baltic plankton community during annual succession. Limnology and Oceanography 38(5): 893 – 905.

Kleppel GS (1993) On the diet of calanoid copepods. Marine Ecology Progress Series 99: 183 – 195.

Kohler CC & Ney JJ (1982) A comparison of methods for quantitative analysis of feeding selection of fishes. Environmental Biology of Fishes 7(4): 363 – 368.

Kondoh M (2003) Foraging adaptation and the relationship between food-web complexity and stability. Science 299(5611): 1388 – 1391.

Koroleff F (1979) Methods for chemical analysis of seawater. Meri 7: 1 – 60 (in Finnish).

Koski M, Viitasalo M & Kuosa H (1999a) Seasonal development of meso-zooplankton biomass and production on the SW coast of Finland. Ophelia 50(2): 69 – 91.

Koski M, Rosenberg M, Viitasalo M, Tanskanen S & Sjolund U (1999b) Is Prymnesium patelliferum toxic for copepods? Grazing, egg production, and egestion of the calanoid copepod Eurytemora affinis in mixtures of ‘’good’’ and ‘’bad’’ food. ICES Journal of Marine Science 56: 131 – 139.

Kratina P, Vos M & Anholt BR (2007) Species diversity modulates predation. Ecology 88(8): 1917 – 1923.

Krylov PI (1988) Predation of the freshwater cyclopoid copepod Megacyclops gigas on lake zooplankton: Functional response and prey selection. Archiv fur Hydrobiologie. Stuttgart 113(2): 231 – 250.

74 Kullenberg G (1981) Physical oceanography. In: The Baltic Sea, Elsevier Netherlands pp. 135 – 181.

Lammens EH (1985) A test of a model for planktivorous filter feeding by breamAbramis brama. Environmental Biology of Fishes 13(4): 289 – 296.

Lammens E, Geursen J & McGillavry PJ (1987) Diet shifts, feeding efficiency and coexistence of bream Abramis( brama), roach (Rutilus rutilus) and white bream (Blicca bjoerkna) in hypertrophic lakes. Paper presented at the Proceedings of the V Congress of European Ichthyologists (Kullander S, Fernholm B, Eds):153 – 162.

Lampitt RS & Gamble JC (1982) Diet and respiration of the small planktonic marine copepod Oithona nana. Marine Biology 66(2): 185 – 190.

Lappalainen A, Rask M, Koponen H & Vesala S (2001) Relative abundance, diet and growth of perch (Perca fluviatilis) and roach (Rutilus rutilus) at Tvärminne, northern Baltic Sea, in 1975 and 1997: Responses to eutrophication? Boreal Environment Research 6(2): 107 – 118.

Lazzaro X (1987) A review of planktivorous fishes: their evolution, feeding behaviours, selectivities, and impacts.Hydrobiologia 146(2): 97 – 167.

Lefébure R, Larsson S & Byström P (2014) Temperature and size-dependent attack rates of the three-spined stickleback (Gasterosteus aculeatus); are sticklebacks in the Baltic Sea resource-limited? Journal of Experimental Marine Biology and Ecology 451: 82 – 90.

Lehman JT & Sandgren CD (1985) Species-specific rates of growth and grazing loss among freshwater algae.Limnology and Oceanography 30(1): 34 – 46.

Lehtiniemi M, Engström-Öst J & Viitasalo M (2005) Turbidity decreases anti-predator behaviour in pike larvae, Esox lucius. Environmental Biology of Fishes 73(1): 1 – 8.

Lehtonen H & Rask M (2004) Fishes and fisheries. In: Eloranta P (ed.)Inland and Coastal Waters of Finland. University of Helsinki. SIL XXIX Congress Lahti Finland.

Leibold MA (1996) A graphical model of keystone predators in food webs: trophic regulation of abundance, incidence, and diversity patterns in communities. American Naturalist 147(5):784 – 812.

Lemmetyinen R & Mankki J (1975) The three-spined stickleback (Gasterosteus aculeatus) in the food chains of the northern Baltic. HavsforskningsInstitutes Skrivelser 239: 155–161.

Lepori F & Malmqvist B (2009) Deterministic control on community assembly peaks at intermediate levels of disturbance. Oikos 118(3): 471 – 479.

Li M, Gargett A & Denman K (2000) What determines seasonal and interannual variability of phytoplankton and zooplankton in strongly estuarine systems? Application to the semi-enclosed estuary of Strait of Georgia and Juan de Fuca Strait. Estuarine, Coastal and Shelf Science 50(4):467 – 488.

