1. science
2. biology
3. zoology
4. endangered species

Digital Comprehensive Summaries of Uppsala Dissertations
from the Faculty of Science and Technology 1292
Phytoplankton and Physical
Disturbance
Seasonal dynamics in temperate Lake Erken,
Sweden
YANG YANG
ACTA
UNIVERSITATIS
UPSALIENSIS
UPPSALA
2015
ISSN 1651-6214
ISBN 978-91-554-9345-5
urn: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 for
the degree of Doctor of Philosophy. The examination will be conducted in English. Faculty
examiner: Peeter Nõges (Institute of Agricultural and Environmental Sciences,Estonian
University of Life Sciences).
Abstract
Yang, Y. 2015. Phytoplankton and Physical Disturbance. Seasonal dynamics in temperate
Lake Erken, Sweden. Digital Comprehensive Summaries of Uppsala Dissertations from the
Faculty 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 in
biogeochemical processes. Phytoplankton dynamics is the outcome of both autogenic
succession and external disturbances. This thesis focused on the seasonal variation of water
column stability and its effects on phytoplankton, particularly considering the influence of
mixing events on phytoplankton development. Lake Erken is a dimictic lake with weak and often
interrupted summer stratification, which represents an intermediate case between a polymictic
lake 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. A
summer Cyanobacteria bloom – mainly Gloeotrichia echinulata, depended on the length and
stability of stratification.
Winter and spring air temperature is found to play an important role in the annual succession
of phytoplankton by initiating changes in ice/snow-cover and lake thermal stability and setting
the basic status. Instead of starting from zero, the vernal phytoplankton piles up on the
overwintering community, this trans-annual ecological memory influences both the composition
and diversity and taxonomic distinctness of spring phytoplankton.
Water column stability during summer in Lake Erken is mainly influenced by wind-induced
turbulence and internal seiches. As thermal stratification develops from early until late summer,
variations in stability and gradual deepening of the thermocline depth influence phytoplankton
dynamics directly by changing its distribution, and also indirectly by altering the nutrient
and light availability. A new disturbance index (DI) was defined to quantify environmental
stability/disturbance and tested well to indicate phytoplankton equilibrium status in two summer
stratification periods. The concept of species and functional groups was generally used in this
study. However, a next generation sequencing based approach was also tested and proved to
provide an excellent candidate for revealing distribution patterns of phytoplankton in inland
waters.
Keywords: Phytoplankton dynamics, high-frequency measurements, thermal stratification,
water column stability, equilibrium, disturbance
Yang Yang, Department of Ecology and Genetics, Limnology, Norbyv 18 D, Uppsala
University, SE-75236 Uppsala, Sweden.
© Yang Yang 2015
ISSN 1651-6214
ISBN 978-91-554-9345-5
urn: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
䘱㔉ᡁ⡡Ⲵ⡨⡨ྸྸ
List of Papers
This thesis is based on the following papers, which are referred to in the text
by their Roman numerals.
I
II
III
IV
V
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 phytoplankton by a next generation sequencing based approach. PLoS
ONE, 8(1): e53516. doi: 10.1371/journal.pone.0053516
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. Hydrobiologia. doi: 10.1007/s10750-015-2314-1
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).
Yang, Y., Pettersson, K., Padisák, J. Development of a disturbance index based on high frequency temperature measurements
and its test on phytoplankton assemblage equilibrium during
summer stratification in Lake Erken. (manuscript).
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 mining, 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
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 primary producer, could mirror changes in aquatic ecosystems and carry basic
information to assess the trophic status of aquatic environments. In freshwater 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 development, 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 indirect ecological factors, including temperature, pH, salinity, alkalinity, nutrients and seasons, as well as the presence of competitors, predators, and parasites (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 succession 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 adaptations of the planktonic algae (in combining mechanism for remaining in
11
suspension and for maximizing nutrient uptake) to exploit light and nutrients.
