Crespo, BG, FG Figueiras, and S. Groom. Role of across

Limnol. Oceanogr., 52(6), 2007, 2668–2678
2007, by the American Society of Limnology and Oceanography, Inc.
E
Role of across-shelf currents in the dynamics of harmful dinoflagellate blooms in the
northwestern Iberian upwelling
B. G. Crespo1 and F. G. Figueiras
Instituto de Investigacións Mariñas, Consejo Superior de Investigaciones Cientı́ficas (CSIC), Eduardo Cabello 6, 36208
Vigo, Spain
S. Groom
Plymouth Marine Laboratory, Prospect Place, Plymouth PL1 3DH, United Kingdom
Abstract
Harmful dinoflagellate blooms are frequent in the Rı́as Baixas, which are made up of four open bays on the
northwest part of the Iberian Peninsula. The relationship between surface currents resulting from wind forcing
and the microplankton composition on the shelf offshore of the Rı́as Baixas was studied from May 2001 to April
2002. The aim was to assess the role of shelf currents in the dynamics of harmful dinoflagellate blooms in the Rı́as
Baixas shelf system. In summer, upwelling-favorable northerly winds forced a variable but persistent
southwestward flow on the shelf, which reverted to an onshore flow following the change to downwellingfavorable southwesterly winds in autumn. During winter and spring, there was an intense alongshore flow to the
north. Diatoms and dinoflagellates were common components of the microplankton community in summer.
Although diatoms increased their abundance during summer upwelling events, a dinoflagellate assemblage was
also present on the shelf. This dinoflagellate assemblage acquired higher importance during the intermediate
periods of upwelling relaxation and during the autumn downwelling in particular, when satellite images revealed
the accumulation of phytoplankton in a narrow band close to the coast. A dinoflagellate bloom of Prorocentrum
minimum (10,564 cells mL21) and Karenia cf. mikimotoi (3,022 cells mL21) developed in the interior section of the
Rı́a de Vigo coincident with the onshore flow imposed by the autumn downwelling. As these two species were
components of the dinoflagellate assemblage present on the shelf in summer, it is inferred that downwelling
caused their accumulation in the interior section of the Rı́a de Vigo.
Coastal upwelling systems, like many other coastal
regions of the world’s oceans, suffer from the occurrence
of harmful algal blooms (HABs), which impact the
structure and functioning of pelagic food webs and may
also cause important economic losses as well as problems of
public health (GEOHAB 2005). Research on HAB
dynamics in coastal zones has been motivated for many
years by the need to forecast blooms and mitigate the
impacts. Consequently, it is possible now to draw
a common picture for HAB dynamics in regions where
across-shelf and alongshore currents play a fundamental
role (Franks and Anderson 1992; Raine and McMahon
1 Corresponding
author ([email protected]).
Acknowledgments
We thank the captain and crew of the RV Mytilus, the
members of the Oceanography team at the Instituto de Investigacións Mariñas, and the Physical Oceanography Group at the
Universidade de Vigo for their help. We are also grateful to the
Área de Clima Marı́timo of the Spanish Agency Puertos del
Estado for providing meteorological and current data from the
Silleiro buoy. Special thanks are due to J. L. Cortijo, M. Gil-Coto,
and S. Piedracoba for their assistance. We acknowledge two
anonymous reviewers for their comments.
This work was funded by the Spanish DYBAGA project
(MAR99-1039-C02-01) and the EU HABILE project (EVK3-CT2001-00063). B.G.C. was supported by a CSIC-ESF I3P fellowship.
This is a contribution to the GEOHAB Core Research ProjectHABs in upwelling systems.
1998; Anderson et al. 2005). Frequently, HABs have an
impact on the coast following advection from offshore
(Tester and Steidinger 1997; Sackmann and Perry 2006).
Conversely, the impact normally vanishes when HABs are
removed from the coast by offshore currents (Tester et al.
1991). Alongshore currents, which essentially contribute to
the spread of HABs along the coast (Tester et al. 1991),
may also interact with across-shelf currents to intensify or
diminish their impact (Tester et al. 1991; Trainer et al. 2002;
Pitcher and Nelson 2006).
Despite this general role played by across-shelf and
alongshore currents in HAB dynamics, there are considerable differences between regions, not only due to the
specific environmental conditions and the different species
that cause HABs within each region, but also from the
interaction between coastal currents and physical singularities. Coastline features and permanent or transient
mesoscale physical structures, such as eddies, fronts,
filaments, and buoyant plumes, induce instabilities in the
general current pattern at diverse scales that can contribute
to an increase or reduction in the impact of HABs (Trainer
et al. 2002; Keafer et al. 2005; Pitcher and Nelson 2006).
Coastal embayments are especially relevant in this respect
because they are places with reduced exchange potential
where blooms and their effects can be intensified (Figueiras
et al. 1994; Keafer et al. 2005; Pitcher and Nelson 2006).
Therefore, understanding of the interactions between
coastal currents and HAB dynamics within each affected
region is important in order to develop or adapt existing
models and so improve forecasting.
2668
Harmful dinoflagellates and downwelling
2669
2002; Piedracoba et al. 2005) because of their almost
perpendicular orientation to the main coastline. Thus,
during upwelling, the circulation of the Rı́as Baixas consists
of a surface outflow that is compensated by the inflow of
coastal upwelling water at the bottom. During downwelling, the circulation reverses—shelf water enters the
Rı́as Baixas at the surface, and outflow occurs at the
bottom. Therefore, the Rı́as Baixas and the adjacent shelf
exchange properties and plankton populations continuously (Tilstone et al. 1994).
