FINNISH INSTITUTE OF MARINE RESEARCH – CONTRIBUTIONS
No. 15
Sanna Suikkanen
Allelopathic effects of filamentous cyanobacteria on
phytoplankton in the Baltic Sea
Finnish Institute of Marine Research, Finland
Helsinki 2008
.
ISSN 1457-6805
ISBN 978-951-53-3022-2 (Paperback)
ISBN 978-952-10-4457-1 (PDF)
Allelopathic effects of filamentous cyanobacteria on
phytoplankton in the Baltic Sea
Sanna Suikkanen
Academic dissertation in Hydrobiology to be presented, with the permission of the Faculty of Biosciences of
the University of Helsinki, Department of Biological and Environmental Sciences, for public examination in
Auditorium Aura, Dynamicum, Erik Palménin aukio 1, Helsinki, on February 8th, 2008, at 12 o’clock noon.
Supervisors:
Doc. Jonna Engström-Öst
Finnish Institute of Marine Research
Helsinki, Finland
Prof. Markku Viitasalo
Finnish Institute of Marine Research
Helsinki, Finland
Reviewers:
Doc. Pirjo Kuuppo
Finnish Environment Institute
Helsinki, Finland
Dr. Norbert Wasmund
Baltic Sea Research Institute
Warnemünde, Germany
Opponent:
Assoc. Prof. Karin Rengefors
Lund University
Lund, Sweden
CONTENTS
List of original articles..................................................................................................................................... 7
Contributions ................................................................................................................................................... 7
Abstract ............................................................................................................................................................ 9
1. Introduction................................................................................................................................................ 11
1.1 Allelopathy ............................................................................................................................................ 11
1.1.1 Phytoplankton allelopathy: evolutionary and ecological roles........................................................ 11
1.1.2 Allelochemicals and their modes of action ..................................................................................... 12
1.1.3 Cyanobacterial allelopathy.............................................................................................................. 17
1.2 Ecosystem changes in the Baltic Sea ..................................................................................................... 17
1.3 Bloom-forming cyanobacteria ............................................................................................................... 19
1.3.1 Anabaena spp.................................................................................................................................. 20
1.3.2 Aphanizomenon flos-aquae............................................................................................................. 20
1.3.3 Nodularia spumigena...................................................................................................................... 20
2. Objectives of the study .............................................................................................................................. 21
3. Methods ...................................................................................................................................................... 21
3.1 Laboratory studies (I–III)...................................................................................................................... 21
3.2 Long-term data analysis (IV)................................................................................................................. 23
4. Results and discussion ............................................................................................................................... 24
4.1 Allelopathy of Baltic cyanobacteria....................................................................................................... 24
4.1.1 Effects of cyanobacteria on monocultures ...................................................................................... 24
4.1.2 Role of nodularin in allelopathy...................................................................................................... 24
4.1.3 Mode of allelopathic action............................................................................................................. 26
4.1.4 Effects of cyanobacteria on a natural plankton community ............................................................ 26
4.2 Long-term trends of phytoplankton and environmental factors ............................................................. 28
5. Conclusions................................................................................................................................................. 29
Acknowledgements ........................................................................................................................................ 30
References....................................................................................................................................................... 31
Allelopathic effects of filamentous cyanobacteria on phytoplankton in the Baltic Sea
7
LIST OF ORIGINAL ARTICLES
This thesis is based on the following papers, which are referred to in the text by their Roman numerals:
I
Suikkanen, S., Fistarol, G.O. & Granéli, E. 2004: Allelopathic effects of the Baltic cyanobacteria
Nodularia spumigena, Aphanizomenon flos-aquae and Anabaena lemmermannii on algal monocultures. – Journal of Experimental Marine Biology and Ecology 308: 85–101.
II
Suikkanen, S., Engström-Öst, J., Jokela, J., Sivonen, K. & Viitasalo, M. 2006: Allelopathy of Baltic
Sea cyanobacteria: no evidence for the role of nodularin. – Journal of Plankton Research 28: 543–550.
III
Suikkanen, S., Fistarol, G.O. & Granéli, E. 2005: Effects of cyanobacterial allelochemicals on a natural plankton community. – Marine Ecology Progress Series 287: 1–9.
IV
Suikkanen, S., Laamanen, M. & Huttunen, M. 2007: Long-term changes in summer phytoplankton
communities of the open northern Baltic Sea. – Estuarine, Coastal and Shelf Science 71: 580–592.
The original communications were reproduced with the kind permission of Elsevier Science (I and IV), Oxford
University Press (II) and Inter-Research Science Publisher (III).
CONTRIBUTIONS
I
II
III
IV
Original idea
S. Suikkanen
G. Fistarol
S. Suikkanen
J. Engström-Öst
G. Fistarol
S. Suikkanen
M. Laamanen
M. Viitasalo
Study design and
methods
S. Suikkanen
G. Fistarol
S. Suikkanen
J. Engström-Öst
M. Viitasalo
G. Fistarol
S. Suikkanen
S. Suikkanen
M. Laamanen
Data gathering
S. Suikkanen
G. Fistarol
S. Suikkanen
J. Jokela
S. Suikkanen
G. Fistarol
M. Huttunen
S. Suikkanen
M. Laamanen
Responsible for
manuscript
preparation
S. Suikkanen
S. Suikkanen
S. Suikkanen
S. Suikkanen
8
Suikkanen
Finnish Institute of Marine Research – Contributions No. 15
Allelopathic effects of filamentous cyanobacteria on phytoplankton in the Baltic Sea
9
Allelopathic effects of filamentous cyanobacteria on
phytoplankton in the Baltic Sea
Sanna Suikkanen
Finnish Institute of Marine Research, Erik Palménin aukio 1,
P.O. Box 2, FI-00561 Helsinki, Finland
Suikkanen, S. 2008: Allelopathic effects of filamentous cyanobacteria on
phytoplankton in the Baltic Sea. Finnish Institute of Marine Research – Contributions
No. 15, 2008.
ABSTRACT
Eutrophication and enhanced internal nutrient loading of the Baltic Sea are most clearly reflected by increased late-summer cyanobacterial blooms, which often are toxic. In addition to
their toxicity to animals, phytoplankton species can be allelopathic, which means that they produce chemicals that inhibit competing phytoplankton species. Allelopathy may lead to the formation of harmful phytoplankton blooms and the spread of exotic species into new habitats. The
aim of my thesis was to investigate whether the Baltic filamentous cyanobacteria Anabaena sp.,
Aphanizomenon flos-aquae and Nodularia spumigena have allelopathic properties, and if indications of such interactions can be detected in the long-term development of the Baltic phytoplankton community structure.
My studies provide the first evidence for allelopathic effects in brackish water cyanobacteria.
In laboratory experiments employing both monocultures of the target species and a natural
phytoplankton community from the Baltic Sea, exudates of all three cyanobacteria inhibited
cryptophytes. The allelopathic effects are rather transitory, and some co-occurring species show
tolerance to them. The allelochemicals are excreted during active growth and they decrease cell
numbers, chlorophyll a content and carbon uptake of the target species. Although the more specific modes of action or chemical structures of the allelochemicals remain to be studied, the results clearly indicate that the allelopathic effects are not caused by the hepatotoxin, nodularin,
produced by N. spumigena.
On the other hand, cyanobacteria stimulated the growth of bacteria, other cyanobacteria,
chlorophytes and flagellates in a natural phytoplankton community. The stimulation is probably
due to the ability of these taxa to utilize organic matter or bacteria, or nutrients provided by the
bacteria or released from the damaged cryptophyte cells. Therefore, the allelochemicals may act
via lysis of the target algal cells, making them release nutrients, which will lead to the proliferation of the allelopathic organism.
In a long-term data analysis of phytoplankton abundances and hydrography of the northern
Baltic Sea, a clear change was observed in the phytoplankton community structure, together with
a transition in environmental factors, between the late 1970s and early 2000s. Surface water salinity has decreased, whereas the water temperature and concentration of dissolved inorganic nitrogen have increased. In the phytoplankton community, the biomass of cyanobacteria, chrysophytes and chlorophytes has significantly increased, and the late-summer phytoplankton community has become increasingly cyanobacteria-dominated. In contrast, the biomass of cryptophytes has decreased. The increased temperature and nutrient concentrations probably explain
10
Suikkanen
Finnish Institute of Marine Research – Contributions No. 15
most of the changes in the phytoplankton, but my results suggest that the possible effect of
chemically mediated biological interactions should also be considered.
Cyanobacterial allelochemicals can cause additional stress to other phytoplankton in the nutrient-depleted late-summer environment and thus contribute to the persistence of long-lasting
cyanobacterial mass occurrences. On the other hand, cyanobacterial blooms may either directly
or indirectly promote or retard the growth of some phytoplankton species. Therefore, a further
increase in cyanobacteria will probably shape the late-summer pelagic phytoplankton community by stimulating some species, but inhibiting others.
Key words: allelopathy, cyanobacteria, Baltic Sea, eutrophication, long-term changes, Anabaena
sp., Aphanizomenon flos-aquae, Nodularia spumigena, nodularin
Allelopathic effects of filamentous cyanobacteria on phytoplankton in the Baltic Sea
1. INTRODUCTION
1.1 Allelopathy
The term ‘allelopathy’, originating from the
Greek words allelon (= of each other) and pathos (=
to suffer), was introduced by Molisch (1937) to describe the biochemical interactions between all types
of plants and microorganisms. Rice (1984) modified
the definition to refer to any direct or indirect harmful or beneficial effect of one plant or microorganism on another through chemicals that are released
into the environment. Most recently, allelopathy was
formulated as ‘any process involving secondary
metabolites produced by plants, algae, bacteria, and
fungi that influence the growth and development of
agricultural and biological systems’ (International
Allelopathy Society 1996). Some authors also include grazer deterrence (e.g. Leflaive & Ten-Hage
2007), but in a strict sense and within this thesis,
only the inhibitory effects among competing plants
and autotrophic microorganisms are considered allelopathic, although the possibility of ‘positive allelopathy’ (stimulatory effects) is speculated (article
III).
Competition for resources can occur as exploitation and/or interference. Exploitation means the direct use of a resource, reducing its availability to a
competing individual or species. In interference,
access to a resource is denied to competitors by the
dominant individual or species, due to the release of
antibiotics, territorial behaviour and social hierarchies (Valiela 1995). Allelopathy is an example of
interference competition with a passive character
(Reigosa & al. 1999), compared with e.g. territorial
behaviour. The allelopathic organism releases
chemicals that inhibit the growth of a competing
organism and thus indirectly prevents it from using
common resources. In the present work, the term
‘growth inhibition’ is used widely to refer to the
negative effects on either the growth rate or the accumulation of cells of the target phytoplankton species. Here, ‘phytoplankton’ also includes cyanobacteria, which are photoautotrophic prokaryotes that
functionally belong to phytoplankton.
Due to the economic importance of agricultural
and forest ecosystems, terrestrial allelopathy has
been widely studied (Rice 1984, Rizvi & al. 1999).
In aquatic environments, studies are complicated e.g.
by the high diffusive potential of compounds, as
well as difficulties in collecting and culturing the
organisms. Definitive evidence for allelopathy in the
field is almost impossible to obtain due to the complexity of natural interactions. However, allelopathy
is considered as an important process that occurs
among all groups of marine and freshwater primary
producers (Gross 2003, Legrand & al. 2003). Most
of the studies on aquatic allelopathy have focused on
11
freshwater macrophytes, but the interest in allelopathic interactions within the phytoplankton has
recently been kindled (reviewed by Maestrini &
Bonin 1981, Lewis 1986, Cembella 2003, Gross
2003, Legrand & al. 2003, Leflaive & Ten-Hage
2007, Macías & al. 2008). Among phytoplankton,
allelopathic effects have been reported in cyanobacteria, dinoflagellates, haptophytes, diatoms, raphidophytes and chlorophytes, but not in cryptophytes,
chrysophytes or euglenophytes.
