Recent trends in plankton and upwelling intensity off Galicia (NW Spain)

A. Bode
a,
*
, M.T. Alvarez-Ossorio
a
, J.M. Cabanas
b
, A. Miranda
b
, M. Varela
a
a
Instituto Espaol de Oceanografa, Centro Oceanogrco de A Corua, Apdo. 130, 15080 A Corua, Spain
b
Instituto Espaol de Oceanografa, Centro Oceanogrco de Vigo, Cabo Estai, Canido. 36200 Vigo, Spain
a r t i c l e i n f o
Article history:
Received 18 July 2008
Received in revised form 18 March 2009
Accepted 16 July 2009
Available online 26 July 2009
a b s t r a c t
The mean intensity of the NE Atlantic upwelling system at its northern limit (Galicia, NW Spain)
decreased during the last 40 years. At the same time, warming of surface waters was detected. Plankton
biomass and composition are expected to reect such changes when integrated over large time and space
scales. In this study, biomass, abundance and species composition of phyto- and zooplankton were ana-
lysed to search for signicant patterns of annual change and relations with upwelling intensity. Region-
ally integrated, mostly offshore, data were obtained from the Continuous Plankton Recorder (since 1958)
whereas coastal data from Vigo and A Corua came from the Radiales program (since 1987). No signi-
cant trends were found in phytoplankton biomass at either regional or local scales. However, there was a
signicant decrease in diatom abundance at regional scales and also of large species at local scales. Zoo-
plankton abundance (mainly copepods) signicantly decreased offshore but increased near the coast. Bio-
mass of zooplankton also increased near the coast, with the fastest rates in the south. Warm-water
species, like Temora stylifera, were increasingly abundant at both regional and local scales. Signicant cor-
relations between upwelling intensity and plankton suggest that climatic effects were delayed for several
years. Our results indicate that the effects of large scale climatic trends on plankton communities are
being effectively modulated within the pelagic ecosystem in this upwelling region.
2009 Elsevier Ltd. All rights reserved.
1. Introduction
Plankton has been shown to respond rapidly to large scale cli-
mate-induced changes in the ecosystem (Beaugrand et al., 2000,
2003; Richardson and Schoeman, 2004; Leterme et al., 2005,
2006; ICES, 2006; Valds et al., 2007). Short life cycles and high fre-
quency variability in their abundance and biomass made these
organisms a sensitive index of environmental changes. The large
scale responses, however, are highly dependent on the oceanic re-
gion, with different regional effects produced by a given climatic
forcing (ICES, 2006). In this way, Richardson and Schoeman
(2004) showed increasing phytoplankton abundance in cooler re-
gions of the North Atlantic and decreasing phytoplankton in war-
mer regions as a consequence of warming. Still, this analysis did
not examine in detail the response of plankton in upwelling re-
gions. Increases in phytoplankton biomass are expected if nutrient
inputs increase as a consequence of enhanced upwelling (Gregg
et al., 2005). On the contrary, a decrease in wind induced upwelling
will translate to a drastic reduction in the biomass of nearly all tro-
phic levels of the ecosystem and changes in species composition,
because of the increase in stratication in the upper ocean, as de-
scribed for large upwelling systems (e.g. Escribano et al., 2004).
Galicia (NWSpain) is at the northern limit of the eastern bound-
ary upwelling system off NW Africa and SW Europe. Northerly
winds induce coastal upwelling in this region during most of
spring and summer (Fraga, 1981) and induce frequent phytoplank-
ton blooms dominated by diatoms (Varela, 1992; Casas et al.,
1997). Recent estimations based on geostrophic winds indicate
that both the average intensity of upwelling and the length of
the upwelling season have reduced signicantly over the second
half of the XX century (Alvarez-Salgado et al., 2008). Similar
changes were also reported for the Portuguese coast (Lemos and
Sans, 2006) and an increase in water column stratication was re-
ported for the southern Bay of Biscay since 1990 (Valds et al.,
2007). Such changes may have important consequences for the
ecosystem productivity and composition.
The objective of this study is the analysis of annual variability of
plankton abundance and biomass variables in relation to changes
in climate conditions and upwelling intensity off Galicia based on
the longest available data series of eld observations. Both coastal
and oceanic domains are considered.
2. Materials and methods
2.1. Climatic and upwelling time series
Variability in climatic conditions is represented by values of the
North Atlantic Oscillation index (NAO, Hurrell and Dickson, 2004),
0079-6611/$ - see front matter 2009 Elsevier Ltd. All rights reserved.
doi:10.1016/j.pocean.2009.07.025
* Corresponding author. Tel.: +34 981205362.
E-mail address: antonio.bode@co.ieo.es (A. Bode).
Progress in Oceanography 83 (2009) 342350
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constructed from differences in normalised values of sea-level
atmospheric pressure between the Azores high and the Icelandic
low. Although NAO is not the only source of variability of climate
over the North Atlantic it has been related to major changes in a
number of environmental and planktonic variables in this region
(e.g. Beaugrand et al., 2000). In this study we used the NAO winter
index computed as the average of values between December and
March, since this index is correlated with oceanographic condi-
tions for most of the year (Hurrell and Dickson, 2004). The NAO
time series used in this study covered the period between 1958
and 2006 (http://www.cru.uea.ac.uk), thus matching plankton data
(Table 1).
Upwelling intensity (UI) was indicated by the offshore Ekman
transport estimated from geostrophic winds computed from syn-
optic maps of sea-level atmospheric pressure in a 2 2 cell cen-
tred at 42N, 11W (Lavn et al., 1991). In this study we used the
average value computed between April and September, the season
of maximum probability of upwelling events in Galicia. The UI ser-
ies employed in this study extended from 1966 to 2006, as wind
data with the required frequency (6-h observations) were not
available before 1966.
