Download Strong small-scale temporal bacterial changes associated with the

Harmful Algae 4 (2005) 771–781
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Strong small-scale temporal bacterial changes associated
with the migrations of bloom-forming dinoflagellates
Josep M. Gasol *, Esther Garcés, Magda Vila
Departament de Biologia Marina i Oceanografia, Institut de Ciències del Mar-CMIMA, CSIC,
Pg. Marı́tim de la Barceloneta 37–49, E08003 Barcelona, Catalunya, Spain
Received 19 July 2004; received in revised form 5 November 2004; accepted 8 December 2004
Abstract
Bacterial abundances in nearshore Mediterranean planktonic environments tend to change seasonally by 10-fold. Strong
daily changes in bacterial abundance, at least as large as seasonal range, occurred in the presence of large dinoflagellate
populations performing daily vertical migrations. The daily variability of heterotrophic bacteria was associated with the daily
migrations of a bloom of Alexandrium taylori in La Fosca Bay, and Gymnodinium impudicum in Barcelona harbor. Bacterial
abundance in surface waters can change daily as much as from 1 106 to 5 106 with apparent net change rates of 0.24 h1. We
suggest that the migrating dinoflagellates create microstructures exploited by the bacteria, and that the large algal populations
(>106 cells l1) make this microstructure visible with conventional sampling protocols. We also show evidence of the link
between dinoflagellate abundance and relative bacterial activity in these waters, as measured by the percentage of bacteria with
high nucleic acid content.
# 2005 Elsevier B.V. All rights reserved.
Keywords: Alexandrium taylori; Bacteria; Gymnodinium impudicum; High-nucleic acid content bacteria; Daily cycles; Dinoflagellates; HAB
1. Introduction
Large research efforts are centered in the understanding of the ecology of algae that produce harmful
algal blooms (HABs), given their economic and
sanitary impact (Anderson, 1997; Smayda, 1997).
HAB events are thought to have strongly increased in
frequency and importance in recent years (Millie et al.,
* Corresponding author. Tel.: +3493 2309500;
fax: +3493 2309555.
E-mail address: [email protected] (J.M. Gasol).
1999; Garcés et al., 2000). Because of that, the
interactions between the HAB and zooplankton or
other components of the microbial food web are
commonly studied from the perspective of the HAB
species, i.e. whether zooplankton can impede the
development or terminate the bloom (e.g. Turner and
Tester, 1997; Calbet et al., 2003), or whether symbiotic
bacteria might affect development or the dynamics of
the dinoflagellates (e.g. cyst formation, Adachi et al.,
1999), or their toxin production (e.g. Doucette, 1995;
Doucette et al., 1998). While researchers have studied
the toxic effects of the dinoflagellates on zooplankton
1568-9883/$ – see front matter # 2005 Elsevier B.V. All rights reserved.
doi:10.1016/j.hal.2004.12.007
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J.M. Gasol et al. / Harmful Algae 4 (2005) 771–781
(i.e. Frangópulos et al., 2000; Calbet et al., 2002), not
much attention has been given to the effects of the HAB
species on the free-living bacteria in the same waters.
There are reasons to expect that the presence of
high dinoflagellate concentrations (a bloom can reach
106 cells l1) should affect the dynamics of the
bacterial community in the surrounding water, and
more so if the dinoflagellate performs daily vertical
migrations, as has commonly been shown (Eppley
et al., 1968; Kamykowski, 1995; Kamykowski et al.,
1998). Ecological factors promoted by the dinoflagellate that could influence the accompanying bacteria
are: (a) the possible grazing by dinoflagellates directly
on bacteria (Porter, 1988), or indirectly on bacterial
predators (i.e., HNF, ciliates, Bockstahler and Coats,
1993; Li et al., 1996), (b) the daily variations in the
organic matter and/or inorganic nutrient field caused
by the daily light forcing on the migrating dinoflagellate population, or (c) the degradation of the dead
or decaying algal cells (i.e. Vaqué et al., 1989). The
interactions of a bloom-forming dinoflagellate with
the autochthonous bacteria are not expected to be
different from those between normal non-blooming
algal populations and their bacterial neighbors, but
they may appear exaggerated because of the large
abundances reached by the blooming species. It is,
thus, appealing to think that the study of the
interactions between a dinoflagellate bloom and the
natural bacterioplankton community might typify the
processes commonly occurring between algae and
bacteria (i.e. Cole, 1982), and illustrate the relationship of an almost monospecific algal community and
its associated bacteria.