Li KZ, Yin JQ, Huang LM & Tan YH (2006) Spatial and temporal variations of mesozooplankton in the Pearl River estuary, China. Estuarine, Coastal and Shelf Science, 67(4): 543 – 552.

Lignell R, Kaitala S & Kuosa H (1992) Factors controlling phyto- and bacterioplankton in late spring on a salinity gradient in the northern Baltic. Marine Ecology Progress Series 84: 121 – 131.

Likens GE (Ed) (2010) Plankton of Inland Waters. Academic Press, Elsevier. MA, USA. 412 p.

Ljunggren L, Sandström A, Bergström U, Mattila J, Lappalainen A, Johansson G, Sundblad G, Casini M, Kaljuste O & Eriksson BK (2010). Recruitment failure of coastal predatory fish in the Baltic Sea coincident with an offshore ecosystem regime shift. ICES Journal of Marine Science 67:1587 – 1595.

Maes J, Taillieu A, Van Damme PA, Cottenie K & Ollevier F (1998) Seasonal patterns in the fish and crustacean community of a turbid temperate estuary (Zeeschelde Estuary, Belgium). Estuarine, Coastal and Shelf Science 47(2): 143 – 151.

Magill SH & Sayer MDJ (2002) Seasonal and interannual variation in fish assemblages of northern temperate rocky subtidal habitats. Journal of Fish Biology 61(5): 1198 – 1216.

Mauchline J (1998) The Biology of Calanoid Copepods: Advances in Marine Biology Series. (Vol. 33) (Blaxter JH, Douglas B & Tyler PA, Eds) Academic Press, San Diego CA. 710 p.

McCann K, Hastings A & Huxel GR (1998) Weak trophic interactions and the balance of nature. Nature 395(6704): 794 – 798.

McGrady-Steed J, Harris PM & Morin PJ (1997) Biodiversity regulates ecosystem predictability. Nature 390(6656): 162 – 165.

McLusky DS & Elliott M (2004) The Estuarine Ecosystem: Ecology, threats and management. 3rd edn. Oxford University Press, Oxford. 214 p.

Meerhoff M, Clemente J, de Teixeira Mello F, Iglesias C, Pedersen AR & Jeppesen E. (2007) Can warm climate-related structure

75 of littoral predator assemblies weaken the clear water state in shallow lakes? Global Change Biology 13: 1888 – 1897.

Mehner T & Thiel R (1999) A review of predation impact by 0+ fish on zooplankton in fresh and brackish waters of the temperate northern hemisphere. Environmental Biology of Fishes 56(1-2): 169 – 181.

Menge BA & Sutherland JP (1987). Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment. American Naturalist 130(5): 730 – 757.

Menge BA & Olson AM (1990) Role of scale and environmental factors in regulation of community structure. Trends in Ecology and Evolution 5(2): 52 – 57

Michaelis H, Fock H, Grotjahn M & Post D (1992) The status of the intertidal zoobenthic brackish-water species in estuaries of the German Bight. Netherlands Journal of Sea Research 30: 201 – 207.

Mikheev VN, Wanzenböck J & Pasternak AF (2004) An interplay between foraging and antipredator behavior in 0+ perch (Perca fluviatilis) at the demersal phase. Proceedings of Percis III: The Third International Percid Fish Symposium (Barry TP, Malison JA, Eds): 81 – 82.

Mobley CD (1994) Light and water: Radiative transfer in natural waters. Academic Press, San Diego. 592 p.

Mohr S & Adrian R (2000) Functional responses of the rotifers Brachionus calyciflorus and Brachionus rubens feeding on armored and unarmored ciliates. Limnology and Oceanography 45(5): 1175 – 1179.

Müller-Navarra D (1995) Evidence that a highly unsaturated fatty acid limits Daphnia growth in nature. Archiv fur Hydrobiologie 132(3): 297 – 297.

Müller-Navarra DC, Brett MT, Liston AM & Goldman CR (2000) A highly unsaturated fatty acid predicts carbon transfer between primary producers and consumers. Nature 403(6765): 74 – 77.

Munk P & Kiorboe T (1985) Feeding behaviour and swimming activity of larval herring (Clupea harengus) in relation to density of copepod nauplii. Marine Ecology Progress Series 24(1): 15 – 21.

