ACTAUNIVERSITATIS

UPSALIENSISUPPSALA

2015

Digital Comprehensive Summaries of Uppsala Dissertationsfrom the Faculty of Science and Technology 1292

Phytoplankton and PhysicalDisturbance

Seasonal dynamics in temperate Lake Erken,Sweden

YANG YANG

ISSN 1651-6214ISBN 978-91-554-9345-5urn:nbn:se:uu:diva-262461

Dissertation presented at Uppsala University to be publicly examined in Friessalen,Evolutionary Biology Center, Norbyvägen 14, Uppsala, Friday, 6 November 2015 at 10:00 forthe degree of Doctor of Philosophy. The examination will be conducted in English. Facultyexaminer: Peeter Nõges (Institute of Agricultural and Environmental Sciences,EstonianUniversity of Life Sciences).

AbstractYang, Y. 2015. Phytoplankton and Physical Disturbance. Seasonal dynamics in temperateLake Erken, Sweden. Digital Comprehensive Summaries of Uppsala Dissertations from theFaculty of Science and Technology 1292. 43 pp. Uppsala: Acta Universitatis Upsaliensis.ISBN 978-91-554-9345-5.

Phytoplankton mirrors changes in the environment and plays an important role inbiogeochemical processes. Phytoplankton dynamics is the outcome of both autogenicsuccession and external disturbances. This thesis focused on the seasonal variation of watercolumn stability and its effects on phytoplankton, particularly considering the influence ofmixing events on phytoplankton development. Lake Erken is a dimictic lake with weak and ofteninterrupted summer stratification, which represents an intermediate case between a polymicticlake and a lake with strong summer stratification.

There are two diatom phases annually. The spring bloom is caused by pioneer centric diatoms,and the autumn diatom phase is dominated by meroplanktonic diatoms induced by turnover. Asummer Cyanobacteria bloom – mainly Gloeotrichia echinulata, depended on the length andstability of stratification.

Winter and spring air temperature is found to play an important role in the annual successionof phytoplankton by initiating changes in ice/snow-cover and lake thermal stability and settingthe basic status. Instead of starting from zero, the vernal phytoplankton piles up on theoverwintering community, this trans-annual ecological memory influences both the compositionand diversity and taxonomic distinctness of spring phytoplankton.

Water column stability during summer in Lake Erken is mainly influenced by wind-inducedturbulence and internal seiches. As thermal stratification develops from early until late summer,variations in stability and gradual deepening of the thermocline depth influence phytoplanktondynamics directly by changing its distribution, and also indirectly by altering the nutrientand light availability. A new disturbance index (DI) was defined to quantify environmentalstability/disturbance and tested well to indicate phytoplankton equilibrium status in two summerstratification periods. The concept of species and functional groups was generally used in thisstudy. However, a next generation sequencing based approach was also tested and proved toprovide an excellent candidate for revealing distribution patterns of phytoplankton in inlandwaters.

Keywords: Phytoplankton dynamics, high-frequency measurements, thermal stratification,water column stability, equilibrium, disturbance

Yang Yang, Department of Ecology and Genetics, Limnology, Norbyv 18 D, UppsalaUniversity, SE-75236 Uppsala, Sweden.

© Yang Yang 2015

ISSN 1651-6214ISBN 978-91-554-9345-5urn:nbn:se:uu:diva-262461 (http://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-262461)

This thesis is dedicated to my parents with

love

List of Papers

This thesis is based on the following papers, which are referred to in the text by their Roman numerals.

I Eiler, A., Drakare, S., Bertilsson, S., Pemthaler, J., Peura, S.,

Rofner, C., Simek, K., Yang, Y., Znachor, P., Lindstrom, E. (2013) Unveiling distribution patterns of freshwater phyto-plankton by a next generation sequencing based approach. PLoS ONE, 8(1): e53516. doi: 10.1371/journal.pone.0053516

II Yang, Y., Pettersson, K., Padisák, J. (2015) Repetitive baselines of phytoplankton succession in an unstably stratified temperate lake (Lake Erken, Sweden): a long-term analysis. Hydrobiolo-gia. doi: 10.1007/s10750-015-2314-1

III Yang, Y., Colom, W., Pierson, D., Pettersson, K. Water column stability and summer phytoplankton dynamics in a temperate lake (Lake Erken, Sweden). (accepted Inland Waters).

IV Yang, Y., Pettersson, K., Padisák, J. Development of a disturb-ance index based on high frequency temperature measurements and its test on phytoplankton assemblage equilibrium during summer stratification in Lake Erken. (manuscript).

V Yang, Y., Pettersson, K. Effects of physical factors on spring phytoplankton in a temperate lake (Lake Erken, Sweden). (Submitted).

Reprints were made with permission from the respective publishers. I was responsible for counting and gathering phytoplankton data from Lake Erken in Paper I. In Paper II, III, IV, and V, I was responsible for data min-ing, statistical analyses and writing the text. The co-authors have contributed with ideas, suggestion, and comments of the text in all papers. In Paper II to V data from the manual and automatic monitoring program for Lake Erken was used. I counted the phytoplankton samples from year 2008 to 2011.

Contents

Introduction ................................................................................................... 11 Phytoplankton in freshwater ecosystems ................................................. 11 Thermal stratification and lake stability ................................................... 12 Phytoplankton seasonal development ...................................................... 14 Disturbances and phytoplankton equilibrium ........................................... 15

Aim of this thesis .......................................................................................... 17

Material and methods .................................................................................... 18 Study location and monitoring program ................................................... 18 Database and Statistical analyses ............................................................. 19

Results ........................................................................................................... 23 Annual development of physical and chemical factors in Lake Erken .... 23 Baselines of phytoplankton development in Lake Erken ......................... 24 Spring phytoplankton in cold, normal and warm years ............................ 25 Summer thermal stratification and phytoplankton ................................... 27 Disturbance index (DI) and phytoplankton equilibrium .......................... 28

Discussion ..................................................................................................... 30 Conclusions .............................................................................................. 33

Acknowledgement ........................................................................................ 34

Sammanfattning på svenska .......................................................................... 37

Summary in Chinese (Sammanfattning på kinesiska) 中文摘要 ................. 39

References ..................................................................................................... 40

Abbreviations

CDH Critical Depth Hypothesis

CTH Critical Turbulence Hypothesis

DHR Disturbance-Recovery Hypothesis

DI Disturbance Index

IDH Intermediate Disturbance Hypothesis

NMDS Non-parametric Multi-dimensional Scaling

PAR Photosynthetically Active Radiation

PEG model Plankton Ecology Group model

RWCS Relative Water Column Stability

SIMPER Similarity Percentage Analysis

SN2 Buoyancy Frequency

SRP Soluble Reactive Phosphorus

SRSi Soluble Reactive Silica

St Schmidt Stability

SW Wedderburn Number

TD Taxonomic Distinctness

TR Total Radiation

WS Wind Speed

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Introduction

Phytoplankton in freshwater ecosystems

Identification and understanding of factors underlying patterns in species abundance in nature is a central issue in ecology. Phytoplankton, as the pri-mary producer, could mirror changes in aquatic ecosystems and carry basic information to assess the trophic status of aquatic environments. In freshwa-ter phytoplankton assemblages, it is often observed that the phytoplankton undergoes a series of seasonal changes, with waxes and wanes in biomass and shift in composition, this phenomenon is coined as ‘seasonal succession’ (Reynolds 1980). Succession, even though borrowed from terrestrial ecology, was given a wide meaning in plankton ecology – the pattern of annual de-velopment, and the sequential changes in species dominance (Smayda, 1980). Phytoplankton development occurs at different temporal scales: short-term variations induced by local weather are driven by stochastic disturbances, and annual variations lead to seasonal succession.