2.2. Plankton time series
Observations on plankton abundance and biomass came from
both ocean and coastal areas (Fig. 1). The oceanic region was rep-
resented by the standard grid F4 of the Continuous Plankton Recor-
der Survey (CPR, http://www.sahfos.org/CPR). These data came
from surface samples (ca. 7 m depth) of phyto- and zooplankton
collected by an autonomous net sampler (270 lm mesh size)
towed by voluntary ships along commercial routes (Richardson
et al., 2006). For the purpose of this study only the phytoplankton
colour index (PCI), total copepod abundance (COP), and the abun-
dances of selected species or groups were averaged for each year
(Table 1). CPR data for grid F4 were not available in the period
19871996. Diatoms and dinoagellates were selected as they rep-
resent clearly different strategies in the phytoplankton community
(Smayda et al., 2004). Zooplankton species were selected as repre-
sentative of small (Acartia spp.) and large organisms (Calanus hel-
golandicus) in the community, or as representative of warm
waters (Temora stylifera). Among the former, Acartia clausi was
the most abundant species of this genus in Galician coastal sta-
tions, where it was separately recorded, and was also dominant
in CPR samples, although in the latter case only genus was re-
corded (Richardson et al., 2006). The expansion of T. stylifera was
previously noted in other studies in the NE Atlantic (ICES, 2006;
Valds et al., 2007).
Coastal plankton was studied by using the data series collected
between 1987 and 2006 by the Radiales Program of the Instituto
Espaol de Oceanografa (http://www.seriestemporales.net). In
this case two stations (Fig. 1) were selected at two locations of
the Galician coast. Both stations were in open shelf waters and
had similar maximum depth (<80 m) but station E3 was under
the inuence of the large Ria de Vigo whereas station E2 was in
the vicinity of the much smaller Bay of A Corua. The former
was thus representative of the highly productive Galician rias,
where the interaction of upwelling with local topography deter-
mines a highly efcient use of nutrients, while the latter represents
typical conditions of open shelf waters, with low inuence of
coastal inputs. Phytoplankton biomass in the coast was estimated
from water-column integrated chlorophyll-a concentrations
(CHL) and phytoplankton species by abundance data (integrated
in the water column down to 40 m depth) of diatoms and dinoag-
Table 1
Variables analysed and signicant linear trends in annual mean values before variance decomposition.
Variable Name Units Zone Period a b r
2
P n
North Atlantic Oscillation NAO 19582006 111.334 0.056 0.133 0.010 49
Upwelling index UI m
3
s
1
km
1
43N, 11W 19682006 15193.598 7.647 0.308 0.000 39
Phytoplankton color index PCI F4 19582006 9.362 0.005 0.033 0.266 39
Chlorophyll CHL mg m
2
E2 19892006 2379.551 1.110 0.010 0.697 18
Chlorophyll CHL mg m
2
E3 19942006 614.653 0.267 0.002 0.911 10
Diatom abundance DIAT n m
3
F4 19582006 4267909.111 2096.290 0.163 0.011 39
Diatom abundance DIAT n 10
6
m
2
E2 19892006 1908157.294 947.311 0.224 0.055 17
Dinoagellate abundance DINO n m
3
F4 19582006 347505.582 195.787 0.018 0.421 39
Dinoagellate abundance DINO n 10
6
m
2
E2 19892006 154851.395 78.599 0.155 0.118 17
Copepod abundance COP n 10
3
m
3
F4 19582006 26098.555 12.870 0.283 0.000 39
Copepod abundance COP n 10
3
m
3
E2 19902006 193.433 0.098 0.421 0.004 18
Copepod abundance COP n 10
3
m
3
E3 19942006 1099.602 0.552 0.457 0.011 13
Zooplankton biomass DWZ mg m
3
E2 19892006 1093.781 0.559 0.243 0.032 19
Zooplankton biomass DWZ mg m
3
E3 19872006 1936.934 0.985 0.235 0.030 20
Acartia spp. ACA n 10
3
m
3
F4 19582006 12103.697 6.009 0.256 0.001 39
Acartia clausi ACA n 10
3
m
3
E2 19942006 21.686 0.011 0.080 0.349 13
Acartia clausi ACA n 10
3
m
3
E3 19942006 85.128 0.043 0.202 0.123 13
Calanus helgolandicus CHEL n 10
3
m
3
F4 19582006 118.641 0.058 0.028 0.313 39
Calanus helgolandicus CHEL n 10
3
m
3
E2 19942006 7.034 0.004 0.050 0.462 13
Calanus helgolandicus CHEL n 10
3
m
3
E3 19942006 108.734 0.054 0.556 0.003 13
Temora stylifera TSTY n 10
3
m
3
F4 19582006 570.274 0.290 0.066 0.115 39
Temora stylifera TSTY n 10
3
m
3
E2 19942006 537.970 0.276 0.009 0.708 18
Temora stylifera TSTY n 10
3
m
3
E3 19942006 0.557 0.000 0.014 0.699 13
Fig. 1. Map of plankton sampling locations. Stations E2 and E4 correspond to the
series of the RADIALES Program. The inset indicates the extent of the grid F4 of the
continuous plankton recorder survey.