Munsterhjelm R (2005) Natural succession and human-induced changes in the soft-bottom macrovegetation of shallow brackish bays on the southern coast of Finland. PhD thesis, University of Helsinki.

Murdoch WW (1969) Switching in general predators: experiments on predator specificity and stability of prey populations. Ecological Monographs 39(4): 335 – 354.

Muylaert K, Declerck S, van Wichelen J, de Meester L & Vyverman W (2006) An evaluation of the role of daphnids in controlling phytoplankton biomass in clear water versus turbid shallow lakes. Limnologica 36(2): 69 – 78.

Möllmann C, Kornilovs G, Fetter M & Köster FW (2005) Climate, zooplankton, and pelagic fish growth in the central Baltic Sea. ICES Journal of Marine Science: Journal du Conseil 62(7): 1270 – 1280.

Naeem S & Li S (1997) Biodiversity enhances ecosystem reliability. Nature 390(6659): 507 – 509.

Nagata T & Hanazato T (2006) Different predation impacts of two cyclopoid species on a small-sized zooplankton community: An experimental analysis with mesocosms. Hydrobiologia 556(1): 233 – 242.

Nicolle A, Hansson LA, Brodersen J, Nilsson PA & Brönmark C (2011) Interactions between predation and resources shape zooplankton population dynamics. PloS One 6(1): e16534.

Niemi Å (1973) Ecology of phytoplankton in the Tvärminne area, SW coast of Finland. I. Dynamics of hydrography, nutrients, chlorophyll a and phytoplankton. Acta Botanica Fennica 100: 1 – 68.

Norberg J (2004) Biodiversity and ecosystem functioning: a complex adaptive systems approach. Limnology and Oceanography 49(4-2): 1269 – 1277.

Nurminen L, Horppila J (2006) Efficiency of fish feeding on plant-attached prey: Effects of inorganic turbidity and plant- mediated changes in the light environment. Limnology and Oceanography 51(3): 1550 – 1555.

Nurminen L, Pekcan‐Hekim Z & Horppila J (2010) Feeding efficiency of planktivorous perch (Perca fluviatilis) and roach (Rutilus rutilus) in varying turbidity: An individual-based approach. Journal of Fish Biology 76(7): 1848 – 1855.

Oaten A & Murdoch WW (1975) Switching, functional response, and stability in predator-prey systems. American Naturalist 109(967): 299 – 318.

O’Brien WJ (1979) The predator-prey interaction of planktivorous fish and zooplankton: recent research with planktivorous fish and their zooplankton prey shows the evolutionary thrust and parry of the predator-prey relationship. American Scientist 67(5): 572 – 581.

O’Brien WJ (1987) Planktivory by freshwater fish: thrust and parry in the pelagia. In: Kerfoot WC & Sih A (eds)Predation. Direct and indirect impacts on aquatic communities. University Press of New England, Hanover. pp 3 – 16.

76 Ohlberger J, Edeline E, Vøllestad LA, Stenseth NC & Claessen D (2011) Temperature-driven regime shifts in the dynamics of size-structured populations. The American Naturalist 177(2): 211 – 223.

Ojaveer E, Lumberg A & Ojaveer H (1998) Highlights of zooplankton dynamics in Estonian waters (Baltic Sea). ICES Journal of Marine Science 55: 748 – 755.

Ojaveer H, Jaanus A, MacKenzie B, Martin G, Olenin S, Radziejewska T, Telesh I, Zettler ML & Zaiko A (2010) Status of biodiversity in the Baltic Sea. PloS One 5(9): e12467.

O’Keefe TC, Brewer MC & Dodson SI (1998) Swimming behavior of Daphnia: Its role in determining predation risk. Journal of Plankton Research 20(5): 973 – 984.

Onbé T & Ikeda T (1995) Marine cladocerans in Toyama Bay, southern Japan Sea: seasonal occurrence and day-night vertical distributions. Journal of Plankton Research 17(3): 595 – 609.

Paine RT (1966) Food web complexity and species diversity. American Naturalist 100(910): 65 – 75.

Paffenhöfer GA, Strickler JR & Alcaraz M (1982) Suspension-feeding by herbivorous calanoid copepods: a cinematographic study. Marine Biology 67(2): 193 – 199.

Paffenhöfer GA, Ianora A, Miralto A, Turner JT, Kleppel GS, Ribera d’Alcalà M… & Wichard T (2005) Colloquium on diatom- copepod interactions. Marine Ecology Progress Series 286: 293 – 305.

