Harmful Algae 6 (2007) 189–205
www.elsevier.com/locate/hal
Phytoplankton vertical distributions and composition
in Baltic Sea cyanobacterial blooms
Susanna Hajdu *, Helena Höglander, Ulf Larsson
Department of Systems Ecology, Marine and Brackish Water Ecology, Stockholm University, SE-106 91 Stockholm, Sweden
Received 17 January 2006; received in revised form 27 July 2006; accepted 31 July 2006
Abstract
We studied the vertical structure of the phytoplankton community in two toxic cyanobacterial blooms in the offshore Baltic Sea.
In 1994, vertically separated potentially toxic, diazotrophic and mixotrophic species (belonging to Cyanophyceae, Dinophyceae
and Prymnesiophyceae) dominated. In 1997, picocyanobacteria, mainly in colonies, made up 40–50% of the total phytoplankton
carbon biomass in the top 20 m both day and night. Colony-forming species of picocyanobacteria seem to be occasionally important
and hitherto underestimated in the Baltic Sea.
We found species-specific depth distribution patterns. Nodularia spumigena and Anabaena spp. were observed mainly above
10 m depth, while Aphanizomenon sp. was mostly found deeper, especially at night. Dinophysis norvegica was only abundant near
the seasonal pycnocline and showed very limited diurnal migration. Other flagellates, including small Cryptophyceae and 10
identified Chrysochromulina species, occurred down to 40 m depth. Their vertical migration may help to retrieve nutrients from
below the summer pycnocline.
We conclude that considerable differences in dominating functional groups may occur between years/bloom stages, and that the
vertical distribution pattern of many species is recurring at similar environmental conditions, suggesting species-specific nicheseparation.
# 2006 Elsevier B.V. All rights reserved.
Keywords: Baltic Sea; Chrysochromulina; Picocyanobacteria; Phytoplankton; Vertical distribution
1. Introduction
Species-specific nutrient requirements are key
factors in regulating the phytoplankton community
(Tilman, 1982) and will lead to modifications in the
community structure when nutrient availability changes
(Sommer, 1989). Physical and biological interactions
also determine the success of different species (e.g.
Cushing, 1989; Hansen et al., 1995; Granéli et al., 1995;
Suikkanen et al., 2004). Strong water stratification may
* Corresponding author. Tel.: +46 8 161730/18 425827;
fax: +46 8 158417.
E-mail address: [email protected] (S. Hajdu).
1568-9883/$ – see front matter # 2006 Elsevier B.V. All rights reserved.
doi:10.1016/j.hal.2006.07.006
lead to a nutrient-depleted euphotic zone, isolated from
the nutrient-rich water below. This condition strongly
influences the species composition (Smayda, 1997) and
the vertical distribution of phytoplankton (Cushing,
1989) affecting the coupling between primary and
secondary production. It may also lead to harmful algal
blooms (Smayda, 1997) and favour diazotrophs,
mixotrophs or phytoplankton species with other
qualities, e.g. ability to migrate vertically, or possession
of a high surface to volume ratio that gives them
competitive advantages in a nutrient-depleted environment (Kilham and Kilham, 1980; Smayda, 1997).
In the brackish Baltic Sea proper, noxious blooms of
diazotrophic cyanobacteria are common (Kononen,
1992; Wasmund, 1997) due to nitrogen limitation of the
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S. Hajdu et al. / Harmful Algae 6 (2007) 189–205
spring bloom, which leaves unused dissolved inorganic
phosphorus (DIP) that favours N2-fixing cyanobacteria
in summer (Larsson et al., 2001). Their intensive growth
depletes DIP in the illuminated water column (Walve,
2002) while leakage of nitrogen during growth and the
decomposition of the bloom add new nitrogen (Larsson
et al., 2001). The bloom co-occurs with a rapid build up
of heterotrophic biomass (Johansson et al., 2004) and
fish biomass (Hjerne and Hansson, 2002) that result in
increased grazing pressure and nutrient sequestering
(e.g. Hjerne and Hansson, 2002). These factors affect
the phytoplankton community during a cyanobacteria
bloom and influence the structure of the pelagic food
web. Several Baltic studies have focused on cyanobacteria blooms and N2-fixation (e.g. Niemistö et al.,
1989; Kononen, 1992; Larsson et al., 2001), but only
Kononen et al. (1998) have studied the phytoplankton
community change during a bloom in the northern
Baltic proper.
The Baltic Sea proper surface water is separated
from the deep water by a permanent halocline at 60–
70 m depth and in summer a seasonal pycnocline
separates an upper mixed layer of 10–20 m depth from
the underlaying winter water. This winter water
contains some nutrients, particularly phosphorus that
could be a source of nutrients for vertically migrating
phytoplankton when mixed layer nutrients are
exhausted (e.g. Niemistö et al., 1989; Carpenter
et al., 1995). This nutricline may contribute to the
deep chlorophyll maxima observed in several parts of
the Baltic Sea (Niemi et al., 1970; Kuosa, 1990a;
Kononen et al., 1998), involving also potentially toxic
species (Kaas et al., 1991; Carpenter et al., 1995; Hajdu
et al., 1996). Physical and biological mechanisms have
been invoked to explain such subsurface cell concentrations (e.g. Kononen et al., 1998) and their role in
population dynamics (Kuosa, 1990a; Maestrini and
Granéli, 1991).
The vertical distributions of many species differ
between day and night, indicating either migration or
differences in production/mortality rates. Due to
sampling difficulties and the time consuming analysis,
studies of phytoplankton vertical distributions have
been limited to individual species in the Baltic Sea and
elsewhere (e.g. Sommer, 1982; Olsson and Granéli,
1991; Olli et al., 1998; Olli, 1999), and performed
mostly in coastal areas (Olli et al., 1998; Olli, 1999), in
the laboratory (Arvola et al., 1991), or in mesocosm
experiments (Olli and Seppälä, 2001). However, little is
still known about the phytoplankton community
composition in offshore cyanobacterial blooms, as well
as the depth preferences and migration patterns of the
different summer species in the open Baltic Sea. Here,
we report on phytoplankton composition, including
picocyanobacteria, and the vertical distribution patterns
during toxic, N-fixing cyanobacteria blooms in the open
Baltic Sea.