A. Bode et al. / Progress in Oceanography 83 (2009) 342350 343
ellates (Casas et al., 1997). Abundance data were available for the
whole study period only in the case of station E2. Zooplankton bio-
mass was available as dry weight for both coastal stations (Table
1). In addition, zooplankton species abundance counts of total
copepods, A. clausi, C. helgolandicus and T. stylifera were also ana-
lysed. Although both the size of the mesh of the plankton net used
in the coastal stations (200250 lm, Valds et al., 2007) and the
type of sample (vertical or double oblique tows) differed from that
of the CPR study (Richardson et al., 2006), both series retain the
characteristic species composition of the plankton community in
either oceanic or coastal domains and can be used to ascertain ma-
jor changes at annual time scales. We did not attempt to compare
directly the absolute values of the same or similar variables mea-
sured in each series.
2.3. Data analysis
Mean monthly values were rst computed for all series to re-
duce high frequency variability. As the main purpose of the study
was to determine annual trends, series were averaged for each year
before variance analysis. Only annual mean values computed from
eight or more monthly mean values were retained. Temporal var-
iability in annual mean values for each series was decomposed
sequentially in trend, periodic, autocorrelation and residual vari-
ance (white noise) terms (e.g. Nogueira et al., 1997). To ensure
the continuity of the series for the variance decomposition, several
periods were considered for each variable (Table 2). None of the
series analysed showed signicant periodic components and only
a few displayed signicant trends or autocorrelation. Cross-corre-
lation between NAO or UI and plankton variables was analysed
using residual variance of each series and the linear trends at sig-
nicant lags were determined by regression. Statistical analysis
were made using MATLAB (Component Run Time version 7.7).
3. Results
3.1. Regional climate and upwelling
Both climate and upwelling indices displayed large seasonal (i.e.
within year) variability (Fig. 2). NAO values were characteristically
variable from month to month but an annual increase during win-
ter was observed in recent years, particularly since late 1980s and
during the decade of 19902000. The overall trend is positive and
signicant (Table 1) and had a measurable impact on European cli-
mate, as noted in previous studies (Hurrell and Dickson, 2004). In
turn, the upwelling-favourable season seemed to be concentrated
between April and September after early 1980s, while in the previ-
ous period there was almost continuous upwelling between March
and November (Fig. 2). In addition, both monthly (Fig. 2) and mean
upwelling intensity between April and September (Table 1) signif-
icantly decreased in the studied series.
3.2. Oceanic plankton
Despite the high monthly variability, oceanic time series of
plankton variables allowed for the identication of major seasonal
blooms. Phytoplankton biomass (PCI) generally displayed two
main maxima each year, the rst in the late winterspring transi-
tion and the second in the summerautumn period, although sec-
ondary maxima can be recognised during the upwelling period
(Fig. 3). These maxima, however, appeared reduced in recent years
compared to the values observed at the beginning of the series but
the mean annual values did not display signicant trends either for
the whole data period (Table 1) or for the 19581986 and 1997
2006 periods. Diatoms were always very abundant in the region,
displaying frequent blooms for most of the year (Fig. 3). Their
abundance always exceeded that of dinoagellates, as expected
in an upwelling region (Varela, 1992; Casas et al., 1997). Annual
mean values showed a signicant negative linear trend when con-
sidering the whole period (Table 1), although the trend was not
signicant in periods with continuous data, as for PCI. In contrast,
dinoagellates were more abundant in summer months between
1958 and 1986, with a signicant positive trend (r
2
= 0.322,
Table 2
Linear trends between NAO or UI (X, independent variable) and plankton (Y,
dependent variables measured in different zones). The lag in plankton variables is
expressed in years. r
2
: determination coefcient. a: intercept. b: slope. P: signicance.
Period X Y_zone Y-lag r
2
a b P
19581986 NAO COP_F4 0 0.141 0.000 75.069 0.045
NAO COP_F4 +4 0.348 10.949 121.880 0.002
UI COP_F4 +4 0.235 16.320 1.213 0.014
19892005 NAO CHL_E2 +5 0.412 6.338 19.673 0.024
NAO DINO_E2 +5 0.596 322.570 373.800 0.002
19902006 UI CHL_E2 +1 0.279 1.945 0.224 0.036
UI COP_E2 +1 0.317 0.036 0.003 0.023
19942006 UI TSTY_E2 +1 0.458 0.608 0.072 0.016
UI TSTY_E2 +2 0.386 1.042 0.066 0.041
UI CHEL_E3 +5 0.661 0.001 0.001 0.014
NAO TSTY_E3 +1 0.515 0.000 0.003 0.009
Fig. 2. Variability of monthly mean values of the North Atlantic oscillation (NAO, Hurrell and Dickson, 2004) and the upwelling index at 43N, 11W (UI, Lavn et al., 1991).
344 A. Bode et al. / Progress in Oceanography 83 (2009) 342350
P < 0.001), while the trend for the overall series was not signicant
(Table 1) due to the pattern observed after 1997, which was similar
to that of the early 1960s (Fig. 3).
Zooplankton abundance, represented by the total number of
copepods, generally displayed two main maxima each year, as
PCI (Fig. 3). The largest values were observed in the period 1960
1970 with values decreasing progressively, especially those in
the spring. Both small (Acartia spp.) and large sized copepods (C.
helgolandicus) displayed a variability pattern similar to that of total
copepods. Signicant linear trends in annual mean values were
found for the whole series of total copepods (r
2
= 0.283,
P < 0.001) and Acartia spp. (r
2
= 0.256, P = 0.001), while for C. helgo-
landicus the trend was only signicant for the period 19972006
(r
2
= 0.469, P < 0.05).