Peltonen H, Vinni M, Lappalainen A & Pönni J (2004) Spatial feeding patterns herring (Clupea harengus L.), sprat (Sprattus sprattus L.) and the three-spined stickleback (Gasterosteus aculeatus L.) in the Gulf of Finland, Baltic Sea. ICES Journal of Marine Science 61: 966 – 971.

Persson L (1987a) The effects of resource availability and distribution on size class interactions in perch, Perca fluviatilis. Oikos 48(2): 148 – 160.

Persson L (1987b) Effects of habitat and season on competitive interactions between roach (Rutilus rutilus) and perch (Perca fluviatilis). Oecologia 73(2): 170 – 177.

Persson J & Vrede T (2006) Polyunsaturated fatty acids in zooplankton: variation due to taxonomy and trophic position. Freshwater Biology 51(5): 887 – 900.

Perrow MR, Jowitt AJD, Stansfield JH & Phillips GL (1999) The practical importance of the interactions between fish, zooplankton and macrophytes in shallow lake restoration. Hydrobiologia 395/396: 199 – 210.

Petchey OL & Gaston KJ (2002) Functional diversity (FD), species richness and community composition. Ecology Letters 5(3): 402 – 411

Peterka J & Matěna J (2011) Feeding behavior determining differential capture success of evasive prey in underyearling European perch (Perca fluviatilis L.) and roach (Rutilus rutilus L.) Hydrobiologia 661:113 – 121.

Pitkänen H, Lehtoranta J & Räike A (2001) Internal nutrient fluxes counteract decreases in external load: the case of the estuarial eastern Gulf of Finland, Baltic Sea. Ambio: A Journal of the Human Environment 30(4):195 – 201.

Porter KG, Orcutt Jr JD & Gerritsen J (1983) Functional response and fitness in a generalist filter feeder, Daphnia magna (Cladocera: Crustacea). Ecology 64(4): 735 – 742.

Price HJ & Paffenhöfer GA (1985) Perception of food availability by calanoid copepods. Archiv für Hydrobiologie–Beiheft Ergebnisse der Limnologie 21: 115 – 124.

Quesenberry N, Allen P & Cech Jr J (2007) The influence of turbidity on three-spined stickleback foraging.Journal of Fish Biology 70(3): 965 – 972.

Rajasilta M & Vuorinen I (1983) A field study of prey selection in planktivorous fish larvae.Oecologia 59(1): 65 – 68.

Rajasilta M, Mankki J, Ranta-Aho K & Vuorinen I (1999) Littoral fish communities in the Archipelago Sea, SW Finland: a preliminary study of changes over 20 years. Hydrobiologia 393: 253 – 260.

Redfield GW (1980) The effect of zooplankton on phytoplankton productivity in the epilimnion of a subalpine lake. Hydrobiologia 70(3): 217 – 224.

Reiriz L, Nicieza A & Brañta F (1998) Prey selection by experienced and naive juvenile Atlantic salmon. Journal of Fish Biology 53(1): 100 – 114.

Remane A & Schlieper C (1971) Biology of Brackish Water. John Wiley and Sons, Inc., New York. 372 p.

Remmert H (1983) Studies and thoughts about the zonation along the rocky shores of the Baltic. Zoologica 22: 121-125.

Repka S (1997) Effects of food type on the life history of Daphnia clones from lakes differing in trophic state. I. Daphnia

77 galeata feeding on Scenedesmus and Oscillatoria. Freshwater Biology 38(3): 675 – 683.

Roughgarden J & Feldman M (1975) Species packing and predation pressure. Ecology 56(2): 489 – 492.

Rowe DK (1984) Factors affecting the foods and feeding patterns of lake-dwelling rainbow trout (Salmo gairdnerii) in the North Island of New Zealand. New Zealand Journal of Marine and Freshwater Research 8(2): 129 – 141.

Rowe DK & Dean TL (1998) Effects of turbidity on the feeding ability of the juvenile migrant stage of six New Zealand freshwater fish species.New Zealand Journal of Marine and Freshwater Research 32(1): 21 – 29.

Rowe DK, Dean TL, Williams E & Smith JP (2003) Effects of turbidity on the ability of juvenile rainbow trout, Oncorhynchus mykiss, to feed on limnetic and benthic prey in laboratory tanks. New Zealand Journal of Marine and Freshwater Research 37(1): 45 – 52.

