Download Mechanisms structuring the pelagic microbial food web

Mechanisms structuring the pelagic
microbial food web
– Importance of resources and predation
Kristina Samuelsson
Umeå 2003
Department of Ecology and Environmental Science
Umeå University
SE-901 87 Umeå
Sweden
AKADEMISK AVHANDLING
kommer med vederbörlig tillstånd av rektorsämbetet vid Umeå universitet,
för erhållande av filosofie doktorsexamen i ekologi, offentligen försvaras
torsdagen den 12 Juni 2003, kl. 09.00 i Stora hörsalen, KBC.
Examinator: Professor Lars Ericson
Opponent: Doctor Christiane Lancelot, Ecologie des Systèmes Aquatiques,
Université Libre de Bruxelles, Brussels, Belgium
-------------------------------------------------------------------------------------------ISBN 91-7305-464-X
Kristina Samuelsson 2003
Cover: Flagellates from the Baltic Sea by Kristina Samuelsson
Printed by VMC KBC, Umeå University
Organisation
Document name
Umeå University
Doctoral dissertation
Dept. of Ecology and Environmental Science
Author
Kristina Samuelsson
June 2003
Date of issue
Title
Mechanisms structuring the pelagic microbial food web – Importance of resources and
predation.
Abstract
Temporal and spatial variations of pelagic microorganisms in the northern Baltic Sea were
studied, as well as factors influencing their abundance and growth rates. Three main
questions were asked 1) How does increased productivity influence the structure of the
microbial food web? 2) Does predation limitation vary between trophic levels? 3) What is
the relative importance of resource and predation limitation at different trophic levels?
A field study in the northern Baltic Sea showed that dominating protozoa,
flagellates and ciliates, increased with increasing primary productivity from north to south.
Furthermore, relatively small protozoan cells dominated in the low productive north, while
larger cells became more dominant in the south. The relationship between plankton size
structure and productivity was further studied in an experimental system. In agreement with
present theories regarding nutrient status of pelagic food webs, increased productivity
caused a lengthening of the food chain as well as a change in plankton size structure. While
microplankton dominated in nutrient rich treatments pico- and nanoplankton dominated
during nutrient poor treament. The flagellate community was dominated by a potentially
mixotroph, Chrysochromulina sp., at low nutrient concentrations. To our knowledge this is
the first experimental study showing that Chrysochromulina sp. in resemblance with other
mixotrophs is favoured by nutrient poor conditions compared to strict autotrophs and
heterotrophs.
During a stratified summer period autotrophic microorganisms in the northern
Baltic Sea did not respond to removal of potential predators, indicating that they were
primarily limited by inorganic nutrients. An exception was small eucaryotic picoplankton
that showed a large response to predator removal. Among the heterotrophic microorganisms
direct effect of predation seemed to increase from ciliates, heterotrophic bacteria, small
heterotrophic flagellates, medium flagellates to large flagellates. No quick indirect effect
was observed, but after four days trophic cascades were detected.
The relative importance of resource and predation limitation was studied among
heterotrophic bacteria, flagellates and ciliates in the northern Baltic Sea. For all these
groups, resource limitation seemed to prevail during the summer period. The results also
indicated that the relative importance of predation increased with the productivity of the
system. To our knowledge there are no earlier measurements on the relative importance of
resource and predation limitation for micoorganisms in the pelagic environment.
Key words: pelagic microbial food web, bacteria, flagellates, ciliates, phytoplankton,
mixotrophy, nutrient status, predation limitation, resource limitation, Baltic Sea
Language: English
Signature:
ISBN: 91-7305-464-X
Number of pages: 129
Date: 16 May 2003
“As in most sciences, ecologists are concerned with attempting to
discern order from the seeming chaos present in natural systems.“
Menge BA 2000
TABLE OF CONTENTS
INTRODUCTION……………………………………………………….…7
The pelagic microbial food web …………………………………….7
Phytoplankton …………………………………………..…………..9
Heterotrophic bacteria……………………………………………..10
Phagotrophic flagellates……………………………….…….……..11
Phagotrophic ciliates…..……...………………….……………...…13
Study area……………………....……………………………...…...14
OBJECTIVES………………………………………………………...…...16
MAJOR RESULTS & DISCUSSION……………………………………16
Importance of resource limitation………………………………….16
Importance of access to attachment sites and
metazooplankton grazing…………………………………………...20
Importance of predation limitation……..………………………..…21
Relative importance of resource and predation limitation…….....23
CONCLUSIONS AND FUTURE PERSPECTIVES………………….26
REFERENCES…………………...……………………………………….27
Appendices: Papers I-V
LIST OF PAPERS
I: Samuelsson Kristina, Berglund Johnny, Haecky Pia, Andersson Agneta (2002)
Structural changes in an aquatic microbial food web caused by inorganic nutrient
addition. Aquatic Microbial Ecology 29: 29-38.
II: Kuuppo Pirjo, Samuelsson Kristina, Lignell Risto, Seppälä Jorma, Tamminen
Timo, Andersson Agneta (2003) Fate of increased production due to nutrient
enrichment in late-summer plankton communities of the Baltic Proper. Aquatic
Microbial Ecology (in press)
III: Samuelsson Kristina, Andersson Agneta (manuscript) Factors structuring the
protozoan community along a brackish water productivity gradient.
IV: Samuelsson Kristina, Andersson Agneta (2003) Predation limitation of the
pelagic microbial food web in an oligotrophic aquatic system. Aquatic Microbial
Ecology 30:239-250
V: Berglund Johnny, Samuelsson Kristina, Müren Umut, Kull Thomas, Andersson
Agneta (manuscript) Simultaneous resource and predation limitation in the marine
microbial food web.
Papers I and III are reprinted with the kind permission of Inter Research Science
Publisher.
INTRODUCTION
In aquatic systems the properties of dominating organisms and food web structure
to a large extent determine the flow of material and energy (Verity and Smetacek
1996). To understand how environmental changes, such as eutrophication and
climate change, influence the function of these systems we thus need to understand
the processes determining food web structure. It is known, that the concentrations
of nutrients and the process of nutrient cycling greatly influence the dynamics and
food web structure within pelagic systems. For example, in nutrient-rich waters the
classical or herbivorous food web is predominant, while in nutrient constrained
environments the microbial food web is of larger importance (Legendre and
Rassoulzadegan 1995). In the classical food web that consists of large
phytoplankton, zooplankton and fish both resource and predation seems to be
important structuring factors (Carpenter et al. 1985, 1987). Less clear is, however,
the structure and regulation of the microbial food web. In resemblance to the
classical food chain resources and predation are believed to be two of the main
structuring factors. In addition it has been shown that other factors such as
mutualism (e.g. between photosynthetic and heterotrophic organisms), symbiosis
(e.g. Mesodinium rubrum with a cryptophycean symbiont), excretion of nutrients
and parasites influence food web structure (Fenchel 1988, Coats et al. 1996). Since
microbes constitute more than 50 % of the total plankton biomass (Gasol et al.