The Rı́as Baixas are especially prone to harmful
dinoflagellate blooms at the end of summer to beginning
of autumn, during the seasonal upwelling–downwelling
transition, when dinoflagellates are important components
of the local microplankton community (Margalef 1958;
Figueiras and Rı́os 1993; Crespo et al. 2006). Although
previous research has revealed a strong relationship
between downwelling and harmful dinoflagellate blooms
in the Rı́as Baixas (e.g., Fraga et al. 1988; Figueiras et al.
1994), the connection between HABs in the Rı́as Baixas
and the physical and biological processes that occur on
the shelf is still poorly understood. Here, we present the
results obtained from weekly sampling on the shelf offshore
of the Rı́a de Vigo and in the Rı́a de Vigo itself over a yearlong period. Microplankton abundance and composition
on the shelf were studied in combination with surface
currents induced by upwelling–downwelling with the aim of
establishing the role of across-shelf currents and microplankton succession on HAB dynamics in the Rı́as Baixas.
Methods
Fig. 1. Map of the NW Iberian margin showing (A) the
location of the four Rı́as Baixas and the position of the Silleiro
buoy (black diamond) where winds and surface currents were
recorded, and (B) the positions of the sampled stations at the shelf
and in the Rı́a de Vigo (black circles).
On the NW Iberian Peninsula, there are four bays, the
Rı́as Baixas of Galicia (Fig. 1A), where harmful dinoflagellate blooms are recurrent (Fraga et al. 1988; Figueiras
et al. 1994). The coastal circulation in this region is
determined by seasonal upwelling–downwelling cycles
(Wooster et al. 1976). Between spring and autumn,
northeasterly winds induce upwelling on the shelf and
force a surface circulation characterized by an equatorward
offshore flow (Wooster et al. 1976). The seasonal transition
to downwelling occurs at the beginning of autumn and
coincides with the rapid change to southwesterly winds
(Figueiras et al. 2002). During winter, the coastal circulation is dominated by the presence of the Iberian Poleward
Current (IPC) on the shelf (Frouin et al. 1990; Peliz et al.
2005); this current is a northward surface stream that also
induces a shoreward flow and, hence, causes downwelling
near the coast (Álvarez-Salgado et al. 2003). Across-shelf
transport imposed by coastal upwelling and downwelling is
extremely intensified in the Rı́as Baixas (Figueiras et al.
Sampling—Two stations (Fig. 1B), one on the shelf
offshore of the Rı́a de Vigo and the other inside the Rı́as,
were sampled weekly between 15 May 2001 and 24 April
2002 on board the RV Mytilus. The maximum depth at the
station on the shelf was 150 m, while the depth at the
station in the Rı́a de Vigo, located in the middle channel,
was 40 m at low tide. Sampling was made with a conductivity–temperature–depth (CTD) probe (SBE 9/11) that was
fitted with a fluorometer and attached to a rosette equipped
with 12 polyvinyl chloride (PVC) Niskin bottles. Water
samples for nitrate, chlorophyll a (Chl a), and microplankton determinations were taken from the CTD upcasts.
Meteorology and surface currents—Winds on the shelf
were recorded hourly by the meteorological SeaWatch
buoy deployed by the Spanish Agency Puertos del Estado
at 42u07.29N, 9u24.09W (the Silleiro buoy, Fig. 1A). These
polyvingl wind data were used to calculate the Ekman
transport components (m2 s21) perpendicular (Qx) and
parallel (Qy) to the coast following Wooster et al. (1976):
Qx,y ~
ra Cd jV jVy,x
,
f rw
where ra is the air density (1.22 kg m23), Cd is an empirical
drag coefficient (1.3 3 1023, dimensionless), |V | is the wind
speed (m s21) at the sea surface with components Vx,y, rw is
the density of seawater (,1,025 kg m23), and f is the
2670
Crespo et al.
were filtered under low-vacuum pressure through 25-mm
Whatman GF/F filters. The filters were stored frozen at
220uC until pigment extraction, which was done in 90%
acetone during 24 h in the dark at 4uC.
Fig. 2. (A) Cross-shore and (B) alongshore Ekman transport
components deduced from the winds recorded by the Silleiro buoy
on the NW Iberian shelf. The seven identified phases, designated 1
to 7 (see text for details), are given on the top.
Coriolis parameter (9.946 3 1025 s21). Qx and Qy are
related to north–south and east–west winds, respectively.
The sign of Qx was changed to associate positive values
with offshore transport (upwelling) of surface waters
(Fig. 2A).
The Silleiro buoy also measured currents at 3-m depth
with a UCM60 acoustic current meter from 15 June 2001 to
the end of the sampling period. The current data, which
were recorded hourly, were processed using a movingaverage filter A242A25 (Godin 1972) and a cutoff period of
30 h to remove the tidal signal.
Satellite images—Advanced very high-resolution radiometer (AVHRR) and sea-viewing wide field-of-view sensor
(SeaWiFS) data were received by the United Kingdom
Natural Environment Research Council (UK NERC)
Satellite Receiving Station at the University of Dundee
and processed at the Plymouth Marine Laboratory, UK,
following the methods described in Álvarez-Salgado et al.