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 available’ 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 zooplankton and bacteria also compete and interact with its cohabitant, phytoplankton. In this way, phytoplankton is controlled by both bottom-up (resources)
and top-down (predators) sources.
Species
Traits
Interactions
Biological:
zooplankton
STRUCTURE
ECOSYSTEM
Production
Decomposition
Recycling
COMMUNITY
Diversity
Distribution
Biomass
ENVIRONMENT
Phytoplankton
Environment
disturbances
Physical: temperature, light, wind
Chemical: nutrients
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 between the current lake status and the potential energy of the lake were it
completely mixed. The kinetic energy describes the fluid motion. Solar radi12
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 simultaneously, 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 density 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 turbulence and upwelling influence directly the surface layer and indirectly the
hypolimnion, entrain metalimnetic water into the surface layer, and potentially tilt the thermocline. Wedderburn Number (SW) indicates the likelihood of upwelling events under stratified conditions. And Buoyancy frequency (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).
13
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 oligotrophic 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 winter 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 eutrophic 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 proposed from various perspectives, which involve the microbial loop, the potential impact of parasites and the effects of food quality.
Phytoplankton are affected by both physical, chemical and biotic environmental factors. Since Sverdrup’s critical depth hypothesis (CDH)
(Sverdrup, 1953), biological and physical control and their intertwined nature, 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), emphasizing 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 preypredator 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,
14
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 windinduced 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 increasing 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 disturbances 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 stochastic events interfering with internally-driven progress together that result
in changes in the composition of phytoplankton. The equilibrium and nonequilibrium 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 interferes with internally driven succession (Reynolds et al., 1993). The outcome
15
of algal succession is influenced by disturbances that prevent progress towards equilibrium.
According to the definition of equilibrium state (Sommer et al., 1993), it
requires three conditions: 1) dominance - no more than three species contribute to more than 80% of total biomass; 2) longevity - dominance should
persist for more than 1-2 weeks; 3) constancy - there is no significant variation in total biomass. Some modifications were allowed and used in some
studies. For dominance, the number of species increased to 4-5 (NaselliFlores 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 meteorological factors: total radiation (TR) and wind speed (WS) (Wetzel, 2001).
16
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 influence 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 community research;
• Paper II applied 16 years of monitoring data spanning 20 years in Lake
Erken, to reveal the so far undescribed, basic annual successional baseline of phytoplankton;
• Paper III focused on the summer stratification period in Lake Erken,
based on time-series of high-frequency meteorological and water temperature 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 regime – one longer and stable stratification and one shorter and unstable
stratification. Phytoplankton development was associated to a newly defined disturbance index to test its performance on indicating phytoplankton 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 taxonomic diversity of the spring phytoplankton community in order to figure out
the influence of winter severity on spring development.
17
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 stratification in summer. Phytoplankton and water chemistry data were sampled
weekly during the ice-free period and biweekly during the ice-covered period 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 isothermal.
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 conducted 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, Photosyn18
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 functioning of the ecosystem, there is the need for a marriage of taxonomy and
ecology. Recently, the trait-based approaches are introduced to group phytoplankton 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 succession 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 phytoplankton development in Lake Erken. Clustering analysis and Nonparametric 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 (PerMANOVA) 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
19
species that are responsible for the difference between clusters. Package
‘vegan’ in R (Oksanen, et al., 2013) was the major program to conduct multivariate 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 calculate lake stability indices (Read, et al., 2011). The input of this program requires 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 =
20
(2)
(Padisák et al., 2003a)
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 bottom 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 extent 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 sensitivity are often the issue concerning the traditional univariate diversity
measures. TD is found to be an excellent index with a high level of robust21
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+=
Λ+=
22
∑
∑
(
∑
∑
∑
∑
)/
(4)
(5)
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 remained at low concentrations in epilimnion during the whole summer and
replenishment from hypolimnion generally started in September. SRSi exhibited 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 nutrient-rich hypolimnetic water up into epilimnion. Epilimnetic nutrient replenishment 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).
