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Dense sub-ice bloom of dinoflagellates
in the Baltic Sea, potentially limited
by high pH
KRISTIAN SPILLING1,2*
1
FINNISH ENVIRONMENT INSTITUTE, PO BOX
10900 HANKO,
140, 00251 HELSINKI,
2
FINLAND AND TVÄRMINNE ZOOLOGICAL STATION, UNIVERSITY OF HELSINKI,
FINLAND
*CORRESPONDING AUTHOR: [email protected]
Received February 27, 2007; accepted in principle June 27, 2007; accepted for publication August 15, 2007; published online August 18, 2007
Communicating editor: K.J. Flynn
The phytoplankton community, carbon assimilation, chlorophyll a (Chl a), pH, light and attenuation and inorganic nutrients were monitored under the ice in the coastal Gulf of Finland, Baltic
Sea. Maximum ice and snow thickness was 40 and 15 cm, respectively. Freshwater influence had
created a halocline 1 – 2 m below the ice – water interface, and above this halocline, a dense bloom
of dinoflagellates developed (max: .300 mg Chl a L21). The photosynthetic uptake of carbon
dioxide by this “red tide” increased the pH to a maximum of 9.0. The sub-ice phytoplankton
community was dominated by the dinoflagellate Woloszynskia halophila (max: 3.6 107 cells L21). The pH tolerance of this species was studied in a monoculture and the results
indicate that pH .8.5 limits growth of this species at ambient irradiance. This study shows that
primary productivity may raise the pH to growth limiting levels, even in marine, low-light environments where pH normally is not considered important.
I N T RO D U C T I O N
The Baltic Sea is a semi-enclosed, brackish ocean
where ice is an important element of the ecosystem
during winter. In the northern part of Baltic Sea and
western part of Gulf of Finland, the probability of freezing is .90% and ice coverage normally lasts for 2 – 6
months (Mälkki and Tamsalu, 1985). There have been
observations of dense, dinoflagellate dominated blooms
under the ice in the Baltic Sea, but there is relatively
little information about this phenomenon (Larsen et al.,
1995; Haecky et al., 1998; Kremp and Heiskanen,
1999). These types of blooms are often called red tides
because of the obvious discoloration of the water, but a
cold-water red tide is very much in contrast to the main
distribution and bloom patterns of dinoflagellates,
which typically avoid winter and spring in temperate
areas (Smayda and Reynolds, 2001).
In marine environments, the high concentration of
inorganic carbon functions as an effective buffer against
changes in the pH. Traditionally, pH has not been considered an important factor in marine ecosystems, but it
has started to receive more attention. During periods of
high primary production, the pH can raise considerably
even in salt water, and high pH in marine ecosystems
may affect heterotrophic protists (Pedersen and Hansen,
2003a), macroalgae (Menéndez et al., 2001) and phytoplankton (Pedersen and Hansen, 2003b; Lundholm
et al., 2004; Havskum and Hansen, 2006; Møgelhøy
et al., 2006). The main reason for change in pH during
primary production is the photosynthetic fixation of
carbon dioxide, which when dissolved in water is a
weak acid. Additionally, there are other biological
mechanisms that alter the pH to a lesser degree, e.g.
uptake of nitrate raises the pH (Stumm and Morgan,
1996). Rising pH may reach levels limiting algal growth,
and may function as a driving force for plankton succession, as pH tolerance for both phytoplankton and
zooplankton is highly species specific, i.e. some species
are more tolerant of high pH than others (Goldman
doi:10.1093/plankt/fbm067, available online at www.plankt.oxfordjournals.org
# The Author 2007. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected]
JOURNAL OF PLANKTON RESEARCH
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et al., 1982; Hansen, 2002; Pedersen and Hansen,
2003a).