(2003). Briefly, sea-surface temperature (SST) was produced
from the AVHRR data, and estimates for Chl a concentration were produced from SeaWiFS data using the latest
version of the OC4v4 algorithm (O’Reilly et al. 1998).
Nutrients and chlorophyll—Nitrate and Chl a were
determined at several depths from the surface to bottom
of the shelf (7–8 depths) and in the Rı́a de Vigo (4–5
depths). Nitrate concentrations (mmol kg21) were analyzed
by segmented flow analysis with Alpkem autoanalyzers
according to Hansen and Grasshoff (1983).
Chl a (mg m23) was determined by fluorometry using
a Turner Designs fluorometer calibrated with pure Chl
a (Sigma Chemical). Seawater volumes of 100–250 mL
Microplankton—Samples for microplankton counts and
identification were collected from four depths within the
photic layer at the shelf station. The depths were selected
after the inspection of the fluorescence profiles. Microplankton samples from the station in the Rı́a de Vigo were only
taken from the surface layer and from 25 September onward,
when a sudden increase in Chl a concentrations (.20 mg
m23) in the surface waters pointed to the occurrence of
a dinoflagellate bloom. Samples of 100 mL were preserved
in Lugol’s iodine and sedimented in composite sedimentation chambers. The organisms were counted and identified
to the species level when possible using an inverted
microscope. Two transects scanned at 3400 and 3250 were
used to enumerate the small species. The larger species were
counted from scanning the whole slide at 3100.
Principal component analysis (PCA) was employed to
evaluate the structure of the microplankton community at
the shelf station. Starting from the original data matrix of
microplankton abundances, the species or groups of species
present in at least 30% of the samples were extracted and
combined into a new matrix (54 species, 161 samples) to
perform the analysis. This reduction was used to eliminate
the double zero values, which can distort the analysis results.
Abundances were transformed to log(x + 1), where x 5 cells
100 mL21, to reduce and homogenize the variance.
Results
Meteorological forcing and water-column responses—
Based on the Ekman transport components (Fig. 2) and
the evolution of thermohaline properties, nitrate, and Chl
a concentrations on the shelf (Fig. 3) and in the Rı́a de Vigo
(Fig. 4), seven phases (1–7) could be distinguished in the
responses of the water column to meteorological forcing.
Phase 1, which lasted from the beginning of the sampling
to the end of August, was characterized by highly variable
northerly winds (2Qx 5 0.34 6 0.47 m2 s21; Fig. 2A) and
weak east–west winds (Qy 5 20.04 6 0.22 m2 s21; Fig. 2B)
that persisted until 13 August. These northerly, upwellingfavorable winds were, however, not strong enough to cause
upwelling on the shelf, where the water column appeared to
be stratified (Fig. 3A,B), with low nitrate concentrations
(,1 mmol kg21) in the surface layer (Fig. 3C). Nonetheless,
the nitracline and the associated subsurface chlorophyll
maximum (Fig. 3C,D) showed a progressive uplift during
this period. The water column in the Rı́a de Vigo was also
stratified (Fig. 4A,B) and manifested a more pronounced
uplift of the nitracline, which led to a weak upwelling at the
end of July to beginning of August (Fig. 4C). Phase 1 ended
with a relaxation during the second half of August
characterized by extremely low winds, across-shelf Ekman
transport (Qx 5 0.07 6 0.3 m2 s21; Fig. 2A), and,
particularly, alongshore transport (Qy 5 0.008 6 0.07 m2
s21; Fig. 2B). The wind relaxation induced a downwelling
event on the shelf and in the Rı́a de Vigo that was clearly
Harmful dinoflagellates and downwelling
2671
Fig. 4. Evolution of (A) temperature (uC), (B) salinity, (C)
nitrate concentration (mmol kg21), and (D) chlorophyll a concentration (mg m23) at the station in the Rı́a de Vigo. The seven
hydrographic phases (1 to 7) are shown on the top.
Fig. 3. Evolution of (A) temperature (uC), (B) salinity, (C)
nitrate concentration (mmol kg21), and (D) chlorophyll a concentration (mg m23) at the station on the shelf. The seven
hydrographic phases (1 to 7) are shown on the top.
traceable by the downward orientation of temperature and
nitrate isolines on the shelf (Fig. 3A,C) and temperature,
salinity, and nitrate isolines in the Rı́a de Vigo (Fig. 4A,B,C). This downwelling, however, had contrasting effects
on the Chl a concentrations at the shelf and in the Rı́a de
Vigo. Whereas Chl a concentration decreased to ,1 mg m23
in shelf waters (Fig. 3D), in the Rı́a de Vigo, concentrations
were .25 mg m23 at ,20-m depth at the start of downwelling (14 August; Fig. 4D). Later, Chl a values also
decreased noticeably in the Rı́a de Vigo (Fig. 4D).