1997) and a dominant part of the biosurface in pelagic systems, they are
fundamental for the function of these systems (e.g. Azam 1998, del Giorgio and
Duarte 2002, Hoppe et al. 2002). However, we still know too little about the
mechanisms structuring the pelagic microbial food web to fully understand the
spatial and temporal occurrence of different functional groups or species, and to
predict the response to future environmental changes. It seems as one of the largest
challenges in aquatic microbial ecology lies in determining how different food web
processes influence ecosystem structure and functioning (Pace and Cole 1994).
The pelagic microbial food web
Within the pelagic system prokaryotic and eukaryotic algae are the main primary
producers. These phytoplankton vary more than 100-times in cell size from small
picoplankton (0.2-2 µm) and nanoplankton (2-20 µm) to large microplankton (20200 µm, Fig. 1). The picoplankton fraction mainly consists of prokaryotes
(unicellular cyanobacteria and Prochlorococcus), but also eukaryotes are included.
In the nanoplankton fraction flagellates are common, while diatoms and
dinoflagellates usually dominate the microplankton fraction. The main herbivores in
the pelagic system are protists and metazooplankton (Valiela 1995). Among the
7
Size, µm
200
20
CO2
2
0.2
DOC
Fig. 1. The pelagic microbial food web. Pico-, nano- and micro- phytoplankton (unfilled
symbols) use carbon dioxide (CO2) during photosynthesis. Phytoplankton are grazed within
the phagotrophic food chain represented by flagellates, ciliates and metazooplankton (filled
symbols). Dissolved organic carbon (DOC) is exudated from cells or produced during
“sloppy feeding” and utilized by heterotrophic bacteria. Redrawn from Fenchel 1987
protists, flagellates and ciliates are the most numerous. Flagellates vary in size from
about 1 to 20 µm and ciliates from 5 to 100 µm. According to Calbet et al. (2001)
there are at least six trophic levels within the phagotrophic food chain (bacteria, <2,
2-3, 3-5, 5-10 and >10 µm heterotrophic protists). However, the number of trophic
levels probably varies considerably between systems. A portion of the carbon fixed
within the microbial food web is excreted or lost from the phytoplankton as
dissolved organic carbon (DOC). In addition DOC is produced due to incomplete
ingestion and digestion by metazooplankton and protozoa i.e. sloppy feeding (Fig.
1). Due to their small cell size, osmotrophic bacteria are probably the only
heterotrophs that effectively can utilize this carbon source. Depending on food web
structure and assimilation efficiency the bacterial production either reaches higher
trophic levels through the phagotrophic food chain or is respired within the
microbial loop (Azam et al. 1983). A rough estimate is that due to channelling
through the microbial loop web only 3-9 % of the primary production reaches
higher trophic levels compared to channelling through the classical food chain
(Fenchel 1988). The microplankton fraction is usually not grazed within the
microbial food web. Instead microplankton influence the food web structure due to
release of dissolved organic substances or due to competition with the smaller cells.
They can also be of importance as attachment site for other microorganims.
8
Phytoplankton
Pelagic microbial food web structure and functioning is to a large extent determined
by the dominating primary producers. For example, in a system dominated by
diatoms a large part of the primary production is channelled through the classical
food web or lost from the system through sedimentation (Wassmann 1993;
Heiskanen and Kononen 1994). Contrary, in systems dominated by unicellular
cyanobacteria a large part of the energy and carbon will be processed within the
microbial food web and recycled in the photic zone. The fate of the primary
production (grazing, exudation, aggregate formation, sedimentation) seems to a
large extent depend on cell size. In general high concentrations of micro sized
plankton are connected to turbulent waters e.g. upwelling areas, fronts or spring and
autumn mixed waters, while pico- and nanoplankton dominate in stagnant waters
e.g. open sea areas or during summer period stratification (Kiørboe 1993). Wellmixed waters are characterized by high input of “new” nutrients resulting in high
nutrient concentrations, while stratified water usually are characterized by
regenerated nutrients and a poor nutrient situation (Legendre and Rassoulzadegan
1995). According to Thingstad and Sakshaug (1990) the first algae to be established
at low nutrient concentrations are the ones with the lowest value of K/µm. Since
small algae generally have a lower half-saturation constant for inorganic nutrients
(K) and a higher maximal growth rate (µm) than large cells they will dominate in
nutrient poor waters (Malone 1980, Banse 1982, Probyn et al. 1990). If more
nutrients are added to the system, the growth rate of small algae will increase until
nutrient concentrations equal saturation levels. Still higher nutrient concentrations
will allow large cells to be established. At saturated nutrient concentrations uptake
is proportional to cell surface and there is no advantage in being small.
The phytoplankton community composition is also influenced by the elementary
composition of the water. Species with special requirements such as diatoms need a
Si:N relationship of 1:1 (e.g. Harris 1986). A ratio > 25:1 is, however, needed for
diatoms to be favoured over other algae (Sommer 1994). Phytoplankton demand for
C:N:P is generally 106:16:1 (Redfield ratio). Filamentous cyanobacteria can,
however, take up nitrogen from the atmosphere and should consequently be
favoured in situations were other phytoplankton are nitrogen-limited (Larsson et al.
2001).
When the phytoplankton biomass in a system is high enough herbivores will be
established (Thingstad and Sakshaug 1990). Measurements from the northern Baltic
Sea indicate that heterotrophic nanoflagellates are the main predators on picocyanobacteria, while nano-phytoplankton (2-10 µm) were grazed by ciliates (59%)
and by metazooplankton (41%), and micro-phytoplankton were grazed by large
9
dinoflagellates (20%) and by metazooplankton (80%, Uitto et al. 1997). The
phytoplankton size structure, thus, seem to have a large impact on the size
composition of the herbivore community. The consumers also influence the
phytoplankton community both due to predation, for example the outcome of
competition between small and large phytoplankton cells for inorganic nutrients
will change if the small cells are removed through predation (Thingstad and
Sakshaug 1990), and because consumers are the main source of regenerated
nutrients (Caron and Goldman 1990).
Among the phytoplankton, as well as among other aquatic microorganisms, one
common strategy to avoid predation is size. Large cell size can be advantageous
both due to size-limited predators and due to slower numerical response of large
predators (Kiørboe 1993). Population oscillations between diatoms and copepods
lag about one month, while bacteria and protozoa lag about 2 to 6 days (Fenchel
1982, Kiørboe 1993, Tanaka et al. 1997). Other known strategies among
phytoplankton to keep away from the predators are production of toxic substances
(Wolfe and Steinke 1996).