1.1.1 Phytoplankton allelopathy: evolutionary and
ecological roles
Allelopathic interactions can occur in all aquatic
habitats. In littoral or benthic ecosystems, the distances between organisms are smaller than in the
pelagial and allelopathic interactions are probably a
means of competing for space. The allelochemicals
may be translocated by direct contact from the
emitter species to targets in their vicinity (Gross
2003). In the pelagic zone, the larger distances between cells and dilution of compounds have been
considered as major problems for allelopathy; thus,
it was argued that allelopathy is not an evolutionarily stable strategy for phytoplankton (Lewis 1986).
In the light of recent studies, however, the advantages versus costs from the production of allelopathic compounds appear high enough for it to also
be adaptive in the pelagic environment (Leflaive &
Ten-Hage 2007). Compared with terrestrial and
benthic/littoral allelochemicals, pelagic metabolites
are probably more efficient and work at lower concentrations, and/or their production and excretion
rates are higher, thus ensuring their effects on the
target species (Gross 2003).
Coexisting organisms are probably adapted to
each other’s presence, which was suggested to reduce the importance of allelopathic interactions in
natural environments (Reigosa & al. 1999). On the
other hand, Legrand & al. (2003) assumed that in a
complex community with a mix of different species,
some targets may become adapted to an allelopathic
compound, and some will remain sensitive, which
confers a sufficient advantage for the emitter. Allelopathy has even been proposed as one of the
many mechanisms explaining ‘the paradox of the
plankton’ (Hutchinson 1961), where the coexistence
of a large number of competing species in phytoplankton communities, limited by only a few resources, contradicts the competitive exclusion principle that predicts the exclusion of all but the best
adapted species for each limiting factor (Hardin
1960). The presence of allelopathic species was suggested to reduce the competition among other, nontoxic species, and thus prevent the competitive exclusion of species that would otherwise not coexist
(Roy & Chattopadhyay 2007).
12
Suikkanen
The importance of allelopathy is probably enhanced in cases of abiotic stress (e.g. nutrient availability, light), invasion by exotic organisms, synthesis of a new molecule by the producer and delayed
adaptation of the target species, or continuous release and limited (e.g microbial) degradation of allelochemicals, which leads to their accumulation in
the environment (Reigosa & al. 1999). For example,
allelochemicals released by an invasive plant into a
new environment may result in its predominance,
because native organisms lack the defence/detoxification mechanisms developed through coevolution.
Many terrestrial (Bais & al. 2003, Hierro &
Callaway 2003) and also some aquatic plants are
suggested to use allelopathy as a spreading
mechanism (Macías & al. 2008).
In addition to many environmental factors, allelopathy can be important in explaining community
structure and its spatiotemporal changes, such as
algal successions and the induction and termination
of blooms (Vance 1965, Keating 1977, 1978,
Schagerl & al. 2002, Sukenik & al. 2002, Vardi &
al. 2002, Chiang & al. 2004, de Figueiredo & al.
2006). Some species, such as the dinoflagellate
Peridinium aciculiferum, apparently use allelopathy
to compensate for their low rates of growth and nutrient uptake (Rengefors & Legrand 2001). However, the problem of distinguishing between allelopathy and resource exploitation competition makes it
difficult to evaluate the importance of allelopathy in
natural environments.
1.1.2 Allelochemicals and their modes of action
Allelochemicals produced by aquatic macrophytes resemble those produced by terrestrial plants
(e.g. fatty acids, phenolic compounds, terpenoids,
polysaccharides), whereas the allelochemicals of
microalgae and cyanobacteria have apparently
evolved in their own direction (Macías & al. 2008).
Macrophytes usually live attached to a solid substrate and need a means to control epiphytes; thus,
they produce lipophilic compounds that will remain
attached to their surface or in the vicinity of the producer. In contrast, pelagic organisms need more hydrophilic compounds with a high degree of activity
to overcome dilution effects (Gross 2003, Macías &
al. 2008). Few microalgal allelochemicals have been
chemically identified to date, and they include cyclic
peptides, alkaloids, organic acids and long-chain
polyunsaturated fatty acids (Legrand & al. 2003).
The major difficulty for the isolation of bioactive
compounds from phytoplankton is that they often are
produced in very small amounts, because under nutrient limitation, the production of a highly active
Finnish Institute of Marine Research – Contributions No. 15
compound at low concentrations is a cost-effective
strategy (Leflaive & Ten-Hage 2007).
Allelochemicals may inhibit photosynthesis or
protein activity of the target species, modify or activate its other physiological functions, damage cell
membranes, kill the competitor or exclude it from
the donor vicinity, e.g. by settling (Uchida & al.
1995, Smith & Doan 1999, Kearns & Hunter 2001,
Schmidt & Hansen 2001, Legrand & al. 2003, Fistarol & al. 2004a). Allelochemicals tend to simultaneously affect many physiological processes, and
one species can produce several allelochemicals that
work synergistically in the environment (Reigosa &
al. 1999).
Inhibition of photosynthesis, the central physiological process of competing primary producers, is
an especially widespread mode of allelopathic action
among cyanobacteria (Smith & Doan 1999). The
majority of the allelochemicals acting on photosynthesis interfere with the photosynthetic electron
transport in photosystem II (PSII), located in the
thylakoid membranes of the chloroplasts. This decreases oxygen evolution and carbon incorporation
of the target cells, leading to a decreased growth rate
and biomass accumulation. Examples of isolated and
characterized cyanobacterial allelochemicals that are
known to inhibit PSII include fischerellins from
Fischerella spp., cyanobacterin LU-1 from Nostoc
linckia, nostocyclamide from Nostoc sp. and cyanobacterin from Scytonema hofmanni (Smith & Doan
1999). In addition, several yet unidentified allelochemicals apparently act similarly (Table 1 and references therein).
Both environmental factors and the physiological
status of a phytoplankton cell can affect allelochemistry (Legrand & al. 2003). Abiotic stress, such as
nutrient limitation (von Elert & Jüttner 1996, Ray &
Bagchi 2001, Rengefors & Legrand 2001, Granéli &
Johansson 2003, Fistarol & al. 2005), or extreme
conditions of light (von Elert & Jüttner 1996, Hirata
& al. 2003), temperature (Gromov & al. 1991, Issa
1999, Hirata & al. 2003) or pH (Ray & Bagchi
2001) can enhance both the production of the allelochemicals and the vulnerability of the target
(Reigosa & al. 1999). The intensity of the interaction
may also be dependent on biotic factors, such as
growth phase or donor/target cell concentrations
(Bagchi & al. 1990, Arzul & al. 1999, Kearns &
Hunter 2000, Rengefors & Legrand 2001, Schmidt
& Hansen 2001, Uronen & al. 2005, Volk 2007).
After release, abiotic factors (light, oxygen and redox conditions), as well as bacterial activity, may
influence the stability of allelochemicals (Gross
2003).
Synechocystis aquatilis
Oscillatoriales
Arthrospira laxissima
A. maxima
Geitlerinema
splendidum
Synechococcus sp.*
Chroococcales
Chroococcus minutus*
Microcystis aeruginosa*
Group/species
Microcystin-LR, -RR
CC
CC
CC
Riverine,
epipelic, Spain
Culture medium
Culture medium
Methanol extracts, microcystins
Culture medium
Cell-free filtrate
Microcystin-LR, -RR
Microcystin-LR, -RR, -YR
FW, CC
CC
FW plankton,
USA
CC
Microcystin-RR
Culture medium, microcystin-LR
Kasumigamide (linear
tetrapeptide)
Crude bloom extract,
microcystin-LR, -RR
Microcystin-LR
Microcystin-RR (cyclic
heptapeptide)
Polyunsaturated fatty acids
Culture medium
Extracellular metabolites
Active component
FW plankton,
China
FW plankton,
India
FW plankton,
Israel
FW plankton,
Germany
FW, CC
CC
FW plankton,
USA, New
Zealand
FW plankton,
USA
FW plankton,
Slovenia
Origin
Cyanobacteria
Cyanobacteria
Cyanobacteria,
chlorophyte
Chrysophyte
Cyanobacteria,
chlorophyte
Cyanobacterium,
chlorophytes
Cyanobacteria,
diatoms, chlorophytes
Cyanobacteria
Cyanobacterium
Cyanobacteria,
chlorophytes
Dinoflagellate
Chlorophyte
Cyanobacteria,
cryptophyte,
chlorophytes
Chlorophyte
Cyanobacteria
Cyanobacteria,
cryptophytes,
chlorophytes
Chlorophyte
Target
Growth inhibition
Growth inhibition
Growth inhibition, morphological and ultrastructural alterations
Growth inhibition
Growth inhibition
Growth inhibition
Growth inhibition, cell lysis, loss of O2 evolution, reduction in
14
CO2 uptake, loss of nitrogenase activity
Growth and photosynthesis inhibition, depression of internal
carbonic anhydrase activity, activation of protein kinases,
accumulation of reactive oxygen species (ROS), oxidative stress,
cell death
Growth inhibition, chlorosis, chlorophyll (chl) a and
phycocyanin synthesis inhibition, PSII inhibition, changes in
protein and carbohydrate concentrations and nitrate reductase
activity, increases in ROS, malondialdehyde and detoxication
enzymes, oxidative stress
Growth stimulation, but oxidative stress
Increased cell aggegation, volume and pigment production
Elevation of detoxication enzyme activity, inhibition of
photosynthesis
Immobilization of flagella, settling
Growth inhibition or stimulation
Growth inhibition
Growth inhibition
Growth inhibition
Action
Volk 2005
Volk 2005
Valdor & Aboal 2007
Volk 2005
Keating 1978, 1987
Babica & al. 2007
Ou & al. 2005
Sedmak & Eleršek 2005
Hu & al. 2004, 2005
Sukenik & al. 2002, Vardi & al.
2002
Singh & al. 2001
Pietsch & al. 2001
Ishida & Murakami 2000
Sedmak & Kosi 1998
Ikawa & al. 1996
Volk 2005
Vance 1965, Lam & Silvester 1979
References
Table 1. Allelopathic effects of cyanobacteria on microalgae. Species names are from the cited literature (with new names, when available, in brackets, according to Hällfors (2004)). * denotes species
occurring in the Baltic Sea. CC = culture collection, BW = brackish water, FW = freshwater, M = marine. Names of isolated and characterized chemicals causing the effects are underlined.
Allelopathic effects of filamentous cyanobacteria on phytoplankton in the Baltic Sea
13
O. elegans
A. torulosa*
A. spiroides*
A. inaequalis*
A. cf. lemmermannii*
A. holsaticum
Nostocales
Anabaena cylindrica*
A. flos-aquae*
FW plankton,
USA
CC
BW plankton,
Sweden
FW plankton,
Thailand
FW plankton,
Austria
CC
CC
CC
Cyanobacteria,
chlorophytes
Extracellular C25 alkane with a
phenol group and an α, βunsaturated carbonyl residue
Cell-free filtrate
Living cells
Spiroidesin (linear lipopeptide)
Culture medium
Cell-free filtrate
Culture medium
Siderophores produced under Felimitation
Culture medium, microcystin-LR,
anatoxin-a (alkaloid)
Cell-free filtrate
Cyanobacteria,
diatom, chlorophytes
Cyanobacterium
Cyanobacteria,
diatoms
Cyanobacteria
Cryptophyte, diatom
Chlorophyte
Cyanobacteria
Chlorophytes
Cyanobacteria,
diatoms, chlorophytes
Growth inhibition
Growth inhibition
Growth inhibition
Growth inhibition
Growth inhibition
Growth inhibition, paralysis, increased settling rate
Growth inhibition
Growth inhibition, by Fe deprivation or direct toxicity
Growth inhibition
Growth inhibition, morphological and ultrastructural alterations
Cyanobacteria
Methanol extracts, microcystins
Cell-free filtrate
Growth inhibition
Cell lysis
Schagerl & al. 2002
Kaya & al. 2002
Volk 2005
I, III
Keating 1977, 1978
Volk 2005
Murphy & al. 1976, Matz & al.