2. Materials and methods
2.1. Study areas and sampling methods
In 1994, we visited the station WGB (588220 N,
188280 E), depth 128 m, in the western Gotland basin
and in 1997, the station EGB (578210 N, 198400 E), depth
110 m, in the eastern Gotland basin (Fig. 1). In 1994,
samples were collected daily, between 11 a.m. and 3
p.m., from 24 to 29 July. In 1997, samples were taken at
noon and at mid-night for two 24-h periods (8–9
August).
Wind speed data are from the Swedish Meteorological and Hydrological Institute’s (SMHI) weather
station at Landsort (1994) and from ship readings
(1997).
Salinity and temperature were measured by CTD
casts (Meerestechnik Elektronik GmbH). Vertical
Fig. 1. Study areas. Station Western Gotland Basin (WGB) sampled
in 1994 and station Eastern Gotland Basin (EGB) sampled in 1997.
S. Hajdu et al. / Harmful Algae 6 (2007) 189–205
profiles of irradiance were measured with a Li-193SA
Spherical Quantum Sensor (Li-Cor Bioscience).
In 1994, nutrients were analysed from the surface to
80 m depth (0, 1, 2, 5 m, then every fifth meter down to
30 m, and thereafter every 10th meter) and chlorophyll
a every fifth meter down to 20 m depth. In 1997, we
used CTD-data and data on nutrient concentrations (0,
20, 40, 60, 80, 100 and 125 m depth) collected at the
same time by the Baltic Sea Research Institute
(Warnemünde, Germany) at a nearby station
(578170 N, 208050 E).
Phytoplankton (including picoplankton) were analysed from discrete and integrated water samples
(0–20 m) collected with a Ruttner water bottle and a
20 m long plastic hose (inner diameter 19 mm),
respectively. In 1994, discrete samples were taken
from 0, 1, 2, 5, 10, 15, 30 m for picoplankton, and
from every 2 m down to 20 m depth for phytoplankton
>2 mm. On July 25, additional samples were taken
every 6 h, from 3 a.m. to 11 p.m., to study diurnal
vertical migration of Dinophysis spp. In 1997, we
collected phytoplankton samples on August 8, at
13:30 h GMT, from the surface and then every second
meter to 20 m depth and on 9 August, at 0:30, 12:00
and 23:00 h GMT, from every 5 to 30 m and at 40 and
60 m. In daytime, additional samples from every
meter between 10 and 20 m depth were taken for
enumeration of Dinophysis cells.
2.2. Analytical methods
In 1994, phosphate and inorganic nitrogen (ammonium, nitrite, and nitrate) concentrations were measured
on ship using standard methods (Grasshoff et al., 1983).
Detection limits for phosphate, ammonium, nitrite and
nitrate were 0.016, 0.07, 0.02 and 0.02 mM, respectively. Chlorophyll a samples (2 l) were filtered on
47 mm Whatman GF/F filters and stored frozen
(20 8C) over silica gel until analysis. Filters were
homogenised in 90% acetone in a piston grinder,
centrifuged and the clear supernatant analysed in a
Hitachi U2000 spectrophotometer. Calculations followed Jeffrey and Humphrey (1975).
Picoplankton (cell size <2 mm) were fixed with
paraformaldehyde solution (final concentration 0.2%)
directly after sampling and stored at 4 8C. Subsequently,
4–20 ml of the samples was filtered onto black 0.2 mm
polycarbonate membrane filters (diameter 25 mm). The
filters were placed on glass slides and a small drop of nonfluorescent immersion oil and a cover slip added. The
slides were stored frozen (20 8C) until enumeration. In
1994, single-celled picocyanobacteria were counted
191
directly with an Olympus VANOX-T microscope with
a 100 W mercury lamp and a green filter set (excitation
545 nm, barrier 590 nm) at 1250 magnification. In
1997, we used the same microscope and filter set as in
1994, but counts were performed after transferring
epifluorescence images to an image analyser through a
grey level camera (MTI-SIT 66). Cell sizes of 50 cells
per sample were measured with the OPTIMAS 5.0
software (cell length ranged from 0.4 to 2.37, cell width
from 0.24 to 1.71 mm). In both years, at least 300 cells
were counted per filter (MacIssac and Stockner, 1993).
Mucilaginous colony-forming taxa with cells <2 mm
(henceforth called colony-forming picocyanobacteria,
for species see Table 1) were counted with a NIKON
inverted microscope and phase contrast at 600
magnification in samples preserved with acid Lugol’s
solution in 1994. In 1997, colony-forming taxa were
counted on the same filter as single-celled picocyanobacteria in epifluorescence (Olympus VANOX-T microscope) in two diagonals, at 750 magnification. Number
of cells per colony, colony size and individual cell size
were determined from epifluorescence images (Table 2).
Cell density of the colonies was calculated as number of
cells per colony divided by the colony area measured in
the two dimensional epifluorescence images (Table 2).
To simplify counting, colonies were enumerated in three
groups with different cell densities (Table 2) and cell
volumes (Table 1): compact colonies (Fig. 2a), loose
colonies (Fig. 2b) and colonies with cells organised in
rows (Aphanothece parallelliformis Cronberg) (Fig. 2c).
Picoplankton cell volumes were calculated either as
spheres or as ovoid cells (V = p [(W2 L)/4 W3/
12]) (Hagström et al., 1979). Cells with length/width
ratio >0.8 and <1.20 were considered as spheres
and with ratio 1.20 as ovoid. In 1994 cell volume of
single-celled picocyanobacteria was not measured
and therefore the mean cell volume of 516 cells from
1997 was used. Average cell volumes of single-celled
and colony-forming picocyanobacteria are shown in
Table 1.
Nanoplankton (cell size 2–20 mm) and microplankton
(cell size 20–200 mm) were counted in samples
preserved with acid Lugol’s solution, after sedimentation
in Utermöhl chambers using a NIKON inverted microscope with phase contrast. Microplankton was counted in
diagonals or on the half/whole chamber bottom at 150
magnification. Dinophysis was always enumerated on the
whole chamber bottom. For nanoplankton 1–4 diagonals
were counted at 600 magnification. Several taxa were
counted in size groups, some of them including several
species in each (Table 1). Micro- and nanoplankton
biomass was calculated by multiplying the cell number
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S. Hajdu et al. / Harmful Algae 6 (2007) 189–205
Table 1
Average cell volume (mm3) of all taxon included in the calculation of the total phytoplankton biomass
Taxon
Cyanophyta (cyanobacteria)
Nostocophyceae
Single picocyanobacteria
Colonial picocyanobacteria (‘‘loose’’)a
Colonial picocyanobacteria (‘‘compact’’) a
Woronichinia spp.