Primary production associated with ice is generally
governed by temperature and light (Harrison and Platt,
1986), and photosynthetic rates of the algal ice community is generally low compared with phytoplankton
assimilation numbers in temperate seas (Kirst and
Wiencke, 1995). However, at times when the light
environment promotes positive production, the biomass
may raise to considerable amounts (Arrigo et al., 1995;
Gradinger et al., 1999), and the pH may accordingly
raise to levels limiting growth (Gleitz et al., 1996).
The present study was initiated after observations of a
dense Woloszynskia halophila (Biecheler) Elbrächter and
Kremp dominated bloom under the ice cover, which had
raised the pH to 9.0. The objective of the study was to
examine whether pH can be a factor influencing growth
in the typical low light environment prevailing under ice.
METHOD
In situ study
Water was collected from under the ice through a small
hole (ø 15 cm) at 59849.20 N, 23816.50 E situated in the
outer archipelago, SW coast of Finland. Water depth at
the sampling station is 30 m. Sampling took place
weekly from March to May 2006. Additionally, a sample
taken from the same location in February during routine
monitoring sampling (at Tvärminne Zoological Station,
University of Helsinki) was added to the phytoplankton
counts. Water was collected with a Niskin bottle from
the ice– water interface and from 5 to 10 m depth
during the ice-covered period. The water was stored in
acid-washed, polycarbonate bottles and was taken to
the laboratory for determination of dissolved inorganic
nutrients (N, P and Si), inorganic carbon, chlorophyll a
(Chl a) and cell enumeration.
Irradiance was recorded with a spherical light meter
(Biospherical Instruments, QSL 2101, San Diego, CA,
USA) above the ice, in the snow and below the ice
cover. Incident irradiance was recorded with the sensor
placed over a black cloth preventing recording of
backscattered light. The coefficient of light attenuation
(K0, m21) was estimated according to the equation:
K0 ¼
lnðEB =EA Þ
D
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recorded with a light sensor (Davis, GroWeather II,
Hayward, CA, USA) placed on top of Tvärminne
Zoological Station, University of Helsinki, 3 km north
of the sampling area. Long-term light milieu under the
ice was calculated using these data and recordings of
ice and snow thickness and the estimated K0.
Salinity and temperature profiles were obtained with a
CTD Plus 100 meter (Sis-Fieldsoft, Klausdorf, Germany).
The CTD probe measured the salinity and temperature
from 1 m depth to the bottom with 0.5 m intervals.
Temperature and salinity directly under the ice was determined using a combined conductivity- and thermo-meter
(Radiometer, CDM 83, Copenhagen, Denmark).
Nutrient determinations and Chl a filtrations were
done immediately after the return to the laboratory.
Inorganic nutrients (nitrate + nitrite, phosphate and silicic
acid) were determined according to standard oceanographic methods (Grasshoff et al., 1983). Dissolved inorganic carbon (DIC) was measured on a Unicarbo
carbon analyzer (Electro Dynamo, Laitila, Finland),
and PCO2 and CO2 aq was calculated using the dissociation constants of carbonic acid presented by
Lueker et al. (Lueker et al., 2000). Samples for Chl a
were filtrated onto GF/F filters, extracted in 10 mL,
96% ethanol (Jespersen and Christoffersen, 1987) and
stored in a freezer before determination using a spectroflurophotometer (Shimadzu, RF 5000, Columbia, MD,
USA), calibrated against pure Chl a (Sigma, St Louis,
MO, USA). The pH was determined with a pH meter
(Schott Geräte, CG 820 with a Scott N6280 sensor,
Mainz, Germany).
Water for cell enumerations were preserved with acid
Lugol’s solution and enumerated under an inverted
microscope (Lomo, HT-30.01, St Petersburg, Russia)
using a Sedgewick Rafter chamber (Wildlife Supply
Company, Buffalo, NY, USA), when the cell concentration was dense, otherwise by using the settling
method of Utermöhl (Utermöhl, 1958). Growth rate
was calculated according to the equation:
m¼
ðln Nt ln N0 Þ
t
ð2Þ
where m is the specific growth rate day21, N0 the initial
biomass, Nt the biomass at time t and t is the time in days.