23
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 diatom 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 Aulacoseira granulata and Fragilaria sp. or/and other large centric species. Some
diatom species have an intermediate stage between holoplanktonic and holobenthic 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 under 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 stratification. 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 physiological features give this cyanobacteria species advantages in summer.
24
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 temperature (Paper V), there was significant difference in ice cover duration in cold,
normal and warm years. Temperature stood as a good proxy for winter severity. The spring community is dominated by Bacillariophyceae, coexisting 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 features, such as morphology, optimal temperature and light for metabolism as
well as overwintering strategy.
25
Table 1. Main functional groups in Lake Erken and representative species in each group
Functional
group
A
Representative species
B
Centric diatom (> 15µm), Aulacoseira italic, Aulacoseira islandica
C
Centric diatom (< 5µm), Asterionella formosa
D
Stephanodiscus hantzschii, Synedra
acus
H2
Gloeotrichia echinulata
L0
Aphanocapsa sp., Chroococcus sp.,
Peridinium bipes
LM
Microcystis sp., Ceratium hirundinella
MP
Fragilaria construens, Navicula
sp., Nitzschia sp.
Aulacoseira granulata, Fragilaria
crotonensis
P
Centric diatom (5-10 µm)
X2
Chrysochromulina parva,
Chroomonas sp.
Y
Peridinium aciculiferum, Gymnodinium sp., Cryptomonas
Physiological characteristics (revised
from Reynolds et al., 2002)
Clear, often mixed lakes; Low P halfsaturation, tolerance to fluctuating light
intensity during stratification, high
resistance to sinking; some species
could form resting cells, meroplanktonic
Mixed, mesotrophic small-medium
lakes; adapted to low light; some species could form resting cells, meroplanktonic
Temperate monomictic lakes, associated
with pre-stratification spring conditions;
sensitive to Si depletion; some species
could form resting cells, meroplanktonic
Shallow,
nutrient-enriched,
wellventilated waters; sensitive to nutrient
depletion; some species could form
resting cells
Tolerant to low nitrogen; sensitive to
mixing, poor light
Oligo- to mesotrophic lakes, stratified
nutrient layer, sensitive to long or deep
mixing
Motile or buoyant taxa, summer epilimnia in eutrophic lakes, low light tolerant,
sensitive to mixing and low light intensity
Constant mixing, shallow water body;
could form resting cells, meroplanktonic
Eutrophic epilimnia; Tolerant of carbon
dioxide depletion, more eutrophic waters; sensitive to stratification; could
form resting cells, meroplanktonic
Clear mixed layers in meso-eutrophic
lakes; Tolerance to stratification, sensitive to mixing and filter-feeding grazers;
Reduced grazing leads to high relative
biomass
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 nor26
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 related (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 factor, in combination with species-specific physiological characteristics, explains 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 partial/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 summer (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 (Chrysoflagellates), 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 midsummer. 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 autumn. In addition, diatoms from group A, B and P appeared in the community occasionally during the whole summer.
27
The trajectory of phytoplankton development from early to midsummer was correlated with St in Lake Erken detected by ordination analysis (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 temperature and light availability, and the relative independence of nutrient conditions. It is noticed in Paper II that Gloeotrichia echinulata blooms only occur 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 phytoplankton 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 phytoplankton 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 stratification, 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 column stability, and according to the equilibrium theory this time should be
28
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 mixing 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 Gloeotrichia echinulata bloom formed.
29
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, different 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.
30
To our knowledge, Paper II revealed the so far undescribed annual phytoplankton succession patterns in Lake Erken, which symbolized an intermediate 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 phytoplankton 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 period, they accumulate in the relative cold and dark hypolimnion. The onset of
autumn turnover could transport cells of meroplanktonic diatoms or semidormant 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 autumn in Lake Erken (Fig. 1c in Paper II), contributing to assist meroplanktonic 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 column stability. The more-Gloeotrichia years had relative more stable stratification for a certain period indicated by RWCS (Fig. 9 in paper II).