Aphanothece parallelliformis Cronberg
Pseudanabaena limnetica (Lemmermann) Komárek
Anabaena spp. (mostly A. lemmermannii P. Richter)
Aphanizomenon sp.
Nodularia spumigena Mertens (diameter 11 and 9 mm, resp.)
Cryptophyta
Cryptophyceae
Hemiselmis virescens Droop
Plagioselmis prolonga Butcher (6–7 4 mm)
P. prolonga (8 4.5 mm)
Rhodomonas cf. baltica Karsten
Teleaulax amphioxeia (Conrad) Hill
T. acuta (Butcher) Hill
Dinophyta (Dinophyceae)
Prorocentrum minimum (Pavillard) Schiller
Dinophysis acuminata Claparéde and Lachmann
D. norvegica Claparéde and Lachmann
Gymnodinium simplex (Lohmann) Kofoid and Swezy
Gymnodinium cf. sanguineum Hirasaka
Gymnodinium sp. (45–55 mm 23–27 mm)
Gymnodiniales (diameter <10 mm)
Gymnodiniales (diameter 10–15 mm)
Gymnodiniales (diameter 20–25 mm)
Gyrodinium spp. (10–15 mm 7–10 mm)
Gyrodinium spp. (25–35 mm 18–23 mm)
Heterocapsa rotundata (Lohmann) Hansen
Heterocapsa triquetra (Ehrenberg) Stein
Lingulodinium cf. polyedrum (Stein) Dodge
Peridiniales spp. (diameter 10–15 mm)
Peridiniales spp.(diameter 15–20 mm)
Volume 1994
Volume 1997
0.30
0.88
0.88
6
0.19–0.51
0.81
0.77
6
1.03
6
117
87
313
40
160
260
12,180
28,000
113
10
35
53
612
117
238
1400
10,350
28,000
256
24,800
10,400
2000
100
960
580
820
1700
370
5270
228
14,100
1400
2700
Haptophyta
Prymnesiophyceae
Chrysochromulina spp. (2–4 mm) b
Chrysochromulina spp. (4–6 mm) c
Chrysochromulina spp. (>6 mm) d
14
60
133
Chrysophyta
Chrysophyceae
Uroglena/Lepidochrysis
Dinobryon faculiferum (Willén) Willén
Pseudopedinella tricostata (Rouchijajnen) Thomsen
Apedinella radians (Lohmann) Campbell
73
50
34
268
Diatomophyceae
Attheya septentrionalis (Østrup) Crawford
Chaetoceros danicus P.T.Cleve
C. impressus K.G. Jensen and Moestrup
C. throndsenii (Marino, Montresor and Zingone) Marino, Montresor and Zingone
Coscinodiscus granii Gough
Cyclotella choctawhatcheeana Prasad
Thalassiosira baltica (Grunow) Ostenfeld
117
87
171
900
74,500
108
14
60
230
50
96
2050
3500
44
71,400
106
62,800
S. Hajdu et al. / Harmful Algae 6 (2007) 189–205
193
Table 1 (Continued )
Taxon
Nitzschia sp. (40 mm 7 mm)
Nitzschia longissima (Brébisson) Ralfs
N. paleacea (Grunow) Grunow
Pseudonitzschia sp.
Volume 1994
Volume 1997
773
455
149
369
Euglenophyta
Euglenophyceae
Eutreptiella spp.
500
430
Chlorophyta
Prasinophyceae (Micromonadophyceae)
Pyramimonas spp. (7 mm 5 mm and 5 mm 4 mm, respectively)
Pyramimonas spp. (9 mm 7 mm)
110
270
77
Chlorophyceae
cf. Chlamydomonas sp.
Monoraphidium contortum (Thuret) Komárková-Legnerová
Monoraphidium cf. komarkovae Nygaard
Oocystis spp.
Planctonema lauterbornii Schmidle
Ciliophora
Litostomatea
Mesodinium rubrum (Lohmann) Hamburger and Buddenbrock
diameter 14–16 mm
diameter 20–27 mm
diameter 27–33 mm
diameter 33–37 mm
diameter 37–45 mm
Others
Unidentified flagellates
2–3 mm (sphere)
3–5 mm (ellipsoid)
5–7 mm (ellipsoid)
7–10 mm (ellipsoid)
10–15 mm (ellipsoid)
Miscellaneous
3–5 mm (sphere)
10–15 mm (sphere)
5–7 mm (ellipsoid)
7–10 mm (ellipsoid)
23
255
200
2200
7000
14,100
8
34
12
175
95
2200
7000
14,100
22,400
33,500
36
92
220
517
21
536
81
265
a
Included mainly Cyanodictyon balticum Cronberg, C. imperfectum Cronberg and Weibull, C. planctonicum Meyer, but also Cyanonephron
styloides Hickel, Aphanothece bachmanii Komarková-Legenerová and Cronberg, Aphanocapsa delicatissima W. and G. S. West, Snowella
septentrionalis Komárek and Hindák and Lemmermaniella pallida (Lemmermann) Geitler.
b
In 1994 included C. minor Parke et Manton, C. brachycylindra Hällfors et Thomsen.
c
In 1994 included C. simplex Estep, Davis, Hargraves et Sieburth em. Birkhead et Pienaar, C. ephippium Parke et Manton, C. fragaria Eikrem et
Edwardsen, C. scutellum Eikrem et Moestrup and C. cymbium Leadbeater et Manton.
d
In 1994 included C. polylepis Manton et Parke, C. hirta Manton, C. ericina Parke et Manton.
with standard mean volumes from the ongoing monitor
programme on a nearby station or from own measurements of 25 cells. Cell volumes were calculated from
geometric shapes and formulas recommended by the
Baltic Monitoring Programme (HELCOM, 1988).
Carbon biomass was estimated with the equations of
Menden-Deuer and Lessard (2000) and used to compare
phytoplankton community compositions.
Species identification of Chrysochromulina was
made on a sample collected on 29 July 1994
preserved with 2% osmium tetroxide (nine drops to
100-ml sample) and concentrated by centrifugation.