The aim of this study was to examine the spatial
and temporal changes in bacterial abundance during
bloom developments of HAB species in semi-enclosed
areas of the Mediterranean coast. We also studied the
daily changes in bacterial abundance, as they relate to
the daily changes in the dinoflagellates. We highlight
the fact that the common daily migrations of several
dinoflagellate species generate daily changes in
bacterial abundances much larger than the seasonal
changes in total community bacterial abundance. To
our knowledge, this is the first report in which such a
strong impact of the dinoflagellates on total bacterial
community is described. The reviews published to
date on the relationship between HABs and bacteria
(Doucette, 1995; Doucette et al., 1998) have not
presented any indications of these effects. When we
study the interactions between bloom-forming algae
and bacteria from the point of view of the
picoplankton, the presence and daily activities of
the migrating dinoflagellate are the most important
factor explaining the daily changes in bacterial
properties.
2. Material and methods
We studied two areas of the NW Mediterranean
coast, where we have described recurrent summer
blooms of the dinoflagellate species Alexandrium
taylori in La Fosca Bay (Garcés et al., 1999; 2000) and
Gymnodinium impudicum in the Barcelona harbor
(Vila et al., 2001). La Fosca bay (418510 N and 3880 E),
located on the Catalan Costa Brava, is approximately
rectangular, measuring 500 m 300 m with the
opening facing southeast. The average and maximum
depths are 3 and 7 m, respectively, with a fairly
uniform and gentle slope between 2 and 7 m (for
details, see Garcés et al., 1999). Tides are irrelevant in
this area of the Mediterranean, and the water was
calmed during the daily cycles studied here. During
the summer of 2000, three fixed stations over 1 m
depth, located 5 m away from the water break
point and separated approximately by 15 m were
sampled every 3–4 days at around GMT noon during
the bloom period (from June to September). The
samples were collected in 1 l bottles and brought
immediately to the laboratory, where they were
appropriately fixed (see below). When cell density
values were higher than 105 cells l1 (and water
discoloration occurred), sampling was carried out
every 2 h during a 24-h period in 1996 (August 19–20)
and in 2000 (July 25–26) to describe the daily changes
in the population of the dinoflagellate and bacteria.
These ‘‘daily’’ samplings were performed at the
central sampling station. Seawater samples for the
description of the vertical migration of G. impudicum
were collected in surface waters of the Barcelona
harbor in July 1998, when a bloom of the non toxic,
chain-forming, red tide dinoflagellate G. impudicum
was taking place. G. impudicum was studied in an
enclosed population inside two transparent Plexiglas
columns (6 cm of diameter and 2 m height). The
Plexiglas columns were filled with the natural water in
J.M. Gasol et al. / Harmful Algae 4 (2005) 771–781
the Barcelona harbor at 6:00 GMT, and placed in the
harbor so that the cells could freely migrate, but
advection was prevented. We started sampling at 8:00
GMT for the following 36 h, using a syringe with an
extension tube to sample inside the columns.