Besides RWCS, Wedderburn number (SW) provides a way of predicting wind-induced internal waves, and the relative importance of upwelling.
SW values suggested that internal waves were present throughout the summer, 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 under the climate change scenario.
31
Paper III suggested that for a non-motile species dominated communities, total biomass was mainly limited by sedimentation loss when thermocline depth was shallow (early summer), by nutrient re-supply rates when
thermocline depth was intermediate (mid-summer) and by light when thermocline 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 preference 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 mixingdependent diatom domination and small-sized or motile species domination.
Diatoms (group A, B and P) appeared several times during the whole summer, which results from wind-induced turbulence in Lake Erken and also
indicates the intermittent mixing events.
Species composition of phytoplankton shifted in response to disturbance 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 related 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 phytoplankton 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 complementary 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 physical factor – water temperature, acted as the primary driving force for phyto32
plankton development, it not only sets the initial background environment,
but also triggers changes of other related factors, which subsequently involved 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, morphology and stratification pattern. The two diatom phases are determined by species-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 phytoplankton 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 development 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 discontinuously cold polymicitc lakes. The weather-related physical disturbance is the
governing factor influences phytoplankton directly by wind-induced turbulence and internal seiches, and also indirectly by altering other environmental processes that establish the niche for phytoplankton. The weather dependent successional patterns revealed in this study may help to calibrate
climate change models related to impact of foreseen changes on lake ecosystems.
33
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, patient, 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 discussion, I could always get inspired by your sparkling ideas, new methods and
different perspective thoughts. And you are cordially thanked for coauthorship in paper II and IV, counselling and valuable comments on manuscript IV and this thesis.
I feel so lucky to have you both as my supervisors. Your patience and enthusiasm 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 highfrequency 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 mining, Anders, thank you for your support with JMP and great ideas about data
handling. And William, so grateful for your support on my project.
34
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 department, 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 together in the research school. Nicole, Johanna, Christer, thank you for
helping me with sampling with the spring blitz project. It was quite an experience 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 helping me every step. Thanks to everyone from GLEON and Netlake. Eleanor
helped me with statistical methods when I did my scientific mission in Ireland. 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, enjoying 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
(张雨), my close friend in Uppsala, I am so happy to meet you in Sweden,
doing our PhD together in Uppsala university. Chen (邓琛), thank you for all
the encouragement. Thank you all my friends sincerely for your listening
and companion. That means so much to me.
35
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 selfless love.
This last word of acknowledgment I have saved for myself, for my insistence, 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 memories, and the truly interesting and amazing things I learned. ‘Success is not
measured by what you accomplish but by the opposition you have encountered, and the courage with which you have maintained the struggle against
overwhelming odds.’ (Orison S. Marden).
36
Sammanfattning på svenska
Växtplankton, som primärproducenterna i akvatiska ekosystem, spelar en
avgörande roll i näringsväven och i en sjös ekosystem. Växtplanktonutvecklingen 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 växtplanktons säsongsutveckling i sjön Erken och avslöja de påverkande miljöfaktorer, särskilt väderrelaterade. Denna dimiktiska sjö representerar ett mellanting 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 mellan tillväxtreglerande faktorer och förlustprocesser. En viss arts specifika
fysiologiska företräden leder till förskjutningar av dominansen i växtplanktonsamhället. 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 dominerande gruppen samexisterar flera sällsynta arter. Främst är det ickebiotiska, stokastiska händelser som leder till tydliga och plötsliga förändringar i sammansättningen och som stör internt drivna framsteg mot ekologisk 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 näringsbehov samt svar på vattenmassan stabilitet. Höstens kiselalger utgjordes främst
av meroplanktoniska arter, som transporteras upp från bottenområden genom
37
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 stabilitet av vindinducerad turbulens och seicher. Växtplanktons totalbiomassa
var beroende av näringstillgången i epilimnion och artsammansättningen av
temperaturskiktningens utveckling. Arter med lågt kritiskt ljusintensitetsbehov 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 växtplanktondynamiken 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 utvecklingen 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 miljöns stabilitet, fungerade indexet väl för att indikera jämviktsstatus hos växtplankton i sjön Erken. Autogen växtplanktonsuccession och störningar i
omgivningen spelar lika viktiga roller för att modifiera växtplanktons biomassa 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 växtplanktonsamhället 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.