3.3. Coastal plankton
High seasonal variability in phytoplankton biomass, as indi-
cated by CHL at E2, was also found in the coast (Fig. 4), with
blooms concentrated between spring and autumn. In recent years,
blooms occurring in the summer seemed to increase relative to
those in early spring or autumn, in contrast with the period be-
tween 1991 and 1995. The values observed at station E3 (not
shown), although available for a shorter period than those for E2,
displayed a similar pattern. In the overall, however, there were
no signicant linear trends in annual mean values either for the
whole data series or for periods with continuous data at both sta-
tions (Table 1). As for the ocean, diatoms were also a dominant
component of the phytoplankton community, displaying high
monthly variability (Fig. 4). Dinoagellates, in contrast, were more
abundant during the summerautumn transition, particularly in
recent years (e.g. 20002001). Annual mean values of diatoms
showed a negative linear trend (but barely signicant, P = 0.055,
Table 1) while no trend was found for dinoagellates (Table 1).
Coastal zooplankton displayed large differences between the
two stations (Fig. 4). Both biomass and abundance series revealed
an increase in maximum values at station E3, with blooms concen-
trated in late summer and fall in recent years, but not at E2, where
values were in general lower than those at E3. Although the in-
crease was not continuous during the whole period (e.g. DWZ de-
creased at E3 between 1997 and 2000), the annual mean values of
zooplankton biomass and total copepod abundance showed signif-
icant positive trends considering the whole series (Table 1). De-
spite the selected zooplankton species had monthly variability
resembling that of total copepod abundance or biomass, only C.
helgolandicus at station E3 showed a signicant linear trend in an-
nual mean values.
3.4. Warm-water species
The copepod T. stylifera was not recorded in the region until
1978 (Fig. 5). Thereafter, it appeared with increasing regularity in
the ocean (F4) as well as in the more recent series at coastal sta-
tions (E3, E2). This species was mainly associated with the autumn,
in the case of the ocean and station E2, but in the case of station E3
it was found occasionally and in low numbers. Although the high
Fig. 3. Variability of monthly mean values of plankton variables measured at grid F4 of the continuous plankton recorder survey. PCI: Phytoplankton colour index. r.u.:
relative units.
A. Bode et al. / Progress in Oceanography 83 (2009) 342350 345
abundance recorded in some years (e.g. at station E2 in 1997
2000) the trend in annual mean values was not signicant for
either oceanic or coastal series.
3.5. Plankton and climate
Considering periods with continuous data for all years, and after
removal of trends and autocorrelation, only a few plankton vari-
ables were signicantly correlated with either NAO or UI at annual
time scales (Table 2). Indeed, most of the variables were correlated
with lags between 1 and 5 years with environmental indices. The
abundance of copepods in the ocean (grid F4) was negatively re-
lated to NAO values from the previous winter but positively inu-
enced by NAO values measured 4 years ago for the period 1958
1986. No signicant correlations appeared when using CPR data
for the most recent period (19972006). Negative trends of phyto-
plankton biomass or dinoagellate abundance with NAO at 5-years
lag were found for station E2, and also for T. stylifera abundance at
station E3 with 1-year lag.
As opposed to NAO, upwelling intensity was negatively corre-
lated with copepod abundance in the ocean at 4-years lag (Table
2). Positive correlations were found, however, between UI and
copepods in the coast. Total copepod abundance was correlated
with UI from the previous upwelling season and similar correla-
tions were observed for T. stylifera at both coastal stations, with
lags between 1 and 2 years. In contrast, the abundance of C. helgo-
landicus at station E3 displayed a negative correlation with UI val-
ues measured 5 years ago. Phytoplankton biomass in the coast was
negatively correlated with average upwelling intensity observed
the previous year (station E2) or 2 years ago (Table 2). As for
Fig. 4. Variability of monthly mean values of plankton variables measured at coastal stations E2 and E3. Chl: chlorophyll-a concentration; DWZ: dry weight of zooplankton.
346 A. Bode et al. / Progress in Oceanography 83 (2009) 342350
NAO, none of CPR variables showed signicant correlations with
environmental indices for the period 19972006.
4. Discussion
4.1. Environmental trends and plankton responses
The positive trend of NAO reects multidecadal changes in cli-
mate over the North Atlantic ocean for the last 40 years. In this
way, changes in sea surface temperature and scalar wind were clo-
sely related to winter NAO values with warm anomalies at temper-
ate latitudes during positive NAO phases (Hurrell and Dickson,
2004). The consequences for the ocean waters near Galicia is the
warming trend of surface waters and the weakening in upwell-
ing-favourable winds observed since 1940 (e.g. Lemos and Sanso,
2006; Alvarez-Salgado et al., 2008). The decrease in upwelling
intensity, surface warming and consequent increase in the strati-
cation of the upper layers, was more evident for coastal waters, and
all trends increased from Galicia to the inner part of the Bay of Bis-
cay, where upwelling events are less frequent (Valds et al., 2007).
Such environmental changes have measurable effects on plankton.
First, an increase in temperature of the surface ocean affects the
distribution of plankton species, as shown in the North Atlantic
(Beaugrand et al., 2000; Beaugrand, 2003), and indicated in our
study by the increase in the copepod T. stylifera. Temperature
determines not only short term physiological responses but also
population processes at seasonal and larger time scales. For in-
stance, the warming of surface waters is likely to affect reproduc-
tive success, as most species have preferential temperature ranges
for successful hatching (Bonnet et al., 2005). Second, stratication
may limit primary production, as nutrient inputs from deep waters
are reduced. In this way, Valds et al. (2007) showed a signicant
reduction in primary production values in the Bay of Biscay in the
period 19932003. Finally, the decrease in upwelling may also af-
fect the distribution of plankton by changing the dynamics of sur-
face currents. For instance, the reduction in the upwelling during
the last 40 years has been related with an increase in the renewal
time of water inside the Galician rias, which in turn was related to
an increase in the occurrence of harmful algal blooms (Alvarez-Sal-
gado et al., 2008).