Between 30 August and 24 September (phase 2;
Fig. 2A,B), northeasterly winds defined an upwelling event
(Qx 5 0.55 6 0.43 m2 s21; Qy 5 0.30 6 0.25 m2 s21) that
supplied nutrients to the surface layer of the water column
on the shelf (Fig. 3C) and in the Rı́a de Vigo (Fig. 4C) and
promoted the increase in Chl a concentrations in both
domains (Figs. 3D, 4D). This upwelling event was followed
by a month (25 September–30 October) of dominance by
southwesterly winds (phase 3; Fig. 2A,B) that caused
downwelling (Qx 5 20.42 6 0.49 m2 s21; Qy 5 20.16 6
0.35 m2 s21). This downwelling event, which was longer
and more intense than the previous one at the end of phase
1, left the shelf waters with low Chl a concentrations
(,1 mg m23; Fig. 3D), while Chl a values of ,23 mg m23
were measured in the Rı́a de Vigo (Fig. 4D). In contrast to
the preceding downwelling at the end of August, when the
highest Chl a concentrations in the Rı́a de Vigo were
recorded at ,20 m, now the highest values were found at
the surface (Fig. 4D). A new strong upwelling event (Qx 5
0.60 6 0.48 m2 s21; Qy 5 0.66 6 0.54 m2 s21) occurred in
November (phase 4) due to northeasterly winds (Fig. 2).
This upwelling caused a conspicuous increase in Chl
a concentration on the shelf (Fig. 3D), but it had little
impact in the Rı́a de Vigo, where Chl a values (,3 mg m23)
were lower than those attained during the previous
upwelling of phase 2 (.10 mg m23; Fig. 4D).
Phase 5 (29 November–12 February) was characterized
by highly variable downwelling-favorable winds (Qx 5
2672
Crespo et al.
20.31 6 0.70 m2 s21; Qy 5 0.02 6 0.49 m2 s21; Fig. 2A,B)
that favored the presence of the Iberian Poleward Current
(IPC) on the shelf. The IPC was defined by a homogeneous
water body at 14uC and salinity .35.8 (Fig. 3A,B) with
relatively low nitrate (,3 mmol kg21) and Chl a (,0.5 mg
m23) concentrations (Fig. 3C,D). Salinity (,35.5) and
temperature (,13uC) were slightly lower in the Rı́a de
Vigo (Fig. 4A, B), while nitrate (,5 mmol kg21) and Chl
a (,1 mg m23) concentrations were higher (Fig. 4 C,D).
Phase 6 (13 February–21 March; Fig. 2A), which roughly
coincided with the maximum vertical homogenization of the
water column on the shelf (Fig. 3), began with a month (12
February–10 March) of upwelling-favorable winds (2Qx 5
0.68 6 0.70 m2 s21; Qy 5 0.32 6 0.70 m2 s21) but ended with
10 d (11–21 March) of downwelling (2Qx 5 20.81 6
0.55 m2 s21; Qy 5 20.16 6 0.46 m2 s21). During this
downwelling event, Chl a concentration was higher on the
shelf (Fig. 3D) than in the Rı́a de Vigo (Fig. 4D).
Finally, the spring transition from winter homogenization to stratification occurred during phase 7, when
upwelling (2Qx 5 0.42 6 0.61 m2 s21) coincided with
a slight increase in surface temperature (Figs. 3A, 4A).
Surface currents on the shelf and satellite imagery—
Surface currents on the shelf (Fig. 5) were roughly consistent
with the Ekman transport components. Thus, there was
a southwestward flow from June to August (phase 1), which
was in agreement with the sustained upwelling-favorable
winds during this period (Fig. 2A). The upwelling relaxation
that occurred at the end of this phase is depicted as a loop in
the surface flow at the end of August. The upwelling of
September (phase 2) induced the westward flow of surface
waters, whereas the downwelling of October (phase 3) had
the opposite effect of forcing eastward flow. Surface waters
flowed to the northwest during the upwelling of November
(phase 4). The differences in the flow direction during these
three upwelling phases might have been due to variations in
the intensity of the alongshore transport caused by east–west
winds. Northward transport was stronger in November (Qy
5 0.66 6 0.54 m2 s21) than in September (Qy 5 0.30 6
0.25 m2 s21), while alongshore transport due to winds was
virtually nonexistent during phase 1 (Qy 5 20.04 6 0.22 m2
s21). The flow was intense and to the north during phase 5,
when the IPC was present on the shelf (Fig. 5B). Except for
the first half of phase 6, when northerly winds forced the
surface flow to the south, less intense northward flow
persisted until the end of the sampling period (Fig. 5C).
According to this current pattern, shelf surface waters
were advected to the open ocean (during upwelling) or to the
north (in winter), and they could only enter the Rı́as Baixas
during the downwelling of October (Fig. 5A inset). This
effect of downwelling on advection of shelf surface waters to
the Rı́as Baixas is illustrated by the satellite images recorded
on 25 September and 03 October (Fig. 6). The relatively high
Chl a concentrations (.5 mg m23) observed on the western
shelf of Galicia at the end of upwelling phase 2 (25
September; Fig. 6A,B) were confined to a very narrow band
close to the Rı́as Baixas a week later, on 03 October
(Fig. 6D), when the downwelling of phase 3 brought warm
water to the coast (Fig. 6C). This transport of shelf waters to
Fig. 5. Progressive vector diagrams of the surface currents
recorded by the Silleiro buoy on the NW Iberian shelf during (A)
upwelling–downwelling (phases 1 to 4), (B) the winter IPC (phase
5), and (C) winter mixing and spring transition (phases 6 and 7).