Heterotrophic bacteria
Resource level is also an important factor controlling the bacterial biomass and
production (Gasol and Duarte 2000). Bacteria utilize dissolved organic carbon
(DOC) produced within or outside the system. Of the primary production within
aquatic systems about 40-45% is generally assumed to be consumed by the bacteria
(Larsson and Hagström 1979, White et al. 1991). If the nutrient composition of the
resource is poor, bacteria will also take up dissolved inorganic nutrients. During
these situations bacteria will compete with phytoplankton for nutrients. Since
bacteria have a higher affinity for mineral nutrients than phytoplankton and due to
higher surface to volume ratio, they should out compete the phytoplankton. At too
low phytoplankton concentration, however, the bacteria will become carbon
limited, since often the main source of carbon is derived from the phytoplankton.
This situation allows co-existence between the two competitors (Thingstad and
Lignell 1997). Carbon limitation of bacteria is implied from field observations
where higher primary production or chl a level often is followed by higher bacterial
production (Cole et al. 1988, Dufour and Torréton 1996). Another mechanism
allowing co-existence between bacteria and phytoplankton is bacterivory, keeping
the biomass of the competing bacteria low. In this situation surplus nutrients are
taken up by phytoplankton, and bacteria can become nutrient limited (Thingstad
and Lignell 1997).
10
The main grazer on bacteria is thought to be nanoplanktonic protists (Fenchel 1982,
Wikner and Hagström 1988, Sherr et al. 1989). The importance of these predators
for the regulation of bacterial abundance seems, however, to differ between systems
(Billen et al. 1990, Pace and Cole 1994, Dufour and Torréton 1996). A study from
the Baltic Sea showed that most of the intra-annual variability in bacterial
production was due to a variation in the specific growth rate, controlled by
environmental factors such as temperature, substrate quality and competition
(Wikner and Hagström 1999). In other studies heterotrophic flagellates have been
found to control bacterial numbers, production and population structure (KuuppoLeiniki 1990, Gasol et al. 2002). Another important mortality factor for bacteria is
viral lysis (Fuhrman 1999, Tuomi and Kuuppo 1999, Bettarel et al. 2003). The
phage-host interaction has high species specificity and in a theoretical model
viruses controlled the diversity more than the actual numbers (Thingstad and
Lignell 1997). The importance of viral lysis compared to grazing have been
compared in several studies. The results vary from viral lysis being more than 11
times higher to 30 times lower than flagellate grazing (Guixa-Boixarey 1996,
Fischer and Velmirov 2002, Bettarel et al. 2003). In general the importance of viral
lysis increase with enrichment.
Phagotrophic flagellates
Phagotrophic flagellates utilize energy and substrate from particulate organic
material. The most common obligate phagotrophic flagellates are found within
heterokont taxa (chrysomonads and bicosoecids), dinophycean and
choanoflagellates (Boenigk and Arndt 2002). In addition a large group of known
species have not been possible to characterize and are classified in an incertae sedis
group (Vørs 1992). Flagellates are versatile in their habitat choice and they are
common both as free-living and attached forms. In general about half of the cells
are free swimming and the rest attached or temporarily attached (Boenigk and
Arndt 2002). The attached forms are found on phytoplankton such as diatoms and
filamentous cyanobacteria or on aggregates of bacteria or detritus (Leadbeater 1991,
Carrias et al. 1998). Bacterivory seems to be the main energy source among the
smallest flagellates (<5µm) and choanoflagellates, while algivory, detrivory and
osmotrophy seems to be important in larger heterotrophic flagellates (Sherr 1988,
Simek et al. 1997, Sleigh 2000). Viruses can also make up a large pool of the
ingested carbon (9%, Gonzalez and Suttle 1993). The flagellates show at least three
different feeding mechanisms: filter feeding, direct interception and raptorial
feeding (Fenchel 1987). Filter feeding organisms produce a feeding current through
a filtration structure for sieving the water for food particles, examples are
helioflagellates and choanoflagellates. Interception feeders also produce a feeding
11
current but the prey is taken up by direct interception, chrysophyceans are
interception feeders. In contradiction to filter and interception feeders, raptorial
feeders are actively searching for the prey that is taken up by direct interception,
examples are Katablepharis sp. and Goniomonas sp. (Boenigk and Arndt 2000a). A
comparison of the handling time between these strategies showed that a filter feeder
(Monosiga ovata) had much longer handling time (~ 300 s) than interception and
raptorial feeders (3.7-95 s, Boenigk and Arndt 2000a,b). The long handling time is,
however, compensated by the capacity to handle several preys at a time. Due to
morphological limitations of the different feeding apparatuses there seems to be a
passive selection for prey of a special size. Filter feeders generally take up smaller
cells than interception and raptorial feeders (Boenigk and Arndt 2000). In addition
to passive food selection there is evidence of active food selection due to
differences in the size, swimming speed and the biochemical surface composition of
the prey (Matz et al. 2002). The existence of specific predation pressure on different
bacteria indicates that flagellate feeding should be an important factor structuring
the bacterial community composition (Boenigk and Arndt 2000a).
In natural aquatic environments the concentration of bacteria vary from 105 to 107
ml-1. Threshold bacteria concentrations supporting flagellate growth have been
reported to be in the range of 105–106 bacteria ml-1 (Eccleston-Parry and Leadbeater
1994). Maximum growth rates are possibly reached at concentrations of 1-2 * 107
bacteria ml-1 (Boenigk and Arndt 2002). This comparison indicates that flagellates
probably are resource limited in many aquatic systems. A frequently used indicator
for resource limitation of flagellates is a positive correlation to their main prey, the
bacteria. Using this criterion, both evidence for and against prey limitation of
flagellates have been suggested (Sherr 1984, McManus and Fuhrman 1990,
Berninger 1991, Sanders et al. 1992, Weisse 1997). In general bacterial numbers
increase with nutrient status of a system and the importance of resource limitation
for the flagellates should consequently decrease. However, this increase in bacteria
could be due to inedible forms, known to increase with nutrient enrichment (Gasol
et al. 2002). By using simple models Sanders et al. (1992) and Gasol (1994)
suggested that resource limitation of flagellate decrease with increased nutrient
status.
Absence of a positive relationship between bacteria and flagellates could be due to
alternative prey or high predation control of the flagellates. In many aquatic
environments flagellate density varies in a rather narrow range because of tight
constraints imposed by different kind of predators (Weisse 1991; ciliates, Dolan and
Gallegos 1991; rotifers, Kuparinen and Bjørnsen 1992; dinoflagellates). Despite this
high predation pressure few predation resistant forms of flagellates have been found
and it seems like heterotrophic flagellates have little potential for shifting to forms
12
resistant to predation. High predation pressure might, however, favour species with
high growth rates. Small fast growing heterotrophic flagellates can probably
compensate predation losses faster than larger forms, which have a slower growth
and reproduction (Pace at al. 1998, Auer and Arndt 2001). Little is, however,
known about the growth rates and variation in growth rate of heterotrophic
flagellates in their natural habitats (Weisse 1997). Another strategy to avoid
predation may be to attach to particles (Jürgens et al. 1996, Carrias et al. 1998).