2004
Kearns & Hunter 2000, 2001
Keating 1978, 1987
Volk 2005
Murakami & al. 1990, 1991,
Yamada & al. 1993
Valdor & Aboal 2007
Valdor & Aboal 2007
Growth inhibition, morphological and ultrastructural alterations
Cyanobacteria
Itself
Volk 2005
Keating 1977, 1987
Bagchi & al. 1990, 1993, Chauhan
& al. 1992, Bagchi 1995, Marwah
& al. 1995, Ray & Bagchi 2001
Keating 1977, 1978, 1987
Keating 1978
Infante & Abella 1985
Issa 1999
Keating 1978, 1987
Berry & al. 2004
References
Growth inhibition
Growth inhibition
Growth inhibition, cell lysis, inactivation of photosynthetic PSIImediated reactions and O2 evolution, damage of thylakoid
membranes, loss of chl, proteins and toxicity
Growth inhibition
Growth inhibition
Growth inhibition
Inhibition of growth and O2 evolution
Growth inhibition
Inhibition of growth and hormogonia development
Action
Culture medium
Polyunsaturated fatty acids
Methanol extracts, microcystins
Culture medium
Cell-free filtrate
Cyanobacteria,
diatoms, chlorophytes
Cyanobacteria
Cyanobacteria,
diatoms, chlorophytes
Cyanobacteria
Cryptophyte
Cyanobacteria,
chlorophytes
Diatoms
Living cells
Antibiotic, extracted with ethyl
acetate
Cell-free filtrate
Cell-free filtrate
Cyanobacterium,
chlorophytes
Diatoms
Target
Pahayokolide A (cyclic peptide)
Active component
Suikkanen
Pseudanabaena galeata
Phormidium foveolarum
P. tenue (Leptolyngbya
tenuis)*
Phormidium sp.*
O. sancta*
Oscillatoria sp.*
O. rubescens
FW plankton,
USA
CC
FW plankton,
USA
Riverine,
epilithic, Spain
CC
FW plankton,
Japan
Riverine,
epipelic, Spain
FW plankton,
USA
FW plankton,
USA
FW plankton,
India
O. angustissima
O. laetevirens
Edaphic, Egypt
Oscillatoria agardhii
(Planktothrix agardhii)*
Origin
FW periphyton,
USA
FW plankton,
USA
Lyngbya sp.*
Group/species
14
Finnish Institute of Marine Research – Contributions No. 15
Sessile, Australia
FW plankton,
Brazil
FW plankton,
Austria
Benthic, CC
Benthic, CC
Benthic, CC
Sessile,
Australia,
Indonesia, Nepal,
Vietnam
Riverine,
benthic, Brazil
Edaphic,
Marshall Islands
M plankton, Italy
Calothrix sp.
Cylindrospermopsis
raciborskii
Cylindrospermum sp.
F. muscicola
F. tisserantii
Fischerella sp.
Hapalosiphon fontinalis
Nodularia harveyana*
Fischerella ambigua
Edaphic, Egypt
FW plankton,
USA
CC
FW plankton,
USA
FW plankton,
Austria
FW plankton,
USA
FW plankton,
USA
BW plankton,
Finland
Benthic, CC
CC
Origin
C. parietina
Calothrix brevissima
A. flos-aquae*
Anabaenopsis siamensis
Aphanizomenon
elenkinii
A. flexuosum
Anabaena sp.*
Group/species
Fischerellin A,
12-epi-hapalindole F
Hapalindole A, smaller amounts
of several minor indoles
Lipophilic substances
Living cells,
12-epi-hapalindole E isonitrile
(alkaloid)
Fischerellin A
Fischerellin A
(aminoacylpolyketide)
Fischerellin A, fischerellin B
Living cells
Cell-free filtrate
Acetone or methanol / chloroform
extract
Antibiotic, extracted with ethyl
acetate
Living cells
Long-chain unsaturated fatty
acids
Cell-free filtrate
Cell-free filtrate
Living cells
Culture medium
Cell-free filtrate
Siderophores produced under Felimitation
Cell-free filtrate
Active component
Cyanobacteria,
chlorophyte
Cyanobacteria
Cyanobacteria
Cyanobacteria,
chlorophytes
Cyanobacteria,
chlorophytes
Cyanobacteria,
chlorophytes
Cyanobacteria,
chlorophytes
Cyanobacteria,
chlorophytes
Cyanobacteria,
chlorophytes
Cyanobacteria,
chlorophytes
Cyanobacteria,
chlorophytes
Flores & Wolk 1986, Gross & al.
1991, 1994, Hagmann & Jüttner
1996, Papke & al. 1997, Srivastava
& al. 1998
Gross & al. 1991
Schlegel & al. 1999,
Doan & al. 2000
Cell lysis, inhibition of photosynthetic electron transport at PSII
Cell lysis, inhibition of photosynthesis
Growth inhibition
Growth inhibition
Growth and photosynthesis inhibition
Pushparaj & al. 1999
Moore & al. 1984, 1987, 1989
Etchegaray & al. 2004
Gross & al. 1991
Inhibition of photosynthetic electron transport
Inhibition of photosynthetic electron transport,
Schagerl & al. 2002
Figueredo & al. 2007
Growth inhibition
Photosynthesis (PSII activity) inhibition
Schlegel & al. 1999
Issa 1999
Inhibition of growth and O2 evolution
Cell lysis
Abarzua & al. 1999
Growth inhibition
I, II
Growth inhibition, decrease of cellular chl a and CO2 uptake
Cryptophyte, diatom
Diatom
Ikawa & al. 1994
Keating 1978, 1987
Schagerl & al. 2002
Volk 2005
Keating 1977, 1978
Keating 1987
Bailey & Taub 1980
References
Growth inhibition
Growth inhibition
Growth inhibition
Growth inhibition
Growth inhibition
Growth inhibition
Fe deprivation
Action
Cyanobacteria,
diatoms
Chlorophyte
Cyanobacteria,
diatoms, chlorophytes
Cyanobacteria
Cyanobacteria,
diatoms
Chlorophyte
Chlorophyte
Target
Allelopathic effects of filamentous cyanobacteria on phytoplankton in the Baltic Sea
15
N. spongiaeforme
Trichormus doliolum
(syn. Anabaena
doliolum)
Tolypothrix distorta
S. myochrous
Scytonema hofmanni
Rivularia haematites
Living cells
Living cells, exudate
FW plankton, CC
Methanol extracts, microcystins
Methanol extracts, microcystins
Cyanobacterin
(chlorine-containing γ-lactone)
Culture medium
Methanol extracts, microcystins
Living cells
Riverine,
epilithic, Spain
Riverine,
epilithic, Spain
CC
Sessile,
Australia,
Indonesia
FW plankton,
Austria
CC
Riverine,
epilithic, Spain
FW, benthic, CC
Living cells
Nostocyclamide (cyclic
hexapeptide), nostocyclamide M
Living cells
Growth inhibition, morphological and ultrastructural alterations
Cyanobacteria,
chlorophyte
Cyanobacteria
Cyanobacteria,
chlorophytes
Growth inhibition, morphological and ultrastructural alterations
Cyanobacteria
Inhibition of growth, photosynthetic electron transport and O2
production, increased chl fluorescence
Cell lysis
Inhibition of photosynthetic electron transport in PSII,
deterioration of thylakoid membranes and cell walls, loss of chl
Cyanobacteria,
diatom, euglenophyte,
chlorophytes
Growth inhibition
Growth inhibition, morphological and ultrastructural alterations
Growth inhibition
Cell lysis
Inhibition of growth, chl, carotenoid and protein synthesis,
altered morphology
Cell lysis, inhibition of photoautotrophic growth
Growth inhibition, ROS generation
Growth inhibition
Growth and photosynthesis inhibition (O2 evolution, PSII
electron transport)
Growth inhibition
Growth inhibition
Growth inhibition
Growth inhibition
Growth inhibition, decrease of cellular chl a and CO2 uptake
Growth inhibition
Action
von Elert & Jüttner 1996, 1997
Flores & Wolk 1986
Valdor & Aboal 2007
Mason & al. 1982, Pignatello & al.
1983, Gleason & Paulson 1984,
Gleason & Baxa 1986, Gleason
1990, Lee & Gleason 1994,
Abarzua & al. 1999
Valdor & Aboal 2007
Volk 2005
Valdor & Aboal 2007
Schagerl & al. 2002
Flores & Wolk 1986
Todorova & al. 1995, Todorova &
Jüttner 1996, Jüttner & al. 2001
Schlegel & al. 1999
Hirata & al. 2003
Schagerl & al. 2002
Keating 1978, 1987
Volk 2005
Volk 2005
Volk 2005, 2006, Volk & Furkert
2006
Gromov & al. 1991
Volk 2005, 2006, Volk & Furkert
2006
I, II, III
References
Suikkanen
Cyanobacteria,
diatom, chlorophytes
Cyanobacteria
Cyanobacteria
FW plankton,
Austria
FW, Thailand
CC
FW, benthic, CC
Living cells
CC
N. muscorum
Nostoc sp.*
Cyanobacteria,
chlorophytes
Cyanobacteria,
diatoms, chlorophytes
Cyanobacteria,
chlorophytes
Cyanobacteria,
chlorophytes
Cyanobacteria
Cyanobacteria,
diatom, chlorophytes
Cyanobacteria,
chlorophytes
Cyanobacterin LU-1 (phenolic
compound)
Cell-free filtrate
Edaphic, Russia
Nostocine A (violet pigment)
Cyanobacteria
Cyanobacteria
Cyanobacteria
Cryptophyte, diatom
Cyanobacteria
Target
Culture medium
Culture medium
4,4′-dihydroxybiphenyl
N. linckia
Norharmane, norharmalane
(indole alkaloids)
Cell-free filtrate
CC
Nostoc carneum
N. commune
N. insulare
Active component
Origin
BW plankton,
Sweden
CC
CC
CC
N. spumigena*
Group/species
16
Finnish Institute of Marine Research – Contributions No. 15
Allelopathic effects of filamentous cyanobacteria on phytoplankton in the Baltic Sea
1.1.3 Cyanobacterial allelopathy
Most observations on phytoplankton allelopathy
originate from freshwater habitats and most of them
concern cyanobacteria (Gross 2003). In contrast,
allelopathy in marine ecosystems was described
mainly for bloom-forming dinoflagellates, haptophytes and raphidophytes (Smayda 1997, Cembella
2003). Little is known of the allelopathic interactions of marine or brackish water cyanobacteria,
which were the group of interest in the present
study, due to their annual mass occurrences in the
Baltic Sea (described below). An exception is the
Mediterranean Nodularia harveyana, which is allelopathic against other cyanobacteria and a chlorophyte (Pushparaj & al. 1999). Observations on the
allelopathic effects among cyanobacteria, including
their isolated allelochemicals and modes of action,
are listed in Table 1.
It has been argued that allelopathy is one of the
main factors contributing to the formation and/or
persistence of cyanobacterial blooms in eutrophic
lakes (Keating 1978, Bagchi & al. 1990). By combining laboratory experiments and field studies,
Keating (1977, 1978) showed that the phytoplankton
bloom sequence in a eutrophic lake correlated with
the effects of cell-free filtrates of dominant cyanobacteria on both their phytoplankton successors and
predecessors. The filtrates of each cyanobacterial
species generally inhibited its immediate predecessors in the natural phytoplankton bloom sequence,
whereas filtrates of the same species generally
stimulated their immediate successors. Filtrates of
cultured cyanobacteria, as well as lake waters collected during cyanobacterial blooms, also inhibited
the growth of diatoms isolated from the same lake,
and diatom bloom populations in situ varied inversely with the preceding cyanobacterial populations over several years (Keating 1978).
In Lake Kinneret, Israel, the reciprocal allelopathic interactions of the cyanobacterium Microcystis sp. and the dinoflagellate Peridinium gatunense
determine the species dominating the phytoplankton
assemblage (Sukenik & al. 2002, Vardi & al. 2002).
Cyanobacterial allelochemicals have also been suggested to contribute to a shift from macrophytedominated to more phytoplankton-dominated lakes
(van Vierssen & Prins 1985, Pflugmacher 2002),
although the principal cause of such a change in
eutrophic lakes is probably increased pelagic production, together with increased turbidity and reduced light availability for littoral and benthic production. Moreover, Figueredo & al. (2007) suggested that allelopathy contributed to the recent geographical expansion of the toxic, bloom-forming
cyanobacterium Cylindrospermopsis raciborskii
from tropical and subtropical regions to temperate
lakes and rivers.