Inset in (A) is the downwelling of October (phase 3). More details
are given in the text. Note that progressive vector diagrams depict
the virtual trajectory of a particle for an ideal homogeneous
current field on the shelf similar to that at the point where currents
were recorded. They do not denote the actual current field over
the entire region on the figure. Black diamonds show the position
of the Silleiro buoy, and black circles indicate the first day of the
following months.
the coast coincided with the sudden increase in Chl
a concentration (,23 mg m23) recorded in the surface
waters of the interior of Rı́a de Vigo (Fig. 4D). The IPC,
shown as northerly flow on Fig. 5B, can be clearly seen on
a satellite SST image for 15 December (Fig. 6E) as a warmer
band over the outer shelf and continental slope. The IPC
also is apparent as a slightly lower chlorophyll band on
a SeaWiFS composite image for 06–08 January 2002
(Fig. 6F) offshore of the 200-m bathymetry contour north
of 42.5uN and around the northwestern Galician coast. The
IPC is less commonly observed with a satellite color
signature since chlorophyll is usually relatively uniform
offshore in winter (Álvarez-Salgado et al. 2003).
Microplankton abundance in shelf waters—The total
microplankton abundance and Chl a concentration on
Harmful dinoflagellates and downwelling
2673
Fig. 6. AVHRR sea-surface temperature for (A) 25 September 2001, (C) 03 October 2001,
and (E) 15 December 2001 (note different color palettes). Chlorophyll values derived from
SeaWiFS for (B) 25 September 2001, (D) 03 October 2001, and (F) a composite of images from
06–08 January 2002. The sequence represents the end of an upwelling event (25 September; phase
2) that was followed by a strong downwelling (03 October; phase 3) event a week later and
snapshots of the temperature (15 December) and color signature (06–08 January) of the IPC
during phase 5. Clouds and land are masked black. The 200-m and 2000-m isobaths are included.
the shelf were positively correlated (r 5 0.72, p , 0.001, n 5
161), and the two variables showed a similar evolution
(Figs. 7A, 3D). The total cell abundance increased from
,1,000 cells mL21 in the subsurface chlorophyll maximum
(,30 m) at the beginning of the sampling period to
maximum abundances .5,000 cells mL21 at the surface
during the upwelling of September (phase 2) and the first
days of the downwelling of October (phase 3). Somewhat
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Crespo et al.
(20% 6 10%) during the whole sampling period, also
showed higher abundances in summer and at the beginning
of autumn (Fig. 7C). Their highest abundances (.200 cells
mL21) coincided with those recorded for diatoms, and,
hence, they were found in surface waters during the
upwelling of September (phase 2) and the first days of the
October downwelling (phase 3). The lowest abundances
(,20 cells mL21) occurred during the IPC (phase 5).
Ciliates (data not shown) only accounted for 2% 6 4% of
the total microplankton abundance.
Fig. 7. Evolution of abundance (cells mL21) of (A) total
microplankton, (B) diatoms, (C) dinoflagellates, and (D) flagellates other than dinoflagellates at the shelf station. The seven
hydrographic phases (1 to 7) are given on the top.
lower abundances (,3,000 cells mL21) were recorded
during the relaxation at the end of phase 1. While diatoms
dominated in the three surface maxima (Fig. 7B), where
they accounted for 70–83% of total cell abundance, small
flagellates (Fig. 7D), representing 89% of the total microplankton abundance, were responsible for the subsurface
maximum at the beginning of phase 1.
Cell abundance dropped to values of ,200 cell mL21
during the rest of the downwelling of October (phase 3),
and it did not increase appreciably during the upwelling of
November (phase 4). The lowest abundance (,80 cells
mL21) was recorded during phase 5, when the IPC was
present on the shelf. Microplankton abundance increased
again during the winter mixing period (phase 6; ,200 cells
mL21) and during the spring transition (phase 7; ,400 cells
mL21). Although diatoms represented 24% of total cell
abundance during the upwelling of phase 4, microplankton
was dominated by small flagellates (,70%) during all these
phases.
Dinoflagellates, which accounted for a relatively small
and variable fraction of the total microplankton abundance
Microplankton assemblages in shelf waters—Principal
component analysis (PCA) performed with the original data
set of microplankton abundance extracted three principal
components (Table 1) that explained 35% of the total
variance. The first principal component (PC1) explained
18%, the second (PC2) explained 11%, and the third (PC3)
accounted for 6%. Only four species (Dictyocha fibula,
Solenicola setigera, Gymnodinium nanum, and a small
Torodinium robustum) showed low negative loads with PC1
(Table 1), while the other 50 species had positive loads. This
load arrangement, where almost all species had positive
loads, and the positive correlation (r 5 0.73) between the
scores of this component and the logarithm of total cell
abundance, illustrates that PC1 explained the variability due
to changes in microplankton abundance. Thus, the distribution of the PC1 scores (Fig. 8A) shows the highest positive
values during phases 1 and 2 and the beginning of phase 3.
The highest negative scores occur during phase 5, when the
total microplankton abundance was the lowest (Fig. 7A).
Cryptophyceae, diatoms (Pseudo-nitzschia cf. seriata,
Asteromphalus sarcophagus, Guinardia delicatula, Nitzschia
longuissima, and Proboscia alata), large heterotrophic
dinoflagellates (Torodinium robustum, Gyrodinium fusiforme,
and Cochlodinium helix), and two medium-sized heterotrophic dinoflagellates (Amphidinium flagellans and Amphidinium sphenoides) showed the highest positive loads with PC2
(Table 1). Several small- and medium-sized naked and
armored dinoflagellates and Leucocryptos spp. were the
organisms with the highest negative loads (Table 1). The
evolution of PC2 scores (Fig. 8B) indicates that this
component differentiated between a spring–summer assemblage composed of diatoms and large dinoflagellates
(positive values) and an assemblage composed of small
species (negative values) that dominated in autumn and
winter. The change from positive to negative scores occurred
during the upwelling of September (phase 2).