Rudstam LG, Aneer G & Hildén M (1994) Top-down control in the pelagic Baltic ecosystem. Dana 10: 105 – 129.

Saage A, Vadstein O & Sommer U (2009) Feeding behaviour of adult Centropages hamatus (Copepoda, Calanoida): functional response and selective feeding experiments. Journal of Sea Research 62(1): 16 – 21.

Saiz E & Calbet A (2011) Copepod feeding in the ocean: scaling patterns, composition of their diet and the bias of estimates due to microzooplankton grazing during incubations. Hydrobiologia 666(1): 181 – 196.

Salonen M, Urho L & Engström-Öst J (2009) Effects of turbidity and zooplankton availability on the condition and prey selection of pike larvae. Boreal Environment Research 14(6): 981 – 989.

Salonen M & Engström-Öst J (2010) Prey capture of pike Esox lucius larvae in turbid water. Journal of Fish Biology 76(10): 2591 – 2596.

Salonen M & Engström-Öst J (2013) Growth of pike larvae: effects of prey, turbidity and food quality. Hydrobiologia 717(1): 169 – 175.

Sanders RW & Wickham SA (1993) Planktonic protozoa and metazoa: predation, food quality and population control. Aquatic Microbial Ecology 7(2): 197 – 223.

Sargent J, Bell G, McEvoy L, Tocher D & Estevez A (1999) Recent developments in the essential fatty acid nutrition of fish. Aquaculture 177(1): 191 – 199.

Sarnelle O & Wilson AE (2008) Type III functional response in Daphnia. Ecology 89(12): 1723 – 1732.

Scheffer M (2004) Ecology of shallow lakes. Springer Science & Business Media. 358 p.

Scheinin M & Mattila J (2010) The structure and dynamics of zooplankton communities in shallow bays in the northern Baltic Sea during a single growing season. Boreal Environment Research 15(4):397 – 412.

Schiewer U (2008) Ecology of Baltic Coastal Waters. Ecological Studies 197. Springer-Verlag Berlin. 417 p.

Schultz M & Kiørboe T (2009) Active prey selection in two pelagic copepods feeding on potentially toxic and non-toxic dinoflagellates. Journal of Plankton Research 31(5): 553 – 561.

Segerstråle SG (1959) Brackish water classification, a historical survey. In Symposium on the Classification of Brackish Waters. Venice 8–14th April 1958. Archivio di Oceanografia e Limnologia Volume 11, Supplemento

Sell AF, van Keuren D & Madin LP (2001) Predation by omnivorous copepods on early developmental stages of Calanus finnmarchicus and Pseudocalanus spp. Limnology and Oceanography 46(4): 1780 – 1783.

Shurin JB (2001) Interactive effects of predation and dispersal on zooplankton communities. Ecology 82(12): 3404-3416.

Shurin J, Winder M, Adrian R, Keller WB, Matthews B, Paterson AM, Paterson MJ, Pinel-Alloul B, Rusak JA & Yan ND (2010) Environmental stability and lake zooplankton diversity – contrasting effects of chemical and thermal variability. Ecology Letters 13(4): 453 - 463.

Shurin JB, Borer ET, Seabloom EW, Anderson K, Blanchette CA, Broitman B, Cooper SD & Halpern BS (2002) A cross- ecosystem comparison of the strength of trophic cascades. Ecology Letters 5(6):785–791.

Sieben K, Rippen AD & Eriksson BK (2011) Cascading effects from predator removal depend on resource availability in a benthic food web. Marine Biology 158(2): 391 – 400.

Siefert RE (1972) First food of larval yellow perch, white sucker, bluegill, emerald shiner, and rainbow smelt. Transactions of the American Fisheries Society 101(2): 219 – 225.

Snickars M, Sandström A, Lappalainen A, Mattila J, Rosqvist K & Urho L (2009) Fish assemblages in coastal lagoons in land- uplift succession: The relative importance of local and regional environmental gradients. Estuarine, Coastal and Shelf Science 81: 247 – 256.

78 Snoeijs P (1999) Marine and brackish waters. Acta Phytogeographica Suecica 84: 187 – 212.

Solomon ME (1949) The natural control of animal populations. Journal of Animal Ecology 18(1): 1 – 35.

Sommer U, Gliwicz ZM, Lampert W & Duncan A (1986) The PEG-model of seasonal succession of planktonic events in fresh waters. Archiv Fur Hydrobiologie 106(4): 433 – 471.