In addition to obligate phagotrophs some flagellates are capable of both
phagotrophic heterotrophy and phototrophic autotrophy, these flagellates are called
mixotrophs. Mixotrophy has developed independently in several taxonomic groups
and is found mainly among the dinophyceans, prymnesiophyceans and
chrysophyceans (Jones 1994, Jones 2000). Mixotrophs includes nutritional
strategies from species being almost 100% autotrophic to almost 100%
heterotrophic (Jones 1994). For the former, mixotrophy can be a strategy to survive
during nutrient poor situations. In this situation a mixotrophic flagellate has an
advantage compared to an obligate autotroph due to the capacity to take up nutrients
through bacterivory. In addition this behaviour involves eating the main competitor
for inorganic nutrients during nutrient poor conditions (Thingstad et al. 1996).
Phagotrophy can also be a strategy to supplement growth during light limitation, to
survive during darkness or to aquire essential substances for growth e.g.
micronutrients, vitamins or phospholipids (Kimura and Ishida 1989, Maranger et al.
1998). For mainly phagotrophic flagellates mixotrophy can be beneficial during
situations with low prey concentrations. The importance of mixotrophs as
bacterivores compared to heterotrophs has been reported to vary from 0 to 86 % in
aquatic systems (McManus and Fuhrman 1986, Havskum and Riemann 1996).
Phagotrophic ciliates
The ciliates are a heterogenous group consisting of about 3000 free-living species.
Cilia are used for feeding or motion. Nutrient strategies include both mixotrophy
and heterotrophy. Small prey particles are taken up through filtration feeding, while
raptorial feeding is used for uptake of larger particles. Ciliates are thought to be the
main predator on nanoplankton (2-20 µm), but are also known to feed on bacteria
(Sherr and Sherr 1987, Sherr et al. 1989). Due to sensory and behavioural capacities
ciliates can locate and exploit food patches (Jonsson and Johansson 1997).
Increased swimming under starvation can therefore increase survival.
Metazooplankton seems to be the main predator on ciliates and to be the main
limiting factor in some areas (Kivi et al. 1996). Other studies imply that resource
limitation is the main limiting factor (Johansson et al. 2002). Ciliates are known to
13
escape predation due to behavioural escape mechanisms (Jonsson and Tiselius
1990, Stoecker and Capuzzo 1990, Broglio et al. 2001). The hard lorica of tintinnids
is also suggested to be a protection against predation (Fenchel 1987, Kivi et al.
1996). In a study comparing these two strategies it was shown that the swimming
behaviour was of a larger importance to avoid predation than hard covering
(Broglio et al. 2001).
All these species-specific differences in nutritional demands, prey selection, habitat
choice and susceptibility to predation imply that the species composition of
microorganisms varies both temporally and spatially depending on factors such as
nutritional status, access to attachment sites, prey community composition and type
of predators.
The study area
The field sampling in this work was performed in the Baltic Sea. The three main
basins within this sea are the Bothnian Bay in the north, Bothnian Sea and Baltic
Proper in the south (Fig. 2). The Baltic Sea is an almost enclosed brackish sea area
with an average depth of only 52m (Niilonen 2002). Due to high rate of freshwater
input in the north and inflowing saltwater in the south the surface water salinity
varies from 1-3 PSU in the Bothnian Bay, 3-7 PSU in the Bothnian Sea to 6-8 PSU
in the Baltic Proper (Wulff et al. 1990). The inflow of saltwater to the deeper parts
creates a strong permanent halocline in the Baltic Proper. In the two northern basins
the halocline is weaker but a strong thermocline is developed during the summer.
Ice is normally covering the Bothnian Bay and Bothnian Sea in winter, while the
Baltic Proper is only partially covered. Nitrogen and phosphorous are mainly
discharged to the southern parts (Wulff et al. 1990). Silicate enters the Baltic Sea
with freshwater running into the northern parts. This freshwater input also imports
humic substances into the Baltic Sea. This inflow is largest in the Bothnian Bay
with about twice the inflow compared to the Baltic Sea (Mikulski and Falkenberg
1986). There is a gradient in mineral nutrients with relatively high nitrogen and low
phosphorous concentration in the north compared to the south. The elemental ratio
(SI:N:P) in the Bothnian Bay are in average 98:60:1 and 19:4:1 in the Baltic Proper
(Wulff et al. 1990). Since phytoplankton requires an elemental composition of
16:16:1 (Redfield et al. 1963) phosphorous limitation is dominating in the north and
nitrogen limitation in the south. Low phosphorous concentrations in the Botnian
Bay probably cause the low primary production, which is ten times lower than in
the Baltic Proper (Andersson et al. 1996, III).
14
In the Baltic Sea area there are large seasonal variations in light and temperature as
well as in water column stability and nutrient concentrations (Andersson et al.
1994). These changes influence the growth of the phytoplankton community, and
different phytoplankton groups will show maximal growth rates during different
times of the year, resulting in a seasonal succession of phytoplankton. In general
microplankton e.g. diatoms and dinoflagellates are dominating during spring, while
nano and picoplankton eg. flagellates and unicellular cyanobacteria are dominating
during summer and autumn. During spring the dinoflagellate Peridiniella catenata,
and diatoms of the genera Chaetoceros and Thalassiosira are dominating
(Andersson et al. 1996). After the spring bloom the chlorophyte Monoraphidium
contortum shows high values. In the nano-fraction Pyramimonas spp. and
Cryptophyceans are important. Unicellular cyanobacteria often peak in August.
During late summer and autumn blooms of filamentous cyanobacteria are common.
These blooms often consists of Aphanizomenon sp., Nodularia spumigena and
Anabaena sp.. In the Baltic Proper there can be a second peak of microplankton in
autumn.
I, II, IV, V
II
Fig. 2. Map of the Baltic Sea showing sampling stations for experiments performed in
paper I, II, III, IV and V. In the field study six stations were sampled located in the
Bothnian Bay (BB1, BB2), the Bothnian Sea (BS1, BS2) and the Baltic Proper (BP1, BP2).
15
In this study we have performed four experiments with water sampled from a
coastal station in the northern Bothnian Sea (I, III, IV, V) and one experiment with
water from the Gotland Basin (II, Fig. 2). All these experiment were performed
during the summer when regenerated production was dominating. In addition we
performed a field survey studying the seasonal succession of protozoa (III). This
study was performed at two stations in each of the three basins (Fig. 2).