The PC3 component differentiated between an assemblage (positive loads, Table 1) containing several harmful
dinoflagellates (Heterocapsa niei, Prorocentrum minimum,
Prorocentrum micans, and Karenia cf. mikimotoi), and
another assemblage (negative loads, Table 1) primarily
composed of diatoms (Thalassionema nitzschioides, Navicula ostrearia, medium-sized centric diatoms, and Pseudonitzschia cf. seriata). Positive and negative scores of PC3
alternated in the water column (Fig. 8C), and the highest
negative scores (diatoms) occurred during the upwelling
phases. The highest positive scores (harmful dinoflagellates) were found during the downwelling of phase 3 in
October.
Harmful dinoflagellates and downwelling
2675
Table 1. Correlation coefficients (loads) of the species and taxa selected for principal component analysis (PCA) with the first three
principal components. Species and taxa are ordered according to PC1. The highest positive and negative loads for PC2 and PC3 are in
bold type. The species were grouped into diatoms (Diat), dinoflagellates (Dinof), flagellates other than dinoflagellates (Flag), and
ciliates (Cil).
Group
Cil
Dinof
Dinof
Diat
Diat
Cil
Dinof
Diat
Dinof
Flag
Dinof
Diat
Diat
Cil
Dinof
Dinof
Dinof
Dinof
Dinof
Flag
Dinof
Cil
Dinof
Diat
Cil
Diat
Diat
Dinof
Diat
Dinof
Cil
Dinof
Dinof
Cil
Dinof
Dinof
Flag
Dinof
Dinof
Dinof
Diat
Dinof
Flag
Dinof
Diat
Dinof
Dinof
Dinof
Dinof
Diat
Dinof
Dinof
Flag
Flag
Taxon
Choreotrich ciliates (medium, 30–60 mm)
Gyrodinium fusiforme
Cochlodinium helix
Pseudo-nitzschia cf. seriata
Thalassionema nitzschioides
Strombilidium spiralis
Protoperidinium spp. (medium, ,30 mm)
Nitzschia longissima
Protoperidinium steinii
Unidentified small flagellates (,10 mm)
Gymnodinium spp. A (small, ,20 mm)
Centric diatom spp. (medium, 20–30 mm)
Navicula ostrearia
Choreotrich ciliates (small, ,30 mm)
Naked dinoflagellate spp. (large, .60 mm)
Gymnodinium simplex
Gymnodinium cf. hamulus
Karenia cf. mikimotoi
Gymnodinium spp. A (medium, 20–40 mm)
Euglenophyceae spp.
Heterocapsa niei
Mesodinium rubrum
Gymnodinium spp. B (small, ,20 mm)
Centric diatom spp. (small, ,20 mm)
Ciliates other than choreotric (medium, 30–60 mm)
Pseudo-nitzschia cf. delicatissima
Proboscia alata
Prorocentrum micans
Pennate diatom sp. (medium, ,30 mm)
Armored dinoflagellate spp. (medium, 20–40 mm)
Choreotrich ciliates (large, .60 mm)
Naked dinoflagellate spp. (medium, 20–40 mm)
Gyrodinium cf. fusiforme (medium, ,40 mm)
Ciliates other than choreotrich (small, ,20 mm)
Amphidinium flagellans
Prorocentrum minimum
Leucocryptos spp.
Gyrodinium spp. A (medium, 20–40 mm)
Amphidinium sphenoides
Torodinium robustum
Guinardia delicatula
Naked dinoflagellate spp. (small, ,20 mm)
Cryptophyceae spp.
Gyrodinium spp. B (medium, 20–40 mm)
Asteromphalus sarcophagus
Armored dinoflagellate spp. (small, ,20 mm)
Gymnodinium spp. B (medium, 20–40 mm)
Amphidinium cf. flagellans (small, ,20 mm)
Oxytoxum variabile
Pennate diatom spp. (small, ,20 mm)
Torodinium robustum (small, ,30 mm)
Gymnodinium nanum
Solenicola setigera
Dictyocha fibula
PC1
PC2
PC3
0.68
0.67
0.66
0.62
0.61
0.60
0.60
0.60
0.59
0.57
0.56
0.55
0.52
0.52
0.52
0.52
0.51
0.49
0.49
0.49
0.46
0.46
0.45
0.43
0.42
0.42
0.40
0.40
0.39
0.39
0.36
0.35
0.35
0.35
0.33
0.32
0.32
0.25
0.25
0.25
0.24
0.23
0.22
0.19
0.18
0.14
0.13
0.04
0.02
0.01
20.01
20.07
20.12
20.23
20.07
0.44
0.39
0.47
0.06
0.15
0.35
0.38
20.26
0.27
20.53
20.21
20.10
20.18
20.28
0.08
0.02
20.05
20.28
0.08
0.20
20.09
20.64
20.20
20.26
0.06
0.30
0.25
20.30
20.11
20.26
20.71
20.41
0.07
0.32
0.20
20.56
20.29
0.31
0.45
0.42
20.40
0.49
20.46
0.45
20.41
0.01
20.37
20.46
0.25
20.61
0.21
0.11
20.37
0.32
20.12
20.09
20.38
20.41
20.15
20.08
20.18
20.26
0.24
0.23
20.46
20.41
0.23
20.24
0.32
0.24
0.31
0.18
0.01
0.58
20.25
0.19
20.34
20.27
0.04
20.12
0.36
0.12
20.15
0.13
0.04
20.21
0.11
0.02
0.42
0.25
0.00
20.39
0.31
20.07
0.02
0.50
20.02
0.16
0.02
0.30
0.10
0.31
20.14
20.06
0.27
20.41
0.07
2676
Crespo et al.