Cyanobacteria produce a wide array of compounds (cyanotoxins) that are extremely toxic to
17
vertebrates. However, the ecological role of
cyanotoxin production is still largely unknown. One
hypothesis concerns allelopathy, suggesting that the
toxins are allelochemicals directed against competing photoautotrophic organisms (Sedmak & Kosi
1998, Pflugmacher 2002). Indeed, several cases
were reported in which cyanobacterial toxins exerted
inhibitory effects on photoautotrophs. These include
negative effects of microcystins on terrestrial (Abe
& al. 1996, Gehringer & al. 2003) and aquatic plants
(Pflugmacher 2002, 2004, Yin & al. 2005b), including phytoplankton (Kearns & Hunter 2000,
2001, Sedmak & Eleršek 2005, Table 1), anatoxin-a
on phytoplankton and aquatic plants (Kearns &
Hunter 2001, Mitrovic & al. 2004), cylindrospermopsin on a terrestrial plant (white mustard, Sinapis
alba; Vasas & al. 2002) and nodularin on a brown
macroalga (bladder wrack, Fucus vesiculosus;
Pflugmacher & al. 2007).
The observed harmful effects of cyanotoxins
may not occur as a consequence of the same mechanism as for mammals [e.g. protein phosphatase 1
(PP1) inhibition of microcystins and nodularin], but
to the enhanced production of reactive O2 species
and oxidative stress (Mitrovic & al. 2004, Pflugmacher 2004, Hu & al. 2005, Yin & al. 2005a,
Pflugmacher & al. 2007). However, the evidence
concerning the role of toxins as allelochemicals is
inconclusive, since the concentrations of toxins used
in the experiments have often been higher than those
occurring in natural waters (reviewed by Babica &
al. 2006).
1.2 Ecosystem changes in the Baltic Sea
The Baltic Sea is a brackish water sea (about
422 000 km2, mean depth 55 m), with a restricted
connection to the North Sea and the Atlantic Ocean.
The residence time of the water is long, more than
30 years (Dybern & Fonselius 1981). The Baltic Sea
area is characterized by strong seasonal temperature
variation and there is a steep north-south surface
water salinity gradient, from 1–2 psu in the northern
and eastern areas to ca. 20 psu in the Kattegat. The
northern and eastern parts (most of the Gulfs of
Bothnia and Finland, Fig. 1) are usually ice-covered
between January and March. The water is stratified,
with a deep, permanent halocline at a depth of ca. 60
m (except in the Gulf of Bothnia) and a thermocline
at ca. 20 m in summer. The halocline prevents mixing of the deep saline water with the less saline surface water layer. Consequently, O2 deficiency frequently occurs in the deep water. Only episodic intensive salt water inflows from the North Sea,
largely governed by meteorological variability, occasionally renew the deep water (Schinke &
Matthäus 1998). The flora and fauna of the Baltic
Sea are mixtures of freshwater, brackish water and
18
Suikkanen
marine species, although the species diversity is low
and food webs are simple compared with in the
oceans (e.g. Furman & al. 1998).
Approximately 85 million people in 14 industrialized countries inhabit the Baltic Sea catchment
area (1 720 000 km2), and thus the sea is heavily
influenced by anthropogenic pressures. In recent
decades, the ecosystem of the Baltic Sea has undergone considerable changes, which either directly or
indirectly are associated with increased human activities (HELCOM 2002). For example, increased
shipping has contributed to introductions of alien
species via ballast water and increased the risk of oil
spills and other accidents. Overfishing has not only
affected the target fish stocks (e.g. salmon, cod), but
probably also the remaining marine food web by
removing key species from the top of the food chain
(HELCOM 2002). Heavy metals and organic contaminants [e.g. dichloro-diphenyl-trichloroethanes
(DDTs), polychlorinated biphenyls (PCBs) and
hexachlorocyclohexanes (HCHs)], have accumu-
Finnish Institute of Marine Research – Contributions No. 15
lated in and affected especially long-lived organisms
such as the white-tailed sea eagle and grey seal. The
cold climate and slow water exchange of the Baltic
Sea further slow down the decay of these humaninduced contaminants.
Global climate change will most likely be one of
the most important factors shaping the future ecosystem of the Baltic Sea (HELCOM 2007a). There is
a close association between the functioning of the
pelagic ecosystem and hydrographic features (such
as ice, stratification and landbased runoff), as well as
large-scale weather patterns (Northern Atlantic Oscillation, NAO) over the runoff area of the Baltic
Sea (Alheit & al. 2005). The change in the NAO
index during the late 1980s from a negative to a
more positive phase was attributed to both increasing freshwater runoffs and a decreasing salinity of
the Baltic Sea (Hänninen & al. 2000), as well as a
regime shift involving all trophic levels in the pelagic areas of the central Baltic Sea and the North
Sea (Alheit & al. 2005).
Fig. 1. Map of the Baltic Sea and the study locations. The laboratory experiments were performed at Kalmar University (KU), Sweden
(I, III), and Tvärminne Zoological Station (TZS), Finland (II). Sampling sites for the natural community experiment (NC; III) and longterm data analysis (F1, F3, H1, H2 and H3; IV) are indicated.
Allelopathic effects of filamentous cyanobacteria on phytoplankton in the Baltic Sea
Eutrophication, caused by anthropogenic nutrient
inputs, is currently the most serious problem in the
Baltic Sea ecosystem. The Baltic Sea is especially
susceptible to eutrophication due to its shallowness,
stratification and slow water exchange, combined
with heavy external nutrient loading from the watershed (HELCOM 2004). Significant increases in the
surface water nitrogen and phosphorus concentrations have been recorded since the late 1960s
(Larsson & al. 1985). Despite recent successful reductions in point-source nutrient (especially P)
loading and a slight decrease in dissolved nutrient
concentrations in some areas (Fleming-Lehtinen &
al. in press), the eutrophication process continues,
due to external inputs of N and P and internal P
loading from anoxic sediments (Pitkänen & al. 2001,
Vahtera & al. 2007a, HELCOM 2007b).
The most common signs of eutrophication, i.e.
reduced water transparency, as well as increased
primary production, phytoplankton biomass (chlorophyll a concentrations), algal blooms, deposition of
organic matter and O2 deficiency of bottom waters,
and dead bottom fauna, are clearly detected in the
Baltic Sea (Bonsdorff & al. 2002). Perhaps the most
conspicuous sign of eutrophication is the increased
late-summer phytoplankton biomass (FlemingLehtinen & al. in press), expressed to a large degree
as annual mass occurrences of filamentous N-fixing
cyanobacteria.
1.3 Bloom-forming cyanobacteria
A late-summer phytoplankton biomass peak,
dominated by filamentous cyanobacteria, is a typical
feature of the Baltic Sea (Niemi 1973, Bianchi & al.
2000). However, the extent and frequency of cyanobacterial mass occurrences have increased during the
last half of the 20th century, which has been verified
by satellite observations (Kahru & al. 1994, 2007),
plankton monitoring (Finni & al. 2001) and sediment records (Poutanen & Nikkilä 2001). The increase in bloom intensity is most probably associated with anthropogenic nutrient loading, and in
some areas, such as the Gulf of Finland, especially
with the recently enhanced internal P loading originating from anoxic sediments (Pitkänen & al. 2003).
The bloom-forming cyanobacteria of the open
Baltic Sea fix atmospheric N and are therefore independent of dissolved N, which is generally the limiting nutrient in the open sea area (Granéli & al.
1990). However, external N inputs enhance the internal P loading by increasing the magnitude of the
spring bloom and thereby the amount of sedimenting
organic material. The decomposition of organic
matter depletes the oxygen in the bottom waters,
facilitating phosphate (PO4) release. The Baltic Sea
is considered to be in a state of a self-sustaining ‘vicious circle’ regarding eutrophication and cyano-
19
bacterial blooms, due to the feedback between the
cycles of O2, P and N (Tamminen & Andersen 2007,
Vahtera & al. 2007a).
Diazotrophic cyanobacterial blooms develop in
areas where the N:P ratio is below the Redfield ratio
of 16 (Niemi 1979, Stal & al. 2003), because in
these conditions, the N-fixing cyanobacteria are
better competitors than other species of phytoplankton whose growth depends on dissolved N. A
low N:P ratio may be a prerequisite for cyanobacterial blooms, while the temperature (>16 °C) was
claimed to be the main factor determining the onset
and intensity of toxic Nodularia spumigena blooms
(Wasmund 1997, Kanoshina & al. 2003). High temperatures stabilize the water column and decrease
the mixing depth, which increases the light irradiance available for the cyanobacterial community
(Stal & al. 2003).
In addition to N-fixation, the bloom-forming
cyanobacteria have several competitive advantages
compared with other phytoplankton species. They
are able to store significant quantities of P early in
the growing season to sustain later growth in a Pdepleted mixed layer (Larsson & al. 2001, Vahtera
& al. 2007b). The cyanobacteria have gas vacuoles
in their cells, which allow them to regulate their
buoyancy and vertical position in the water column
(Walsby & al. 1997). Furthermore, their large size
and excretion of bioactive substances such as toxins,
antibiotics and allelochemicals may deter grazers
and competing microorganisms (Sellner 1997).
In the Baltic Sea, the most conspicuous blooms
are formed by the large diazotrophic, heterocystous,
akinete-forming filamentous cyanobacteria of the
order Nostocales: Aphanizomenon flos-aquae and
Nodularia spumigena, and to a minor part, Anabaena spp. (contributing to ca. 10% of the total
Nostocalean late-summer biomass, based on the
HELCOM data presented in IV), although another
functional group, the small-sized (ca. 2 µm), nonheterocystous picocyanobacteria (e.g. Synechococcus
spp.), may be much more important in terms of biomass (Stal & Walsby 2000). The filamentous cyanobacteria in question possess gas vacuoles, which
make them buoyant. During calm conditions, cyanobacterial filaments and aggregates concentrate in the
uppermost (ca. 0–5 m) water layers, forming visible
surface scums that may also drift ashore. Other
cyanobacterial species, mostly of freshwater origin,
that may also form visible mass occurrences in the
coastal zone (salinity <3 psu) include Microcystis
aeruginosa (order Chroococcales) and Planktothrix
agardhii (order Oscillatoriales) (Niemi 1988,
Kauppila & al. 1995). However, most studies
concerning Baltic cyanobacteria have focused on the
filamentous species, and especially on the toxinproducing N. spumigena.
20
Suikkanen
1.3.1 Anabaena spp.
The genus Anabaena Bory ex Bornet & Flahault
is a cosmopolitan group of planktonic and benthic
species that occur in fresh and brackish water habitats (Komárek & Hauer 2004). The taxonomy of the
Baltic Anabaena spp. is still unclear, but the Anabaena populations appear to be genetically more
diverse than the Baltic Aphanizomenon or Nodularia
populations, and there are probably several species
present (Janson & Granéli 2002, Halinen & al.
2007). Based on recent phylogenetic analyses, the
Baltic Anabaena strains are closely related to strains
isolated from freshwater areas (Sivonen & al. 2007).
In lakes, Anabaena spp. often form dense monospecific blooms, but in the Baltic Sea they coexist,
mostly in small numbers, with A. flos-aquae and N.
spumigena. The reason for the low abundance of
Anabaena spp. in Baltic cyanobacterial blooms may
be that many of the species occur as single filaments, in contrast to N. spumigena and A. flosaquae, which form large colonies and aggregates.
The high floating velocities of colonies, as opposed
to filaments, allow them to spend more time in the
euphotic zone (Stal & al. 2003). Anabaena spp. only
occur in the Baltic plankton community during the
warmest summer period (July–August; Laamanen &
Kuosa 2005), and probably overwinter as akinetes
(Olli & al. 2005).