Drops of material were transferred to Formvar/
carbon-coated copper grids, dried, rinsed in distilled
water, dried again and shadowcast with chromium
and examined in a JEM 100SX electron microscope
194
S. Hajdu et al. / Harmful Algae 6 (2007) 189–205
Table 2
Dimensions of the colony-forming picocyanobacteria
Group
N
Cell length (mean 1 S.D.)
Cell width (mean 1 S.D.)
Cell density (mean 1 S.D.)
Compact colonies
Loose colonies
A. parallelliformis
188
97
48
1.35 0.3
1.42 0.24
1.65 0.29
0.94 0.18
0.94 0.16
1.0 0.24
0.306 0.189
0.087 0.036
0.336 0.128
Cell length (mm), cell width (mm) and cell density (cells mm2).
by Professor Ø. Moestrup at the University of
Copenhagen.
The Baltic Sea Aphanizomenon, previously reported
as A. flos-aquae (Linné) Ralfs, is here called sp. due to
taxonomic uncertainties (Janson et al., 1994), although it
has been suggested to be a genotype of the freshwater A.
flos-aquae (Laamanen et al., 2002). This paper follows
the nomenclature and system of Hällfors (2004).
Diel changes in vertical distribution are estimated
from the weighed mean depth (WMD) of individual
populations (Pearre, 1973):
P
ni d i
WMD ¼ P
ni
(1)
where ni is cell number per litre seawater at depth di.
Fig. 2. Epiflourescence images recorded by video camera showing the three dominating types of colonial picocyanobacteria observed in the samples
in August 1997 at station EGB: (a) ‘‘compact’’ colony, (b) ‘‘loose’’ colony and (c) Aphanothece parallelliformis with cells organized in rows.
Bars = 10 mm.
S. Hajdu et al. / Harmful Algae 6 (2007) 189–205
Fig. 3. Phytoplankton biomass (incl. picocyanobacteria) (mg C l1) in
(a) integrated (0–20 m) and discrete water samples (b) surface and (c)
15 m in 24–29 July 1994 at the station WGB. DINO: Dinophyceae
(autotrophic dinoflagellates); PRYM: Prymnesiophyceae (Chrysochromulina spp.); UNID < 15 mm: unidentified nanoflagellates
(mostly Chrysophyceae); OTHERS: Pyramimonas spp. (Chlorophyceae), P. prolonga, T. acuta, T. amphioxeia (Cryptophyceae) and E.
gymnastica (Euglenophyceae) as most important; CYAN (fil.): filamentous cyanobacteria; CYAN (p.col.): colony-forming picocyanobacteria; CYAN (p.s.): single-celled picocyanobacteria.
3. Results
3.1. Western Gotland Basin, 1994
The weather during the sampling period was calm
and sunny, with wind speeds mostly below 6 m s1. The
195
water temperature was exceptionally high and occasionally reached 25 8C in the top surface layer in
daytime. The 1% irradiance level occurred at 10 m
depth from 24 to 26 July and at 15 m depth on 27 July,
corresponding to 25 and 5.7 mmol quanta m2 s1.
Dissolved inorganic phosphorus (DIP) and nitrogen
(DIN) concentrations were low in the mixed layer
(below 0.05 and 0.4 mM, respectively) except towards
the end of the bloom when the ammonium concentration increased (from 0.11 to 0.27 mM). Below the
seasonal pycnocline, DIP concentrations increased
sharply to 0.2–0.5 mM while DIN concentrations were
only moderately higher (<0.7 mM). Salinity ranged
from 6.3 to 6.8 and the chlorophyll a from 1.5 to
6.5 mg l1 in the mixed layer, with a deep maximum
(6.5 mg l1) at 15 m on 24 July. The hepatotoxic
Nodularia spumigena just started to accumulate on the
surface when we arrived at the sampling site.
Filamentous cyanobacteria (mainly N. spumigena
and Aphanizomenon sp.) and dinoflagellates dominated
the phytoplankton community (as carbon biomass,
Fig. 3a, Table 3). The biomass of N. spumigena varied
between 31 and 34 mg C l1. The biomass of unidentified flagellates was very low, and colony-forming
picocyanobacteria constituted less than 1% of the total
phytoplankton carbon (Table 3). The phytoplankton
communities differed considerably between the surface
and in the seasonal pycnocline (15 m depth) (Fig. 3b
and c). Filamentous nitrogen-fixing cyanobacteria
decreased at the surface towards the end of the cruise
(Fig. 3b), while the biomass of Prymnesiophyceae
(Chrysochromulina spp.) and Dinophyceae (Dinophysis
norvegica) increased in the seasonal pycnocline
(Fig. 3c).
Depth distributions of the occurring taxa, mostly
toxic and potentially toxic species, differed considerably. Most of the single-celled picocyanobacteria were
found above the seasonal pycnocline, with abundances
varying between 1.7 and 4 108 cells l1 (Fig. 4a). N.
spumigena population accumulated mainly in the top
5 m of the water mass, while Aphanizomenon sp. was
found in the whole trophogenic layer and had bimodal
vertical distributions (Fig. 4b and c). Their weighted
mean depth (WMD) also showed distinct differences
(Table 4). Anabaena spp. (mostly Anabaena lemmermannii P. Richter) also had bimodal abundance depth
distributions with the deeper peak somewhat shallower
compared to Aphanizomenon sp. (Fig. 4d, Table 4). D.
norvegica was abundant in the seasonal pycnocline (18–
34 103 cells l1), but virtually absent above 10 m
depth (Fig. 4e, Table 4). It migrated upward in the
morning and downward in the afternoon, but only
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S. Hajdu et al. / Harmful Algae 6 (2007) 189–205
Table 3
Cyanobacterial and total phytoplankton biomass (mg C l1) in 0–20 m samples at the stations WGB (July 1994) and EGB (August 1997) and % of
total phytoplankton biomass in brackets
Date
Western Gotland Basin (WGB)
24 July (day)
CYAN (fil.)
CYAN (p.col)
CYAN (p.s.)