Phytoplankton development is the outcome of interplay between both internal community-directed processes and external forcing (Reynolds, 1993; Reynolds et al., 1993), and at the same time, abiotic and biotic factors. Figure 1 exhibits freshwater phytoplankton with its relevant direct and indi-rect ecological factors, including temperature, pH, salinity, alkalinity, nutri-ents and seasons, as well as the presence of competitors, predators, and para-sites (Likens, 2010). For phytoplankton, i) suspension in epilimnion with sufficient light to support photosynthesis; ii) getting access to nutrient; and iii) resisting the grazing pressure from zooplankton, are the key points to survive. Phytoplankton biomass accumulation is the trade-off between growth-controlling factors and loss processes (Tilzer, 1984; Forsberg, 1985). Margalef (1978) has argued that the ‘main sequence’ of phytoplankton suc-cession is governed by the interaction between a) developing organization within the ecosystem, arising as a consequence of thermal stability and the depletion of nutrients; and b) the morphological and physiological adapta-tions of the planktonic algae (in combining mechanism for remaining in

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suspension and for maximizing nutrient uptake) to exploit light and nutri-ents.

It has long been known that the overall biomass in the pelagic system is mainly set by the nutrient loads and energy input, which for the lake, is solar radiation. Ecosystem develop in such a way as to ‘fill the eco-space availa-ble’ until light or nutrients become limiting. Tilman (1977, 1982) proposed the resource-ratio hypothesis which provides an explanation for successional changes in species composition. Species-specific physiological preferences determine the composition. The predator pressure from zooplankton is the primary factor affecting the phytoplankton growth (Roelke et al., 2004). Studies showed that there were species-specific selection of zooplankton, which could account for the variation of composition in the community (Straile, 2000; Wiltshire and Manly, 2004). At the same time, the zooplank-ton and bacteria also compete and interact with its cohabitant, phytoplank-ton. In this way, phytoplankton is controlled by both bottom-up (resources) and top-down (predators) sources.

Fig. 1 Phytoplankton in an aquatic ecosystem with its key ecological factors.

Thermal stratification and lake stability

The total energy for water column stability includes three parts, the thermal energy, potential energy, and kinetic energy (Imboden & Wüest, 1995). Thermal energy is the energy stored in the random velocity distribution of atoms and molecules. The potential energy is referred as the difference be-tween the current lake status and the potential energy of the lake were it completely mixed. The kinetic energy describes the fluid motion. Solar radi-

SpeciesTraits

Interactions Biological:zooplankton

DiversityDistributionBiomass

ProductionDecompositionRecycling

STRUCTURE

ECOSYSTEM COMMUNITY

ENVIRONMENTPhysical: temperature, light, windChemical: nutrients

Phytoplankton

Environmentdisturbances

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ation provides the major energy input for stratification, while wind, adding kinetic energy to the water body, is the major external input responsible for mixing and relocate potential energy. Wind pushes the surface water towards downwind direction, causing surface wind, and a so-called surface set-up. This also leads to a basin circulation: bottom water fills up the surface-water motion. So when the wind stops, the potential energy is released, and simul-taneously, basin-scale waves oscillate back and forth, which is seiches.

There are several indexes defined to indicate water column stability. Relative water column stability (RWCS) is defined as the ratio of water den-sity difference between bottom and top layer to water density difference at 4℃ and 5 ℃ (Padisák, et al., 2003a). Schmidt stability (St), refers to the degree and the stability of thermals stratification, is a function of density differences mainly dependent on water temperature. It is a measure of the energy that requires to mix a thermally stratified lake. Wind-induced turbu-lence and upwelling influence directly the surface layer and indirectly the hypolimnion, entrain metalimnetic water into the surface layer, and poten-tially tilt the thermocline. Wedderburn Number (SW) indicates the likeli-hood of upwelling events under stratified conditions. And Buoyancy fre-quency (SN2) measures the work against gravity in order to break down the thermal stratification (Read et al., 2011).

Fig. 2 Schematic overview of mixing processes in a lake (taken from Imboden & Wüest, 1995) (general types of mixing mechanisms: i) wind-induced currents and waves, strong wind could induce Langmuir circulations; ii) boundary mixing; iii) inflows and outflows generate mixing; iiii) radiation causes mixing).

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Phytoplankton seasonal development

In thermally stratified, eutrophic lakes, phytoplankton spring bloom usually is followed by a distinct spring clear water phase and then a summer bloom of large, less edible algae and decreases again in winter; while in oligo-trophic lakes, this pattern usually turns out to be unimodal – with a spring bloom as the main event. The classical Plankton Ecology Group (PEG) model (Sommer et al. 1986) emphasizes that plankton dynamics during win-ter and spring are mainly under abiotic control, such as light and nutrients, whereas later in the year it shifts to biotic interactions limitation. Based on the trophic type of lake, succession pattern differs: for oligotrophic lakes, after the spring bloom, there is no obvious summer peak; whereas in eu-trophic water, the summer peak is present due to the abundance of nutrients. A minor autumn peak occurs in both types of ecosystems. As knowledge has accumulated, more factors affecting plankton seasonality have been pro-posed from various perspectives, which involve the microbial loop, the po-tential impact of parasites and the effects of food quality.

Phytoplankton are affected by both physical, chemical and biotic envi-ronmental factors. Since Sverdrup’s critical depth hypothesis (CDH) (Sverdrup, 1953), biological and physical control and their intertwined na-ture, combined with the intrinsic physiological ability of organisms to react to external pressures have been found to drive phytoplankton blooms. Spring blooms begin when the seasonal mixing layer is lower than critical depth. Huisman et al. (1999) proposed a critical turbulence hypothesis (CTH), em-phasizing that a subsurface bloom could occur if the turbulence is low enough. Later, Taylor and Ferrari (2011) summarized the CTH as the spring bloom is initiated by the cease of convective overturn in the end of winter. The Disturbance-Recovery-Hypothesis (DRH) emphasized the seasonally variable top-down control, with the dilution effect as deepening of the mixed layer in winter leads to a reduction in grazing pressure as ‘disturbance’ (Landry and Hassett, 1982), thereafter, blooms are triggered by a reduction in the loss process during deep mixing in spring, which increases prey-predator interaction as ‘recovery’. Decoupling and recoupling was defined to describe the association between phytoplankton biomass and zooplankton grazing pressure during different periods (Behrenfeld, 2010; Evans and Parslow, 1985; Behrenfeld and Boss, 2014). Physical forcing, particularly thermal stratification and mixing regime has been identified as a steering factor for phytoplankton development (Peeters et al., 2007, 2013; Wagner and Adrian, 2011; Sommer et al., 2012). In addition of the spring bloom,

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elimination of light-limitation after ice breakup is critical for the initiation of the spring bloom (Zohary et al., 2010). Thermal stratification starts to form when the upper water gets warm from solar radiation, together with wind-induced disturbance, determine both the surface layer and the hypolimnion. Surface wind induce turbulent shear flow, entrainment of metalimnetic water into the upper layer (Spiegel & Imberger 1980), and tilting the thermocline (Mortimer 1952, 1974; Thorpe 1968).