4.2. Phytoplankton
Short time scale variability characteristically dominates phyto-
plankton biomass and abundance. As a consequence, phytoplank-
ton populations are able to cope with most of the changes in
weather-driven environmental conditions (e.g. temperature, irra-
diance, stratication, mixed-layer depth, etc.) and display more
or less predictable recurrences in blooms and species assemblages
(Smayda et al., 2004). Climate-driven changes, however, are more
difcult to detect because of uncertainties in the denition of base-
lines and the confounding effect of intrinsic trends in the commu-
nity and external effects (e.g. anthropogenic eutrophication). Both
characteristics were apparent in our study, as phytoplankton bio-
mass off Galicia exhibited high within-year variability but did
not display any signicant trend at annual time scales in the last
40 years, either in the coast or in the nearby ocean. Similarly, the
records of phytoplankton uorescence measured by satellites in
Atlantic waters near Galicia did not show signicant increases, in
contrast to other upwelling regions of the world (Gregg et al.,
2005). Increasing trends in phytoplankton biomass, however, were
reported for other areas of the North Atlantic (e.g. Leterme et al.,
2005) and related to NAO variability through the balance between
surface temperature and upper layer mixing affecting timing and
magnitude of blooms (Ueyama and Monger, 2005). The decrease
in primary production in the period 19932003 in the southern
Bay of Biscay (Valds et al., 2007) was attributed to changes in
the availability of nutrients (Llope et al., 2007). Primary production
did not show any signicant trend off Galicia in the same period
(Valds et al., 2007), however, our analysis showed a lagged nega-
tive response of coastal phytoplankton biomass to upwelling con-
ditions from the previous 2 years, which may be related to non-
linear responses to nutrient inputs (e.g. Llope et al., 2007) or to
intrinsic cycles of the phytoplankton community (Smayda et al.,
2004). The apparent lack of response of phytoplankton biomass
and production in Galician waters to signicant changes in climate
and upwelling during the last 40 years may be explained by the
large high frequency variability, as upwelling events dominate
the formation of blooms for most of the year. Despite the reduction
Fig. 5. Variability of monthly mean values of Temora stylifera abundance recorded
in the study area.
A. Bode et al. / Progress in Oceanography 83 (2009) 342350 347
in upwelling, stratication did not decrease signicantly (Valds
et al., 2007) and therefore bloom development is not altered yet.
Changes in the phytoplankton community were more detect-
able than changes in biomass as there are species and groups
with clearly different adaptations to the ever changing environ-
ment in the upper ocean. In this way, diatoms are species partic-
ularly suited to turbulent, nutrient-rich waters, like those
occurring in upwelling regions. Diatoms characteristically domi-
nated the phytoplankton community in Galician shelf waters
(Varela, 1992; Casas et al., 1997), as found in this study, but their
dominance decreased in recent years, particularly offshore. In
turn, the abundance of dinoagellates increased, notably at the
coast. Such changes, although gradual and observed during a rel-
atively long period, are indicative of a sensible effect of climate
change, through the decrease in upwelling intensity during
springsummer in Galicia. Diatoms, although still dominating
blooms in shelf waters, are giving way to dinoagellates, more
adapted to weakly stratied waters. Indeed, low renewal of
water inside the Galician rias, as a consequence of reduced
upwelling (Alvarez-Salgado et al., 2008), would favour the
growth of dinoagellates over diatoms and thus the persistence
of species typically responsible for harmful algal blooms in this
region (Varela, 1992; Figueiras and Rios, 1993; Casas et al.,
1997).
Previous studies of phytoplankton community responses in
the NE Atlantic indicated that the rates of change in different
subregions, if any, were not simply related to climatic indices
(as the NAO) or the warming of surface waters (Beaugrand
et al., 2000, 2003; Richardson and Schoeman, 2004; Leterme
et al., 2005, 2006). Most of the largest changes occurred in
waters above 50N, where sea surface temperature and wind
determine the supply of nutrients to the photic layer, and the
warming of typically cold waters enhances stratication of tur-
bulent waters and thus favours phytoplankton growth (Beau-
grand, 2003; Richardson and Schoeman, 2004). In these waters,
total phytoplankton biomass and dinoagellates were reported
to increase in recent years (Leterme et al., 2005, 2006). On the
contrary, at subtropical latitudes the warming of the surface
exacerbates stratication, already a limiting condition for phyto-
plankton growth because nutrient exhaustion and will eventually
decrease phytoplankton biomass. These previous results were
conrmed by our analysis of phytoplankton off Galicia, as there
were no signicant correlations between concurrent measure-
ments of phytoplankton biomass or abundance of characteristics
groups and NAO or upwelling intensity. We obtained, however,
signicant correlations at relatively large lags (45 years), but
the meaning of such correlations is difcult to interpret as they
imply that the effects of the climatic or oceanographic signal
are carried out over time scales much larger that the life span
of phytoplankton cells. Abundance cycles with large period were
reported both for marine (e.g. Russell et al., 1971) and lake phy-
toplankton (e.g. Bondarenko and Evstafyev, 2006) and related to
solar dynamics. Our analysis, however, did not detect any signif-
icant periodicity in phytoplankton variables. Alternatively, the
lagged correlations may result from ecosystem changes not dri-
ven by climate, such as oil spills or anthropogenic eutrophication.
Again, studies of phytoplankton composition and biomass before
and after major oil spills in Galician waters did not report any
signicant changes in the community that could be unequivo-
cally attributed to the spill (Varela et al., 2006). Similarly, trophic
studies have shown the dominance of upwelling-derived nutri-
ents over anthropogenic sources in coastal ecosystems (Bode
et al., 2006). In any case, the apparent long-term effects of cli-
mate and upwelling on phytoplankton deserve further attention
in future studies when the observational series allow for the
study of multidecadal variability.