Culture study
ð1Þ
where EA is the incoming radiance above the ice, EB
irradiance below the ice, and D the depth of ice and
snow cover in meter. Long-term light data were
For the culture study, a clonal, but not axenic, culture of
W. halophila was used. The culture strain was isolated
from a single cyst by A. Kremp, University of Helsinki.
The culture was in the initial phase of the stationary
growth phase, and the pH was 9.2. Inorganic nutrients,
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trace metals and vitamins were added in concentrations
equaling f/10 media (Guillard, 1975), in order to
prevent nutrient limitation of primary production. The
culture was distributed in five bottles, one did not
receive any treatment and kept at the original pH, the
other bottles were gently shaken for different length of
time (30 sec – 3 min), which increased the amount of
DIC and decreased the pH. DIC was determined as
described earlier, for all treatments at the start of the
incubation period.
The assimilation numbers were determined using the
14
C isotope (Steeman-Nielsen, 1952). For determining
the photosynthetic irradiance (PE) relationship, an
activity of 0.73 kBq was added to 50 mL sample, which
subsequently was distributed in scintillation vials (3 mL
in each). These were placed inside a PE incubator
(a prototype constructed by B.G. Mitchell, Scripps
Institute of Oceanography, University of California, CA,
USA). Briefly, the incubator is shaped like a rectangular
box (65 8 15 cm) with a halogen light source in
one end. On the top of the box, there are 18 holes, i.e.
incubation chambers (only 16 of them were used in this
study), distributed on the longitudal axis, and each of
these incubation chambers can hold one 7 mL scintillation vial. The light is channeled along the bottom part
of the box and shines up through the different incubation
chambers, and the photon flux density in each chamber is
adjusted with a shutter. On the sides of the PE-incubator,
there are water pipes enabling water-cooling of the whole
system. The water enters from the opposite side of the
light source, makes a loop around the incubation
chambers and flows out next to the inflow.
Four PE incubators were used simultaneously, and
the temperature was kept at 28C. For the incubations,
2 dark and 14 light bottles were used, and irradiance
ranged from 0 to 570 mmol photons m22 s21. After an
incubation period of 2 h, 200 ml 1 M HCl was added
and the scintillation vials were left open for 2 days, after
that 4 mL Hi Safe scintillation liquid was added
(Schindler et al., 1972). The radioactivity was determined directly from the scintillation vials used in the
incubation, using a liquid scintillation counter
(PerkinElmer Inc., Wallac Winspectral 1414, Wellesley,
MA, USA). The PE relationship was examined by
fitting the function (Platt et al., 1980):
a E
bE
exp
P Chl ¼ PsChl 1 exp
PsChl
PsChl
ð3Þ
to the obtained data, where P Chl
is the maximum
s
potential production in the absence of photoinhibition
and production has the units mmol C (mg Chl a)21 h21,
E irradiance in mmol photons m22 s21, a the initial
slope and b the slope of the curve beyond the point of
photoinhibition in mmol C m2 (mg Chl a)21 (mol
photons)21. At light saturation, the maximum photosynthetic rate, normalized to Chl a (P Chl
m ), is
PmChl ¼ PsChl
a
ða þ b Þ
b
ða þ b Þ
ðb=aÞ
ð4Þ
Confidence limits for the PE relationships were calculated using the Curve Fitting Tool in MatLab software,
and are based on the confidence bounds for the fitted
coefficients in equation (3).