Stratification reduces vertical exchange and drives horizontal exchange by enforcing a vertical structure. Mixing promotes the exchange of hypo- and epilimnion and introduces the disturbance to the community. The physical factors summarized above are essential to deeper understanding of the mechanisms of the phytoplankton succession, functioning of ecosystems and better management of freshwater resources.

Disturbances and phytoplankton equilibrium

Since Hutchinson (1961) formulated the ‘paradox of plankton’ (how can so many species coexist in a seemingly homogeneous environment?) an in-creasing number of mechanisms have been proposed by ecologists. Reynolds applied Connell’s (Connell, 1979) intermediate disturbance hypothesis (IDH) into phytoplankton succession, which originally aims to interpret the high diversity in tropic rain forest. IDH encapsulates the idea that maximum diversity occurs at disturbances with intermediate frequency and intensity. A set of species sharing some functional characteristics are more adapted to certain environment, thus they become the dominant group during some specific period, as environment changes temporally, other assemblages adapted to new situations will out-compete the earlier dominant species and become take over the dominance ( Reynolds, 1973). Competitive exclusion in the phytoplankton is frequently avoided by strong intermediate disturb-ances and exclusion is not common except in stable environment such as the metalimnion (Sommer, 1985; Reynolds, 1987). The gradual environmental change is probably a major explanation for the paradox. Non-biotic and sto-chastic events interfering with internally-driven progress together that result in changes in the composition of phytoplankton. The equilibrium and non-equilibrium hypotheses highlighted the influence of disturbance on diversity (Sommer et al., 1993; Wilson, 1994; Padisák, 1994; Naselli-Flores et al., 2003). Niche differentiation is formed in stable conditions (Selmeczy et al., 2015) without disturbance that disrupts the progress to equilibrium and inter-feres with internally driven succession (Reynolds et al., 1993). The outcome

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of algal succession is influenced by disturbances that prevent progress to-wards equilibrium.

According to the definition of equilibrium state (Sommer et al., 1993), it requires three conditions: 1) dominance - no more than three species con-tribute to more than 80% of total biomass; 2) longevity - dominance should persist for more than 1-2 weeks; 3) constancy - there is no significant varia-tion in total biomass. Some modifications were allowed and used in some studies. For dominance, the number of species increased to 4-5 (Naselli-Flores et al., 2003; Nixdorf et al., 2003; Lengyel et al., 2014).

Criticism of with IDH is directed to the difficulty to define and quantify external environmental disturbances in planktonic systems (Hambright & Zohary, 2000). In lakes, disturbance is generally frequent except during brief periods of stratification. The sudden deepening of mixing depth would be the ideal indicator of physical disturbance following a period of stratification. The variation of thermocline depth and the water column stability appear as ideal indicators of disturbance and they are influenced mainly by two mete-orological factors: total radiation (TR) and wind speed (WS) (Wetzel, 2001).

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Aim of this thesis

The primary goal of this thesis was to investigate the relationship between physical disturbance and phytoplankton development. Studies were carried out to identify the seasonal succession pattern of phytoplankton in Lake Erken and reveal the associated environmental factors, especially the influ-ence of physical forcing on phytoplankton development. More specifically:

• Paper I applied both classic taxonomic and sequencing approaches to study the phytoplankton distribution in several freshwater ecosystems, in order to estimate the applicability of sequencing into ecology communi-ty research;

• Paper II applied 16 years of monitoring data spanning 20 years in Lake Erken, to reveal the so far undescribed, basic annual successional base-line of phytoplankton;

• Paper III focused on the summer stratification period in Lake Erken, based on time-series of high-frequency meteorological and water tem-perature measurements, the development of thermal stratification was linked to phytoplankton dynamics in order to investigate the relationship between water stability and phytoplankton;

• Paper IV compared two summer period with different disturbance re-gime – one longer and stable stratification and one shorter and unstable stratification. Phytoplankton development was associated to a newly de-fined disturbance index to test its performance on indicating phytoplank-ton equilibrium and environmental stability;

• Paper V classified the past two decades into cold, normal and warm years according to winter air temperature, and investigated the taxonom-ic diversity of the spring phytoplankton community in order to figure out the influence of winter severity on spring development.

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Material and methods

Study location and monitoring program

Lake Erken (59°510N, 18°360E) is a moderately deep, meso-eutrophic dimictic lake, located in eastern Sweden, with a volume of 23.5 X 106 m3. The total area of the lake is 24.2 km2, mean depth is 9 m, and maximum depth is 21 m. Proximity to the Baltic coast results in dominant winds along the lake’s longest West-East fetch. Water retention time is seven years and the drainage area is dominated by coniferous forest, therefore the external phosphorus loading is lower than 0.02 mg m-2 during summer (Pettersson, 1985).

Lake Erken is a typical dimictic lake with ice cover in winter and strati-fication in summer. Phytoplankton and water chemistry data were sampled weekly during the ice-free period and biweekly during the ice-covered peri-od at the deepest point of the lake, 700 m from the shoreline. A temperature profile was manually measured before collecting water and phytoplankton samples. Based on the temperature profile epilimnion depth was determined. Volume-integrated samples were collected from epilimnion, metalimnion and hypolimnion or from the whole water column when the lake was iso-thermal.

The monitoring program on phytoplankton and water chemistry has been running since 1991 and there has been occasional sampling since the 1940s. Water chemical analyses, including soluble reactive phosphorous (SRP), nitrate-nitrogen (nitrate-N), soluble reactive silica (SRSi), was con-ducted in the analytical laboratory of the Lake Erken Laboratory. The Utermöhl method was used to enumerate the phytoplankton to the lowest taxonomical level possible, usually species level (Lund et al., 1958), and then they were classified into Functional Groups (Reynolds et al., 2002; Padisák et al., 2009).

High-frequency meteorological and physical monitoring dated back to 1989. Measurements was performed at the Malma islet station (50.345’N, 18° 37.774’E). Water temperature was measured continuously each hour at 3 depths (1, 3, and 15 m) all year round, besides, total radiation, Photosyn-

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thetically active radiation (PAR), air temperature, water level, humidity and wind speed were monitored. Another monitoring float moored system (59° 50.578’N, 18° 38.126’E) was used during the ice-free period, and a water temperature profile was registered every 30 min each 0.5 m from surface (0.5 m) to 15 m depth. Wind speed was measured by this system, set 1.5 m above the surface.