4.3. Zooplankton
The different trends found in coastal and offshore waters in zoo-
plankton abundance and biomass (mainly due to copepods) can be
the consequence of the interaction between climate and hydrody-
namics in each zone. Copepod abundance signicantly decreased
offshore and was related to an increase in winter NAO values,
while the abundance of coastal copepods increased and was re-
lated to favourable upwelling conditions in the previous year. De-
spite the multidecadal decreasing trend in upwelling intensity, the
consequent reduction in offshore transport of surface water (e.g.
Alvarez-Salgado et al., 2008) would have favoured the retention
of zooplankton near the coast, thus preventing export of organisms
to the nearby ocean. In this way, the nursery effect of the produc-
tive Galician rias, would explain the larger increase of copepods off
the larger Ria de Vigo while there was no signicant change off A
Corua. In addition high winter NAO could have contributed to de-
crease oceanic copepod populations by reducing their fecundity, as
estimated for the CPR data series in the English Channel (Beau-
grand et al., 2000). These authors indicate that an increase in win-
ter temperature and wind-induced turbulence may cause an
increase in copepod metabolism and a decrease in fertility, which
translates to a reduction in the spring populations. In contrast with
oceanic populations, coastal zooplankton appeared more directly
related to upwelling conditions, as there were several signicant
correlations between upwelling intensity and zooplankton vari-
ables (Table 2). In this way, copepods off A Corua were positively
correlated with favourable upwelling conditions of the previous
year, thus suggesting that the reproductive success of overwinter-
ing populations depends on the availability of resources during the
upwelling season. This is further supported by the negative corre-
lation found between upwelling conditions of the previous year
and phytoplankton biomass at station E2, which could be the result
of the enhanced grazing of phytoplankton by copepods.
Most of the studies on long-term changes in North Atlantic zoo-
plankton highlighted the large changes observed in boreal ecosys-
tems (Pershing et al., 2004; ICES, 2006). Even when considering
other temperate and low latitude areas, the magnitude and signif-
icance of changes are still larger for the former. For instance, there
is substantial evidence that the progressive substitution of the
cold-water copepod Calanus nmarchicus by the warm-water C.
helgolandicus at high latitudes in the period 19591996 was caused
by both the warming of surface waters and by the advection of dif-
ferent water masses (Beaugrand, 2003; Pershing et al., 2004). In
Galicia only C. helgolandicus was observed and its annual mean
abundance increased signicantly only at the coastal station near
Vigo, while no changes were detected at other locations (Table
1). Similarly, no changes were detected either in species typically
associated with coastal upwelling, as A. clausi, and there were no
signicant correlations between the analysed species and NAO or
upwelling intensity even considering 2 year lags (Table 2). These
results further support that the observed changes in climate and
upwelling in this region were not large enough to induce signi-
cant changes in most plankton populations, already well adapted
to the magnitude of environmental uctuations. In this way,
Nogueira et al. (2000) concluded that meteorological and thermo-
haline disturbances operating at intermediate frequency during
the productive season in the Ria de Vigo allowed the maintenance
of plankton assemblages with relatively high functional diversity,
thus preventing competitive exclusion. This conclusion may ex-
plain the lack of apparent response of plankton to climate forcing
at mid latitudes compared to boreal locations (e.g. Beaugrand
et al., 2000).
Noticeable changes in the composition of zooplankton commu-
nities off Galicia, however, are in progress. The increasing presence
of warm-water species, such as T. stylifera, is an indication of the
348 A. Bode et al. / Progress in Oceanography 83 (2009) 342350
modications in the environment even if trends in the variables are
not statistically signicant. Similar increases in thermophylic and
opportunistic species (such as Oncaea media and Ditrichocorycaeus
anglicus) were described for the southern Bay of Biscay in recent
years (Valds et al., 2007) as well as for boreal regions of the North
Atlantic (Beaugrand, 2003). In our study, annual mean abundance
of T. stylifera off A Corua was signicantly correlated with upwell-
ing from the previous 12 years, while off Vigo there was a nega-
tive correlation with the NAO value of the previous winter. In
contrast, there was no signicant correlation between concurrent
values of T. stylifera abundance and either climatic or upwelling
variables. One possible explanation is that T. stylifera is transported
to Galicia from southern (and warmer) waters by currents not di-
rectly associated with either NAO or upwelling intensity. Another
possibility is that the response of this species to large scale vari-
ability in environmental conditions may be delayed for more than
the life span of the individuals present in the ecosystem at the time
of the environmental change (in this case perturbations in climate
or upwelling). C. helgolandicus also showed a 5 year lagged re-
sponse (Table 2). Such long lags between environmental change
and changes in the community are indicative of non-linear interac-
tions, likely acting through the food web, and modelling exercises
have shown that the lags are in fact destabilizing mechanisms for
the community when acting at time scales longer that the time
scale of the system (May, 1973). Time delays between environ-
mental changes and phytoplankton growth were well known
(e.g. Duarte, 1990) and they are amplied both through the food
web and in space. In this way, delayed responses of the phyto-
plankton community at specic sites would be tracked by consum-
ers (both zooplankton but also bacteria and the microbial food
web) with and added lag and transmitted to nearby sites. In our
study, small lags (such as those included in seasonal responses)
were ltered as we analysed annual mean values, therefore the ob-
served lags in both phyto- and zooplankton variables may indicate
underlying mechanisms of regulation of climatic perturbations at
large time (i.e. multidecadal) and space scales. Such mechanisms
may take the form of non-linear interactions through the food
web, as shown by Llope et al. (2007) with nutrient ratios and phy-
toplankton composition in the Bay of Biscay, and eventually would
be transmitted to zooplankton populations. If the delayed re-
sponses of zooplankton were indeed a consequence of accumu-
lated lags through the food web then the abundance of a
particular species of zooplankton (as those selected in our study)
at annual time scales would be due not only to a primary response
to the change of a single environmental or climatic variable (as the
surface warming in the case of T. stylifera) but a combination of ef-
fects through the food web and those caused by direct transport by
currents. In contrast, other species (as A. clausi), would be more
adapted to the high frequency variability of the upwelling and less
dependent of long term interactions with climate, at least while
the upwelling maintains a minimum intensity and frequency.