Sommer U, Sommer F, Santer B, Jamieson C, Boersma M, Becker C & Hansen T (2001) Complementary impact of copepods and cladocerans on phytoplankton. Ecology Letters 4(6): 545 – 550.

Sommer U & Stibor H (2002) Copepoda – Cladocera – Tunicata: the role of three major mesozooplankton groups in pelagic food webs. Ecological Research 17(2): 161 – 174.

Sopanen S, Koski M, Kuuppo P, Uronen P, Legrand C & Tamminen T (2006) Toxic haptophyte Prymnesium parvum affects grazing, survival, egestion and egg production of the calanoid copepods Eurytemora affinis and Acartia bifilosa. Marine Ecology – Progress Series 327: 223 – 232.

Sterner RW (1989) The role of grazers in phytoplankton succession. In: U Sommer (ed) Plankton Ecology: Succession in Plankon Communities. Springer-Verlag New York. pp 107 – 170.

Sterner RW, Hagemeier DD, Smith WL & Smith RF (1993) Phytoplankton nutrient limitation and food quality for Daphnia. Limnology and Oceanography 38(4): 857 – 871.

Strong DR (1992) Are trophic cascades all wet? Differentiation and donor control in speciose ecosystems. Ecology 73(3):747– 754.

Suikkanen S, Pulina S, Engström-Öst J, Lehtiniemi M, Lehtinen S & Brutemark A (2013) Climate change and eutrophication induced shifts in northern summer plankton communities. PloS One 8(6): e66475.

Symstad AJ, Tilman D, Willson J & Knops JM (1998) Species loss and ecosystem functioning: effects of species identity and community composition. Oikos 81(2): 389 – 397.

Symstad AJ, Siemann E & Haarstad J (2000) An experimental test of the effects of plant functional group diversity on arthropod diversity. Oikos 89(2): 243 – 253.

Telesh I (2004) Plankton of the Baltic estuarine ecosystems with emphasis on Neva Estuary: a review of present knowledge and research perspectives. Marine Pollution Bulletin 49(3): 206 – 219.

Telesh IV & Heerkloss R (2002) Atlas of Estuarine Zooplankton of the Southern and Eastern Baltic Sea. Part I: Rotifera. Hamburg: Verlag Dr. Kovač. 89 p.

Telesh IV & Heerkloss R (2004) Atlas of Estuarine Zooplankton of the Southern and Eastern Baltic Sea. Part II: Crustacea. Hamburg: Verlag Dr. Kovač. 118 p.

Telesh IV, Schubert H & Skarlato SO (2011) Revisiting Remane’s concept: evidence for high plankton diversity and a protistan species maximum in the horohalinicum of the Baltic Sea. Marine Ecology Progress Series 421:1 – 11.

Thorp JH (1986) Two distinct roles for predators in freshwater assemblages. Oikos 47: 75 – 82.

Tilman D, Wedin D & Knops J (1996) Productivity and sustainability influenced by biodiversity in grassland ecosystems.Nature 379(6567): 718 – 720.

Tiselius P (1990) Foraging behavior and grazing pattern of calanoid copepods. PhD thesis, Göteborg University.

Turner JT (1984) The feeding ecology of some zooplankters that are important prey items of larval fish. NOAA Technical Report NMFS 7: 1 – 28.

Turner JT & Tester PA (1997) Toxic marine phytoplankton, zooplankton grazers, and pelagic food webs. Limnology and Oceanography 42(5-2): 1203 – 1213.

Uitto A, Kaitala S, Kuosa H & Pajuniemi R (1995) Effect of nutrient addition and predation of mysid shrimp (Neomysis integer) on a plankton community in a short-term enclosure experiment in the northern Baltic. Aqua Fennica 25: 23 – 31.

Uitto A, Heiskanen AS, Lignell R, Autio R & Pajuniemi R (1997) Summer dynamics in the coastal planktonic food web in the northern Baltic Sea. Marine Ecology Progress Series 151:27 – 41.

Uye S (1996) Introduction of reproductive failure in the planktonic copepod Calanus pacificus by diatoms. Marine Ecology Progress Series 133: 89 – 97.

Van Den Berg C, Van Den Boogaart JGM, Sibbing FA & Osse JWM (1993) Zooplankton feeding in common bream (Abramis brama), white bream (Blicca bjoerkna) and roach (Rutilus rutilus): experiments, models and energy intake. Netherlands Journal of Zoology 44 (1-2): 15 – 42.