Freshwater blooms of Anabaena are often toxic
and the group belongs to the main genera responsible for cyanobacterial intoxications worldwide
(Carmichael 2001). Anabaena spp. produce both
neurotoxins, such as anatoxin-a, anatoxin-a(s) and
saxitoxins, and hepatotoxins, such as microcystins
and cylindrospermopsin (Sivonen & Jones 1999,
Schembri & al. 2001). The Baltic Anabaena species
have commonly been considered nontoxic; however,
microcystins have occasionally been recorded in
water samples from the coastal southern Baltic Sea
(Mazur & Pliński 2003, Luckas & al. 2005), as well
as at the entrance to the Gulf of Finland, with Anabaena sp. as the likely toxin producer (Karlsson &
al. 2005). Recently, microcystin-producing Anabaena strains were isolated from the Gulf of Finland
(Halinen & al. 2007).
In addition to toxins, freshwater Anabaena spp.
produce a number of bioactive compounds, mostly
lipopeptides, that have antibiotic, antialgal, anticancer, anti-inflammatory, cytotoxic and enzyme-inhibiting effects (Burja & al. 2001, Fujii & al. 2002, Table 1). Benthic Anabaena spp. from the Baltic Sea
are highly cytotoxic and induce programmed cell
death (Herfindal & al. 2005, Surakka & al. 2005).
1.3.2 Aphanizomenon flos-aquae
Aphanizomenon flos-aquae (L.) Ralfs ex Bornet
& Flahault is a euryhaline species, able to adapt to a
wide range of salinities (Pankow & al. 1990) and
Finnish Institute of Marine Research – Contributions No. 15
thus common in fresh and brackish water globally.
In the Baltic Sea, A. flos-aquae is most abundant
during July–September, although vegetative filaments occur in the water column throughout the year
(Niemi 1973, Laamanen & Kuosa 2005). Therefore,
akinetes probably do not play a role as a seed population for A. flos-aquae in this region, similar to the
situation in some temperate lakes (Jones 1979, Head
& al. 1999).
The growth of A. flos-aquae is promoted by
short-term nutrient pulses from below thermocline,
accompanied by upwelling (Kononen & al. 1996)
and mixing events, whereas N. spumigena is favoured by a stable water column (Stal & Walsby
2000). Aphanizomenon flos-aquae prefers lower
irradiances (25–45 µmol m-2 s-1), salinities (0–10
psu) and temperatures (16–22 °C) than N. spumigena (45–155 µmol m-2 s-1, 5–20 psu, 25–28 ºC,
respectively; Lehtimäki & al. 1997). Consequently,
A. flos-aquae often occurs in water layers below N.
spumigena and is more common than N. spumigena
in the northern parts of the Baltic Sea, such as the
Gulf of Finland and the northern Baltic proper
(Niemistö & al. 1989).
In lakes, A. flos-aquae produces neurotoxins,
such as saxitoxins and anatoxin-a (Carmichael 1986,
Sivonen & al. 1989a), and a hepatotoxin, cylidrospermopsin (Preuβel & al. 2006). The Baltic genotype probably originates from lakes (Laamanen & al.
2002), but apparently produces no known hepatotoxins (Lehtimäki & al. 1997). Furthermore, the
production of enzyme inhibitors (Cannell & al.
1988, Murakami & al. 2000), antibiotics (Falch & al.
1995, Østensvik & al. 1998), allelochemicals
(Keating 1978, 1987, Ikawa & al. 1994), and compounds that inhibit feeding of Daphnia (Haney & al.
1995) and development of fish larvae (Papendorf &
al. 1997) have also been documented in freshwater
strains of A. flos-aquae. It is not known how the
genotype affects allelopathy. Recently, Cox & al.
(2005) reported widespread production of a neurotoxic amino acid, β-N-methylamino-L-alanine
(BMAA) within cyanobacterial taxa, including the
Baltic A. flos-aquae and N. spumigena.
1.3.3 Nodularia spumigena
Nodularia spumigena Mertens ex Bornet &
Flahault occurs in temperate and subtropical marine
and brackish waters, shallow seas and bays, saline
coastal and inland lakes and swamps, and in reservoirs with high contents of mineral salts (Komárek
& al. 1993). In the Baltic Sea, the N. spumigena
biomass usually peaks during late summer (July–
August), when the water temperature reaches its
annual maximum. During the remaining year, N.
spumigena is virtually absent from the water column, although it can be encountered in the sea ice
(Laamanen 1996). The overwintering strategy of
Allelopathic effects of filamentous cyanobacteria on phytoplankton in the Baltic Sea
Baltic N. spumigena is currently unknown, since
akinetes are only rarely found in natural samples
(Kononen 2002).
Mass occurrences of N. spumigena have caused
intoxications of domestic animals in the coastal areas of the Baltic Sea (Persson & al. 1984, Edler &
al. 1985, Nehring 1993), due to the production of a
cyclic pentapeptide hepatotoxin, nodularin (Rinehart
& al. 1988, Sivonen & al. 1989b,c). Nodularin inhibits the eukaryotic serine/threonine-specific PPs (1
and 2A), in a manner similar to that of microcystin,
causing liver damage, and potentially promoting
tumours (Yoshizawa & al. 1990). As with most
cyanobacterial toxins, nodularin mainly remains
inside the cells and is only released when the cells
die (Lehtimäki & al. 1997). Concentrations as high
as 18 mg nodularin g-1 dry weight or 18 mg nodularin l-1 were measured in the Baltic Sea (Kononen
& al. 1993, Mazur & Pliński 2003).
Although the effects of nodularin on zooplankton
are variable (DeMott & al. 1991, Koski & al. 2002,
Reinikainen & al. 2002), the toxin may accumulate
at higher trophic levels via copepods (Engström-Öst
& al. 2002b). Nodularin can be transferred to zooplankton (Karjalainen & al. 2006), littoral gammarids (Korpinen & al. 2006), prawns (Van Buynder
& al. 2001), fish (Sipiä & al. 2001), clams and mussels (Falconer & al. 1992, Sipiä & al. 2002), sea
birds (Sipiä & al. 2006), as well as to sediments
(Kankaanpää & al. 2001, Mazur-Marzec & al.
2007). Nodularin may induce severe liver damage in
trout (Kankaanpää & al. 2002) and oxidative stress
in mussels (Kankaanpää & al. 2007) and macroalgae
(Pflugmacher & al. 2007). However, it has been
suggested that compounds other than nodularin, present in N. spumigena extract, are responsible for its
negative impact on fish larval growth (Karjalainen &
al. 2005).
In addition to nodularin and its variants (MazurMarzec & al. 2006), other types of peptides, such as
nodulapeptins A and B and spumigins A–C, have
been isolated from N. spumigena (Fujii & al. 1997),
but the potential bioactivity of these compounds is
unknown. Baltic N. spumigena is also weakly antiviral (Mundt & al. 2001). In contrast, the related
Mediterranean N. harveyana produces lipophilic
substances with antibacterial, antifungal, allelopathic
and toxic activities (Pushparaj & al. 1999). Cytotoxicity was also observed in benthic Nodularia
strains originating from the Baltic Sea (Surakka &
al. 2005).
2. OBJECTIVES OF THE STUDY
The aim of my thesis was to increase the level of
understanding of allelopathic interactions in phytoplankton and, especially, to conduct the first known
21
studies on the allelopathy of brackish water bloomforming cyanobacteria. This was done by studying
the effects of Baltic filamentous cyanobacteria experimentally in a natural phytoplankton community
and in monocultures of other phytoplankton species,
originating from the same habitat. Subsequently, the
results of the experimental studies were evaluated
against the long-term development of Baltic cyanobacterial biomass in relation to other phytoplankton
groups.
The more specific objectives of the individual
studies were:
1. To study the potential allelopathic effects of Baltic cyanobacteria on eukaryotic phytoplankton
species, their duration and association with the
growth phase and measured hepatotoxicity of
cyanobacteria (I).
2. To compare the allelopathic effects of cyanobacterial filtrates with those of purified nodularin, to
determine whether nodularin acts as an allelochemical, and to study the potential mechanism
of action of cyanobacterial allelochemicals (II).
3. To study the effects of cyanobacterial filtrates on
the abundance and species composition of
phytoplankton and other organisms in a natural
microplankton community (III).
4. To reveal the long-term trends in summer biomass of cyanobacteria in relation to other phytoplankton and environmental factors in the northern Baltic Sea and to determine whether evidence of allelopathic interactions can be detected
on a time scale of several years (IV).
3. METHODS
3.1 Laboratory studies (I–III)
I conducted three experimental studies (I–III) to
investigate the allelopathic effects of Baltic cyanobacteria (Table 2). Two of these (I, III) were undertaken at Kalmar University, Sweden, and one (II) at
Tvärminne Zoological Station, Finland (Fig. 1). In
these experiments, I used the cyanobacteria Anabaena sp. 1 (strain KAC 16, cited as A. lemmermannii in I), Aphanizomenon flos-aquae (Tr183) and
Nodularia spumigena (KAC 13 and AV1) as allelopathic donor species, and the cryptophyte Rhodomonas sp. (KAC 30), the haptophyte Prymnesium parvum (KAC 39) and the diatom Thalassiosira weissflogii (KAC 32) as target species, to have representatives of different systematic groups and due to
their availability in cultures. The strains KAC 13,
KAC 16, KAC 30, KAC 32 and KAC 39 were obtained from the Kalmar Algal Collection (KAC),
Kalmar University, and strains Tr183 and AV1 from
22
Suikkanen
Finnish Institute of Marine Research – Contributions No. 15
the Division of Microbiology, University of Helsinki. All species used in the experiments were
nonaxenic monocultures originating from the Baltic
Sea. The sample of a natural plankton community
was collected from site NC in the central Baltic Sea
(Fig. 1) and filtered through a 150-µm net to remove
mesozooplankton (III).
Allelopathic effects can only be separated from
those of exploitation competition in microcosm experiments, e.g. by cross-culturing. In this technique,
the target species is cultured in medium enriched
with cell-free filtrate from the donor species (Legrand & al. 2003). I used cell-free filtrates of the
donor species to study the allelopathic influence of
the selected cyanobacteria. The filtrates were prepared as gently as possible, i.e. by using as low pressure as possible and by keeping the filter wet. This
was done to avoid cell lysis and the release of intracellular toxins, because the effects caused by chemicals excreted by the donor cells only are considered
allelopathic (Rice 1984). Although cross-culturing,
i.e. the use of filtrates, does not allow for direct
identification of the allelochemicals, it is a starting
point that has been widely employed for studying
the allelopathic effects of a particular phytoplankton
species (Legrand & al. 2003).
Table 2. Summary of the laboratory experiments (I–III) presented in this thesis.
Article
I
Experimental
unit (volume)
Donor species
Extract
Target species
Scintillation
vial (20 ml)
1. Anabaena sp. 1
(cf. lemmermannii)
1. Filtrate, exponential phase
1. Rhodomonas
sp.
2. Aphanizomenon
flos-aquae
2. Filtrate, stationary phase (N.
spumigena)
2. Prymnesium
parvum
3. Nodularia
spumigena
II
Erlenmeyer
flask (400 ml)
3. Filtrate, coexisting bacteria
1. A. flos-aquae
1. Filtrate
2. N. spumigena
2. Purified
nodularin
Chl a ratio
Analyses
donor:target
1:1
Target cell counts
2:1
1. Chl a concentration
3. Thalassiosira
weissflogii
Rhodomonas
sp.
2. 14CO2 uptake
3. Target cell
counts
4. Transfer of
nodularin
5. pH
III
Erlenmeyer
flask (400 ml)
1. Anabaena sp. 1
Filtrate
Plankton community (<150
µm)
2. Aphanizomenon
sp.