Total phyto
78 (42)
1 (0.5)
20 (11)
185
26 July (day)
88 (52)
1 (0.5)
11 (6)
171
Eastern Gotland Basin (EGB)
29 July (day)
41 (37)
1 (0.5)
10 (9)
109
8 August (day)
34 (22)
41 (26)
35 (23)
157
9 August (night 1)
48 (28)
57 (34)
25 (15)
167
9 August (day)
63 (32)
57 (29)
27 (14)
197
9 August (night 2)
44 (26)
51 (31)
35 (21)
168
CYAN (fil.): filamentous cyanobacteria; CYAN (p.col.): colony-forming picocyanobacteria; CYAN (p.s.): single-celled picocyanobacteria; Total
phyto.: total phytoplankton including picocyanobacteria.
between 10 and 20 m (abundance maximum was at 17
and 12 m depth at 3 and 9 a.m., respectively, and at 15
and 20 m depth at 3 and 9 p.m., respectively).
Chrysochromulina cells <6 mm resided above the
seasonal pycnocline, with a tendency to be less
abundant in the near surface layer (Fig. 4f, Table 4).
Their abundance increased during the study from 2.2 to
3.7 106 cells l1 in integrated samples. At the end of
the cruise, Chrysochromulina cells >6 mm (dominated
by the potentially toxic C. polylepis) had a pronounced
maximum at 12 m depth (1.2 106 cells l1, Fig. 4g).
Among other nanoflagellates, Eutreptiella gymnastica
occurred mostly above 15 m depth, with maxima
around 6 m, while small cryptophycean species
(Plagioselmis prolonga, Teleaulax amphioxeia and T.
acuta) had their maxima at 20 m depth (altogether
1.4 106 cells l1, data not shown).
Altogether, 10 Chrysochromulina species were
identified from the sample collected on 29 July
(Table 1). Nine of them are known from the area
(Hajdu et al., 1996); C. cymbium is new for the northern
Baltic Sea proper.
3.2. Eastern Gotland Basin, 1997
Weather conditions in early August 1997 were
similar to those in 1994. The mixed layer was 17–18 m
deep, with rather uniform temperatures between 19 and
21 8C and a strong seasonal pycnocline. The 1%
irradiance level was between 12 and 14 m depth. DIP
and DIN concentrations were low in the mixed layer
(below 0.04 and 0.5 mM, respectively) and increased to
0.3 and 0.7 mM at 40 m depth. Salinity ranged from 6.8
to 7.0 above 20 m depth and was slightly higher (about
7.1) between 20 and 40 m; there was a deep chlorophyll
maximum at 12–15 m depth (2–3 mg l1 chlorophyll a).
Cyanobacteria and unidentified nanoflagellates
<15 mm (mostly chrysophycean taxa) dominated the
phytoplankton community (as carbon biomass, Fig. 5).
Most of the total phytoplankton and the single-celled
and colony-forming picocyanobacteria biomass were
found above the seasonal pycnocline (Fig. 6a–c).
Picocyanobacteria contributed a large part (40–50%)
of the total phytoplankton carbon biomass above 20 m
both day and night (Table 3). About one third of the total
phytoplankton carbon was in the form of colonyforming picocyanobacteria (Table 3), and included
several Chroococcal taxa whose cells were embedded in
mucilage (Table 1). Colonies with long-oval cells
organised in ‘‘rows’’ (Fig. 2c) belong to a newly
described species A. parallelliformis Cronberg (Cronberg, 2003). Compact and loose colonies were mostly
species of the genus Cyanodiction: C. imperfectum, C.
planctonicum and the newly described C. balticum
Cronberg (Cronberg, 2003). Other species (Table 1)
occurred only in low numbers.
Filamentous cyanobacteria biomass was lower
compared to 1994 (Table 3), especially due to
considerably lower biomass of N. spumigena
(0.5 mg C l1 compared to 34 mg C l1).
Vertical distributions of the most important species
are shown in Fig. 7. Colony-forming picocyanobacteria
resided mainly above 20 m depth and colonies of
Aphanothece were less common, while compact and
loose colonies were equally common (Fig. 7a). N.
spumigena and A. lemmermannii occurred mainly
above 5 m depth, but N. spumigena filaments were
occasionally observed deeper, especially at night
(Fig. 7b). In contrast, the depth distribution of
Aphanizomenon sp. was centred around 10 m depth,
with few cells at the surface or below the seasonal
pycnocline (Fig. 7c, Table 4). D. norvegica was
confined between 10 and 20 m, both day and night,
with high cell concentrations found in thin layers
(Fig. 7d and e; Table 4). The autotrophic ciliate
Mesodinium rubrum and the nanoflagellate E. gymnastica differed in their diurnal vertical distributions, with
high cell numbers in or below the seasonal pycnocline at
b
a
16.2
12.7
17.0
9.9
7.7
17.7
1.8
1.7
night (Fig. 7f and g; Table 4). Cryptophycean flagellates
were found in high numbers down to 30 m depth
(Fig. 7h–j), with distinct inter-specific differences in
vertical distribution (Table 4). Chrysochromulina spp.
were less abundant (ten to several hundred thousand
cells l1) in 1997 than in 1994, with no significant
differences in vertical distribution between size groups.
Size group >6 mm was, however, dominated by larger
cells compared to 1994 (Table 1). The small diatom,
Chaetoceros throndsenii occurred mainly near the
surface (Table 4), with maximum abundance of
1.2 106 cells l1.
14.9
20.5
20.9
–
–
–
4.2
–
–
–
9.9
–
–
–
9.1
–
–
–
23.1
12.0
18.0
16.7
5.7
14.9
–: No data or very low abundances.
a
The missing 0 m sample is important for the depth distribution of the species.
b
0–20 m is irrelevant depth interval for Teleaulax spp., since a large part of the biomass is found below 20 m.
7.0
6.2
7.8
a
5–40
0–40
0–40
1997
9 August 0:30 h
9 August 12:00 h
9 August 23:00 h
10.8
10.1
14.3
1.6
2.1
–
–
–
16.7
16.0
15.3
7.5
6.0
7.3
–
–
–
9.5
–
–
–
10.1
8.6
6.0
10.9
7.0
7.4
5.7
6.7
7.7
0–20
0–20
0–20
0–20
24 July
26 July
29 July
8 August (day)
1994
8.9
6.8
8.3
10.7
3.5
1.8
3.0
3.1
7.0
3.8
8.0
2.3
16.8
14.1
15.2
14.9
Chrysochromulina
<6 mm
Chrysochromulina
spp. >6 mm
D. norvegica
Anabaena
N. spumigena
Aphanizomenon
Time
Depth
(m)
197
4. Discussion
Year
Table 4
Diel changes in vertical distribution calculated as weighted mean depth (WMD) of individual populations
Hemiselmis
3–5 mm
Plagioselmis
5–7 mm
Teleaulax
7–15 mm
M. rubrum
E. gymnastica
C. throndsenii
S. Hajdu et al. / Harmful Algae 6 (2007) 189–205
Determination of the vertical distribution and
migration patterns of phytoplankton is easily biased
by sampling errors. Phytoplankton may accumulate in
relatively thin layers (Lindholm, 1992) making it
difficult to resolve the real vertical distribution.