38
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。
39
References
Behrenfeld, M.J., 2010. Abandoning Sverdrup’s critical depth hypothesis on
phytoplankton blooms. Ecology 91: 977-989.
Behrenfeld, M.J. & E.S. Boss, 2014. Resurrecting the ecological underpinnings
of ocean plankton blooms. Annual Review of Marine Science 6: 167-194.
Bray, R.J. & J.T. Curtis, 1957. An ordination of the upland forest communities
of southern Wisconsin. Ecology Monography 27: 325-349.
Clarke, K. R., 1993. Non-parametric multivariate analyses of changes in
community structure. Australian Journal of Ecology 18: 117–143.
Clark K.R. & R.M. Warrick, 1998. A taxonomic distinctness index and its statistical properties. Journal of Applied Ecology 35: 523-531.
Clark K.R. & R.M. Warrick, 1999. The taxonomic distinctness measure of biodiversity weighting of step lengths between hierarchical levels. Marine
Ecology Progress Series 184: 21-29.
Connell, J. H., 1978. Diversity of tropical rain forests and coral reefs. Science
199: 1302–1310.
Evans, G. & J. Parslow, 1985. A model of annual plankton cycles. Biological
Oceanography 3: 327- 347.
Forsberg, B.R., 1985. The fate of planktonic primary production. Limnology and
Oceanography 30: 807-819.
Huisman, J., P. van Oostveen & F.J. Weissing, 1999. Critical depth and critical
turbulence: Two different mechanisms for the development of phytoplankton blooms. Limnology and Oceanography 44: 1781-1787.
Hutchinson, G., 1961. The paradox of the plankton. American Naturalist 95:
137–145.
Imboden, D.M. & A. Wüest, 1995. Mixing mechanisms in lakes, in A. Lerman,
D.M. Imboden & J.R. Gat, eds, ‘Physics and Chemsitry of Lakes’, Springer
Verlag, p 83-138.
Landry, M.R. & R.P. Hassett, 1982. Estimating the grazing impact of marine
micro-zooplankton. Marine Biology 67: 283-288.
Lengyel, E., J. Padisák & C. Stenger-Kovács, 2015. Establishment of equilibrium states and effect of disturbances on benthic diatom assemblages of the
Torna-stream, Hungary. Hydrobiologia 750: 43-56 750: 43-56.
Likens, G. E., 2010. Plankton of inland waters. Academic, Oxford, UK.
40
Lund, J. W. G., C. Kipling & E. D. Le Cren, 1958. The inverted microscope
method of estimating algal numbers and the statistical basis of estimations
by counting. Hydrobiologia 11: 143–170.
Marchant, R., 2007. The used of taxomonic distinctness to assess environmental
disturbance of insect communities from running water. Freshwater biology
52: 1634-1645.
Margalef, R., 1978. Life-forms of phytoplankton as survival alternatives in an
unstable environment. Oceanologica acta 1:493-509.
Mortimer, C.H., 1952. Water movements in lakes during summer stratification:
Evidence from the distribution of temperature in Windermere. Philosophical
Transactions of the Royal Society of London. Series B: Biological Sciences
236: 355-398.
Mortimer, C.H., 1974. Lake Hydrodynamics. Mitteilung Internationale Vereinigung fuer Theoretische unde Amgewandte Limnologie 20:124-197.
Mouillot, D., S. Gaillard, C. Aliaume, M. Verlaque, T. Belsher, M. Troussellier
& T. D. Chi, 2005. Ability of taxonomic diversity indices to discriminate
coastal lagoon environments based on macrophytes communities. Ecological
Indicators 5: 1-17.