Database and Statistical analyses

Functional groups of phytoplankton The traditional classification method sorts phytoplankton species according to the morphological characters. As the final aim is to understand the func-tioning of the ecosystem, there is the need for a marriage of taxonomy and ecology. Recently, the trait-based approaches are introduced to group phyto-plankton into assemblages. Algal species which show a high frequency of coincident presence are grouped together as ‘assemblages’ (Reynolds et al. 2002). Functional traits are morphological, phenological or physiological characteristics, measured at the level of the individual, that affect ecological performance, and ultimately fitness. Phytoplankton functional groups are sensitive to periodic, largely weather-driven disturbances that prevent suc-cession from proceeding towards an ecological equilibrium (Reynolds et al. 1993). Reynolds et al. (2002) introduced a functional classification system, which is not only based on individual functional traits, but also on the ranges of environmental conditions over which the species are found to occur. Its basic principle is that similar morphological, physiological and ecological features relate to certain similar functional traits. The system embraced 31 associations at beginning (Reynolds et al., 2002). Subsequent studies defined three further associations (Padisák et al. 2009).

Multivariate analyses Relative annual patterns of biomass of phytoplankton from 1989 till 2007 was clustered into four groups, each one represent one pattern of phyto-plankton development in Lake Erken. Clustering analysis and Non-parametric multi-dimensional scaling (NMDS) are applied using Bray-Curtis dissimilarity to identify the potential similar groups of phytoplankton on compositional level. Permutational multivariate analysis of variance (Per-MANOVA) is a non-parametric method to test whether there is significant difference on the compositional level between communities in pre-defined clusters. Similarity Percentage Analysis (SIMPER) aims at identifying the

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species that are responsible for the difference between clusters. Package ‘vegan’ in R (Oksanen, et al., 2013) was the major program to conduct mul-tivariate analysis. Spearman correlations, ANOVA and Kruskal-Wallis tests were operated in JMP 11.0 (SAS, 2014). Bray-Curtis dissimilarity is defined as equation to measure the distance between each community:

Bray-Curtis index =1 -∑ (1)

Where Xij and Xik refer to the quantity on species i between sample j and k (Bray& Curtis, 1957; Clark, 1993).

Water stability indexes

Lake Analyzer was used to process high-frequency measurements and calcu-late lake stability indices (Read, et al., 2011). The input of this program re-quires temperature profiles, wind speed, and lake bathymetry information, from which the output are Schmidt stability (St), Wedderburn Number (SW), and Buoyancy frequency (SN2) to represent different aspect of the water column stability. Schmidt stability, temperature difference between surface and bottom and relative water column stability (RWCS) were applied to correlation tests. RWCS is calculated as:

RWCS = (2) (Padisák et al., 2003a)

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Fig. 3 An example workflow of Lake Analyzer program (Read et al., 2011). .lke and .bth file specify the depth, area and bathemetry information of the lake, .wtr and .wnd is high-frequency time-series measurements of temperature profile and wind speed. Output file mainly includes thermocline depth (ThermD), top and bot-tom of metalimnion (metaT and metaB), Schmidt stability (St), Wedderburn number (SW), and Buoyancy frequency (SN2).

Taxonomic distinctness Taxonomic distinctness (TD) is a univariate diversity index which is defined as the step length on the taxonomic hierarchy, based on a standard Linnaean classification, that is needed to take up to a rank common to two species (Clark & Warrick, 1989, 1999). Average TD (Delta+/Δ+) is the mean of all species to species distance through the tree of all species within a sample and represents the taxonomic breadth of sample. It describes if and to what ex-tent closely related species constitute the assemblage. Variance of TD (Lambda+/Λ+) is the variation in branch length among all pairs of species and is a measure of the irregularities and divergences in the distribution of branch length in a sample (Clark & Warrick, 1998). The robustness and sen-sitivity are often the issue concerning the traditional univariate diversity measures. TD is found to be an excellent index with a high level of robust-

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ness and it captures phylogenetic diversity and is closely linked to functional diversity (Clark & Warwick, 1999). Several studies have estimated the TD in various ecosystems (Leonard et al., 2006), such as macrophyte communities (Mouillot et al., 2005) and marine benthic diatom assemblages (Petrov et al., 2010).

Δ+= ∑ ∑( )/ (4) Λ+= ∑ ∑∑ ∑ (5)

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Results

Annual development of physical and chemical factors in Lake Erken

There is no trend in annual average total phosphorus during the period 1993 till 2011, thus, variations in phytoplankton biomass and composition were attributed to weather variation within seasonal cycles (Paper II, Fig. 4a and Paper V, Fig. 1a). Lake Erken displayed a typical sequence of: 1) winter –ice cover and inverted stratification; 2) spring – isothermal conditions; 3) summer –stratification; 4) autumn – isothermal condition.

The annual cycle of SRP and nitrate started by accumulation in winter and decreased from early spring and after depletion in late spring, it re-mained at low concentrations in epilimnion during the whole summer and replenishment from hypolimnion generally started in September. SRSi ex-hibited a variable pattern in Lake Erken (Paper II, Fig. 3 and Paper III, Fig. 3). The ammonium in the anaerobic-low oxygen hypolimnion contributed eventually to nitrate (nitrification) in the epilimnion. Generally, SPR was depleted most rapidly in spring and nitrate with some delay. Regeneration of SRP with autumn turnover reached a similar average concentration level as in early spring, while nitrate in autumn was lower than early spring level.

Nutrient accumulation in winter and dynamics in spring is influenced by winter severity as suggested in Paper V. The winter SRP pool was greater in cold years and its depletion in spring occurred later than in normal and warm years. SRSi was not a limiting factor in spring indicated by SRSi/SRP (Paper V, Fig. 3). Nutrient depletion is linked with growth of phytoplankton and its regeneration is mainly due to mixing events which could bring nutri-ent-rich hypolimnetic water up into epilimnion. Epilimnetic nutrient replen-ishment occurs on the seasonal scale by spring and autumn overturn (Paper II) and on the daily/weekly scale by wind-induced episodic mixing events (Paper III).

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Baselines of phytoplankton development in Lake Erken

Total biomass of phytoplankton was low in winter, after a peak in spring caused by diatom blooms, it decreased to a minimum, corresponding to the clear water phase. In summer, total biomass sometimes peaked again, as a consequence of cyanobacterial blooms, and was followed by a second dia-tom peak in the autumn (Paper II, Fig. 3).

The main functional groups of phytoplankton and representative species with specific physiological characteristics are listed in Paper II, Table 1. Basically, there are two diatom-dominated phases observed in Paper II: a spring bloom dominated by centric diatoms larger than 15 μm, which are fast-growing species with high efficiency in using nutrients and an autumn community comprised mainly by meroplanktonic mixing-dependent Aulaco-seira granulata and Fragilaria sp. or/and other large centric species. Some diatom species have an intermediate stage between holoplanktonic and holo-benthic and they spend part of their life in the hypolimnion or in the littoral zone. These species are defined as meroplankton (Reynolds, 2000). These meroplanktonic diatoms emerge upon mixing event after summer, either from resting spores, which subsequent germinate once they get exposed to sufficient light and higher temperature in the upper layer, or directly from vegetative cells. The morphology of common dominant diatom species un-der light microscopy in Lake Erken are displayed in Fig. 4.