OBJECTIVES
The aim of this thesis was to investigate the importance of resources and predation
in structuring the pelagic microbial food web. Questions asked were:
-
How does increased productivity influence the structure of the pelagic
microbial food web?
-
Does predation limitation vary between trophic levels?
-
What is the relative importance of resource limitation and predation
limitation at different trophic levels?
MAJOR RESULTS AND DISCUSSION
Importance of resources
In a theoretical linear food chain with homogenous trophic levels the top level (n)
and level n-2, n-4 etc. will increase in biomass with nutrient concentration while
level n-1, n-3 etc. will remain at constant biomass at equilibrium (Oksanen et al.
1981, Thingstad and Sakshaug 1990). When food supply is sufficient to balance
loss rates a new trophic level will be established. In a more complex food web the
outcome is not as obvious. Several characteristics of the organisms in natural
systems could cause deviations from the predictions made from a simple linear food
chain. One example is, if the different prey types on a particular level are not
substitutable resources (Leibold 1989, McCauley and Murdoch 1990, Leibold and
Wilbur 1992, Steiner 2001), or that the prey develops antipredator behaviour
(Abrams 1992). In addition the theoretical model assumes that all consumers should
have linear functional responses (Akçakaya et al. 1995) and that the predators are
homogenously distributed (Arditi and Saiah 1992). Further, omnivory i.e. a high
16
frequency of predation on more than one trophic level is not allowed (Abrams
1993).
To study how the structure of a natural aquatic food web was affected by nutrient
addition we performed an experiment using seawater from the northern Baltic Sea
(I). The organisms included were divided into three main autotrophic and
heterotrophic groups based on assumed trophic position. Autotrophs where divided
into bacteria, flagellates and diatoms and heterotrophs into bacteria, flagellates and
ciliates representing pico- nano- and microplankton, respectively (Fig. 1). Addition
of nutrients resulted in an increased biomass of all trophic levels and a changed
size-structure of the community. Among the osmotrophs (bacteria and
phytoplankton) diatoms dominated in the enriched system while bacteria and
nanoflagellates dominated the treatment without added nutrients. This change in
size-structure is in agreement with both theoretical studies and earlier empirical
studies (Thingstad and Sakshaug 1990, Kivi et al. 1996, Duarte et al. 2000). Due to
higher biovolume-specific uptake small cells should out compete larger forms in
nutrient poor conditions (Legendre and Rassoulzadegan 1995). First when small
forms are saturated or limited by predation larger forms can establish (Thingstad
and Sakshaug 1990).
The increased energy input into the enriched system also resulted in a lengthening
of the food chain, in the form of a ciliate community. Establishment of new trophic
levels with higher productivity has been shown both theoretically and in
experimental microbial food chains (Oksanen et al. 1981, Kaunzinger and Morin
1998). The occurrence of inedible or toxic forms can stop this transport of material
to higher trophic levels. In experimental systems with bacteria and bacterivorous
flagellates, inedible forms of bacteria are known to dominate (Pernthaler et al. 1997,
Hahn and Höfle 1999, Jürgens and Sala 2000). These inedible bacteria are either too
small or too large for protozoan ingestion. In the study from the northern Baltic Sea
we did not find any inedible bacteria, at least no large filamentous forms. Nor did
we find any known toxic phytoplankton. One explanation to the absence of inedible
forms could be that the duration of the experiment was too short. An earlier study
with metazooplankton as the top predator showed, however, that the ciliates and
phytoplankton could change their taxonomic composition within less than 6 days
(Kivi et al. 1996).
In the nutrient poor treatment the flagellate community was dominated by a
potentially mixotrophic flagellate, while nutrient addition decreased the importance
of this mixotrophic flagellate compared to specialised autotrophic and heterotrophic
flagellates (I). In the nutrient limited situation bacteria were probably acting as a
sink for inorganic nutrients, and due to their higher affinity for inorganic nutrients
17
and small size, bacteria almost out competed the strict autotrophs. During this
situation low bacterial concentrations also made it impossible for the phagotrophic
flagellates to establish a high biomass. The mixotrophs, on the other hand, had an
advantage in being able to utilize both inorganic and organic carbon and nutrient
sources. In theory predation by mixotrophs on bacteria may allow an autotroph
community to establish (Thingstad et al. 1996). In our study autotrophs were,
however, not increasing (I). The reason for that was most likely that the
mixotrophic grazing did not decrease the bacterial number enough to allow
establishments of autotrophs.
The superiority of a generalist in front of a specialist in severe condition are known
in theory and have earlier been shown experimentally for some species. For
example, Ochromonas sp. and a mixotrophic dinoflagellate increased during poor
nutrient conditions (Rothaupt 1996, Havskum and Hansen 1997). No earlier results
are, however, presented on mixotrophic prymnesiophyceans. In our experiment the
potentially mixotrophic flagellate was the prymnesiophycean Chrysochromulina sp.
This species is common in the Baltic Sea and known to occur after periods with low
levels of inorganic phosphorus (Hajdu et al. 1996). In agreement with the results
from the presented experiment a mesocosm study with water from the northern
Baltic Sea showed a decrease in Chrysochromulina sp. with enrichment. In a fourlevel nutrient gradient Chrysochromulina decreased with increasing nutrient
concentrations from 84, 32, 22, to 6 % of the phytoplankton community
(Samuelsson et al. manuscript). It seems that higher nutrients concentrations
generally decrease the importance of mixotrophs compared to strictly phototrophs
(Arenovski 1995, Havskum and Hansen 1997). The picture is, however, not clear
since a comparison of a high productive coastal environment and an oligotrophic
oceanic ecosystem showed that the relative importance of mixotrophy did not differ
(Sanders et al. 2000). In our study the establishment of a mixotrophic flagellate in
nutrient poor treatment probably allowed a third trophic level, the ciliates, to be at
least temporally established despite low concentrations of strict autotrophs and
heterotrophic flagellates. Mixotrophs have traditionally not been included in food
web models. However, they are most likely of large importance, especially in low
productive aquatic environments.