R E S U LT S
The irradiance varied between 15 and 30 mmol
photons m22 sec21 directly under the ice at the sampling dates in March. The coefficient of light attenuation (K0) for snow and ice was 19 and 2.4 m21,
respectively. The calculated sub-ice irradiance based on
monitoring data and ice and snow thickness is presented in Fig. 1. During February, there was very little
snow cover and the average daily irradiance under the
ice cover was relatively high (.50 mmol photons
m22 sec21) and the day length increased from 6 to 9 h
during this month. During the very last days of
February, there was a snow fall which increased snow
thickness 10-fold, and this snow cover decreased the
amount of light penetrating through the ice for the duration of March. At the end of March, the snow cover
melted away and the ice thickness started to decrease,
which increased the irradiance under ice again.
There was a water layer with lower salinity directly
under the ice (Fig. 2). The origin of the low salinity
water was most likely from the mouth of an estuary
(Pohjanlahti) situated 10 km to the north of the
sampling point. The major nutrients were replete at the
ice – water interface until mid-April when nitrate was
depleted ,1 mmol L21. The concentration of dissolved
silicon (DSi) was high (.40 mmol L21) in March, but
from the beginning of April, the DSi started to decrease
and was 12 mmol L21 at the time of the ice break.
The phosphate concentration was 0.2 mmol L21 for
the duration of the sampling period. The amount of
DIC was 1.2– 1.5 mmol DIC L21. The nutrient
concentration directly under the ice was affected by
the freshwater influence; below the halocline (5 m
depth), the inorganic nutrient concentration was
7.7 mmol NO3 L21, 0.7 mmol PO4 L21and 13.7
mmol DSi L21 throughout March.
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Fig. 3. The development of Chl a and pH directly under the ice.
The first Chl a value (cross) was not measured directly, but was
estimated based on the cell counts and average Chl a cell21
concentration on the following sampling dates.
Fig. 1. Average irradiance under the ice cover (line) during the
number of daylight hours (dots). The upper graph shows the snow
and ice thickness. The sub-ice irradiance was calculated from light
monitoring data (measured every 15 min), snow and ice thickness and
coefficient of light attenuation. The day length was defined as number
of hours when irradiance .5 mmol photons m22 sec21 above the ice.
The maximum Chl a concentration recorded was
307 mg Chl a L21, and was found directly under the ice
above the halocline (Fig. 3). The Chl a concentration
below the halocline (5 and 10 m depth) was considerably lower, and was in March determined to be
5 –10 mg Chl a L21. After the initial high biomass in
mid-March, the biomass concentration decreased, probably because of water movement and mixing. The
development of pH followed the pattern of biomass
development.
The phytoplankton community under the ice was
dominated by the dinoflagellate W. halophila. The cell
concentration of W. halophila on the first sampling
(February 23) was 1.7 107 cells L21 and the maximum
recorded cell concentration was 3.6 107 cells L21
(March 15), which co-occurred with the Chl a peak.
Other phytoplankton species represented under ice were
the dinoflagellates Peridiniella catenata (Levander) Balech
(max: 1.3 106 cells L21) and diatom Pauliella taeniata
(Grunow) Round and Basson (max: 1.9 106 cells L21).
There were also small phytoplankters (.5 mm) present,
mainly Chrysophytes, but this group was marginal in
terms of biomass. The autotrophic ciliate Mesodinium
rubrum (Lohmann) Hamburger and Buddenbrock was
present in varying numbers, and had the highest concentration on March 28 (5.6 105 individuals L21) when it
constituted 35% of the carbon biomass.
The pH had an effect on the primary production of
W. halophila in culture. An increase in pH from 7.6 to
8.5 decreased the P Chl
m by 19% (Figs 4 and 5). There
was, however, no change in the a between pH 7.6 and
8.5. At pH of 9.0, there was a drop in both P Chl
m and a
of 38% and 29%, respectively, compared with pH 7.6,
and at pH 9.2, the P Chl
m was decreased by 89% and a
by 71% compared with pH 7.6.
DISCUSSION
Sub-ice characteristics
Fig. 2. Salinity (solid lines) and temperature (dotted lines) (8C)
throughout the water column, under the ice.