Chlorophyll a (Chl) was measured fluorometrically
with a turner design fluorometer after filtration of
60 ml of water through Whatman GF/F glass fibre
filters and extraction in 90% acetone. Phytoplankton
samples from La Fosca (150 ml) were preserved with
formaldehyde (1% final concentration, 1996) or Lugol
iodine (2000), while 25 ml samples from the Barcelona
harbor were taken in duplicate (outside the columns)
and preserved with Lugol iodine solution. In both
cases, an aliquot was settled overnight in 10–50 ml
counting chambers and an appropriate area of the
chamber then scanned for phytoplankton enumeration
at 63–400 magnification using a Leica–Leitz DM-IL
inverted microscope. Heterotrophic nanoflagellate
abundance was determined by epifluorescence microscopy after DAPI (Porter and Feig, 1980) staining of
20–30 ml, that had been filtered through 0.6 mm
Nuclepore filters and stained for 15 min with
5 mg ml1 of DAPI. For bacterial abundance and
relative size by flow cytometry, a 1.2 ml subsample was
preserved with 1% paraformaldehyde + 0.05% glutaraldehyde (final concentration), frozen in liquid
nitrogen and stored at 70 8C. The samples were
later unfrozen, stained for a few minutes with Syto13
(Molecular Probes) at 2.5 mM and run through a flow
cytometer. We used a Becton & Dickinson FACS
Calibur bench machine with a laser emitting at 488 nm.
Samples were run at low speed (approximately,
18 ml min1) and data were acquired in log mode
until around 10,000 events had been recorded. We
added 10 ml per sample of a 106 ml1 solution of
yellow–green 0.92 mm polysciences latex beads as an
internal standard. Bacteria were detected by their
signature in a plot of side scatter (SSC) versus green
fluorescence (FL1). The fixed samples were diluted (2–
4)x with MilliQ water, so that the rate of particle
passage was kept below 500 particles per second and
thus, coincidence could be avoided (Gasol and del
Giorgio, 2000). We used the percentage of high nucleic
acid content bacteria (%HNA) as a proxy for the
activity structure of the bacterial community. The
observation of Syto13-stained bacteria in the flow
cytometer allows the clear separation of two sub-
773
groups, that we have called HighNA and LowNA
bacteria (Gasol et al., 1999). Growing evidence
suggests that, at least in coastal environments, the
HNA bacteria are the active members of the community (Gasol et al., 1999; Servais et al., 1999, 2003;
Lebaron et al., 2001, 2002) while the LDNA bacteria
include ‘‘bacterial ghosts’’ and other inactive bacteria
(Gasol et al., 1999). Apparent net growth rates (ANG)
were computed as ANG = ln(1 + (C1 C0)/C0)/@t,
and apparent doubling times (T) as T = ln(2)/ANG,
where C1 and C0 are the final and initial concentrations
of bacteria in the time interval @t.
3. Results
3.1. Seasonal and spatial changes in bacterial
abundance
Bacterial abundance changed year-round by a
factor of 10 during the summer of 2000 in La Fosca
Bay (Fig. 1C), a typical representative site of NW
Mediterranean coastal waters. On a first glimpse,
bacterial abundance in La Fosca was not related to the
development of the recurrent bloom of A. taylori
during summer (N = 17, Pearson’s correlation
R = 0.51, P = 0.03) that typically occurs from June
to September (Fig. 1A, B and Garcés et al., 1998,
1999). This bloom, which reached cell concentrations
of up to 8000 cells ml1 in the summer of 2000,
produced chlorophyll a values as high as 45 mg l1,
while levels in early summer never exceeded
0.5 mg l1 (Fig. 1A). Similarly, there was no
significant relationship between the abundance of
heterotrophic nanoflagellates and that of bacteria
(N = 16, Pearson’s correlation R = 0.16, P = 0.54,
Fig. 1C). However, and perhaps surprisingly, an index
of bacterial activity, such as the (percentage) of HNA
cells, strongly covaried with dinoflagellate abundance
(Fig. 1B). Log Alexandrium abundance and %HNA
were well correlated (N = 19, Pearson’s R = 0.733,
P < 0.0005), indicating that, even though bacterial
abundance did not respond directly to the presence of
the dinoflagellate, the relative composition of the
community in terms of active and inactive cells did.