Additional factors which may introduce bias are water
exchange (due to turbulent mixing and/or horizontal
advection of the water mass), disruption of vertical
structures by strong wind mixing and patchiness. The
depth distributions of D. norvegica from 1994 and 1997
show the need for high depth resolution to accurately
resolve its vertical abundance pattern. However, the
general vertical distribution patterns of most species
were similar in both years despite differences in
sampling intervals and are in agreement with earlier
studies (see below).
4.1. Community composition
Low concentrations of inorganic nitrogen in the
surface layer, a strong seasonal pycnocline and warm,
sunny and calm weather, as in 1994 and 1997, favour the
formation of Baltic Sea cyanobacterial surface accumulations (Wasmund, 1997), as well as the build up of
phytoplankton concentrations near the seasonal pycnocline (e.g. Carpenter et al., 1995). Total phytoplankton
carbon biomass, species composition (0–20 m) and
vertical distribution of species were similar between
1994 and 1997, but the proportion of the dominating
species, as carbon biomass, differed considerably. One
reason may be differences in nutrient availability during
different stages of the cyanobacterial bloom. During
intensive cyanobacterial growth, phosphorus limitation
may occur (Walve, 2002), which favours species with
abilities to use nutrient resources at depth or have
alternative nutritional modes (e.g. mixo- and phagotrophy) and species producing toxin at nutrient limitation
198
S. Hajdu et al. / Harmful Algae 6 (2007) 189–205
Fig. 4. Vertical distribution of dominating species in July 1994 at the station WGB. (a) Picocyanobacteria, single-cells, (b) N. spumigena, (c) Aphanizomenon sp., (d) Anabaena spp., (e) D. norvegica,
(f) Chrysochromulina spp. <6 mm and (g) Chrysochromulina spp. >6 mm (filamentous species counted as meters per litre (m l1), others as cells l1) (different scales).
S. Hajdu et al. / Harmful Algae 6 (2007) 189–205
Fig. 5. Phytoplankton biomass (incl. picocyanobacteria) (mg C l1) in
the integrated (0–20 m) day sample on 8 August 1997 at the station
EGB (abbreviations as in Fig. 3).
(Granéli et al., 1995; Legrand et al., 1996; Johansson and
Granéli, 1999; Hajdu, 2002). During the decomposition
stage of a bloom nanoflagellates, small diatoms and
single-celled and colony-forming picocyanobacteria, i.e.
efficient competitors for nutrients, are likely to be
favoured. Phytoplankton community structures may
therefore be highly influenced by the N2-fixing cyanobacteria blooms. In 1994, the relative contribution of the
different cyanobacterial groups to the total phytoplankton carbon (Table 3) and the relative proportions of
diazotrophic species (as carbon biomass, N. spumigena,
55% and Aphanizomenon sp., 44%) were very similar to
those found in intensive blooms in the northern Baltic
proper (Niemistö et al., 1989; Kononen et al., 1998). At
the same time, only a few potentially toxic, motile and
mixotrophic species (D. norvegica and Chrysochromulina spp. >6 mm) were abundant near the seasonal
pycnocline. In 1997, the fraction of cyanobacteria present
in the total phytoplankton carbon biomass was con-
199
siderably higher than in 1994 (Table 3), primarily due to
the much higher biomass of colony-forming picocyanobacteria. It is not clear whether their higher biomass in
1997 was due to a late bloom stage, inter-annual
variability or to other factors. The amount of picocyanobacteria may, however, vary considerably between
years and summer months (Albertano et al., 1997). Data
from the Landsort Deep (NW Baltic proper) in Larsson
et al. (2001) indicate that we actually sampled close to the
bloom peak in 1994 and at a considerably later stage in
1997. Data from this station show also that colonyforming picocyanobacteria increased following the
filamentous cyanobacteria peak in both years, and the
total carbon biomass of the colony-forming species was
much higher in 1997 than in 1994 (Hajdu, unpublished
data; Larsson et al., 1998). These data suggest that the
differences between 1994 and 1997 may be related to
successional stage, and perhaps inter-annual variability.
Stal et al. (1999, 2003) suggested that picocyanobacteria
may be nitrogen-limited and, consequently, may be
favoured by fixed nitrogen released from diazotrophs.
We found that aggregates of N. spumigena were
highly colonised by bacteria, the diatom Nitzschia
paleacea and microzooplankton in 1997, in agreement
with Gabrielson and Hamel (1985) and Hoppe (1981)
who observed a rapid colonisation and decomposition
of N. spumigena filaments. The decomposing bloom
may have favoured the development of unidentified
nanoflagellates and picoplankton and the high abundance of the small diatom C. throndsenii (1.2 106 cells l1 near the surface). Many nanoflagellates
are able to ingest bacteria and those with high cell
surface to volume ratio may have benefited from
nutrients released during decomposition.
We conclude that considerable differences in
dominating functional groups may occur between the
growth and the decomposition phase of a cyanobacterial
Fig. 6. Vertical distribution of single-celled (CYAN p.s.) and colony-forming (CYAN p.col.) picocyanobacteria and total phytoplankton biomass
(incl. picocyanobacteria) in mg C l1 on 9 August 1997 at station EGB. (a) Night 1 = 0:30 h, (b) day = 12:00 h and (c) night 2 = 23:00 h.
200
S. Hajdu et al. / Harmful Algae 6 (2007) 189–205
Fig. 7. Vertical distribution of different species during day and night on 8 and 9 August 1997 at the station EGB. (a) Colonial picocyanobacteria
(103 colonies l1) on 9 August (day at 12:00 h); (b and c) N. spumigena and Aphanizomenon sp. (meters per litre, m l1) on 9 August; (d and e) D.
norvegica (103 cells l1) on 8 and 9 August (different scales); (f and g) M. rubrum and E. gymnastica and (h, i and j) the cryptophyceans Hemiselmis
(3–5 mm), Plagioselmis (5–7 mm) and Teleaulax (7–15 mm) (103 cells l1) on 9 August (night 1 = 00:30 h; day = 12:00 h; night 2 = 23:00 h;
different scales).
bloom and that the phytoplankton community composition in 1994 likely represent the growth phase, and in
1997 the decomposition stage of a Nodularia bloom.