Stability of the water right under the ice is probably a
prerequisite for the build-up of such dense dinoflagellate
blooms as described in this study. Ice coverage prevents
effective wind mixing of the water column, and the salinity stratification found during this study further stabilized the sub-ice water layer. This stratification is
probably also the main reason why other immotile phytoplankton competitors, such as diatoms, were only
present in very low number as they tend to sink out of
the upper stratified water layers during low mixing
periods (Fogg and Thake, 1987). Because of the freshwater influence, causing salinity stratification, these
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Fig. 4. The relationship between irradiance and carbon assimilation
for a monoculture of Woloszynskia halophila at pH 7.6 (circle), pH 8.0
(triangle), pH 8.5 (square), pH 9.0 (diamond) and pH 9.2 (cross). The
cells were taken from a stationary culture and inorganic nutrients were
added in f/10-media concentrations (Guillard, 1975). The highest pH
was the initial pH, and lower pH was obtained by gently shaking the
culture bottle, which increased the amount of DIC. The solid line
represents the regression fit using equation (4). The 95% confidence
intervals for the curves are presented in Fig. 5.
which due to high albedo and scattering drastically
decreased the under-ice light environment in March.
Although the day length was shorter in February, the
lack of a thick snow cover provided better conditions for
autotrophe growth and the biomass was dense already
in mid-February.
The taxonomy of cold-water dinoflagellates in the
Baltic Sea has recently been modified and there are
strong indications that the previously much recorded
Scrippsiella hangoei (Schiller) Larsen actually has been
W. halophila as the latter species produces the dominating
dinoflagellate cyst found in the sediment (Kremp et al.,
2005). The two species are hard to tell apart in a light
microscope, but are distinguishable when fixed in acid
Lugol’s solution (Kremp et al., 2005). During my investigation, I did not see any cells with the typical S. hangoei
characteristics, but this species may have been present
and an improvement for phytoplankton work in the
area would be to develop molecular tools to separate
the two species. All the other recorded phytoplankters
are relatively abundant during winter and spring in the
sampling area. Pauliella taeniata is a typical ice diatom
(Niemi, 1975; Heiskanen, 1998) and P. catenata is a
dominant, cold-water dinoflagellate in the Baltic Sea
(Heiskanen, 1998; Spilling et al., 2006).
Effect of pH
Fig. 5. The photosynthetic capacity (P Chl
m ) and photosynthetic
efficiency (a) for the regressed PE relationships presented in Fig. 4.
Error bars represent the 95% confidence interval.
types of dense blooms are probably mainly a coastal
phenomenon. Rivers in the Baltic Sea are known to
produce extensive plumes of low salinity water penetrating out from the coast under the ice (Granskog et al.,
2005), and in the study area, freshwater outflow from
land is relatively more important than ice melt.
However, melting of ice during spring might also create
a similar environment off the coast (Gradinger, 1996).
The obtained K0 (ice 2.4 m21, snow 19 m21)
were within the range of light attenuation obtained previously in the investigated area (Shirasawa et al., 2001).
The result clearly show the effect of a snow cover,
The observation of pH 9.0 under ice and the effect of
pH on the dominating phytoplankton species (Figs 4
and 5) show that pH can be a factor regulating primary
production under ice. In low light environments, i.e.
light well below light saturation, it is only the pH effect
on the photosynthetic efficiency (a) that will effect
carbon assimilation. The culture study presented here
indicates that pH .8.5 decrease the photosynthetic efficiency in W. halophila, and a pH of 9.0 would thus affect
primary production at the low light found below the ice
in March.