In the summer of 2000, we sampled three sites in La
Fosca Bay spaced a few meters apart to check whether
spatial variability was, or was not of the same order of
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J.M. Gasol et al. / Harmful Algae 4 (2005) 771–781
Fig. 1. Summer (June 2–September 9) cycle of: (A) chlorophyll a (*), (B) Alexandrium taylori cell densities (*) and %HNA bacteria ( ), and
(C) Total bacterial (*) and heterotrophic nanoflagellate (*) abundances in La Fosca Bay. The error bars for HNF abundance correspond to
counting errors. The arrow indicates the daily cycle described in Fig. 2.
magnitude as temporal variability. Neither for
Alexandrium nor bacterial abundance, was spatial
variability stronger than temporal variability (CVs of
41% for the spatial variability and 43–56% for the
temporal component in the dinoflagellate, and 19% for
the spatial and 19–29% for the temporal component
for bacteria). This indicated that whatever the spatial
structure measured in the bay, it was not more relevant
than the temporal factor in determining final
abundances.
3.2. Changes in bacterial abundance during daily
cycles
Daily changes in bacterial abundance varied as
much as five-fold in a single day in the summer of
J.M. Gasol et al. / Harmful Algae 4 (2005) 771–781
775
Fig. 2. Daily changes in Alexandrium taylori (*) cell abundance and (%) of HNA bacteria ( ) and total bacteria (*) in La Fosca Bay in August
1996 (left panels) and July 2000 (right panels). The black bar in the bottom indicates the approximate periods of darkness.
1996 (Fig. 2A). In the summer of 2000, the daily
change was slightly smaller (Fig. 2B). Apparent net
growth rates computed from the data showed that the
rates of variation of bacterial abundance throughout a
daily cycle were much larger than the seasonal rates
(Table 1). These rates converted to apparent doubling
times are of 2 days on average in Blanes Bay, 4–5
days in the seasonal study of La Fosca Bay, but as low
as 5 (1996) or 7 (2000) h in the daily cycles.
In 1998, we sampled a population of G. impudicum
that bloomed inside the Barcelona city harbor. This
species reached concentrations of up to 3500 cells
ml1, when we studied its daily variations (see also
Belviso et al., 2000). Gymnodinium migrated to the
bottom of the water column during the dark hours
and to the surface in the early morning (Fig. 3).
Bacteria, again, exhibited strong daily changes, with
rates of apparent change in the order of magnitude of
Table 1
Apparent net growth rates (h1) calculated in each sampled time intervals, along with the number of time intervals; the minimum and maximum
apparent net growth rates in each database; average of the absolute growth rates, and CVs of the rates of growth
N
Minimum
Maximum
Average
CV (%)
Bacteria
Seasonal Blanes Bay
Seasonal La Fosca (2000)
Daily study (1996)
Daily study (2000)
Barcelona harbor (1998)
157
18
15
7
13
0.077
0.011
0.488
0.139
0.158
0.049
0.014
0.248
0.155
0.173
0.012
0.006
0.128
0.098
0.072
11
29
35
45
35
Alexandrium
Seasonal La Fosca (2000)
Daily study (1996)
Daily study (2000)
30
15
9
0.107
1.912
0.809
0.168
2.129
1.021
0.031
0.669
0.509
29
37
40
Gymnodinium
Barcelona harbor (1998)
13
0.658
0.791
0.271
39
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J.M. Gasol et al. / Harmful Algae 4 (2005) 771–781
Fig. 3. In situ daily changes in Gymnodinium impudicum (*) and (percentage) of HNA bacteria ( ), and total bacteria (*) in Barcelona harbor,
summer 1998. The water was kept in 6 cm-diameter Plexiglas columns submerged in the harbor. The black bar in the bottom indicates the period
of darkness.
those detected in La Fosca Bay (Table 1). We
computed an average apparent doubling time of 9 h,
slightly lower than for bacteria in La Fosca. The
changes are important not only as changes in bacterial
abundances, but also in the relative activity of the
members of the community, as seen in the %HNA
values: bacteria were more active at night, when the
abundances were smaller (Fig. 3). Both in La Fosca
Bay and Barcelona harbor, bacterial numbers were
below the daily averages during the night and above
the daily averages during the day (Fig. 4), even though
the cycles were different.