5. Conclusions
Considering annual time scales, weak or non signicant trends
were found for phytoplankton in shelf waters off Galicia in the last
40 years despite measurable changes in climate and particularly in
upwelling. The decrease in upwelling intensity did not translate
into a decrease in phytoplankton biomass but only in diatom abun-
dance, particularly offshore. In turn, zooplankton abundance de-
creased in the nearby ocean but both abundance and biomass
increased or did not changed near the coast. In addition, warm
water zooplankton species (as the copepod T. stylifera) appeared
with increasing abundance in recent years. Interestingly, correla-
tions between climate or upwelling and plankton variables were
signicant mostly at lags between 1 and 5 years, suggesting com-
plex interactions between climate and plankton at large time
scales. These results contrast with those reported for plankton
from boreal ecosystems, where the climatic signal is generally well
detected in the form of signicant changes in species abundance,
biomass and community structure. We hypothesize that the ob-
served resilience of the Galician plankton in shelf waters is a con-
sequence of the high frequency variability characteristic of the
upwelling ecosystem. In this way, the small (although measurable)
uctuations in upwelling intensity were mostly absorbed at annual
scales. Long-term effects, however, cannot be excluded if the ob-
served correlations were indeed due to delays in the response of
plankton populations to climate change.
Acknowledgements
We are grateful to the many scientists and technicians involved
in plankton data collection along the time series employed in this
study. D. Johns (SAHFOS) kindly provided the grid-averaged data
from the CPR survey and L. Mene (IEO) helped with the database
structure. The statistical analysis was improved thanks to discus-
sions and software provided by G. Gonzlez-Nuevo and E. Nogue-
ira. Two anonymous reviewers provided valuable comments and
suggestions to a rst version of the manuscript. This research
was funded in part by the Radiales program (IEO) and by the CLI-
GAL Study (Xunta de Galicia, Spain).
References
Alvarez-Salgado, X.A., Labarta, U., Fernndez-Reirz, M.J., Figueiras, F.G., Rosn, G.,
Piedracoba, S., Filgueira, R., Cabanas, J.M., 2008. Renewal time and the impact of
harmful algal blooms on the extensive mussel raft culture of the Iberian coastal
upwelling system. Harmful Algae. doi: 10.1016/j.hal.2008.04.007.
Beaugrand, G., 2003. Long-term changes in copepod abundance and diversity in the
north-east Atlantic in relation to uctuations in the hydroclimatic environment.
Fisheries Oceanography 12, 270283.
Beaugrand, G., Ibanez, F., Reid, P.C., 2000. Spatial, seasonal and long-term
uctuations of plankton in relation to hydroclimatic features in the English
channel, Celtic Sea and Bay of Biscay. Marine Ecology Progress Series 200, 93
102.
Bode, A., Alvarez-Ossorio, M.T., Varela, M., 2006. Phytoplankton and macrophyte
contributions to littoral food webs in the Galician upwelling (NW Spain)
estimated from stable isotopes. Marine Ecology Progress Series 318, 89102.
Bondarenko, N.A., Evstafyev, V.K., 2006. Eleven- and ten-year basic cycles of Lake
Baikal spring phytoplankton conformed to solar activity cycles. Hydrobiologia
568 (Suppl. 1), 1924.
Bonnet, D., Richardson, A., Harris, R., Hirst, A.B., Edwards, M., Ceballos, S., Diekman,
R., Lopez-Urrutia, A., Valdes, L., Carlotti, F., Molinero, J.C., Weikert, H., Greve, W.,
Lucic, D., Albaina, A., Yahia, N.D., Umani, S.F., Miranda, A., dos Santos, A., Cook,
K., Robinson, S., de Puelles, M.L.F., 2005. An overview of Calanus helgolandicus
ecology in European waters. Progress in Oceanography 65, 153.
Casas, B., Varela, M., Canle, M., Gonzlez, N., Bode, A., 1997. Seasonal variations of
nutrients, seston and phytoplankton, and upwelling intensity off La Corua
(NW Spain). Estuarine, Coastal and Shelf Science 44, 767778.
Duarte, C., 1990. Time lags in algal growth: generality, causes and consequences.
Journal of Plankton Research 12, 873883.
Escribano, R., Daneri, G., Faras, L., Gallardo, V.A., Gonzlez, H.E., Gutirrez, D., Lange,
C.B., Morales, C.E., Pizarro, O., Ulloa, O., Braun, M., 2004. Biological and chemical
consequences of the 19971998 El Nio in the Chilean coastal upwelling
system: a synthesis. Deep-Sea Research II 51, 23892411.
Figueiras, F.G., Rios, A.F., 1993. Phytoplankton succession, red tides and the
hydrographic regime in the Ras Bajas of Galicia. In: Smayda, T.J., Shimizu, Y.
(Eds.), Toxic Phytoplankton Blooms in the Sea. Elsevier Science Publishers B.V,
New York, pp. 239244.