The pH is influenced by several factors in marine
environments, but will mainly be a function of the CO2
uptake by algae, respiration and CO2 exchange with the
atmosphere and adjacent water layers/masses. The high
pH presented in this study was most likely to a combination of high algal biomass and little CO2 exchange
due to the ice cover and stratification. There are several
ways that pH might affect growth of algae. First, the
amount of dissolved CO2 decreases with increasing pH
as the chemical equilibrium of inorganic carbon shifts
22
towards the bicarbonate (HCO2
3 ) and carbonate (CO3 )
forms. This in turn may drive primary production into
carbon limitation (Riebesell et al., 1993). However,
at pH 8.5, the CO2 (aq) was calculated to be
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10 mmol L21, which probably is not limiting carbon
assimilation (Riebesell et al., 1993; Clark and Flynn,
2000). Furthermore many algae are able to enhance
CO2 available for photosynthesis through CO2 concentrating mechanism, which involves active uptake of CO2
and HCO2
3 or through production of the enzyme carbonic anhydrase, which speeds up the conversion rate
and CO2 (Badger et al., 1998).
between HCO2
3
Recently, several dinoflagellates were found not to be
limited by carbon, even at elevated pH, due to uptake
of HCO2
3 (Rost et al., 2006). Second, high pH may
cause alterations in membrane transport processes and
regulation of the intracellular pH reducing growth rate
(Smith and Raven, 1979). Third, changes in pH might
alter the cellular composition of amino acids, which
possibly affects growth rate (Taraldsvik and Myklestad,
2000). However, all the PE incubations were short term
(2 h) and were done with the same culture, having the
same initial physiological state, indicating that difference
in amino acids composition between pH treatments was
minor. Forth, elevated pH in seawater lowers the availability of nutrients such as phosphorus and trace metals
(Sunda et al., 2005). Before the PE incubations of the
W. halophila culture, inorganic nutrients were added in
sufficient amount to avoid any limitation and thus pH
effect on availability of phosphorus and trace metals is
not a likely reason for the observed pH effect. Judging
from the potential effects of pH in the literature, the
most likely explanation for the decreased carbon assimilation with increasing pH for W. halophila was changes
in membrane transport processes and regulation of the
intracellular pH.
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REFERENCES
Arrigo, K. R., Dieckmann, G., Gosselin, M. et al. (1995) High
resolution study of the platelet ice ecosystem in McMurdo
Sound, Antarctica: biomass, nutrient, and production profiles
within a dense microalgal bloom. Mar. Ecol. Prog. Ser., 127,
255 –268.
Badger, M. R., Andrews, T. J., Whitney, S. M. et al. (1998) The diversity and coevolution of Rubisco, plastids, pyrenoids, and chloroplastbased CO2-concentrating mechanisms in algae. Can. J. Botany, 76,
1052–1071.
Clark, D. R. and Flynn, K. J. (2000) The relationship between the dissolved inorganic carbon concentration and growth rate in marine
phytoplankton. Proc. R. Soc. Lond. B, 267, 953– 959.
Fogg, G. and Thake, B. (1987) Algal Cultures and Phytoplankton Ecology.
The University of Wisconsin Press, Madison.
Gleitz, M., Kukert, H., Riebesell, U. et al. (1996) Carbon acquisition
and growth of Antarctic sea ice diatoms in closed bottle incubations. Mar. Ecol. Prog. Ser., 135, 169–177.
Goldman, J. C., Riley, C. B. and Dennett, M. R. (1982) The effect of
pH in intensive microalgal cultures. II. Species competition. J. Exp.
Mar. Biol. Ecol., 57, 15–24.
Gradinger, R. (1996) Occurrence of an algal bloom under Arctic pack
ice. Mar. Ecol. Prog. Ser., 131, 301– 305.
Gradinger, R., Friedrich, C. and Spindler, M. (1999) Abundance,
biomass and composition of the sea ice biota of the Greenland Sea
pack ice. Deep-Sea Res. II, 46, 1457– 1472.
Granskog, M. A., Ehn, J. and Niemela, M. (2005) Characteristics and
potential impacts of under-ice river plumes in the seasonally icecovered Bothnian Bay (Baltic Sea). J. Mar. Sys., 53, 187 –196.
Grasshoff, K., Ehrhardt, M. and Kremling, K. (1983) Methods of
Seawater Analysis. Verlag Chemie, Weinheim.