(Figs. 2 and 3). The percentage of HNA bacteria,
however, varied daily as much as 20% in the 1996 La
Fosca cycle and, most commonly, 10–12% in 2000 in
La Fosca and 1998 in Barcelona harbor. There was an
inverse relationship between total bacterial abundance
and %HNA. The maximum %HNA bacteria was
observed either at the abundance minimum (in the
Barcelona harbor, Fig. 3) or a few hours before the
maximum bacterial abundances (in La Fosca Bay,
Fig. 2).
4. Discussion
3.3. Bacterial relative activity
While seasonally bacterial relative activity, as
measured by the %HNA bacteria, covaried with
dinoflagellate abundance (Fig. 1), this did not seem to
be the case when inspected at the daily variation scale
The seasonal changes in bacterial abundance in La
Fosca Bay are of the magnitude expected in non-tidal
coastal areas of the NW Mediterranean. Vaqué (1996)
studying Blanes Bay, approximately 20 km south of
La Fosca Bay, measured concentrations ranging from
J.M. Gasol et al. / Harmful Algae 4 (2005) 771–781
777
Fig. 4. Daily changes in dinoflagellate (A) and bacteria (B) Alexandrium taylori in La Fosca Bay in 1996 (*) and 2000 (*); and Gymnodinium
impudicum in the Barcelona city harbor in 1998 (~). The values are the ratio between the (log) of the concentration at a given time divided by the
daily-averaged concentration.
2 105 cells ml1 in winter up to maximal values of
1.4 106 ml1 in summer. The range was smaller in
the Medes Islands, approximately 20 km north of La
Fosca Bay: from 3 to 9 105 cells ml1 (Ribes et al.,
1999). Further North, in Villefranche-sur-mer, bacterial abundance ranged seasonally between 2 and
7 105 cells ml1 (Ferrier-Pagès and Rassoulzadegan, 1994). These values contrast with the daily
changes that we report: bacterial abundance can vary
as much as five-fold in a single day, as found in the
summer of 1996 (Fig. 2). These daily changes are of
the same magnitude as the changes measured yearround in the Medes Islands example cited above. They
are also more important than the small-scale temporal
changes recorded in Blanes Bay. Furthermore, the
doubling times calculated from the daily changes
(Table 1) would be unrealistic rates for coastal
bacterial communities, which normally double in
14–35 h (e.g. Ferrier-Pagès and Rassoulzadegan,
1994). The daily bacterial rates are, however, not
greater than those of Alexandrium, that had apparent
doubling times of around 1 h (Table 1).
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J.M. Gasol et al. / Harmful Algae 4 (2005) 771–781
We observed strong changes in bacterial relative
activity during the daily cycles. It is tempting to
suggest that the lower %HNA coinciding with the
maximal dinoflagellate cell density (e.g. Fig. 2) is
related to the demonstrated capability of some
dinoflagellates to produce antibacterial metabolites
that would prevent or retard bacterial attachment and
activity, particularly when in stationary growth (e.g.
Trick et al., 1984). However, the variations in %HNA
that we have identified can be related and/or be
confounded with the daily variations in specific
bacterial activity shown in NW Mediterranean waters
(where the (percentage) of nucleoid-containing cells
were lower in the morning than during the day; Gasol
et al., 1998), and also in the Baltic (Hagström et al.,
2001). With the limited information that we have, we
cannot discriminate whether the variations in %HNA
shown are related strictly to the daily bacterial cycle,
or to different types of bacteria (LowNA, HighNA)
that possibly appear/disappear with different daily
patterns (e.g. Zubkov et al., 2004).