The response of the microbial food web to nutrient addition was also studied in a
situation with high concentrations of filamentous cyanobacteria (II). In late summer
potentially nitrogen fixating cyanobacteria, Aphanizomen sp. and Nodularia
spumigena Mertens, often form dense blooms in the central Baltic Proper. The
development of these blooms is probably favoured by nitrogen-limited conditions
(Larsson et al. 2001). To study how filamentous cyanobacteria influence resource
limitation of primary producers as well as bacteria, nutrient enrichment experiments
18
were performed in the Gotland Basin (II). These blooms might influence the
microbial community due to e.g. an increased N:P ratio (Larsson et al. 2001, Rydin
et al. 2002). Granéli et al. (1990) also showed that during these blooms the primary
production was P limited in otherwise N limited areas. Furthermore, the nutrient
enrichment experiments were used to study the channelling of an eventual increased
production in the pelagic food web. Additions of inorganic nutrients (N,P) and
liable organic carbon were made to both seawater pre-filtered through a 40 µm filter
to exclude filamentous cyanobacteria (<40 µm treatment) and to seawater with a
13-fold concentration of filamentous cyanobacteria (>90 µm treatment). Of the
single additions N gave the highest response in primary and bacterial production in
the <40 µm treatment. In the treatment with addition of filamentous cyanobacteria
(>90 µm) P seemed to be the main limiting nutrient for both bacteria and
phytoplankton. The result indicates that nitrogen fixation by the cyanobacteria
decreased N limitation of other phytoplankton and bacteria. The response to single
additions was, however, small. In general it seemed as phytoplankton primary
production was limited by both nitrogen and phosphorous and bacterial production
co-limited by carbon, nitrogen and phosphorous in both treatments.
The increased production by heterotrophic bacteria due to enrichment did not result
in higher bacterial biomass (II). This was probably a result of grazing control by
protozoa (flagellates and ciliates), which increased in the enriched treatments.
Increased primary production, however, resulted in increased biomass, especially of
picocyanobacteria. The lower loss rate of phytoplankton are in agreement with
other studies showing low grazing rates on phytoplankton, especially
picocyanobacteria (Kuuppo et al. 1998, Boenigk et al. 2001, IV). The larger
response in higher trophic levels due to increased bacterial production compared to
primary production indicated a tighter link on the heterotrophic part of the
microbial food web.
The three main basins in the Baltic Sea, Bothnian Bay in the north, Bothnian Sea
and Baltic Proper in the south form a primary production gradient with highest
production in the south. To study the effect of increased production on the protozoa
community, the spatial and temporal variation in the community composition was
studied during one year (III). The results showed that the biomass of flagellates and
ciliates increased with primary production. Furthermore, relatively small protozoan
cells dominated in the low productive north, while larger cells became more
dominant in the south. Our results are in agreement with studies in lakes showing a
positive influence of lake trophy on flagellate biomass (Sanders et al. 1992, Mathes
and Arndt 1994, Gasol et al. 1995). The effect of enrichment on the species
composition seems to be less clear. One tendency is that Chrysomonads and
Bodonoids increase with trophic status, while choanoflagellates decrease (Auer and
19
Arndt 2001). In contradiction, the results from our study showed that the relative
importance of Chrysomonads decreased with primary productivity from north to
south. In the north high input of allochtonous carbon allow a high bacterial
production despite low primary produciton. This allochtonous based bacterial
production probably explained the relatively high abundance of the bacterivorous
chrysophyceans (Andersson et al. 1989, Rothhaupt 1996).
In lake systems the seasonal dynamics of the protozoan community has been
observed to depend on nutrient status. While oligotrophic lakes have the highest
protozoa concentrations in summer, highest concentrations are reached already in
spring in more eutrophic systems (Laybourn-Parry and Rogerson 1993, Auer and
Arndt 2001). This pattern was also found in the Baltic Sea, with high summer
concentrations in the Bothnian Bay and high spring concentrations in the Bothnian
Sea and Baltic Proper (III). At all stations the concentration of small flagellates
seemed to follow the dynamics of heterotrophic bacteria, while large flagellates and
ciliates showed a positive relation to the concentration of chl a. These results
indicate that resource was an important limiting factor for protozoa in the entire
Baltic Sea.
In conclusion resource had a large influence on food web structure. Addition of
nutrients resulted in a lengthening of the food web according to traditional models
(Oksanen et al. 1981, Thingstad and Sakshaug 1990). In addition higher nutrient
levels resulted in larger autotrophs indicating that small phytoplankton are better
competitors than large cells (I). In agreement, heterotrophs increased in size with
productivity of the system (I, V). Mixotrophs seemed to have a large advantage in
nutrient poor treatments and might explain the temporal establishment of
phagotrophic ciliates at a low nutrient level (I).
Importance of access to attachment sites and metazooplankton grazing
A large part of microorganisms in the aquatic system are adapted to live on
surfaces. Surface attached forms are found among bacteria, flagellates and ciliates.
It has been shown that attachment to surfaces is the most favourable situation for
suspension feeding protozoa (Carrias et al. 1996). The abundance of suitable
attachment sites most likely influences the population dynamics of these forms. In
an in situ experiment we tested if access to attachment sites was an important
limiting factor for protozoa in the northern Baltic Sea (III). The results showed that
increased access to surface promoted the choanoflagellates, while other
nanoflagellates were not promoted by surface alone. In a field study in the Baltic
Sea, we observed that while other bacterivorous flagellates peaked during summer,
20
loricated choanoflagellates showed highest concentrations in spring and autumn
(III). The inverse relationship found between the loricated choanoflagellates and
other nanoflagellates in the field study, was thus probably explained by seasonal
changes in the access to surface attachment sites. In our study in the Baltic Sea the
spring peak of choanoflagellates actually coincided with a peak in diatoms, while
the autumn peak coincided with the autumn re-suspension of detritus material (III).
During both periods, thus, possible attachment sites were enhanced.
Like other heterotrophic flagellates choanoflagellates are thought to be mainly
bacterivorous (Leadbeater 1991, Carrias et al. 1996). In addition some species have
the capacity to ingest pico- and nanoautotrophs, detritus as well as dissolved
organic carbon (Sherr 1988, Buck et al. 1991, Marchant and Scott 1993). Loricated
choanoflagellates, however, differ morphological from other flagellates due to that
the lorica increase its size at least to the double. An explanation to the dynamical
difference between the two groups of flagellates could, thus, also be variation in
vulnerability to predation. Metazoplankton is known to show high densities during
the summer in the Baltic Sea (Johansson et al. 2002). To study the effect of
metazooplankton on the flagellate community we performed an in situ experiment
where metazooplankton were added in different concentrations to a natural
flagellate community (III). In the treatment with highest metazooplankton
concentration the number of loricated choanoflagellates decreased. In the same
treatment the concentration of ciliates decreased while the concentrations of small
flagellates increased. The increase of small flagellates was probably a consequence
of low ciliate concentrations. The results showed that metazooplankton had the
capacity to graze choanoflagellates. Thus, they probably have a negative effect on
the choanoflagellate community during periods of high metazooplankton
abundance, such as the summer. This result also shows that choanoflagellates are a
direct link between bacteria and metazooplankton.
The inverse relationship found between loricated choanoflagellates and small
heterotoprhic flagellates in the field study, was thus probably explained by both
seasonal changes in the predator community and seasonal changes in the access to
surface attachment sites.