Guillard, R. R. L. (1975) Culture of phytoplankton for feeding marine
invertebrates. In Smith, W. L. and Chanley, M. H. (eds), Culture of
Marine Invertebrate Animals. Plenum Press, New York, pp. 26–60.
Haecky, P., Jonsson, S. and Andersson, A. (1998) Influence of sea ice
on the composition of the spring phytoplankton bloom in the
northern Baltic Sea. Polar Biol., 20, 1– 8.
Hansen, P. J. (2002) Effect of high pH on the growth and survival of
marine phytoplankton: implications for species succession. Aquat.
Microb. Ecol., 28, 279–288.
AC K N OW L E D G E M E N T S
I want to thank the staff at the Tvärminne Zoological
Station, University Helsinki, particularly T. Sjölund for
help in the field and M. Sjöblom, E. Salminen, A-M.
Åström and U. Sjölund for help in the laboratory.
I acknowledge A. Kremp for providing the culture and
help with species identification, J. Piiparinen for providing ice thickness and snow cover data outside the main
sampling period and Finnish Institute of Marine
Research for letting me use their PE incubators.
Harrison, W. G. and Platt, T. (1986) Photosynthesis-irradiance
relationships in polar and temperate phytoplankton populations.
Polar Biol., 5, 153–164.
Havskum, H. and Hansen, P. J. (2006) Net growth of the bloomforming dinoflagellate Heterocapsa triquetra and pH: why turbulence
matters. Aquat. Microb. Ecol., 42, 55– 62.
Heiskanen, A. S. (1998) Factors governing sedimentation and pelagic
nutrient cycles in the northern Baltic Sea. Monogr. Boreal Environ.
Res., 8, 1– 80.
Jespersen, A. M. and Christoffersen, K. (1987) Measurements of
chlorophyll-a from phytoplankton using ethanol as extraction
solvent. Arch. Hydrobiol., 109, 445–454.
Kirst, G. O. and Wiencke, C. (1995) Ecophysiology of polar algae.
J. Phycol., 31, 181 –199.
FUNDING
Finnish Academy ( project 111336); Walter and Andreé
de Nottbeck Foundation.
Kremp, A. and Heiskanen, A. S. (1999) Sexuality and cyst formation
of the spring-bloom dinoflagellate Scrippsiella hangoei in the coastal
northern Baltic Sea. Mar. Biol., 134, 771 –777.
900
K. SPILLING
j
DENSE SUB-ICE BLOOM OF DINOFLAGELLATES
Kremp, A., Elbrächter, M., Schweikert, M. et al. (2005) Woloszynskia
halophila (Biecheler) comb. nov.: a bloom-forming cold-water dinoflagellate co-occurring with Scrippsiella hangoei (Dinophyceae) in the
Baltic Sea. J. Phycol., 41, 629–642.
Larsen, J., Kuosa, H., Ikävalko, J. et al. (1995) A redescription of
Scrippsiella hangoei (Schiller) Comb-Nov - a red tide dinoflagellate
from the northern Baltic. Phycologia, 34, 135–144.
Lueker, T. J., Dickson, A. G. and Keeling, C. D. (2000) Ocean pCO2
calculated from dissolved inorganic carbon, alkalinity, and
equations for K-1 and K-2: validation based on laboratory
measurements of CO2 in gas and seawater at equilibrium. Mar.
Chem., 70, 105– 119.
Lundholm, N., Hansen, P. J. and Kotaki, Y. (2004) Effect of pH
on growth and domoic acid production by potentially toxic diatoms
of the genera Pseudo-nitzschia and Nitzschia. Mar. Ecol. Prog. Ser., 273,
1–15.
Mälkki, P. and Tamsalu, R. (1985) Physical features of the Baltic Sea.
Finn. Mar. Res., 252, 23–27.