75:1
3. N. spumigena
Article
1
2
Duration Sampling interval
(days)
(days)
Addition of
extract
Toxin
analyses
Statistical methods
1. Chl a concentration
2. Bacteria, phytoplankton and ciliate
cell counts
# replicates
I
3
1
In the beginning vs. daily
HPLC, PPI
Repeated measures ANOVA,
Tukey’s HSD, t-test
3
II
6
1 (cells), 2 (chl a,
14
CO2, pH), 6
(nodularin)
Every second
day
ELISA
Repeated measures ANOVA,
Tukey’s HSD
3
III
4
1 (chl a, bacteria,
ciliates), 4
(phytoplankton)
Daily
None
Repeated measures ANOVA,
one-way ANOVA, Tukey’s
HSD; hierarchical clustering,
ANOSIM1, SIMPER2
3
Analysis of similarity
Similarity percentages
Allelopathic effects of filamentous cyanobacteria on phytoplankton in the Baltic Sea
Identification of the exact allelochemicals would
require a thorough chemical analysis of the filtrate
and its active fraction(s), followed by isolation and
testing of the effects of the individual extracts and
compounds. One step in this direction was taken
when the hepatotoxin nodularin was purified from
Nodularia spumigena and its effect was tested on a
target species and compared with that of the filtrate
of the entire culture (II). Furthermore, I compared
the effects of a filtrate of an exponentially growing
N. spumigena culture with those of a filtrate of a
culture in the stationary phase to determine how the
growth phase affects the allelopathic potential of the
species (I).
A modified version of the growth medium F/2
(‘F/10’, i.e. 20% of the nutrient concentrations in the
original F/2 medium; Guillard 1975) was used as a
control for the filtrate additions. The same medium
was used for growing the cyanobacterial and target
species to be tested. However, to ensure that the
observed allelopathic effects were not due to nutrient
deficiency in the filtrate treatments, compared with
the nutrient-rich medium, I always measured the
main inorganic nutrient concentrations, nitrate-nitrogen (NO3-N) and phosphate-phosphorus (PO4-P), in
the culture filtrates and adjusted them to the same
level as in the control medium.
The experimental strains were nonaxenic. To ensure that the observed effects were caused specifically by the cyanobacteria, the potential effects of
associated bacteria isolated from the cyanobacterial
cultures were also tested on the target species (I).
This was done by filtering out the cyanobacteria
from the cultures with GF/C filters, incubating the
filtrates (which contained only the associated bacteria) for 7 days, counting the bacteria and testing the
effects of the incubated filtrates on the target algae,
in a manner similar to the tests for cyanobacterial
allelopathy.
I adjusted the biomass ratio of cyanobacteria:target species in the experiments using the chlorophyll a concentrations of the respective cultures.
In III, the chlorophyll a ratio of cyanobacteria:natural community was 75:1, resembling a
cyanobacterial bloom situation (Potter & al. 1983),
whereas in I and II, the ratio was adjusted to 1:1 and
2:1, respectively, to study a more balanced situation
between cyanobacteria and co-occurring species.
The duration of the experiments varied from 3 to
6 days. During a longer cross-culturing experiment,
the effects of the cyanobacterial extracts may gradually decrease due to degradation of the effective
compounds (without continuous excretion from
cells), e.g. by bacteria, if fresh filtrate is not added
(Gleason & Paulson 1984). In a comparison between
one or several additions of filtrate in an allelopathic
23
assay (I), stronger effects were detected when new
filtrate was added continuously. Therefore, in the
other experiments, I added fresh filtrate every second day, at least, when I took samples for the quantification of allelopathic effects.
The allelopathic effects were quantified by cell
counts of the target organisms in all three studies,
using a flow cytometer (I), electronic particle analyzer (II) and inverted microscope (III). In I and II,
the target cultures were also checked qualitatively
under a microscope, to see if the cyanobacterial extracts had induced any changes in target cell morphology. However, no such changes were detected.
In addition to cell numbers, I measured the chlorophyll a concentration (Jespersen & Christoffersen
1987, II, III), 14CO2 uptake (Niemi & al. 1983, II)
and pH (II). I hypothesized that the allelochemicals
of the Baltic cyanobacteria act by inhibiting the
photosynthesis of the target species (II). Thus I expected that the effects are first expressed at the level
of the photosynthetic pigments and primary production capacity, and finally, in cell numbers.
The toxin concentrations of the cyanobacterial
cultures and their extracts were studied with highperformance liquid chromatography (HPLC; Lawton
& al. 1994, Dahlmann & al. 2003, Fistarol & al.
2004b, I), PP1 inhibition assay (Fontal & al. 1999,
I), and enzyme-linked immunosorbent assay
(ELISA; Chu & al. 1990, II). Nodularin uptake of
Rhodomonas cells or its adherence to their surface
was monitored by ELISA (II).
I analysed the results of the laboratory studies (I–
III) with repeated measures analysis of variance
(ANOVA), followed by Tukey’s honestly significant
difference (HSD) post hoc test. In III, species-dependent multivariate techniques of the PRIMER (v5)
package were also applied (Clarke & Warwick
2001).
3.2 Long-term data analysis (IV)
I evaluated a 25-year (1979–2003) Helsinki
Commission (HELCOM) monitoring dataset from
five sampling sites in the northern Baltic Sea (Fig.
1), consisting of quantitative phytoplankton observations, chlorophyll a, and environmental variables
(temperature, salinity, inorganic P, N and Si), for the
late-summer period (end of July – beginning of
September). All data were analysed for the presence
of monotonic increasing or decreasing trends by the
nonparametric Mann-Kendall test (Gilbert 1987). In
addition, I assessed the relationships between the
phytoplankton composition and environmental factors, using redundancy analysis (RDA), which is a
linear method of direct ordination (ter Braak 1994).
24
Suikkanen
Finnish Institute of Marine Research – Contributions No. 15
Allelopathic effects were previously described
for certain Baltic phytoplankton species, such as the
haptophytes Chrysochromulina polylepis (Myklestad
& al. 1995, Schmidt & Hansen 2001) and Prymnesium parvum (Granéli & Johansson 2003, Fistarol &
al. 2003), and the dinoflagellate Alexandrium tamarense (Fistarol & al. 2004b). New research indicates
that the Baltic spring-bloom diatoms Chaetoceros
wighamii, Melosira arctica, Skeletonema costatum,
Thalassiosira baltica and Diatoma tenuis may also
be allelopathic towards co-occurring dinoflagellates
(Spilling, in press). Although it had been suggested a
few times that Baltic cyanobacteria have allelopathic
properties (Sellner 1997, Balode & al. 1998,
Engström-Öst & al. 2002a), it had not been addressed in laboratory experiments prior to the studies
presented in my thesis. Therefore, I is the first report
on cyanobacterial allelopathy in the Baltic Sea and
in brackish waters.
in the observed allelopathic effects, because the incubated filtrate with exudates of the heterotrophic
bacteria did not inhibit Rhodomonas sp.
I speculated that specific group characteristics,
such as membrane permeability, contributes to the
sensitivity of Rhodomonas sp. to cyanobacterial allelochemicals, compared with the other species
studied (I). Thalassiosira spp. are vernal species
(Edler 1979) that probably are not adapted to latesummer cyanobacterial metabolites, whereas
Prymnesium parvum co-occurs with cyanobacteria
(Lindholm & Virtanen 1992) and may therefore be
resistant. Prymnesium parvum itself has deleterious
effects on the natural phytoplankton community, but
cyanobacteria are the least affected group (Fistarol
& al. 2003). This further suggests that the two
groups are reciprocally tolerant. Resistant species
that co-occur with the allelopathic species may benefit from the production of allelochemicals via reduced competition (Legrand & al. 2003). Prymnesium parvum, being mixotrophic (Nygaard &
Tobiesen 1993), may also escape the possible allelopathic effects on photosynthesis by switching to
heterotrophic nutrition.
4.1.1 Effects of cyanobacteria on monocultures
4.1.2 Role of nodularin in allelopathy
Cross-culturing is commonly used to demonstrate the existence of allelopathic interactions between two phytoplankton species. Although the conditions are far from natural, the advantage of the
method is that detailed studies concerning the modes
of action of allelochemicals can be conducted. In my
thesis, I used the cross-culturing technique in two
studies (I, II) to examine the inhibitory effects,
caused by the cyanobacterial filtrates, on different
phytoplankton species. The results showed that all
studied cyanobacteria (Anabaena sp. 1, Aphanizomenon flos-aquae and Nodularia spumigena)
decreased the cell numbers of Rhodomonas sp., but
none of them affected the cell numbers of Prymnesium parvum. Thalassiosira weissflogii was also
inhibited by all cyanobacteria, but only after repeated filtrate additions (I, Table 3). With one filtrate addition at the beginning of the experiment, T.
weissflogii was only inhibited by N. spumigena in
the end. Thus, the allelopathic effect of the other
species only lasted for a couple of days, after which
the chemicals were degraded, or the target species
recovered.
Heterotrophic bacteria associated with the
nonaxenic cyanobacteria were probably not involved
Nodularia spumigena was allelopathic only in
the exponential growth phase, whereas the culture
filtrate was more hepatotoxic in the stationary phase
(135.2 compared with 28.7 ng nodularin (µg chl a)-1
in stationary and exponential phase culture filtrates,
respectively; I). Nodularin mostly remains inside the
intact cells during the exponential growth phase and
is released from the decaying cells to the growth
medium during the stationary phase (Sivonen &
Jones 1999). In contrast, allelochemicals are excreted during active growth, thereby affecting the
competitors of the producer (Vance 1965, von Elert
& Jüttner 1996).
When tested with purified nodularin (10 µg l-1),
no significant effect on Rhodomonas sp. could be
observed, in contrast to the negative effects of the
filtrate of N. spumigena (7 µg l-1 nodularin) (II). It
has been observed that crude cyanobacterial extracts
containing toxins cause stronger effects than purified
toxins, suggesting that extracts contain a mix of
compounds that act synergistically (Pietsch & al.
2001, Wiegand & al. 2002, Leflaive & Ten-Hage
2007). However, my results strongly suggest that
nodularin is not the primary compound causing the
allelopathic effects of N. spumigena.
4. RESULTS AND DISCUSSION
4.1 Allelopathy of Baltic cyanobacteria
Allelopathic effects of filamentous cyanobacteria on phytoplankton in the Baltic Sea
25
Table 3. Allelopathic effects of cyanobacterial extracts, according to the studies included in this thesis. Statistically significant effects
on the last experimental day [after 3 (I), 4 (III) or 6 (II) days] on cell numbers of different phytoplankton species (and cellular
chlorophyll a concentration and 14CO2 uptake of Rhodomonas sp., II) are indicated as percentage decrease or increase of cells (or
other parameters) in the filtrate treatment relative to the control (n = 3, mean ± SD). 0 = nonsignificant effect, n.a. = not analysed.
Cyanobacteria
Snowella spp.
Anabaena
sp. 1
Aphanizomenon
sp.
Nodularia
spumigena
+611 ± 68%
+544 ± 37%
+520 ± 112%
0
+166 ± 21%
0
0
0
0
+106 ± 28%
0
+5070 ± 458%
0
-51 ± 5%
Extract
# extract
additions
Article
4
III
0
+109 ± 35%
+479 ± 129%
0
+415 ± 209%
Exponential
phase (exp.)
filtrate
Exp. Filtrate
Exp. Filtrate
Exp. Filtrate
Exp. Filtrate
Exp. Filtrate
4
4
4
4
4
III
III
III
III
III
-55 ± 2%
-46 ± 15%
Exp. Filtrate
1
I
-67 ± 5%
n.a.
-57 ± 6%
n.a.
-64 ± 5%
0
3
1
I
I
n.a.
-29 ± 5%
-chl a cell-1
n.a.
-34 ± 3%
-14CO2 uptake cell-1
n.a.
-45 ± 5%
-79 ± 9%
0
-14 ± 4%
0
-12 ± 7%
0
-43 ± 11%
0
-72 ± 24%
Exp. Filtrate
Stationary phase
(stat.) filtrate
Exp. Filtrate
Nodularin
Exp. Filtrate
Nodularin
Exp. Filtrate
Nodularin
Exp. Filtrate
3
3
3
3
3
3
4
II
II
II
II
II
II
III
0
+65 ± 17%
0
0
0
0
+59 ± 19%
0
0
0
0
0
0
0
0
Exp. Filtrate
Exp. Filtrate
Exp. Filtrate
Exp. Filtrate
Exp. Filtrate
4
4
4
4
4
III
III
III
III
III
0
0
0
Exp. Filtrate
1
I
0
0
0
Exp. Filtrate
3
I
0
+48 ± 8%
0
0
0
-41 ± 5%
Exp. Filtrate
Exp. Filtrate
4
1
III
I
-69 ± 10%
n.a.