It seems safe to assume that the daily changes in
bacterial abundance are related to the changes in
dinoflagellates, which perform daily vertical migrations from the surface sediment to surface waters
(Garcés et al., 1999), typical movements of blooming
dinoflagellates (e.g. Kamykowski et al., 1998). We can
divide the possible interactions between the migrating
dinoflagellates and bacteria into three types: (i) the
daily changes in bacterial abundance could be related
to daily variations in grazing pressure, (ii) to changes
in the attachment of bacteria to flagellates, or (iii) to
changes in the organic matter microenvironment
consequence of the light-dependence of dinoflagellate
photosynthesis. We explore these possibilities in the
following paragraphs.
(i) Relatively strong daily changes in bacterial
abundance have been associated with changing
protozoan predation pressure in some freshwater
environments (Psenner and Sommaruga, 1992),
but the changes reported in those studies are
below a 2x variation between the maximum and
minimum daily concentration (see also Riemann
et al., 1984). For HNF to have a role in the daily
changes of bacteria in La Fosca Bay, they should
be feeding at rates similar to those of growth (i.e.
Table 1). Thus, average hourly rates of 0.07–0.12
(Table 1), with HNF abundances around
1 103 ml1 (Fig. 1), would translate into
unrealistic (e.g. Vaqué et al., 1994) protozoan
grazing rates (for 1 106 bacteria and 1 103
HNF ml1, between 70 and 200 bacteria
HNF1 h1). While Legrand and Carlsson
(1998) concluded that there was no evidence
of bacterial phagocytosis in Alexandrium, feeding of dinoflagellates on small ciliates and
flagellates is commonly reported (Bockstahler
and Coats, 1993; Jacobson and Anderson, 1996).
While migrating dinoflagellates could be feeding
on the bacterivorous protists, it is not likely that
the reported daily changes in bacterial abundance
are related to that pattern, particularly because in
the 1996 daily cycle the bacterial maxima
followed the dinoflagellate maxima (Fig. 2); in
2000, the bacterial maxima preceded that of the
dinoflagellate; and in Barcelona harbor (Fig. 3)
bacteria and dinoflagellate seemed to covary.
(ii) The rates of apparent change reported in Table 1
are much greater than expected in a coastal
bacterial community (which tend to be in the
range of 0.02–0.05 h1). These rates would
represent extremely high bacterial productions,
and it is most likely that it is not that bacteria
were being produced and consumed at these high
rates, but that they appeared/disappeared from
surface waters (those sampled) at these rates.
Given that we measured bacterial abundances
with a flow cytometer and, consequently our
bacterial numbers represent the concentrations of
free-living bacteria, one could postulate that
daily attachment/unattachment patterns could
explain the data we report. However, the samples
were vortexed before counting so that any
bacteria loosely attached to particles would be
counted as free-living. Bacteria could, instead, be
attached to the surface of the migrating dinoflagellates and, thus, move in association with the
algal cells. If those bacteria were mainly LowNA,
this would explain the daily variation in %HNA
that we report. While a given algal cell has
commonly between 5 and 20 attached bacterial
cells when in full growth (Vaqué et al., 1989),
they might harbor as many as 100 cells per algae
in lab cultures (Doucette, 1985) or during
senescence (Rausch de Traubenberg and Soyer-
J.M. Gasol et al. / Harmful Algae 4 (2005) 771–781
Gobillard, 1990). Microscopical examination
yielded a value of 100 bacteria per Alexandrium in the La Fosca samples, but we could not
detect any relevant daily variations in this
number. Furthermore, not even a daily change
(attachment/unattachment) of 100 bacteria per
dinoflagellate per day could explain the apparent
bacterial net growth rates of Table 1: Alexandrium changed in La Fosca in 1996 from a
minimum of 10 to a maximum of 2000 cells ml1
(Fig. 2). This concentration would translate to a
value of 1.8 105 bacteria per mililiter, if we
assume that there were 100 bacteria per
flagellate. This value, scaled to the 106 bacteria
per mililiter present in the bay (Fig. 1), would
yield a rate of change of 0.014 h1, that does not
compare to the values of Table 1.