Fraga, F., 1981. Upwelling off the Galician coast, Northwest Spain. In: Richards, F.A.
(Ed.), Upwelling Ecosystems. American Geophysical Union, Washington, DC, pp.
176182.
Gregg, W.W., Casey, N.W., McClain, C.R., 2005. Recent trends in global ocean
chlorophyll. Geophysical Research Letters 32, L030606. doi:10.1029/
2004GL021808.
Hurrell, J.W., Dickson, R.R., 2004. Climate variability over the North Atlantic. In:
Stenseth, N.C., Ottersen, G., Hurrell, J.W., Belgrano, A. (Eds.), Marine Ecosystems
and Climate Variation The North Atlantic. Oxford University Press, Oxford, pp.
1531.
ICES, 2006. Zooplankton monitoring results in the ICES area: summary status report
2004/2005. ICES Cooperative Research Report 281, pp. 143.
A. Bode et al. / Progress in Oceanography 83 (2009) 342350 349
Lavin, A., Diaz del Rio, G., Cabanas, J.M., Casas, G., 1991. Aoramiento en el Noroeste
de la Peninsula Iberica. Indices de aoramiento para el punto 43 N 11 W.
Periodo 19661989. Informes Tcnicos del Instituto Espaol de Oceanografa
91, 140.
Lemos, R.T., Sanso, B., 2006. Spatio-temporal variability of ocean temperature in the
Portugal current system. Journal of Geophysical Research 111. doi:10.1029/
2005JC003051.
Leterme, S.C., Edwards, M., Seuront, L., Attrill, M.J., Reid, P.C., John, A.W.G., 2005.
Decadal basin-scale changes in diatoms, dinoagellates, and
phytoplankton color across the North Atlantic. Limnology and Oceanography
50, 12441253.
Leterme, S.C., Seuront, L., Edwards, M., 2006. Differential contribution of diatoms
and dinoagellates to phytoplankton biomass in the NE Atlantic Ocean and the
North Sea. Marine Ecology Progress Series 312, 5765.
Llope, M., Anadn, R., Sostres, J.A., Viesca, L., 2007. Nutrients dynamics in the
southern Bay of Biscay (19932003): winter supply, stoichiometry, long-term
trends, and their effects on the phytoplankton community. Journal of
Geophysical Research 112. doi:10.1029/2006JC003573.
May, R.M., 1973. Stability and complexity in model ecosystems. Monographs in
Population Biology, vol. 6. Princeton University Press, Princeton, New Jersey.
265 pp.
Nogueira, E., Perez, F.F., Rios, A.F., 1997. Seasonal patterns and long-term trends in
an estuarine upwelling ecosystem (Ria de Vigo, NW Spain). Estuarine Coastal
and Shelf Science 44, 285300.
Nogueira, E., Ibanez, F., Figueiras, F.G., 2000. Effect of meteorological and
hydrographic disturbances on the microplankton community structure in the
Ria de Vigo (NW Spain). Marine Ecology Progress Series 203, 2345.
Pershing, A.J., Greene, C.H., Planque, B., Fromentin, J.M., 2004. The inuences of
climate variability on North Atlantic zooplankton populations. In: Stenseth,
N.C., Ottersen, G., Hurrell, J.W., Belgrano, A. (Eds.), Marine Ecosystems and
Climate Variation The North Atlantic. Oxford University Press, Oxford, pp. 59
69.
Richardson, A.J., Schoeman, D.S., 2004. Climate impact on plankton ecosystems in
the Northeast Atlantic. Science 305, 16091612.
Richardson, A.J., Walne, A.W., John, A.W.G., Jonas, T.D., Lindley, J.A., Sims, D.W.,
Stevens, D., Witt, M., 2006. Using continuous plankton recorder data. Progress
in Oceanography 68, 2774.
Russell, F.S., Southward, A.J., Boalch, G.T., Butler, E.I., 1971. Changes in biological
conditions in the English channel off plymouth during the last half century.
Nature 234, 468470.
Smayda, T.J., Borkman, D.G., Beaugrand, G., Belgrano, A., 2004. Responses of marine
phytoplankton populations to uctuations in marine climate. In: Stenseth, N.C.,
Ottersen, G., Hurrell, J.W., Belgrano, A. (Eds.), Marine Ecosystems and Climate
Variation The North Atlantic. Oxford University Press, Oxford, pp. 4958.
Ueyama, R., Monger, B.C., 2005. Wind-induced modulation of seasonal
phytoplankton blooms in the North Atlantic derived from satellite
observations. Limnology and Oceanography 50, 18201829.
Valds, L., Lpez-Urrutia, A., Cabal, J., Alvarez-Ossorio, M., Bode, A., Miranda, A.,
Cabanas, M., Huskin, I., Anadn, R., Alvarez-Marqus, F., Llope, M., Rodrguez, N.,
2007. A decade of sampling in the Bay of Biscay: what are the zooplankton time
series telling us? Progress in Oceanography 74, 98114.
Varela, M., 1992. Upwelling and phytoplankton ecology in Galician (NW Spain) ras
and shelf waters. Boletn del Instituto Espaol de Oceanografa 8 (1), 5774.
Varela, M., Bode, A., Lorenzo, J., Alvarez-Ossorio, M.T., Miranda, A., Patrocinio, T.,
Anadn, R., Viesca, L., Rodrguez, N., Valds, L., Cabal, J., Urrutia, A., Garca-Soto,
C., Rodrguez, M., Alvarez-Salgado, X.A., Groom, S., 2006. The effect of the
Prestige oil spill on the plankton in the N-NW Spanish coast. Marine Pollution
Bulletin 53, 272286.
350 A. Bode et al. / Progress in Oceanography 83 (2009) 342350