0
-32 ± 7%
n.a.
0
-27 ± 3%
0
0
Exp. Filtrate
Stat. filtrate
Exp. Filtrate
3
1
4
I
I
III
0
0
+110 ± 7%
0
0
0
+47 ± 21%
0
0
Exp. Filtrate
Exp. Filtrate
Exp. Filtrate
4
4
4
III
III
III
Other picocyanobacteria
Pseudanabaena spp.
Anabaena spp.
Aphanizomenon sp.
Nodularia spumigena
Cryptophytes
Rhodomonas sp. strain
KAC 30
All cryptophytes
Dinoflagellates
Dinophysis norvegica
Amphidinium sp.
Paulsenella sp.
Other dinoflagellates
Dinoflagellate cysts
Haptophytes
Prymnesium parvum strain
KAC 39
Diatoms
Chaetoceros spp.
Thalassiosira weissflogii
strain KAC 32
Other diatoms
Chlorophytes
Oocystis sp.
Planktonema lauterbornii
Nanoflagellates
26
Suikkanen
Finnish Institute of Marine Research – Contributions No. 15
This conclusion agrees with the review by
Babica & al. (2006), who found no support for the
hypothesis concerning an allelopathic function of
microcystins at environmentally relevant toxin concentrations (1–10 µg l-1). Since the biosynthesis of
microcystins and nodularins developed way before
the evolution of eukaryotic photoautotrophs (Rantala
& al. 2004), it is unlikely that the primary ecological
role of cyanobacterial hepatotoxins is to act as allelochemicals against these organisms (Welker &
von Döhren 2006). Other suggestions for the natural
role of cyanotoxins range from by-products of metabolism to cell-cell signalling, iron-scavenging,
storage substrates, growth regulators and grazer deterrence (Kaebernick & Neilan 2001, Babica & al.
2006 and references therein). Recently, Schatz & al.
(2007) suggested that microcystins may act as infochemicals that are released following lysis of a
fraction of the cyanobacterial population and sensed
by the remaining cells, which increase their ability to
produce microcystins. This would enhance their
fitness due to the toxic effects on grazers and competitors. The specific ecological role of nodularin
remains to be elucidated.
action of phytoplankton allelochemicals (Legrand &
al. 2003). Based on the present data, however, the
target function or site of the cyanobacterial allelochemicals cannot be definitely concluded.
The pH of the environment can affect the growth
of phytoplankton species, depending on their pH
tolerance (Hansen 2002). In some cases, the ‘allelopathic’ effects detected have actually been due to the
elevation of pH by the donor species to a level that is
intolerable to the target species (Kroes 1971, Goldman & al. 1981, Schmidt & Hansen 2001). High pH
tolerance (up to 10.6), instead of allelopathy, has
also been argued as the explanation for the dominance of Nodularia spumigena over other phytoplankton in mixed culture experiments (Møgelhøj &
al. 2006). While it may be the case for some target
species, there was no difference in pH of the
Rhodomonas cultures treated with either N. spumigena or A. flos-aquae filtrates or the control cultures:
the average pH was 8.3 ± 0.2 both in the control and
the N. spumigena treatment and 8.1 ± 0.2 in the A.
flos-aquae treatment (II). Therefore, the inhibitory
effects were not caused by pH changes, but rather by
allelopathy of the cyanobacteria.
4.1.3 Mode of allelopathic action
4.1.4 Effects of cyanobacteria on a natural plankton
community
The effects of cyanobacterial allelochemicals on
the target cells may be manifold (Table 1), although
they often lead to decreasing cell numbers of the
target as an outcome. To more closely examine the
mechanisms of allelopathic actions of Baltic cyanobacteria, underlying the decrease in cell numbers, I
monitored the cellular chlorophyll a concentration
and 14CO2 uptake, pH, and nodularin incorporation
of Rhodomonas sp. exposed to filtrates of Aphanizomenon flos-aquae and Nodularia spumigena and
to purified nodularin (II). As discussed above,
nodularin showed no allelopathic effects, although it
was incorporated into the Rhodomonas cells to some
extent (73.5 x 10-6 pg nodularin equivalents cell-1
after the first nodularin addition at the beginning of
the experiment). In contrast, filtrates of both A. flosaquae and N. spumigena significantly decreased the
cell numbers, cellular chlorophyll a content as well
as 14CO2 uptake of the cryptophyte (Table 3).
Most of the cyanobacterial allelochemicals
whose mode of action and target site have been
clarified to date are directed against oxygenic photosynthetic processes in other phytoplankton (Smith &
Doan 1999). In II, the inhibition of cellular chlorophyll a concentration and 14CO2 uptake, which may
indicate inhibition of photosynthesis, only occurred
some days after a decrease in cell numbers. Therefore, I concluded that the allelopathic effect of the
cyanobacteria was not directly due to an inhibition
of photosynthesis. Instead, the decrease in cell numbers may have been caused e.g. by breakage of the
cell membranes, which is also a common mode of
Combining laboratory and field studies by employing micro- or mesocosm experiments with natural phytoplankton communities may provide more
ecologically reliable data on allelopathy than if using
isolated species combinations. On the other hand,
the results of whole-community experiments may
greatly differ from those of simple cross-culturing
with a few species, due to the multitude of interactions between trophic levels and the various species
in the community. Thus, unless the allelopathic effects are very prominent, it may be difficult to detect
them and confirm the causative organism.
To determine whether Anabaena sp. 1, Aphanizomenon sp. and Nodularia spumigena are able to
produce allelochemicals that affect natural plankton
assemblages, I employed a microplankton community from the central Baltic Sea to study the effects
of cyanobacterial filtrate additions on the phytoplankton biomass (measured as chlorophyll a concentration) of the entire community, and on the
abundances of phytoplankton, bacteria and ciliates
(III). The filtrates increased the cell numbers of
other cyanobacteria (Snowella spp., Pseudanabaena
spp., Anabaena spp., Aphanizomenon sp., N. spumigena), a chlorophyte (Oocystis sp.), a dinoflagellate
(Amphidinium sp.) and nanoflagellates, but decreased the cell numbers of cryptophytes (Fig. 2,
Table 3). The numbers of bacteria were also increased at the beginning of the experiment, following the filtrate addition, whereas it had no effect on
the chlorophyll a concentrations or ciliate abun-
Allelopathic effects of filamentous cyanobacteria on phytoplankton in the Baltic Sea
dances. According to the cluster analysis (III), the
various cyanobacterial filtrate treatments generated
plankton communities that differed both from the
original community and from each other.
In III, I used a high ratio of cyanobacteria:target
chlorophyll a concentration to simulate a cyanobacterial bloom event (Table 2). The high amount of
added organic matter, originating from the filtrates,
probably explains the observed high stimulation of
bacteria and several phytoplankton species that either benefited from nutrients remineralized by the
increased bacteria or directly from the dissolved
organic matter. Alternatively, organically bound
nutrients released from the degrading cryptophyte
cells may have led to stimulation of the remaining
phytoplankton species. The stimulation may also be
considered as a case of ‘positive allelopathy’, because allelopathy in a broad sense includes all effects, both harmful and beneficial, caused by compounds that are released into the environment (Rice
1984). In the natural community, many coexisting
species may have developed resistance to the inhibitory metabolites of cyanobacteria and may even
benefit from these or other compounds. The fact that
reports on positive allelopathy are restricted to a few
(Keating 1977, 1987, Rice 1986, Mohamed 2002),
may simply reflect the shortage of allelopathic experiments done with natural communities.
I suggest that the negative effects of the cyanobacterial filtrates on the cryptophytes were due to
allelochemicals excreted by the cyanobacteria (III).
This agrees with the consistent inhibition of Rhodomonas sp. by the cyanobacterial filtrates, observed in
27
the laboratory studies (I, II). Otherwise it is unclear
why the cryptophytes were negatively affected in the
filtrate treatments, if there was something (e.g. nutrients) in the filtrates that all the other phytoplankton were able to utilize. The cryptophytes may be
less adapted to cyanobacterial exudates than other
phytoplankton groups, because they were the least
abundant group in the community used in the experiment. Nevertheless, cryptophytes are known to
be sensitive to allelochemicals excreted by other
phytoplankton, e.g. cyanobacteria (Vance 1965, Infante & Abella 1985, Sedmak & Kosi 1998, I, II),
dinoflagellates (Rengefors & Legrand 2001, Fistarol
& al. 2004b, Tillmann & al. 2007), and haptophytes
(Schmidt & Hansen 2001, Granéli & Johansson
2003, Skovgaard & al. 2003, Barreiro & al. 2005,
Uronen & al. 2005, 2007), and because they are
ubiquitous and easy to cultivate, they have recently
become model organisms that are often used as targets in allelopathy experiments.
In nature, ciliates may vigorously graze on picoand nanoplankton (Setälä & Kivi 2003), e.g. cryptophytes. As ciliates were present in the experimental
community (III), it is possible that grazing contributed to the loss of cryptophytes to some extent.
However, the initial numbers of ciliates and their
development were similar in all treatments and the
control, although the amounts of cryptophytes decreased only in the filtrate treatments. This strongly
suggests that the filtrates, and not grazing, were
mainly responsible for the decrease in the cryptophytes.
Fig. 2. Effects of cyanobacterial (Anabaena sp.1, Aphanizomenon sp., Nodularia spumigena) filtrates on a natural Baltic phytoplankton community after a 4-day exposure, compared with those of the control medium (n = 3, mean + SD) (III, redrawn from
Karjalainen & al. 2007).
28
Suikkanen
In general, the cyanobacterial filtrates greatly increased the numbers of heterotrophic and smallcelled species (bacteria, cyanobacteria, chlorophytes,
dinoflagellates and nanoflagellates) in the plankton
community, without affecting its total biomass (expressed as chlorophyll a concentration). This is consistent with observations that cyanobacterial blooms
support active microbial food webs due to the leakage of dissolved organic compounds from decaying
cells (Hoppe 1981, Engström-Öst & al. 2002a). Allelopathy is most probably the cause of inhibitory
effects by the cyanobacteria on cryptophytes.
4.2 Long-term trends of phytoplankton
and environmental factors
Both environmental conditions and the phytoplankton community structure have changed considerably in the northern Baltic Sea during recent decades. A transition has occurred from more saline
summer conditions, with higher silicate concentrations in winter in the late 1970s and in the 1980s,
towards higher summer temperatures and higher
absolute and relative winter dissolved inorganic nitrogen (DIN) concentrations in the 1990s and early
2000s (IV). Simultaneously, the summertime chlorophyll a concentration of the surface water has significantly increased, indicating that the eutrophication process continues in the open sea. The decrease
in salinity and silicate concentrations, as well as the
Finnish Institute of Marine Research – Contributions No. 15
increase in temperature, DIN and summer chlorophyll a in the northern Baltic Sea have also been
reported by several other authors (Flinkman & al.
1998, HELCOM 2002, Rönkkönen & al. 2004,
Raateoja & al. 2005, Fleming-Lehtinen & al. in
press.).
In contrast to hydrography, nutrients and chlorophyll a, changes in phytoplankton species composition in the northern Baltic Sea have not been analysed in detail since the late 1980s (Kononen 1988).
The biomass of cyanobacteria in the surface water
layer of the Gulf of Finland increased significantly
between 1979 and 2003 (IV). At the same time, the
biomasses of chrysophytes and chlorophytes have
increased, whereas that of the cryptophytes has decreased. In 1979–1981, cyanobacteria comprised on
average 42% of the total late-summer phytoplankton
biomass, whereas their proportion was 69% in
2001–2003 (Fig. 3). Meanwhile, the relative biomass
of cryptophytes decreased from 26% to 2%.