Importance of predation
Although grazing rates on several groups within the microbial food web have been
measured. Predation limitation in these groups is poorly understood. Predation
limitation has been defined as the degree to which per capita growth rate is
decreased by predation (Osenberg and Mittelbach 1996).
21
A truncation experiment were performed to measure predation limitation within the
microbial food web (III). The main questions asked were if predation limitation
differs at varying trophic levels or in different functional groups, i.e. autotrophs and
heterotrophs. Potential predators of different size were removed and the response on
both autotrophs and heterotrophs was studied. Heterotrophic bacteria, heterotrophic
flagellates and autotrophic picoeukaryotes increased when potential predators were
removed, indicating predation limitation of these groups. Other phytoplankton and
ciliates did not respond to predator removal, showing that predation was not a
limiting factor for these organisms. These results are in agreement with our nutrient
addition experiment (II) showing a higher transport within heterotrophs than
between autotrophs and heterotrophs. Low predation limitation of phytoplankton
during summer has been observed earlier in the Baltic Sea (Lignell et al. 1992, Kivi
et al 1993). Microprotozoans have, however, been observed to effectively graze
autotrophic nanoplankton (Kivi et al. 1993). Only a few measurement of grazing on
picoautotrophs have been performed. In agreement with our result these showed
that picoeukaryotes are limited by predation (e.g. Pernthaler et al. 1996, Reckerman
and Veldhuis 1997). Most likely, the autotrophs in this study were mainly resource
limited.
The appearance of trophic cascades has been used to study the structure of the
microbial food web (e.g. Wikner and Hagström 1988, Calbet et al. 2001).
Alternating positive and negative responses of the bacterial community due to
removal of predators of different sizes have been explained by quick trophic
cascades (within 24 h). We did not find such a quick indirect response to removal of
predators. After about 3-6 days, however, trophic cascades were observed
(II,III,V). Earlier studies have shown both the occurrence and absence of trophic
cascades within the pelagic microbial food web (Güde 1988, Dolan and Gallegos
1991, Reckermann and Veldhuis 1997, Kuuppo et al. 1998, Caron et al. 1999,
Calbet et al. 2001). Several explanations to lack of trophic cascades within
microbial communities have been suggested. For example, that removal of a
predator or prey is quickly compensated due to high turnover rates of the microbes
(Pace et al. 1998, Mikola and Setälä 1998), that indirect trophic links such as
nutrient cycling makes the identification of top-down and bottom-up forces harder
(Mikola and Setälä 1998) or due to predator avoidance in the form of chemical,
morphological, behavioural or life history defence (Verity and Smetacek 1996).
There is also a reason to believe that cascades are less likely in oligotrophic
environments, due to strong resource control and larger importance of mixotrophy.
The trophic cascade theory also assumes a linear food web (Morin and Lawler
1995, Polis and Strong 1996). One explanation for weak importance of trophic
cascades may, thus, be omnivory. In the northern Baltic Sea the main links between
22
the heterotrophs seemed to be from bacteria to small heterotrophic flagellates, from
medium heterotrophic flagellates and small ciliates to large flagellates and ciliates
(IV). The results, however, also indicated omnivory. About 30 % of the predation
on bacteria and small flagellates was due to grazing by a non-adjacent trophic level
.
Relative importance of resource and predation limitation
Both resource and predation limitation seemed to be important factors structuring
the microbial food web. A comparison of their relative importance requires
simultaneous measurement of these two limiting factors (Osenberg and Mittelbach
1996). Some theories hypothesize that predation and resource limitation alternate
between adjacent trophic levels, while others assume simultaneous effects of
resource and predation (Hairston et al. 1960, Oksanen et al. 1981). Others suggest
that top-down regulation is dominating in the top of a food web and bottom-up
regulation at the bottom of a food web (McQueen et al. 1986). To our knowledge
the relative importance of resource and predation limitation of the main microbial
heterotrophs in the pelagic system, bacteria, flagellates and ciliates, have not been
quantified before.
To study the relative importance of resource and predation we used a cross factorial
experimental design were resource and predator level were varied (V). Resource
was added in the form of the bacterium Pseudomonas fluorescence and potential
predators were removed by filtration. The relative importance of resource limitation
for the population growth rate was on average 62% in June and 74% in September.
Thus, during both experiments the heterotrophic flagellates were mainly resource
limited. Unfortunately we did not perform any simultaneous measurements on the
relative importance of resource and predation for bacteria and ciliates. From other
studies we can, however, calculate the relative importance of these two factors for
bacteria and ciliates. In the nutrient addition experiment performed at the Gotland
Basin in 1997 (II), bacteria increased their specific growth rate from – 0.29 d-1 to
0.18 d-1 when predators larger than 0.8 µm were removed. After adding carbon,
nitrogen and phosphorous the specific growth rate increased further to 0.25 d-1. The
relative importance of resource limitation was thus 14%. In the truncation
experiment in the northern Baltic Sea in 1998, the importance of predation on
bacteria was measured (IV). In addition, the treatment with only bacteria was
diluted ten times with particle free water to reduce resource limitation. By removing
predators the growth rate increased from 0 d-1 to 0.49 d-1 and by reducing resource
limitation the growth rate increased to 2.29 d-1. In this case the relative importance
of resource limitation was 79%. In the same experiment removal of potential
predators on ciliates did not affect the specific growth rate of the ciliates. After an
23
increase of their main prey, heterotrophic flagellates, the specific growth rate of the
ciliates increased to 0.80 d-1. Ciliates were, thus, mainly resource limited. These
calculations show that in the Bothnian Sea all three adjacent trophic levels where
mainly resource limited during summer (Fig. 3). In the Baltic Proper, however, it
seemed, that at least the bacteria were mainly predation limited. A rough estimation
of the response of heterotrophic flagellates and ciliates from the experiment in the
Gotland Basin 1998 indicates that also these were mainly predation limited. Our
results indicate that the importance of predation varies at different trophic levels,
but generally the importance of predation limitation within the microbial food web
seems to increase with productivity of the system. This is in agreement with earlier
hypotheses that heterotrophic flagellates should be mainly resource limited in
nutrient poor environments (Sanders et al. 1992, Gasol 1994). The importance of
predation limitation for bacteria has been suggested both to decrease and increase
with system productivity (Billen et al. 1990, Sanders et al. 1992, Gasol 1994, Gasol
et al. 2002). In addition Fenchel (1986) suggested that grazing by heterotrophic
nanoplankton maintained bacteria just below their carrying capacity in oligotrophic
ecosystems, but in eutrophic systems the mean number of bacteria were kept well
below the carrying capacity by heterotrophic flagellate grazing.