Menéndez, M., Martinez, M. and Comin, F. A. (2001) A comparative
study of the effect of pH and inorganic carbon resources on the
photosynthesis of three floating macroalgae species of a
Mediterranean coastal lagoon. J. Exp. Mar. Biol. Ecol., 256,
123–136.
Møgelhøy, M. K., Hansen, P. J., Henriksen, P. et al. (2006) High pH
and not allelopathy may be responsible for negative effects of
Nodularia spumigena on other algae. Aquat. Microb. Ecol., 43, 43–54.
Niemi, Å. (1975) Ecology of phytoplankton in the Tvärminne area,
SW coast of Finland. II. Primary production and environmental
conditions in the archipelago and the sea zone. Acta Bot. Fennica,
105, 1 –73.
Pedersen, M. F. and Hansen, P. J. (2003a) Effects of high pH on the
growth and survival of six marine heterotrophic protists. Mar. Ecol.
Prog. Ser., 260, 33–41.
Pedersen, M. F. and Hansen, P. J. (2003b) Effects of high pH on a natural
marine planktonic community. Mar. Ecol. Prog. Ser., 260, 19–31.
Platt, T., Gallegos, C. L. and Harrison, W. G. (1980) Photoinhibition
of photosynthesis in natural assemblages of marine phytoplankton.
J. Mar. Res., 38, 687–701.
Riebesell, U., Wolf-Gladrow, D. A. and Smetacek, V. (1993) Carbon
dioxide limitation of marine phytoplankton growth rates. Nature,
361, 249– 251.
Rost, B., Richter, K.-U., Riebesell, U. et al. (2006) Inorganic carbon
acquisition in red tide dinoflagellates. Plant Cell Environ., 29,
810 –822.
Schindler, D. W., Schmidt, R. V. and Reid, R. A. (1972) Acidification
and bubbling as an altemative to filtration in determining phytoplankton production by the 14C method. J. Fish. Res. Bd. Can., 29,
1627–1631.
Shirasawa, K., Leppäranta, M., Ehn, J. et al. (2001) Ice and snow
cover as a filter of solar radiation in natural waters. In Levin, I. and
Gilbert, G. (eds), Current Problems in Optics of Natural Waters. Proceedings
of D. S. Rozhdestvensky Optical Society. D. S. Rozhdestvensky Optical
Society, St Petersburg, pp. 278– 282.
Smayda, T. J. and Reynolds, C. S. (2001) Community assembly in
marine phytoplankton: application of recent models to harmful
dinoflagellate blooms. J. Plankton Res., 23, 447–461.
Smith, F. and Raven, J. A. (1979) Intracellular pH and its regulation.
Ann. Rev. Plant Physiol., 30, 289– 311.
Spilling, K., Kremp, A. and Tamelander, T. (2006) Vertical distribution and cyst production of Peridiniella catenata (Dinophyceae)
during a spring bloom in the Baltic Sea. J. Plankton Res., 28,
659 –665.
Steeman-Nielsen, E. (1952) The use of radioactive carbon for measuring organic production in the sea. J. Cons. Perm. Int. Explor. Mer.,
18, 117– 140.
Stumm, W. and Morgan, J. J. (1996) Aquatic Chemistry. WileyInterscience, Hoboken.
Sunda, W. G., Price, N. M. and Morel, F. M. M. (2005) Trace metal
ion buffers and their use in culture studies. In Andersen, R. A.
(ed.), Algal Culturing Techniques. Elsevier, Amsterdam, pp. 35– 63.
Taraldsvik, M. and Myklestad, S. (2000) The effect of pH on growth
rate, biochemical composition and extracellular carbohydrate production of the marine diatom Skeletonema costatum. Eur. J. Phycol., 35,
189 –194.
Utermöhl, H. (1958) Zur Vervollkommnung der quantitativen
Phytoplanktonmethodik. Mitt. Int. Ver. Theor. Angew. Limnol., 9, 1– 38.
901