Vargas CA, Escribano R & Poulet S (2006) Phytoplankton food quality determines time windows for successful zooplankton

79 reproductive pulses. Ecology 87(12): 2992 – 2999.

Viherluoto M & Viitasalo M (2001) Temporal variability in functional responses and prey selectivity of the pelagic mysid, Mysis mixta, in natural prey assemblages. Marine Biology 138(3): 575 – 583.

Viitasalo M, Katajisto T & Vuorinen I (1994) Seasonal dynamics of Acartia bifilosa and Eurytemora affinis (Copepoda: Calanoida) in relation to abiotic factors in the northern Baltic Sea. In Ecology and Morphology of Copepods. Springer Netherlands. pp 415 – 422.

Viitasalo M, Vuorinen I & Saesmaa S (1995) Mesozooplankton dynamics in the northern Baltic Sea: implications of variations in hydrography and climate. Journal of Plankton Research, 17(10): 1857 – 1878.

Viitasalo M, Kiørboe T, Flinkman J, Pedersen LW & Visser AW (1998) Predation vulnerability of planktonic copepods: consequences of predator foraging strategies and prey sensory abilities. Marine Ecology Progress Series 175:129 – 142.

Viitasalo M, Flinkman J & Viherluoto M (2001) Zooplanktivory in the Baltic Sea: a comparison of prey selectivity by Clupea harengus and Mysis mixta, with reference to prey escape reactions. Marine Ecology Progress Series 216: 191 – 200.

Vinyard GL, O’brien WJ (1976) Effects of light and turbidity on the reactive distance of bluegill (Lepomis macrochirus). Journal of the Fisheries Research Board of Canada 33(12): 2845 – 2849.

Vuori KA & Nikinmaa M (2007) M74 syndrome in Baltic salmon and the possible role of oxidative stresses in its development: present knowledge and perspectives for future studies. Ambio: A Journal of the Human Environment 36(2): 168 – 172.

Vuorinen I, Hänninen J, Viitasalo M, Helminen U & Kuosa H (1998) Proportion of copepod biomass declines with decreasing salinity in the Baltic Sea. ICES Journal of Marine Science: Journal du Conseil, 55(4): 767 – 774.

Walker BH (1991) Biodiversity and ecological redundancy. Conservation Biology 6(1): 18 – 23.

Walker B, Kinzig A & Langridge J (1999) Plant attribute diversity, resilience and ecosystem function: the nature and significance of dominant and minor species. Ecosystems 2: 95 – 113.

Walker BH & Langridge J (2002) Measuring functional diversity in plant communities with mixed life forms: a problem of hard and soft attributes. Ecosystems 5(6): 529 – 538.

Webster M, Atton N, Ward A & Hart P (2007) Turbidity and foraging rate in threespine sticklebacks: the importance of visual and chemical prey cues. Behaviour 144(11): 1347 – 1360.

Welborn GA, Skelly DK & Werner EE (1996) Mechanisms creating community structure across a freshwater habitat gradient. Annual Review of Ecology and Systematics 27: 337 – 363.

Wilson DS (1973) Food size selection among copepods. Ecology 54(4): 909 – 914.

Winemiller KO & Layman CA (2005) Food web science: Moving on the path from abstraction to prediction. In: de Ruiter C, Wolters V, Moore JC (eds) Dynamic Food Webs – Multispecies Assemblages, Ecosystem Development and Environmental Change. Elsevier USA. pp 10 – 23.

Witek Z (1995) Biological production and its utilization in marine ecosystem of the Western part of the Gdansk Basin. Gdynia: Sea Fisheries Institute. 145 p.

Wong CK (1996) Response of copepods to hydromechanical stimuli. Crustaceana 69(7): 853 – 859.

Woodward G (2009) Biodiversity, ecosystem functioning and food webs in fresh waters: assembling the jigsaw puzzle. Freshwater Biology 54(10): 2171 – 2187.

Wootton RJ (1984) A functional biology of sticklebacks. University of California Press 265 p.

Worm B, Lotze HK, Hillebrand H & Sommer U (2002). Consumer versus resource control of species diversity and ecosystem functioning. Nature 417(6891): 848 – 851.

Zamora-Terol S & Saiz E (2013) Effects of food concentration on egg production and feeding rates of the cyclopoid copepod Oithona davisae. Limnology and Oceanography 58(1): 376 – 387.