Blooms of Gloeotrichia echinulata are favored by summer stratification, and their occurrence of which depends on the intensity and duration of strati-fication. Gloeotrichia echinulata has opposite preference for water stability with diatoms. It prefers high water temperature and stability as well as light availability, furthermore has internal phosphorus storage and the capacity to fix nitrogen directly from atmospheric dissolved in the water. These physio-logical features give this cyanobacteria species advantages in summer.

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Fig. 4 Dominant diatom species in Lake Erken (a. Stephanodiscus sp.; b. Melosira sp.; c. Fragilaria sp.; d. Asterionella formosa; e. Aulacoseira granulata). Paper I assessed phytoplankton diversity data from 49 lakes by comparing microscopy results with next generation sequencing (NGS) approach, and suggested that the NGS approach is an excellent candidate for monitoring phytoplankton communities in lakes.

Spring phytoplankton in cold, normal and warm years

According to three types of years categorized by average winter air tempera-ture (Paper V), there was significant difference in ice cover duration in cold, normal and warm years. Temperature stood as a good proxy for winter se-verity. The spring community is dominated by Bacillariophyceae, co-existing with Cryptophyceae and Chrysophyceae. Dinophyceae was part of the vernal community and had greater relative biomass in warm years. The spring bloom was caused by diatom species from group A, B and P, but with different contribution in the community after different winters- by group A in cold years, B in normal years and P in warm years. Dominant functional groups with its representative species and physiological characteristics are listed in Table 1. The spring assemblage is added to the initial overwintering community instead of replacing it. Variation of dominance is selected by environmental status, paralleling with species-specific physiological fea-tures, such as morphology, optimal temperature and light for metabolism as well as overwintering strategy.

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Table 1. Main functional groups in Lake Erken and representative species in each group Functional group

Representative species Physiological characteristics (revised from Reynolds et al., 2002)

A Centric diatom (5-10 µm) Clear, often mixed lakes; Low P half-saturation, tolerance to fluctuating light intensity during stratification, high resistance to sinking; some species could form resting cells, meroplanktonic

B Centric diatom (> 15µm), Aulaco-seira italic, Aulacoseira islandica

Mixed, mesotrophic small-medium lakes; adapted to low light; some spe-cies could form resting cells, mero-planktonic

C Centric diatom (< 5µm), Asterion-ella formosa

Temperate monomictic lakes, associated with pre-stratification spring conditions; sensitive to Si depletion; some species could form resting cells, meroplanktonic

D Stephanodiscus hantzschii, Synedra acus

Shallow, nutrient-enriched, well-ventilated waters; sensitive to nutrient depletion; some species could form resting cells

H2 Gloeotrichia echinulata Tolerant to low nitrogen; sensitive to mixing, poor light

L0 Aphanocapsa sp., Chroococcus sp., Peridinium bipes

Oligo- to mesotrophic lakes, stratified nutrient layer, sensitive to long or deep mixing

LM Microcystis sp., Ceratium hirun-dinella

Motile or buoyant taxa, summer epilim-nia in eutrophic lakes, low light tolerant, sensitive to mixing and low light inten-sity

MP Fragilaria construens, Navicula sp., Nitzschia sp.

Constant mixing, shallow water body; could form resting cells, meroplanktonic

P Aulacoseira granulata, Fragilaria crotonensis

Eutrophic epilimnia; Tolerant of carbon dioxide depletion, more eutrophic wa-ters; sensitive to stratification; could form resting cells, meroplanktonic

X2 Chrysochromulina parva, Chroomonas sp.

Clear mixed layers in meso-eutrophic lakes; Tolerance to stratification, sensi-tive to mixing and filter-feeding grazers; Reduced grazing leads to high relative biomass

Y Peridinium aciculiferum, Gym-nodinium sp., Cryptomonas

Small enriched lakes, low light tolerant, sensitive to phagotrophs

Taxonomic distinctness (TD) was applied to compare the biodiversity

of spring phytoplankton in Paper V. No significant correlation was found between TD and either Shannon diversity or evenness, which suggested that TD provides a complementary aspect of diversity different to the Shannon diversity and evenness. It is a univariate index that incorporates information on taxonomic relatedness of species, integrating some of the multivariate nature of biotic communities (Marchant, 2007). Spring communities in nor-

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mal years possessed average TD (Δ+) values close to the expected value estimated by the corresponding funnel plot (Paper V, Fig. 6). Some Δ+ of spring communities distributed below the expected value (92) were from cold and warm years.

Diversity indexes and surface water temperature were significantly re-lated (Paper V, Fig. 9). This suggests that winter temperature, among other factors, was the primary factor setting the initial environmental conditions affecting the phytoplankton development. This external weather-related fac-tor, in combination with species-specific physiological characteristics, ex-plains the variations of spring phytoplankton in Lake Erken.

Summer thermal stratification and phytoplankton

Summer stratification in Lake Erken had large inter-annual and intra-annual variations. The durations of summer thermal stratification varied from year to year. Daily wind was observed strong enough to induce episodic par-tial/complete mixing events. Turbulence and internal seiches are the main factor leading to Lake Erken being an unstably stratified lake during summer.

Cryptophyceae initially dominated the summer community, followed next by Dinophyceae in the middle of summer and finally followed by a Cyanophyceae bloom. However, Bacillariophyceae also appear occasionally in the community in addition to the dominant groups as increased mixing. Close to the end of summer, the community had the tendency shifting to diatom-dominance (Paper III, Fig. 5). Phytoplankton development during summer in Lake Erken was clustered into three groups based on the species weekly biomass, which represented three phases: early, mid- and late sum-mer (Paper III, Fig. 7).

Some diatoms from groups A, B, P and MP, were present in the early summer communities, coexisting with some group X2 and X3 (Chrysoflag-ellates), and group Y (Cryptomonas spp.). This period coincided with the low biomass and diversity clear water phase. Afterwards, LM (Ceratium hirundinella) and J (Scenesedmus spp., Pediastrum sp. and Coelastrum sp.) increased, and H2 (Gloeotrichia echinulata) formed a bloom in the mid-summer. As bloom decayed, species within group P (Aulacoseira granulata and Fragilaria crotonensis) and MP (Fragilaria construens, Navicula sp. and Nitzschia sp.) took over the dominance in the late summer/ early au-tumn. In addition, diatoms from group A, B and P appeared in the communi-ty occasionally during the whole summer.