Fig. 9. Evolution of the abundance (cells mL21) of (A)
Prorocentrum minimum and (B) Karenia cf. mikimotoi in surface
waters in the Rı́a de Vigo from 25 September 2001 until the end of
the sampling period on 24 April 2002. The seven hydrographic
phases (1 to 7) are given on the top.
Fig. 8. Evolution of (A) PC1, (B) PC2, and (C) PC3 scores
extracted by the principal component analysis of microplankton
species abundance. Shaded areas correspond to positive scores.
The seven hydrographic phases (1 to 7) are given on the top.
Downwelling and dinoflagellate dominance in the Rı́a
de Vigo—The sudden increase in Chl a concentration
recorded in surface waters of the Rı́a de Vigo during the
downwelling of October (phase 3; Fig. 4D) prompted
examination of the species composition of this bloom.
Dinoflagellates, representing 80–90% of the total cell
abundance, dominated the microplankton community for
most of the duration of the bloom. The microplankton
composition switched to the dominance of small flagellates
(50–70%) only on the last days of the downwelling, when
Chl a concentration fell to values ,6 mg m23 (Fig. 4D).
Diatoms were never important during this bloom, since
they only accounted for 4% of the microplankton
abundance. Prorocentrum minimum, representing 74% of
the total dinoflagellate abundance, and Karenia cf.
mikimotoi, accounting for 20% of the total dinoflagellate
abundance, were the major components of the bloom.
Although P. minimum and K. cf. mikimotoi were present in
the Rı́a de Vigo at high abundances at the beginning of
downwelling (25 September), their maxima abundances
(10,564 and 3,022 cells mL21, respectively) occurred a week
later, on 04 October (Fig. 9A,B). These abundances were
two orders of magnitude higher than the maximum
abundances recorded on the shelf (data not shown).
Unfortunately, microplankton samples were not collected
at the Rı́a de Vigo before 25 September, but if these species
were present in the Rı́a de Vigo, they would have been in
very low abundances because Chl a concentration during
the previous sampling was ,2 mg m23 (Fig. 4D).
Discussion
The results obtained during these observations indicate
that the water column on the shelf and in the Rı́a de Vigo
responded to upwelling, but with different intensity. Weak
upwelling events (phase 1) that were unable to induce an
obvious signal in the surface layer on the shelf were,
however, strong enough to cause clear responses in the Rı́a
de Vigo. The bathymetry of the Rı́a de Vigo, which is
shallower in the inner part (Fig. 1B), favors the intrusion
and the progressive uplift of the subsurface upwelled water
on the shelf (Figueiras et al. 2002). Therefore, upwelling
was enhanced in the Rı́a de Vigo, where nutrient
concentrations were always higher than on the shelf during
upwelling events (Figs. 3C, 4C). Chl a was also usually
higher in the Rı́a de Vigo (Figs. 3D, 4D); the exception was
the upwelling of November (phase 4), when the homogeneous water column (Fig. 4A) with high nutrient concentrations (Fig. 4C) points to the occurrence of a strong
upwelling event in the Rı́a de Vigo that did not allow
phytoplankton accumulation. The intense surface outflow
imposed by the upwelling on the positive estuarine
circulation of the Rı́a de Vigo (Figueiras et al. 2002;
Piedracoba et al. 2005) probably led to the rapid export of
phytoplankton toward the shelf (Tilstone et al. 2000).
Upwelling relaxation (end of phase 1) and downwelling
(phase 3) events provoked different effects on the shelf and in
the Rı́a de Vigo. Both processes removed phytoplankton from
Harmful dinoflagellates and downwelling
the shelf (Fig. 3D) but caused its accumulation in the Rı́a de
Vigo (Fig. 4D). This resulted in large differences (.30 times)
in Chl a concentration between the Rı́a de Vigo and shelf.
High Chl a concentrations in the interior of the Rı́a de Vigo
that coincide with upwelling relaxation and downwelling have
been previously reported (Figueiras et al. 1994; Fermı́n et al.
1996; Tilstone et al. 2000) and attributed to the reduced
positive estuarine circulation under upwelling relaxation and
the reversal circulation imposed by downwelling. Upwelling
relaxation blocks the export of phytoplankton to the shelf
(Tilstone et al. 2000), while transport of phytoplankton from
the shelf to the interior of the Rı́a de Vigo can occur under
downwelling conditions (Figueiras et al. 1994; Fermı́n et al.
1996). This interpretation is also supported by the surface
currents recorded on the shelf (Fig. 5A), which clearly show
that shelf surface waters could enter the Rı́a de Vigo only
during the downwelling of October. The satellite data
obtained for 03 October (Fig. 6C,D) reinforce this interpretation. The upwelling relaxation at the end of August
probably did not induce such advection of shelf waters to
the Rı́a de Vigo because current records indicate that surface
circulation on the shelf had ceased.