The observation that resource was the main limiting factor at adjacent trophic levels
are not in agreement with the EEH model by Oksanen et al. (1981), predicting that
Limitation (%)
Bothnian Sea
Baltic Proper
100
100
80
80
60
60
40
40
20
20
0
0
June Bact
June Flag
Sept Flag June Ciliates
Aug Bact
Fig. 3. Resource (grey/black bar) and predation (white bar) limitation of heterotrophic bacteria
(Bact), heterotrophic flagellates (Flag) and phagotrophic ciliates (Ciliates) in the Bothnian Sea
in June and September. Limitation of heterotrophic bacteria in the Baltic Proper were measured
in August.
24
the importance of resource and predation alternates between adjacent trophic levels.
Several factors have been presented to cause the discrepancy between the behaviour
of natural food webs and the EEH model (Polis and Strong 1996, Mikola and Setälä
1998, Steiner 2001, see above). Some of these factors may be important in the
pelagic microbial food web. Heterogenous trophic levels is one of these factors
Leibold 1989, McCauley and Murdoch 1990, Leibold and Wilbur 1992, Steiner
2001). For example, at resource addition the increase of the basal level,
phytoplankton or bacteria do not necessarily have to affect primary consumers, due
to the establishment of inedible forms. This is well known for heterotrophic
bacteria, which can escape into size refuges, cells that are too small or too large for
the predator (Simek et al. 1997, Hahn and Höfle1999, Jürgens and Sala 2000).
Spatial heterogeneity of the top predator (Arditi and Saiah 1992) can also result in
resource limitation of adjacent trophic levels. Ciliates and flagellates are known to
aggregate around food patches (Fenchel and Blackburn 1999).
According to a model by Gasol (1994) the relationship between abundance of
heterotrophic bacteria and heterotrophic flagellates can be used to evaluate if
flagellates are bottom-up or top-down regulated. We compared the results from this
model with the results from our empirical measurements of resource and predation
limitation of flagellates. Within this model the maximum attainable abundance
(MAA) describes the linear relationship between bacteria and the maximum
abundance of flagellates attained at equilibrium. The line corresponds to the preypredator zero-isocline in a Lotka-Volterra model. A second line, mean realized
abundance (MRA), describes the relationship between the mean abundance of
flagellates and bacteria from measurements in aquatic systems. This line is assumed
to average the effect of both top-down and bottom-up regulation over the year, and
is used as a reference line to interpret the relative importance of bottom-up or topdown factors regulating heterotrophic nanoflagellates abundance. If the data points
lies above the MRA-line the flagellate community is thought to be bottom-up
regulated, and if the data ends up below the MRA-line they are thought to be topdown regulated. According to this model the flagellates in our resource-predation
experiment were bottom-up regulated in June but top-down regulated in September.
It seemed, thus, that the model worked well in June but not in September. Two
assumptions are made in the model. The first is that flagellates are only eating
heterotrophic bacteria and the other that all bacteria are edible. The relatively low
abundance of flagellates compared to the number of bacteria could in September be
explained by that a large part of the bacterial community was inedible. One
criterion for edibility of bacteria is the size. Assuming that only bacteria in the
range of 0.7 µm3 to 1 µm3 are edible (Andersson et al. 1986, Gonzalez et al. 1990,
Hahn and Höfle 1999) the September point move towards the bottom-up regulated
end of the scale. One years data from a station in the Bothnian Bay and one station
25
in the Bothnian Sea were also plotted in the model. The analysis indicated that all
over the year the flagellates were mainly resource-limited in these two basins (V).
Our data thus fits with earlier hypothesis that flagellates are mainly resource limited
in oligotrophic systems (Sanders et al. 1992, Gasol 1994).
CONCLUSIONS AND FUTURE PERSPECTIVES
A field study in the northern Baltic Sea showed that dominating protozoa,
flagellates and ciliates, increased with increasing primary productivity from north to
south. Furthermore, relatively small protozoan cells dominated in the low
productive north, while larger cells became more dominant in the south. The
relationship between plankton size structure and productivity was further studied in
an experimental system. In agreement with present theories regarding nutrient status
of pelagic food webs, increased productivity caused a lengthening of the food chain
as well as a change in size structure in an experimental system. While
microplankton dominated in nutrient rich treatments pico- and nanoplankton
dominated during nutrient poor treament. The flagellate community was dominated
by a potentially mixotroph, Chrysochromulina sp., during low nutrient
concentrations. This is the first study showing that Chrysochromulina sp. in
resemblance with other mixotrophs seems to be favoured in nutrient poor situations
compared to strict autotrophs and heterotrophs.
During a stratified summer period autotrophic microorganisms in the northern
Baltic Sea did not respond to removal of potential predators, indicating that they
were primarily limited by inorganic nutrients. An exception was small eucaryotic
picoplankton that showed a large response to predator removal. Among the
heterotrophic microorganisms direct effect of predation seemed to increase from
ciliates, heterotrophic bacteria, small heterotrophic flagellates, medium flagellates
to large flagellates. No quick indirect effect was observed, but after four days
trophic cascades were detected.
The relative importance of resource and predation limitation was studied among
heterotrophic bacteria, flagellates and ciliates in the northern Baltic Sea. For all
these groups, resource limitation seemed to prevail during the summer period. The
results also indicated that the relative importance of predation increased with the
productivity of the system. To our knowledge there are no earlier measurements on
the relative importance of resource and predation limitation for micoorganisms in
the pelagic environment.
26
To verify the pattern found in this study, concerning the importance of productivity
and trophic level for the relative importance of resource and predation limitation,
similar questions have to be asked across a variety of aquatic systems. This also
requires careful observation of long time series of bacteria, flagellates, ciliates and
metazooplankton.
In addition to field studies, it is necessary to perform manipulation experiments of
simple culture systems and from these develop model systems. It is necessary to
examine mechanisms structuring the microbial environment such as antipredator
behaviour, behavioural of the predators and the importance of patchiness for the
dynamics within the microbial community. Studies of impact of protistan predation
on the community structure and of chemical communications between predator and
prey in microbial food webs are also lacking. In agreement with the suggestion of
Kaunzinger (1998) future studies should vary trophic complexity and omnivory to
determine how these aspects of natural systems alter responses to changes in
productivity.
Another unanswered question is the abundance of inedible bacteria in the natural
environment. Is this an important mechanism for the dynamic of bacteria? Which
are the processes selecting for inedibility? Is the occurrence of inedible bacteria
connected to predation pressure from flagellates? In addition to bacteria are there
inedible forms of flagellates? The lorica of choanoflagellates could be a strategy to
escape predation from ciliates. There are examples of behavioural antipredator
strategies among ciliates. Can a similar strategy be found for flagellates and perhaps
also for bacteria?
ACKNOWLEDGMENTS: I want to thank Agneta Andersson, Johnny Berglund
and Pia Haecky for comments on earlier versions of this thesis.
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