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The trajectory of phytoplankton development from early to mid-summer was correlated with St in Lake Erken detected by ordination analy-sis (NMDS) with significant environmental gradient. In mid-summer where the lake possesses stable stratification, Gloeotrichia echinulata could form a summer bloom due to its preference for water column stability, high temper-ature and light availability, and the relative independence of nutrient condi-tions. It is noticed in Paper II that Gloeotrichia echinulata blooms only oc-cur when the summer stratification is stable enough for a certain long period. Meroplanktonic diatoms emerged in the epilimnion once water stability was disturbed by wind-induced turbulence or internal waves.

Disturbance index (DI) and phytoplankton equilibrium

The influence of disturbance on the process towards equilibrium of phyto-plankton was associated with the development of thermal stability. Paper IV observed that species composition of phytoplankton shifted in response to disturbance during summer stratification, and an equilibrium of phytoplank-ton could form only when the environment was stable for a long time. Such conditions are limited to a brief stratification period, and during this stable period, the deepening of mixing depth could be an ideal indicator of physical disturbance.

We compared two summers with contrasting stratification patterns in Lake Erken. One of them (2001) had a long period of relative stable stratifi-cation, and the other one (2002) was characterized by intermittent partial mixing events. Based on this study, we defined a new disturbance index (DI) to quantify the disturbance and environment stability. DI was calculated as the step length between the status of two subsequent days in total radiation (TR) and wind speed (WS) according to equation:

DI = ( − ) + ( − ) (3)

The smaller DI value, the less change of solar radiation and wind speed, thus the more stable the physical environment. A high DI value thus indicates high instability. The events with the upper 15% probability of DI values (122) were picked as the threshold for disturbance (Paper IV, Fig. 4). This means once DI is above 122, then the disturbance could be strong enough to induce changes of phytoplankton. Equilibrium could be achieved, as also indicated by a Gloeotrichia echinulata bloom in Lake Erken, only when there was at least a two week long period without DI above 122.

The summer of 2002 was characterized by a long period of water col-umn stability, and according to the equilibrium theory this time should be

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long enough to complete the process of competitive exclusion and achieve an equilibrium. On the other side, no equilibrium state was detected in year 2001, and diatoms took dominance in the community, which indicates mix-ing events. DI in 2001 could not drop below threshold longer than one week, which gave diatoms advantage to survive and grow. One period in 2002 was an equilibrium state, linked with DI value under the threshold and a Gloe-otrichia echinulata bloom formed.

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Discussion

In the thesis results of paper II, III, IV and V primarily arise from long-term monitoring observations in Lake Erken. Paper II, III and V applied time series data of multiple years to investigate temporal pattern of phytoplankton dynamics in Lake Erken. Paper III picked two contrasting summer period to develop a new approach quantifying disturbance, which then was applied to another summer in order to test its performance.

Generally, most research about freshwater phytoplankton is limited to short-term experiment or monitoring, and focused on specific environmental factors. After Nauwerck’s (1963) seminal work was published, Lake Erken became a kind of etalon for phytoplankton research. Less attention was paid to the role of physical stability of the water column though it was found to be a major factor in driving phytoplankton successional events. This study is based on two decades of monitoring data, including meteorology-related factors, hydrodynamics, nutrient status and phytoplankton data, and revealed important mechanisms underneath phytoplankton succession.

Lake Erken is an excellent location to study the relationship between water stability and phytoplankton for the following reasons: i) Lake Erken is a typical dimictic lake, it has a winter period with ice-cover and regular summer stratification which provides a potentially stable period; ii) it is a shallow lake, due to variations of global, regional and local climate, and the duration and intensity of summer stratification is variable, therefore, differ-ent cases are available for comparison; iii) a long time series of weekly water chemistry sampling and phytoplankton enumeration is available. This is highly valuable, in particular combined with high-frequency meteorological measurements which allow reliable statistical analyses to investigate which is the steering factor for phytoplankton development. Paper III and IV both focused on the summer period, with relative stable water column, paper III unveiled the role played by hydrodynamic variability in the succession of phytoplankton in Lake Erken. Paper IV proposed a new way to quantify physical disturbance, which provided a starting point for further modeling to study environmental stability.

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To our knowledge, Paper II revealed the so far undescribed annual phy-toplankton succession patterns in Lake Erken, which symbolized an inter-mediate case between highly mixed polymicitc lakes and strongly stratified lakes, where the observed unstably stratified period allow the development of an autumn diatom phase. The weather-dependent baselines of phytoplank-ton revealed in Paper II may help calibrate climate change models related to impact of foreseen changes on lake ecosystems.

The functional groups B and C of phytoplankton represent fast-growing pioneer species with high nutrient use efficiency, they effectively inoculate the water column with resting stages and form the bloom rapidly in spring. The autumn diatom peak is dominated by species such as Aulacoseira granulata and Fragilaria sp. (Reynolds et al., 2002). These larger species grow slowly and suffer from sedimentation, after summer stratification peri-od, they accumulate in the relative cold and dark hypolimnion. The onset of autumn turnover could transport cells of meroplanktonic diatoms or semi-dormant resting cells up to the euphotic zone and contribute to the autumn community directly. At the same time, weak stratification with convection, circulation and/or upwelling also prevails during late summer and early au-tumn in Lake Erken (Fig. 1c in Paper II), contributing to assist meroplank-tonic diatom seed the community. These two diatom phases are dominated by different species which is determined by species-specific physiological features, including temperature optima, light and nutrient requirements and response to water column stability. Blooms of Gloeotrichia echinulata are characteristic for the summer in Lake Erken (Pettersson et al., 1995). This bloom is found to be dependent on the length and intensity of the water col-umn stability. The more-Gloeotrichia years had relative more stable stratifi-cation for a certain period indicated by RWCS (Fig. 9 in paper II).

Besides RWCS, Wedderburn number (SW) provides a way of predict-ing wind-induced internal waves, and the relative importance of upwelling. SW values suggested that internal waves were present throughout the sum-mer, indicating that daily winds were sufficient to provide the energy to keep that structure. This led to the conclusion in Paper III that the variation of thermocline depth was mainly influenced by wind-induced turbulence and the subsequent seiches during summer stratification. Studies of summer stratification in Lake Erken helps us understand how the mixing processes regulate the phytoplankton development and it could be used as a good case to compare with lakes which underwent significant mixing regime shift un-der the climate change scenario.

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Paper III suggested that for a non-motile species dominated communi-ties, total biomass was mainly limited by sedimentation loss when thermo-cline depth was shallow (early summer), by nutrient re-supply rates when thermocline depth was intermediate (mid-summer) and by light when ther-mocline depth was deep (late summer). The wind-induced turbulence and internal seiches influence phytoplankton development, directly changing the community distribution and composition depending on species-specific pref-erence for water column stability, indirectly by altering the light availability and nutrient status in the epilimnion. Species with low critical light intensity (species-specific saturation light intensity) dominated unstably stratified periods, while species with the capacity to float or migrate would take over the community in stratified period. In the transition between mixing and stratification or vice versa, the community shifted between mixing-dependent diatom domination and small-sized or motile species domination. Diatoms (group A, B and P) appeared several times during the whole sum-mer, which results from wind-induced turbulence in Lake Erken and also indicates the intermittent mixing events.