4.2. Single-celled and colony-forming
picocyanobacteria
Single-celled picocyanobacteria were important in
both years (Table 3). Maximum abundances (4 108
and 6 108 cells l1 in 1994 and 1997, respectively)
were similar to earlier studies in the northern Baltic
(Kuosa, 1988, 1990b; Kononen et al., 1998), but lower
by 1–2 orders of magnitude than reported from the
central Baltic (Albertano et al., 1996). Single-celled
picocyanobacteria grow fast (Kuosa, 1988; Stal et al.,
1999), are sensitive to grazing (Kononen et al., 1998)
and may respond rapidly to upwelling (Kuosa, 1988).
Thus, pronounced spatial and temporal variability may
result. The vertical distribution patterns of single-celled
picocyanobacteria agreed with Kuosa’s (1988) results.
He found them grow fast (m = 1.09 day1) even at 1%
of surface light intensity. Adaptation to low light may be
the prime reason for their relatively high abundance
near the seasonal pycnocline.
Colony-forming species occurred sparsely in 1994,
but in high numbers in 1997. We found a considerably
higher abundance of colonies in 1997 (2–2.5 106 l1
compared to 2.2–4.3 104 l1) than Albertano et al.
(1997) (Middle Bank, Cental Baltic in August 1995),
the only Baltic Sea study that reports colony-forming
picocyanobacteria abundance. The amount of colonyforming picocyanobacteria may vary considerably
between summer months and between years (Albertano
et al., 1997; Hajdu unpublished data; Larsson et al.,
1998). High abundance of colony-forming picocyanobacteria may result from an effective nutrient uptake
S. Hajdu et al. / Harmful Algae 6 (2007) 189–205
due to their small size (Probyn et al., 1990), and reduced
sinking velocity and low grazing pressure due to their
large mucilaginous sheaths (Walsby and Reynolds,
1980; Pearl, 1988).
Despite higher picocyanobacteria abundances, our
total carbon biomass (single and colony-forming) was
considerably lower than the total biomass reported by
Albertano et al. (1997) (76–86 mg C l1 compared to
266 mg C l1). This difference may at least partly
depend on inclusion of larger cells (maximum diameter
3 mm compared 2 mm) and the use of a higher carbon
conversion factor (0.294 pg C cell1 compared to 0.22–
0.24 pg C cell1) by Albertano et al. (1997). According
to their Table IV and VII, 24% of their largest cells
(Class c) in August had an average cell volume of
2.9 1.6 mm3 compared to our highest and considerably less common average cell volume of 1.03 mm3
(A. parallelliformis).
4.3. Vertical distribution of nano- and
microplankton
DIP and DIN concentrations remained low in the
mixed layer during both sampling periods. Nutrients for
phytoplankton growth were probably obtained from
regenerative processes or internal storage (Larsson
et al., 2001; Walve, 2002) and/or from heterotrophic
nutrition. Substantial amounts of DIP were, however,
present below the seasonal pycnocline.
Co-existing species in stratified and nutrient poor
environments have different survival strategies. Many
phytoplankton flagellates are able to rapidly swim
vertically, to satisfy their light as well as nutrient
demands (e.g. Olsson and Granéli, 1991; Passow, 1991).
Mixotrophic species adapted to low light levels,
however, do not necessarily need to migrate, but can
stay near the seasonal pycnocline during long periods
and form distinct abundance peaks at depth (Lindholm,
1992 and references therein; Carpenter et al., 1995).
Vertical niche-separation of co-occurring phytoplankton species has also been documented both in limnetic
and marine waters (e.g. Sommer, 1982; Taylor and
Pollingher, 1987; Olli et al., 1998; Olli and Seppälä,
2001) and is likely essential in maintaining vertical
structures in phytoplankton communities.
In both years, we observed clear species-specific
patterns in the vertical distribution (Table 4) of several
species. Despite their seemingly similar requirements
for bloom development (Wasmund, 1997), the vertical
distribution of the co-occurring nitrogen-fixing cyanobacteria (N. spumigena, Aphanizomenon sp. and
Anabaena spp.) differed considerably, as also found
201
by Niemistö et al. (1989) and Kononen et al. (1998). N.
spumigena preferred surface water (WMD above 3 m),
while Aphanizomenon sp. had a maximum around 10 m
depth (WMD between 7 and 14 m with very small
diurnal differences), in agreement with earlier studies
(e.g. Walsby et al., 1995; Heiskanen and Olli, 1996;
Kononen et al., 1998). The consistent differences in
vertical distribution patterns indicate niche-separation
between the two species. N. spumigena is able to grow
at low DIP concentration due to its affinity to low
phosphorus level (Ks 0.016 mM, Wallström et al.,
1992). High temperature and irradiation stimulate its
growth (Wasmund, 1997). Thus, living near the surface
is advantageous for N. spumigena. In contrast,
Aphanizomenon sp. has a wide temperature tolerance
(Wasmund, 1997), stores phosphorus (Larsson et al.,
2001) and grows at low light (De Nobel et al., 1998)
consistent with its observed vertical distribution and
presence during the entire season.
D. norvegica cells occurred in high numbers in both
years, but only in a thin layer at and below the 1%
irradiance level, and exhibited very limited diurnal
migration, as shown also by Carpenter et al. (1995) and
Gisselson et al. (2002). According to Gisselson et al.
(2002), photosynthesis supports a low Dinophysis growth
rate (m = 0.10–0.17 day1) in the Baltic Sea seasonal
pycnocline, heterotrophic nutrition is needed for higher
growth rates (m = up to 0.4 day1). The alloxanthin
content (a carotenoid typical of cryptophytes) of the
Baltic D. norvegica indicates adaptation to the low light
at depth (Meyer-Harms and Pollehne, 1998). Janson
(2004) has recently shown that in the Baltic D. norvegica
plastids are likely newly acquired from the free-living
Teleaulax amphioxeia, a cryptophycean species, which in
our study co-occurred with D. norvegica below the 1%
irradiance level. The consistent depth distribution
patterns irrespective of the seasonal pycnocline depth
suggest light determines the vertical distribution of D.
norvegica. Ingestion of Teleaulax may be an adaptation
to low light that sustains a higher heterotrophic growth
rate. Other cryptophycean species, which had their
maximum abundance between 10 and 20 m, could also
serve as food resources.