The Rı́a de Vigo and the adjacent shelf were relatively
isolated during phase 5, when the IPC was an offshore
feature. High-saline and nutrient-poor waters (Fig. 3B,C)
typical of the IPC (Álvarez-Salgado et al. 2003) did not
enter the Rı́a de Vigo, where lower-saline and nutrient-rich
water (Fig. 4B,C) pointed to continental influence. At these
times, when the IPC is present on the shelf, a buoyant
plume due to runoff that extends as a narrow coastal band
offshore of the Rı́as Baixas is frequently observed (Peliz et
al. 2005). The front separating the IPC and the buoyant
plume is rarely found in the interior of the Rı́a de Vigo, and
when this occurs, it coincides with strong southwesterly
winds and low runoff (Álvarez-Salgado et al. 2003). The
shelf and the Rı́a de Vigo were connected again after the
IPC vanished, and the continental influence in the Rı́a de
Vigo was less important (Figs. 3, 4).
Like in the Rı́as, where biomass of diatoms and
upwelling intensity are positively correlated (Figueiras
and Rı́os 1993), microplankton on the shelf responded to
upwelling through increasing diatom abundance. Nevertheless, part of this increase might also have been due to
transport from the Rı́as, since the positive estuarine
circulation of the Rı́as Baixas during upwelling continuously exports diatoms to the shelf (Tilstone et al. 2000).
Once on the shelf, the surface flow (Fig. 5A) could
transport these populations to the south and to the open
ocean. On the contrary, the low cell abundance and the
dominance of small species recorded after the first moments
of the strong downwelling of October suggest advection of
oligotrophic waters from the ocean. Downwelling also
confined shelf populations to a narrow band near the coast
(Fig. 6D), from where they could eventually enter the Rı́as.
Low cell abundance in the IPC waters, with dominance of
small species and the absence of large diatoms and
dinoflagellates, has also been reported for the IPC in other
years (Castro et al. 1997), and it has been related to the
subtropical origin of oceanic waters in which piconanoplankton dominate (Rodrı́guez et al. 2006). Therefore,
2677
if the IPC enters the Rı́a de Vigo, it should cause a rapid
change from large to small plankton species.
Although the main factors explaining the microplankton
variability on the shelf were the increase in cell abundance
(Fig. 8A, PC1) in response to upwelling events and the
switch from spring–summer to autumn–winter microplankton assemblages (Fig. 8B, PC2), PCA also identified a third
source of variability (PC3) relevant for understanding HAB
dynamics in the region. According to the evolution of PC3
(Fig. 8C), harmful dinoflagellates, though in low abundance (Fig. 7C), were habitual components of the spring–
summer microplankton community on the shelf, where they
alternated their presence with a diatom assemblage. The
replacement of these two assemblages can be attributed to
the interaction between microplankton distribution and
across-shelf circulation imposed by upwelling–downwelling. In this respect, Tilstone et al. (1994) showed that
diatoms dominate in the interior of the Rı́as Baixas under
upwelling conditions, whereas dinoflagellates are more
important at the outer part of the Rı́as Baixas and the
adjacent shelf. However, this distribution contracts when
upwelling relaxes, allowing dinoflagellates to invade the
interior of the Rı́as Baixas (Tilstone et al. 1994).
Consequently, the intense onshore currents caused by the
downwelling of phase 3 in October (Fig. 5A) could
accumulate harmful dinoflagellates in the interior of the
Rı́a de Vigo (Fig. 9A, B). Diatoms, which were also
necessarily accumulated, probably were not able to
counteract the intense downward velocities generated by
downwelling in the Rı́a, and, as suggested by other
observations (Figueiras et al. 1994; Fermı́n et al. 1996;
Crespo et al. 2006), they would be rapidly removed from
the water column before dinoflagellates accumulated.
Dinoflagellates, owing to their vertical swimming capability, can in part neutralize these downward velocities
(Figueiras et al. 1995), but under strong downwelling, they
can also be removed from the water column (Crespo et al.
2006), as apparently was the case on this occasion
(Fig. 9A,B). The strong and rapid decrease observed in
the abundances of Prorocentrum minimum and Karenia cf.
mikimotoi in the Rı́a de Vigo after the first days of
downwelling (Fig. 9A,B) points to this possibility. Certainly, P. minimum and K. cf. mikimotoi could be accumulated
at the inner parts of the Rı́a de Vigo, but if this were the
case, they would reappear at the surface during the
following upwelling of phase 4 in November.
In contrast to other coastal upwelling systems where
alongshore currents play a decisive role in HAB dynamics
(Trainer et al. 2002; Pitcher and Nelson 2006; Sackmann
and Perry 2006), the dynamics of harmful dinoflagellates in
the Rı́as Baixas and the adjacent shelf in the NW Iberian
upwelling system is virtually dependent on across-shelf
currents. For this, the orientation of the Rı́as, which is
nearly perpendicular to the main coastline, is determinant
because it implies a rapid response to coastal upwelling–
downwelling. Harmful dinoflagellates, which are habitual
components of the spring–summer microplankton community at the adjacent shelf, though they occur in low
abundance, are rapidly advected to and accumulated in
the interior of the Rı́as Baixas during downwelling. The
2678
Crespo et al.
later success into bloom conditions of the selected species
will depend on the strength of downwelling and on the
occurrence of upwelling. Intense and persistent downwelling would remove the previously selected species
through reversal circulation in the Rı́as. Strong upwelling
would export them to the shelf where they could disperse.
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Received: 4 January 2007
Accepted: 8 June 2007
Amended: 9 July 2007