Species composition of phytoplankton shifted in response to disturb-ance during summer stratification, and an equilibrium of phytoplankton could form only when there was a long period of stable environment without strong disturbance. Paper IV suggested that the influence of disturbance on the process towards equilibrium of phytoplankton was associated with the development of thermal stability during summer in Lake Erken. A newly defined disturbance index provide a robust way to quantify disturbance re-lated to change of thermocline depth, identify environmental stability, and phytoplankton equilibrium. Autogenic succession of phytoplankton, plus the disturbance forcing together play equally important role modifying the phy-toplankton biomass and composition.

Paper V revealed that winter played an important role in the vernal phytoplankton development. Cold or warm winter could be regarded as the major disturbance influencing the seed population by narrow down the niche for multi-species to co-exist in the community. Due to this trans-annual memory effect, vernal community piles up on the winter community instead of starting from zero. Taxonomic distinctness (TD) analysis, providing com-plementary information to Shannon diversity and evenness index, suggested that taxonomic diversity of spring community was lower in cold or warm winter compared with that in normal years. Significant relationship between temperature and diversity indexes suggested that this weather-related physi-cal factor – water temperature, acted as the primary driving force for phyto-

33

plankton development, it not only sets the initial background environment, but also triggers changes of other related factors, which subsequently in-volved in phytoplankton succession.

Conclusions

The dynamics of phytoplankton in Lake Erken exhibits a repetitive baseline - two diatoms phases annually shows a clear relationship to mixing, morphol-ogy and stratification pattern. The two diatom phases are determined by spe-cies-specific physiological features, particularly the preference for thermal stratification or mixing.

Lake Erken is an unstably stratified lake during summer due mainly to wind-induced turbulence and internal seiches. Hydrodynamics, characterized by different stability indexes in early, mid and late summer, is the primary factor shaping the phytoplankton dynamics, directly by changing phyto-plankton distribution and epilimnetic composition, and indirectly by altering both the light and nutrient availability in the epilimnion.

The influence of disturbance on the process towards equilibrium of phytoplankton was associated with the development of thermal stability. The DI developed in this study performed well in indicating the environmental stability and provides a robust and novel method to study disturbance in stratified freshwater ecosystems.

Temperature acts as the primary driving force for phytoplankton devel-opment in spring. By species selection filtered by winter severity, different functional group dominates the spring bloom and influences the taxonomic biodiversity of vernal community.

In summary, Lake Erken with its weak and often interrupted summer stratification, represents an intermediate case between highly turbid shallow and common deep lakes that can be considered as template for discontinu-ously cold polymicitc lakes. The weather-related physical disturbance is the governing factor influences phytoplankton directly by wind-induced turbu-lence and internal seiches, and also indirectly by altering other environmen-tal processes that establish the niche for phytoplankton. The weather de-pendent successional patterns revealed in this study may help to calibrate climate change models related to impact of foreseen changes on lake ecosys-tems.

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Acknowledgement

This work would definitely not have been accomplished without contribution from many in different ways. First and foremost, I own my deepest gratitude to Kurt Pettersson, my main supervisor, for his guidance and enthusiasm. You are knowledgeable, pa-tient, enthusiastic and nice. You managed my accommodation at Campus in Norrtälje when I was new to Sweden, and all other detailed stuff. I especially thank you for the encouragement and effortless support. I always remember that you cares about my adaptation to Sweden during the beginning half year, showed your consideration whenever I was at ‘Fika’, you asked my colleagues to talk with me more in case I might feel isolated. You support my attendance at various conferences, and I could talk with you whenever I am confused with the problem I run across in the research. You guided me through my PhD project, and also gave me moral support and the freedom to move on. Secondly, a heartfelt thanks to my co-supervisor, Judit Padisák, for both being supportive and the chance to develop myself as a researcher. I got huge amount of help from you when I visited Hungary. During every discus-sion, I could always get inspired by your sparkling ideas, new methods and different perspective thoughts. And you are cordially thanked for co-authorship in paper II and IV, counselling and valuable comments on manu-script IV and this thesis. I feel so lucky to have you both as my supervisors. Your patience and enthu-siasm touched me and guided to acquire knowledge and skills that prepare me to move on with my pursuit in the future. My sincere thanks also goes to Don Pierson who deserves the credit for your contribution in Paper II and for your support and advice in high-frequency monitoring field, your patient of answering my questions. I am delighted to send my thanks to Vera Istvánovics for her valuable comments on Paper II, and also your support on our DF data. Anders Hasselrot and William Colom, we are a great team to do data min-ing, Anders, thank you for your support with JMP and great ideas about data handling. And William, so grateful for your support on my project.

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I would like to acknowledge the department of limnology. My experience benefited greatly from the course I took, the high-quality seminars that the department organized. Lars, your valuable suggestions are very helpful. Stefan, Alex, Eva, Gesa, Silke, Peter, Sebastian, and Anna thank you all for suggestion about my project. My thanks also go to administrative staff in the department, Eva, Karin, Marie and Tove. Birgit and Karen, thank you for sharing the office with me. Blaize and Monica, thanks for the lift to Erken. Roger, thank you so much for your help with computer, software and everything. Jovana, thanks you for everything you did for our PhD group. Jingying and Yinghua, I feel so happy to have both of you in the depart-ment, and we had a lot of great time after work. And other PhD in the department, thank you all for the companion, you are so kind to me. Karin and Pia, your laughter in the corridor and fika could always lighten the busy working atmosphere. I remember the funny time we working to-gether in the research school. Nicole, Johanna, Christer, thank you for helping me with sampling with the spring blitz project. It was quite an expe-rience for me. Helena, Erika, Björn, Aurora, Kristiina, Rita, thank you for your hard working at Erken, you all make Erken Lab an excellent place to do research. And also thanks for encouraging me to speak Swedish every time. I took part of many other activities, with countless people teaching and help-ing me every step. Thanks to everyone from GLEON and Netlake. Eleanor helped me with statistical methods when I did my scientific mission in Ire-land. Vicky, Luybov and Laura, thank you for taking care of me when I was in Dundalk, Ireland, taking me to the haunted farm during Halloween and a farewell night. My friends, Géza, thank you for everything when I visited Veszprem, you helped me to settle down, we went to Tihany, Lake Balaton together, enjoy-ing the amazing view, and you taught me how to climb. András, thanks for your help about Functional groups. Pille, we can share every topic together, whenever I feel frustrated, you are always there for me and cheer me up. Yu ( 雨张 ), my close friend in Uppsala, I am so happy to meet you in Sweden, doing our PhD together in Uppsala university. Chen ( 琛邓 ), thank you for all the encouragement. Thank you all my friends sincerely for your listening and companion. That means so much to me.

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In the end, the most basic source of my life energy resides: my parents, the most important persons in my life, are endlessly thanked for giving birth to me at the first place and your unconditional sacrifice, care, support and self-less love. This last word of acknowledgment I have saved for myself, for my insist-ence, efforts and hard working. It has been a long four years and also a short four years. Long because of all the courses, field work, readings and writing, short because of the extensive experience, lifelong friendship, lasting memo-ries, and the truly interesting and amazing things I learned. ‘Success is not measured by what you accomplish but by the opposition you have encoun-tered, and the courage with which you have maintained the struggle against overwhelming odds.’ (Orison S. Marden).