Chrysochromulina spp. were also abundant and
unevenly distributed with depth, especially in 1994.
Abundances of Chrysochromulina spp. up to several
million cells per litre are not unusual in the Baltic Sea
when water temperature is above 13 8C and the water
mass is stratified (Hajdu et al., 1996; Hajdu, 1997;
Kononen et al., 1998). High subsurface cell concentrations have also been noted (Kaas et al., 1991; Hajdu et al.,
1996; Kononen et al., 1998). Hajdu (2002) found that the
202
S. Hajdu et al. / Harmful Algae 6 (2007) 189–205
increase in Chrysochromulina spp. abundance in the
northern Baltic proper often coincided with the period of
intensive growth of diazotrophic cyanobacteria. During
the cyanobacteria bloom, phosphorus limitation may
occur (Walve, 2002), which can stimulate phagotrophy
and toxin production of Chrysochromulina spp. (e.g.
Legrand et al., 1996; Johansson and Granéli, 1999). Late
in the 1994 cruise, Chrysochromulina spp. >6 mm had a
pronounced maximum (1.2 106 cells l1) at 12 m
depth. Three species, C. polylepis (dominant), C. ericina
and C. hirta, were involved, according to the SEM
observations (Moestrup personal communication). All
three species can grow at low light intensities (Johnsen
et al., 1992; Rhodes and Burke, 1996), ingest detritus,
bacteria and nanoplankton (Nygaard and Tobiesen, 1993;
Jones et al., 1994; Hajdu, 2002), and are lightly grazed
(Jebram, 1980; Hansen et al., 1995). Low grazing
pressure led to higher Chrysochromulina abundance in
the study of Kononen et al. (1998). The abundance
increase of large Chrysochromulina (>6 mm) at the end
of the 1994 study may be due to regenerated nutrients and
increasing bacterial production (Larsson, unpublished
data), but the increase was too great to be explained by
population growth alone, and water exchange may have
contributed.
Several highly motile flagellates (M. rubrum, E.
gymnastica and small cryptophyceae species) occurred
in significant numbers below 15 m, especially at night,
suggesting their migration to depth to acquire nutrients.
Both M. rubrum and E. gymnastica seem to be well
adapted to exploit stratified waters. They have wide
temperature, salinity and light tolerances (Lindholm
and Mörk, 1990; Lindholm, 1995; Olli et al., 1996), are
fast swimmers (Throndsen, 1973; Lindholm, 1985) and
are able to migrate to layers rich in nutrients (Lindholm
and Mörk, 1990; Olli and Seppälä, 2001). When they
co-occur, competition between them is expected
because of their similar behaviour and requirements.
However, M. rubrum, at times, seems to exploit deeper
layers than E. gymnastica.
Little is known about vertical migration and nicheseparation of marine cryptophycean species. We found
Hemiselmis virescens and P. prolonga to have maximum
abundances of 0.3 and 5.6 105 cells l1, respectively,
below the seasonal pycnocline at night (Fig. 7h–i), while
Teleaulax spp. occurred there in high numbers (2.0–
2.8 105 cells l1 at 20–30 m depth) also during the
day, in contrast to the observation of Olli (1999) (Fig. 7j).
The high cryptophyceaen abundance below the seasonal
pycnocline suggests that these small nanoflagellates
exhibit deep nutrient retrieval behaviour, as shown in lake
populations (Salonen et al., 1984). The factors regulating
the species-specific distribution pattern are not clear from
our study, but light has been considered the most
important external factor regulating diurnal vertical
migration and vertical niche-separation of cryptophytes
(Sommer, 1982; references in Arvola et al., 1991). The
chloroplasts of H. virescens, P. prolonga and Teleaulax
spp. have different colours (Hill, 1992). This indicates
different pigment compositions and suggests different
light requirements, which would influence their vertical
distribution patterns. However, it is difficult to envisage
how these small species can perform diurnal vertical
migrations of considerable distance since, generally,
swimming speed is proportional to size (Throndsen,
1973; Sommer, 1988). Perhaps these observations are
biased by sinking cells and water exchange or are the
result of vertical migrations undertaken on less than a
diurnal basis.
We conclude that considerable differences in
dominant functional groups may occur between years
and/or cyanobacterial bloom stages, and that the vertical
segregation patterns of phytoplankton are speciesspecific, and appear to recur at similar environmental
conditions. The differences in day and night vertical
distributions of some species, e.g. small cryptophycean
flagellates, suggest migrational nutrient retrieval from
depth. Additional factors, e.g. phytoplankton heteroand mixotrophy, toxicity, pigmentation, etc., may
further contribute to a complex and dynamic vertical
structure in Baltic Sea pelagic food webs.
Acknowledgements
We would like to thank Prof. Ø. Moestrup
(Biological Institute, University of Copenhagen) for
his valuable help to identify Chrysochromulina spp. and
his assistant L. Haukrogh for preparing the shadowcast
preparations. Dr. G. Cronberg and Prof. J. Komárek
kindly helped identify some of the colony-forming
picocyanobacteria. Dr. G. Nausch, The Baltic Sea
Research Institute in Warnemünde (Germany) provided
data on nutrients, salinity and temperature for 1997. We
are grateful also to Prof. R. Elmgren and Dr. G. Ejdung
for valuable suggestions on the manuscript and for
linguistic corrections. We would like to thank R.
Mattsson (National Veterinary Institute, Uppsala,
Sweden) for toxicity analyses, Dr. B. Witek
(PHYTO-LaB, Poland) and M. Tirén for careful
phytoplankton analyses, and all technical personnel
involved in this study. Funding was provided by the
European Union (MAST III/BASYS program MAS3CT96-0058), the Swedish EPA’s Marine Monitoring
Program and the Swedish Foundation for Strategic
S. Hajdu et al. / Harmful Algae 6 (2007) 189–205
Environmental Research (MISTRA: SUCOZOMA).
[TS]
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