These results agree with reports that late-summer
blooms of cyanobacteria have increased both in frequency and intensity (Kahru & al. 1994, 2007, Finni
& al. 2001), and with the occurrence of several extensive cyanobacterial blooms in the late 1990s and
early 2000s (Rantajärvi 2003). Other studies also
report increases in flagellate and chlorophyte biomasses in the Baltic Sea (Kononen 1988, Wrzołek
1996). However, the considerable decrease in cryptophyte biomass has not been described before.
Fig. 3. Late-summer phytoplankton community structure (% of total biomass) in the Gulf of Finland in 1979–1981 and 2001–2003
(IV). Cyano = Cyanobacteria, Crypto = Cryptophyceae, Dino = Dinophyceae, Chryso = Chrysophyceae, Diatom = Diatomophyceae,
Eugleno = Euglenophyceae, Chloro = Chlorophyceae, Ebri = Ebriidae.
Allelopathic effects of filamentous cyanobacteria on phytoplankton in the Baltic Sea
Temperature, salinity and nutrient concentrations
are considered the most important environmental
factors affecting the phytoplankton community
structure throughout the Baltic Sea (Kononen 1988,
Alheit & al. 2005, Gasiūnaitė & al. 2005). Multivariate analysis (IV) showed that the elevated summer temperature and winter DIN concentration were
the most significant factors explaining the variance
in phytoplankton data, and the biomass development
of many phytoplankton groups, such as the increase
in chrysophytes, could be attributed to changes in
either of the two factors. In addition, the decreased
salinity probably contributed to the increase in
chlorophytes, many of which are of lacustrine origin
(Niemi 1973). Therefore, I concluded that the
changes in the phytoplankton community in the
northern Baltic Sea reflect both changes in hydrography and the ongoing eutrophication process.
Biological interactions, such as interspecific
competition, may also play a role in the variability
of phytoplankton community composition. For example, in a multivariate analysis of phytoplankton
dynamics in a lake in Portugal, the variance explained for the phytoplankton assemblage was increased when cyanobacterial blooms were also considered as an explanatory variable, in addition to
environmental parameters (de Figueiredo & al.
2006). The authors suggested that this correlation
was due to the competitive advantage and/or allelopathy of the bloom-forming cyanobacteria towards
microalgae.
In the present study (IV), the decrease in cryptophytes, coinciding with the increase in cyanobacteria, suggests that allelopathic interactions are involved, because the sensitivity of the cryptophytes to
cyanobacterial extracts was proven in laboratory
experiments (I, II). The cryptophytes also constituted the only taxon that was significantly inhibited
by cyanobacterial cell-free filtrates added to a natural phytoplankton community, whereas most of the
other phytoplankton taxa were stimulated (III, Fig.
2). In a recent modelling study, it was concluded that
allelopathy, together with mixotrophy, is crucial to
the coexistence and seasonal dynamics of cyanobacteria and cryptophytes in the southern Baltic Sea
(Hammer & Pitchford 2006).
The decrease in cryptophytes may also have affected the dinoflagellates, which showed a trend
toward decrease (IV, Fig. 3). Some dinoflagellate
species, such as Dinophysis spp., need temporary
kleptoplastids from cryptophytes (Hackett & al.
2003, Minnhagen & Janson 2006), and therefore, the
abundance of Dinophysis may be dependent on the
abundance of cryptophytes (Nishitani & al. 2005). It
is even possible that Baltic cyanobacteria compete
with late-summer dinoflagellates by inhibiting
cryptophytes, their essential endosymbionts.
Furthermore, top-down effects, such as grazing
by microzooplankton, probably affect the late-sum-
29
mer phytoplankton community structure. For example, certain species of ciliates (e.g. Euplotes sp.),
potentially important as grazers of cryptophyte-sized
phytoplankton, thrive in the cyanobacterial aggregates (Engström-Öst & al. 2002a). An increase in
cyanobacteria may have favoured these organisms,
which have in turn contributed to the decline in
cryptophytes. Unfortunately, long-term data concerning the microzooplankton abundances are
scarce, and no definite conclusions on their role in
the phytoplankton community changes can be
drawn.
Several authors have described cases in which
field observations of proliferation or decline in certain phytoplankton groups or species have been supported by laboratory experiments revealing allelopathic interactions between the species or groups in
question (Keating 1977, 1978, Sukenik & al. 2002,
Vardi & al. 2002). Most of these field observations
have concerned seasonal phytoplankton succession,
and it is probable that the outcome of allelopathy is
more easily detected on a seasonal than on a longterm scale. Nevertheless, in Lake Neusiedlersee
(Austria), for example, allelopathy was suggested to
contribute to the massive development of cyanobacteria during the late 1980s, coinciding with a
strong decline in chlorophytes (Schagerl & al. 2002).
The field observations agreed with laboratory experiments, where the dominant cyanobacteria inhibited the growth of chlorophytes isolated from the
same lake.
5. CONCLUSIONS
This study shows, on one hand, that the latesummer phytoplankton community in the northern
Baltic Sea has changed towards domination by
cyanobacteria during recent decades and, on the
other hand, that the most common filamentous
cyanobacteria have species- or group-specific effects
on co-occurring phytoplankton, probably mediated
via extracellular metabolites. The most important
new finding is the evidence for Baltic cyanobacterial
allelopathy towards cryptophytes, obtained from
both laboratory experiments and field studies.
The negative allelopathic effects of the cyanobacteria studied are rather transitory, exerted during
active growth, and not caused by the hepatotoxin,
nodularin, in Nodularia spumigena. The specific
allelochemicals, as well as their mode of action remain uncertain, but they apparently act by reducing
cell numbers, cellular chlorophyll a content and carbon uptake of the target species. Exudates of cyanobacteria may also stimulate bacteria, other cyanobacteria, chlorophytes and flagellates, which is due
to the ability of these taxa to utilize organic matter
or bacteria, or nutrients remineralized by the bacte-
30
Suikkanen
ria, their adaptation to cyanobacterial metabolites,
organically bound nutrients released from damaged
cryptophyte cells, unknown stimulatory chemicals or
a combination of several factors.
It is unlikely that allelopathy is the key factor in
the initial phases of phytoplankton bloom formation,
due to the low density of the producer cells (Solé &
al. 2005). However, cyanobacteria may use allelopathy in the maintenance of the bloom to suppress
competing phytoplankton, after the development and
concentration of an adequate amount of cells in the
surface layer during favourable hydrographic conditions. In the nutrient-depleted late-summer environment, allelopathy may be an additional stressor for
many phytoplankton species, leading to long-lasting
blooms of cyanobacteria.
Cyanobacterial allelopathy may not only be a
means to reduce nutrient competition by preventing
other species from attaining high biomasses, but also
to gain more nutrients through stimulation of bacteria or by breaking cryptophyte cells, as suggested for
the dinoflagellate Peridinium aciculiferum (Rengefors & Legrand 2001). Furthermore, the inhibitory
effects of cyanobacteria on cryptophytes may be
associated with the interactions between cyanobacteria and dinoflagellates, which need cryptophytes for
their plastids, or indirectly with grazing of cryptophytes by microzooplankton, which benefit from the
presence of cyanobacteria.
The long-term development of phytoplankton
communities reflects a combination of ongoing eutrophication, expressed as increasing dissolved inorganic nutrient concentrations of the surface water,
climate-driven changes in hydrography, i.e. decreasing salinity and increasing temperature, and
possibly, biological interactions among species of
phytoplankton and between phyto- and zooplankton.
The resulting significant increase in phytoplankton
biomass is due to a considerable increase in cyanobacteria, various flagellates and chlorophytes. Nevertheless, the biomass of some phytoplankton
groups, e.g. cryptophytes, has declined.
The allelopathic effects detected in the laboratory
studies of this thesis are generally in line with the
observed long-term increase in cyanobacteria,
chlorophytes and chrysophytes, and the decrease in
cryptophytes. Thus, while the proliferation of
cyanobacteria in the northern Baltic Sea is known to
be enhanced by internal P loading and favourable
hydrographic factors, my results show that chemically mediated biological interactions should also be
considered as factors affecting the structure of Baltic
phytoplankton communities.
Acknowledgements
This work was funded by the Maj and Tor
Nessling Foundation, the Walter and Andrée de
Finnish Institute of Marine Research – Contributions No. 15
Nottbeck Foundation, University of Helsinki, Societas Pro Fauna and Flora Fennica, the Nordic
Academy for Advanced Study and the Finnish Institute of Marine Research (FIMR).
I am grateful to my both supervisors, Jonna Engström-Öst and Markku Viitasalo for their neverending optimism, confidence and guidance through
all the years, despite my own, somewhat unrealistic,
picture of the amount of side-projects one is able to
handle while concentrating on a PhD thesis. Special
thanks to Make for initially accepting me as a PhD
student in his experimental zooplankton ecology
(EZECO) group, although I had no intentions whatsoever to study experimental zooplankton ecology,
and, consequently, for all the scientific freedom.
Jonna with all her deadlines was crucial in finally
putting an end to this work.
I thank the pre-examiners of this thesis, Pirjo
Kuuppo and Norbert Wasmund, for an efficient review considering my tight schedule and especially
Purjo for all the constructive criticism. Harri Kuosa
and Sari Repka kindly commented on an early version of the manuscript. Leena Parkkonen and Leena
Roine are thanked for editing the text, and Jorma
Kuparinen for taking care of the administrative issues.
I wish to express my gratitude to Edna Granéli
for inviting me to visit her lab at Kalmar University,
to conduct some experiments on allelopathy. It was
an opportunity that really helped me to get started
with my scientific activities. I am indebted to Giovana and Paulo Salomon for making my visit so enjoyable and for arranging all practical things concerning work and freetime. Thank you Giovana for
our joint experiments and for being an advisor, a coauthor as well as a friend. I’m also thankful to
Catherine Legrand in Kalmar for advice concerning
allelopathic experimental set-ups.
Thanks to all the members of the late EZECO
(R.I.P.): Eve, J.-P., Jonna, Maiju, Marja, Make, Miina, Roope, Samuli, Sandra, SannaR, Satu, Tarja and
Tomi, for various hilarious activities both at work
and in the freetime, and especially to SannaR, my
room mate during so many years and in three different places. Futhermore, I wish to thank two exemplary women of science, Maria Laamanen and Anke
Kremp for all their support, advice and co-operation.
Anke skillfully supervised my MSc thesis, concerning vernal dinoflagellates, and is thus to a large part
responsible for my ending up as a phytoplankton
researcher.
Division of Hydrobiology at the University of
Helsinki provided me with a place to work during
my first steps as a PhD student. Later, I was warmly
welcomed by the Department of Biological Oceanography at FIMR, and I want to thank all the people
there for creating an extraordinarily dynamic and
inspiring working environment. A lot of the experimental work was done during long summer and au-
Allelopathic effects of filamentous cyanobacteria on phytoplankton in the Baltic Sea
tumn days and nights at the Tvärminne Zoological
Station. I am indebted to the staff there for all their
help, especially to Anne-Marie Åström and Ulla
Sjölund in the lab, and to Laila Keynäs, Raija
Myllymäki and Jouko Pokki concerning all imaginable practical things.
Kaarina Sivonen is acknowledged for kindly letting me use her cyanobacteria cultures, nodularin
and lab facilities, and Matti Wahlsten and Jouni
Jokela in her lab for helping with all practicalities.
Sari Repka provided the inspiration for my first allelopathic experiments and patiently advised me in
my early attempts to culture cyanobacteria. Miina
Karjalainen is acknowledged for all help and discussions concerning nodularin analysis, as well as for
sharing so many conference trips. Riitta Autio
helped me to get started with primary production
analysis, and Maija Huttunen assisted with all matters concerning phytoplankton microscopy.
All my co-authors are acknowledged for their
help in the various phases of experimental design,
data gathering and article preparation.
During the freetime, the biologist gang Marjorie
has been essential in escaping the world of (hydrobiological) science. Thanks to my nonbiologist
friends from the good old Kannelmäki-Haaga region
as well!
My parents have always believed in me and encouraged me to make my own choices, for which
I’m grateful. Thank you, and Aili as well, for always
taking care of our little Eino when needed. Finally,
my warmest thanks to Jarno for all the help and interest concerning science, statistics and computing,
and above all, for your love and patience all the way.
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