Naselli-Flores, L., J. Padisák, M. T. Dokulil & I. Chorus, 2003. Equilibrium/
steady-state concept in phytoplankton ecology. Hydrobiologia 502: 395-403.
Nauwerck, A., 1963. Die Beziehungen zwischen Zooplankton und
Phytoplankton in See Erken. Symbolae Botanicae Upsaliensis 17: 1-163.
Nixdorf, B., U. Mischke & J. Rücker, 2003. Phytoplankton assemblages and
steady state in deep and shallow eutrophic lakes – an approach to differentiate the habitat properties of Oscillatoriales. Hydrobiologia 502: 111–121.
Oksanen, J., F. G. Blanchet, R. Kindt, P. Legendre, P. R. Minchin, R. B.
O’Hara, G. L. Simpson, P. Solymos, M. H. H. Stevens & H. Wagner, 2013.
Package “vegan.” R package ver. 2.0–8. , 254.
Padisák, J., 1994. Identification of relevant time-scales in non-equilibrium
community dynamics: conclusions from phytoplankton surveys. New
Zealand Journal of Ecology 18: 169–176.
Padisák, J., F. Barbosa, R. Koschel & L. Krienitz, 2003a. Deep layer
cyanoprokaryota maxima in temperate and tropical lakes. Archiv für
Hydrobiologie Special Issues Advances in Limnology 58: 175–199.
Padisák, J., L.O. Crossetti & L. Naselli-Flores, 2009. Use and misuse in the
application of the phytoplankton functional classification: a critical review
with updates. Hydrobiologia 621: 1-19.
Peeters, F., D. Straile, A. Lorke & D. Ollinger, 2007. Turbulent mixing and
phytoplankton spring bloom development in a deep lake. Limnology and
Oceanography 52: 286–298.
41
Peeters, F., O. Kerimoglu & D. Straile, 2013. Implications of seasonal mixing
for phytoplankton production and bloom development. Theoretical Ecology
6: 115–129.
Petrov, A., E. Nevrova, A. Terletskaya, M. Milyukin & V. Demchenko, 2010.
Structure and taxonomic diversity of benthic diatom assemblage in a polluted marine environment (Balaklava bay, Black sea). Polish Botanical Journal
55: 183-197.
Pettersson, K., 1985. The availability of phosphorus and the species composition
of the spring phytoplankton in Lake Erken. Int. Revue ges. Hydrobiologia
70: 527-546.
Read, J. S., D.P. Hamilton, I.D. Jones, K. Muraoka, L.A. Winslow, R. Kroiss,
C.H. Wu & E. Gaiser, 2011. Derivation of lake mixing and stratification indices from high-resolution lake buoy data. Environment Modell Software.
Elsevier Ltd 26:1325-1336.
Reynolds, C.S., 1973. The seasonal periodicity of planktonic diatoms in a shallow eutrophic lake. Freshwater Biology 3: 89-110.
Reynolds, C.S., 1980. Phytoplankton assemblages and their periodicity in stratifying lake systems. Ecography 3: 141-159.
Reynolds, C.S., 1987. Community organization in the freshwater plankton. In
Organisation of Communities, Past and Present (J.H.R. Gee & P.S. Giller,
ed.), p. 297-325. Blackwell Scientific Publications, Oxford.
Reynolds, C. S., 1993. Scales of disturbance and their role in plankton ecology.
Hydrobiologia 249: 157–171.
Reynolds, C. S., J. Padisák & U. Sommer, 1993. Intermediate disturbance in the
ecology of phytoplankton and the maintenance of species diversity: a synthesis. Hydrobiologia 249: 183–188.
Reynolds, C.S., V. Huszar, C. Kruk, L. Naselli-Flores & S. Melo, 2002. Towards a functional classification of the freshwater phytoplankton. Journal of
Plankton Research 24: 417-482.
Roelke, D., Y. Buyukates, M. Williams & J. Jean, 2004. Interannual variability
in the seasonal plankton succession of a shallow, warm-water lake.
Hydrobiologia 513: 205–218.