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Sammanfattning på svenska

Växtplankton, som primärproducenterna i akvatiska ekosystem, spelar en avgörande roll i näringsväven och i en sjös ekosystem. Växtplanktonutveckl-ingen är resultatet av påverkan från en rad miljöfaktorer. Biomassan och artsammansättningen förändras längs miljögradienter både långsiktigt och kortsiktigt. Det primära målet med avhandlingen var att identifiera växt-planktons säsongsutveckling i sjön Erken och avslöja de påverkande miljö-faktorer, särskilt väderrelaterade. Denna dimiktiska sjö representerar ett mel-lanting mellan en kraftigt grumlad grund sjö och en djup sjö, vilket leder till svag och ofta avbruten sommarskiktning.

Ackumuleringen av växtplanktonbiomassa är resultatet av balansen mel-lan tillväxtreglerande faktorer och förlustprocesser. En viss arts specifika fysiologiska företräden leder till förskjutningar av dominansen i växtplank-tonsamhället. En uppsättning av arter kan dela fler egenskaper som gör dem mer toleranta för viss miljö, vilket leder till att de blir den dominerande gruppen under en viss specifik period, därefter kommer andra grupper att konkurrera ut den när förhållandena förändras. Tillsammans med den domi-nerande gruppen samexisterar flera sällsynta arter. Främst är det icke-biotiska, stokastiska händelser som leder till tydliga och plötsliga föränd-ringar i sammansättningen och som stör internt drivna framsteg mot ekolo-gisk jämvikt. Arter når jämvikt genom att ockupera en viss nisch och minska konkurrensen. Fysiska faktorer, särskilt termisk skiktning och omblandning är de starkaste faktorerna som påverkar växtplanktondynamiken.

Resultaten visade att det fanns två kiselalgsdominerade faser i sjön Erken, vårblomningen och hösttoppen. Däremellan blommar cyanobakterier under sommarskiktningen. Anledning till skiftena var arternas motsatta preferens för temperaturskiktning i sjön. Kiselalger kräver konstant omblandning för att hålla dem flytande i epilimnion, medan cyanobakterier har kapacitet att flyta och blommar bara när sjön är stabil nog under tillräckligt lång tid. De två kiselalgsfaserna domineras av olika arter, vilket bestäms av artspecifika fysiologiska egenskaper (inklusive temperaturoptima), ljus- och näringsbe-hov samt svar på vattenmassan stabilitet. Höstens kiselalger utgjordes främst av meroplanktoniska arter, som transporteras upp från bottenområden genom

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vattenomblandningen. Vårsamhället påverkades av hur sträng vintern var, vilket leder till en ”minneseffekt”. Dominansen av olika funktionella grupper bestämdes av specifika fysiologiska egenskaper. En varmare vinter kan minska den taxonomiska tydligheten hos vårsamhället .

Under sommarens skiktningsperiod påverkas temperaturskiktningens sta-bilitet av vindinducerad turbulens och seicher. Växtplanktons totalbiomassa var beroende av näringstillgången i epilimnion och artsammansättningen av temperaturskiktningens utveckling. Arter med lågt kritiskt ljusintensitetsbe-hov dominerade instabilt skiktade perioder och arter med förmåga att flyta eller migrera tog över under stabilt skiktade perioder. Vertikal transport i samband med interna vågor orsakade nischseparation och mildrade arternas konkurrens. Språngskiktets vertikalvariation påverkar växtplanktondynami-ken direkt genom att ändra dess fördelning, och även indirekt genom att närings- och ljustillgängligheten bestäms av omblandningen.

Störningar av förloppet mot jämvikt för växtplankton var kopplade till ut-vecklingen av termisk stabilitet. Ett nytt störningsindex definierades utifrån totalstrålning och vindhastighet relaterat till förändringen av språngskiktets djup under sommarperioden. Med syfte att kvantifiera den omgivande mil-jöns stabilitet, fungerade indexet väl för att indikera jämviktsstatus hos växt-plankton i sjön Erken. Autogen växtplanktonsuccession och störningar i omgivningen spelar lika viktiga roller för att modifiera växtplanktons bio-massa och sammansättning. Fysiska faktorer spelar en viktig roll i växtplanktondynamiken, inte bara genom att justera näringstillgång i epilimnion, men också genom att bidra direkt till samhällsskiften genom att ändra den vertikala fördelningen och produktionen under sommarens skiktninsperiod. Studier av växtplankton-samhället och dess relaterade miljöfaktorer är ett viktigt steg mot ytterligare och djupare förståelse av de mekanismer som styr växtplanktonutvecklingen i sjöar, vilket möjliggör en bättre förvaltning av våra sötvattenresurser.

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Summary in Chinese (Sammanfattning på

kinesiska) 中文摘要

浮游植物作为生态系统的主要初级生产者，能迅速响应水体环境变化。

浮游植物的演替变化是内在演替机制和外在环境因子共同作用的结果。

本论文描述了水体热稳定度和浮游植物在时间序列上的变化特征，进

而研究了水体垂直混合作用对浮游植物演替的影响。Erken 湖是一个典

型的双季对流混合湖，夏季出现水体温度垂直分层，由于其热稳定度

较低且有间断性混合的特点，因此它可以代表介于多混合湖和具有夏

季稳定垂直层的湖泊的一种中间情况，为研究湖泊水体热稳定度和浮

游植物的相关性提供了很好的条件。

Erken 湖每年出现两次硅藻优势群落，春季优势群来自生长迅速的

小形中心纲硅藻。秋季湖泊水体混合，一些季节性浮游硅藻会随着翻

腾作用被携带至光照充足的上层水体中继而成为优势群。两次硅藻期

之间出现了夏季典型的由刺孢胶刺藻(Gloeotrichia echinulata)引发的蓝

藻水华，该水华的发生依赖于夏季水体垂直分层状态的长度和强度。

研究发现，通过影响水体热稳定度，冬季和春季的大气温度可以

调控浮游植物季节演替的初始环境条件。春季的浮游植物并非年度演

替的起始生长点，而是在前一年越冬群落的基础上，继承了其特性继

续发展而来。这种跨年度的记忆特征影响了后续的季节性演替，包括

群落组成结构和生物多样性。

在 Erken 湖，夏季水体热稳定性主要受到风和由风力引导的内假潮

的影响。从夏季早期到末期，随着水体热稳定性的增强，温跃层的变

化可以直接影响浮游植物在水体中的垂直位置分布，也可以间接通过

调节营养盐和光环境来影响浮游植物的变化。本论文定义了一个新的

干扰系数对环境稳定性或者干扰因子进行定量，并且应用该系数指示

浮游植物是否演替到稳定状态，测试结果显示该系数可以有效地用于

湖泊热稳定状态的评估，有助于浮游植物平衡状态的研究。

40

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