(iii) An alternative possibility that our observations
do not allow testing, is that a gyrotaxis-like
(Kessler, 1985) downward movement of the algal
population could potentially force bacterial cells
in the proximity of the algae to perform daily
migrations being transported with the flagellated
algae. The phenomenon of gyrotaxis has been
observed in cultures of A. taylori, and potentially
occurs in situ. At the population level, it has been
suggested that gyrotaxis may contribute to the
formation of shear-mediated cell clusters in
natural water columns that increase passive
descent velocities by 10-fold (Mitchell et al.,
1990). This phenomenon could help the downward movement of the cells in the water column
and contribute to the ‘‘disappearance’’ of
bacterial cells from surface.
(iv) We believe that the most likely explanation for
the daily changes in bacterial abundance associated with changes in the presence of migrating
dinoflagellates has to do with the varying
environmental conditions in the sampled surface
waters caused by the presence/absence of large
quantities of algal cells performing photosynthesis during light hours, and excreting DOC
during only a fragment of the daily cycle.
Dinoflagellates would thus create microenvironments, which would attract motile bacteria, as
suggested by Bell and Mitchell (1972) and later
demonstrated by Blackburn et al. (1998). Up to
70% of the bacteria can be motile in nearshore
779
marine environments (Grossart et al., 2001), and
the strong changes in the nutrient field created by
the moving dinoflagellates could be exploited by
these motile bacteria. Thus, the presence and
dynamics of a dinoflagellate bloom would simply
be an amplified view of the microheterogeneity at
the bacterial scale that different researchers, with
different techniques, have measured (Mitchell
and Furhman, 1989; Duarte and Vaqué, 1992). In
particular, Seymour et al. (2000) using a
pneumatically-operated multiple syringe system
have shown that 40-fold variations in bacterial
abundance can exist over distances as small as a
few milimeters. This microscale variability,
detectable only with special sampling devices,
would appear detectable to us if amplified by the
presence of the dinoflagellate, even if we had
sampled at an inappropriate scale (i.e., one 1.5 ml
sample). If the blooming dinoflagellates perform
strong vertical movements, this would simply
help create such heterogeneity.
Given that bloom dinoflagellates are common in the
Catalan Mediterranean coast (Vila et al., 2001), and that
there are no reasons to believe that it should be different
elsewhere, we believe that the strong daily changes in
bacterial abundance and activity reported could be general in coastal regions rich in natural or man-made,
semi-enclosed bays where low turbulence and high
nutrient levels facilitate dinoflagellate growth (i.e. Vila
et al., 2001). Our data suggest that any seasonal study on
the abundance and activity of coastal bacteria based on
weekly, or even daily samples, might be spurious if, as
shown, strong daily changes in bacterial abundance and
activity are expected to be associated with the development of dinoflagellate populations.
Acknowledgements
We thank the various people that have helped with
sampling and counting: Mercedes Masó, Maxi
Delgado, Daniel Arbós and Nagore Sampedro. Dolors
Vaqué let us access the database of Blanes bay,
organized the PICASSO workshop, and commented
on the manuscript. Ramon Massana also provided
helpful comments. Special thanks to J. Camp for
facilitating the field program. This study was funded
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J.M. Gasol et al. / Harmful Algae 4 (2005) 771–781
by the CIRIT grant FI/948003, the Departament de
Medi Ambient, Agència Catalana de l’Aigua (Generalitat de Catalunya); Integrated Action with France,
Picasso MEC-HF98-207, MATER CE-MAS3-CT960051, project MICRODIFF (DGICYT REN20012120/MAR) and project STRATEGY EVK3-CT2001-00046.
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