SAS Institute Inc. 2014. Using JMP@11, second Edition. Cary, NC:SAS
Institute Inc.
Smayda, T.J. 1980. Phytoplankton species succession. In: Morris, I. (ed.) The
physiological ecology of phytoplankton. Blackwell, Oxford, p. 492-570.
Sommer, U. 1985 Comparison between steady state and non-steady state
competition: Experiments with natural phytoplankton. Limnology and
Oceanography 30: 335–346.
42
Sommer, U., R. Adrian, L. De Senerpont Domis, J.J. Elser, U. Gaedke, B.
Ibelings, E. Jeppesen, M. Lurling, J.C. Molinero, W.M. Mooij, E. van Donk
& M. Winder, 2012. Beyond the Plankton Ecology Group (PEG) model:
Mechanisms driving plankton succession. Annual Review of Ecology, Evolution, and Systematics 43: 429-448.
Sommer, U., U. Gaedre & A. Schweizer, 1993. The first decade of oligotrophication of Lake Constance. Oecologia 93: 276-284.
Sommer, U., Z. M. Gliwicz, W. Lampert & A. Duncan, 1986. The PEG-model
of seasonal succession of planktonic events in fresh waters. Archiv für
Hydrobiologie 106: 433–471.
Spiegel, R.H. & J. Imberger, 1980. The classification of mixed layer dynamics
in lakes of small to medium size. Journal of Physical Oceanography 10:
1104-1121.
Straile, D., 2000. Meteorological forcing of plankton dynamics in a large and
deep continental European lake. Oecologia 122: 44-50.
Sverdrup, H., 1953. On conditions for the vernal blooming of phytoplankton.
Journal du Conseil / Conseil Permanent International pour l'Exploration de
la Mer 18: 287-295.
Taylor, J.R. & R. Ferrari, 2011. Shutdown of turbulence convection as a new
criterion for the onset of spring phytoplankton blooms. Limnology and
Oceanography 56: 2293-2307.
Thorpe, S.A., 1968. On standing internal gravity waves of finite amplitude.
Journal of Fluid Mechanics 32: 489-528.
Tilman, D., 1977. Resource competition between planktonic algae: an experimental and theoretical approach. Ecology 58: 338-348.
Tilman, D. 1982. Resource competition and community structure. Princeton
University Press, Princeton, NJ.
Tilzer, M.M., 1984. Estimation of phytoplankton loss rates from daily photosynthetic rates and observed biomass changes in Lake Constance. Journal of
Plankton Research 6: 309-324.
Wagner, C. & R. Adrian, 2011. Consequences of changes in thermal regime for
plankton diversity and trait composition in a polymictic lake: a matter of
temporal scale. Freshwater Biology 56: 1949–1961.
Wiltshire K.H. & B.F.J. Manly, 2004. The warming trend at Helgoland Roads,
North Sea: Phytoplankton response. In Helgoland Marine Research (ed.
Wiltshire K.H.) 58: 269-273.
Zohary, T., J. Padisák & L. Naselli-Flores, 2010. Phytoplankton in the physical
environment: beyond nutrients, at the end, there is some light.
Hydrobiologia 639: 261–269.
43
Acta Universitatis Upsaliensis
Digital Comprehensive Summaries of Uppsala Dissertations
from the Faculty of Science and Technology 1292
Editor: The Dean of the Faculty of Science and Technology
A doctoral dissertation from the Faculty of Science and
Technology, Uppsala University, is usually a summary of a
number of papers. A few copies of the complete dissertation
are kept at major Swedish research libraries, while the
summary alone is distributed internationally through
the series Digital Comprehensive Summaries of Uppsala
Dissertations from the Faculty of Science and Technology.
(Prior to January, 2005, the series was published under the
title “Comprehensive Summaries of Uppsala Dissertations
from the Faculty of Science and Technology”.)
Distribution: publications.uu.se
urn:nbn:se:uu:diva-262461
ACTA
UNIVERSITATIS
UPSALIENSIS
UPPSALA
2015