SCI. MAR., 60 (Supl. 2): 45-53
SCIENTIA MARINA
1996
THE EUROPEAN ANCHOVY AND ITS ENVIRONMENT, I. PALOMERA and P. RUBIÉS (eds.)
Phytoplankton ecology in the Bay of Biscay*
MANUEL VARELA
Instituto Español de Oceanografía, Apdo nº 130, 15080 La Coruña, Spain.
SUMMARY: General studies on phytoplankton ecology are very scarce, and have been undertaken mostly in the southern
part of Bay of Biscay. The annual cycle of phytoplankton is typical of a temperate sea, with some special peculiarities. In
winter time the water column is well mixed, and light is the main factor controlling primary production. During spring, water
stratification previous to bloom development has a saline origin, in contrast to other areas where this stratification has a thermal origin. In summer, a thermal stratification with a subsurface chlorophyll maximum (SCM) associated to the nitracline
was found. Maximum primary production was above the SCM. This situation can be ascribed to the typical tropical structure. Nevertheless, this basic pattern of phytoplankton cycle, is modified by two important processes: the intrusion of saline
waters (ENAWt) during winter-spring that when it is strong and extensive, it causes a decrease in the phytoplankton biomass and the pulsating upwelling in summer time connected to the stronger Galician upwelling that causes an elevation of
SCM. Both processes greatly influence the phytoplankton dynamics.The classical food web, dominated by autotrophic
processes, predominates in periods of high productivity. However, during stratification and saline intrusion the food web
based on microbial loop prevails, this system being of great efficiency in nutrient regeneration. The hydrographic events, in
particular fronts, play a crucial role as barriers for eggs and larval transport. The success of recruitment of pelagic fishes is
highly dependent on spawning taking place in areas where the newly hatched larvae find the appropriate food type and size.
The different trophic food webs which characterize both sides of the front were exploited by different fish species for reproduction
Key words: Phytoplankton, fronts, upwelling, food webs, Cantabrian Sea, Bay of Biscay.
RESUMEN: ECOLOGÍA DEL FITOPLANCTON EN EL GOLFO DE VIZCAYA. – Los estudios generales sobre ecología del fitoplancton en el Golfo de Vizcaya son escasos, y se han llevado a cabo principalmente en la parte sur del Golfo. El ciclo anual del
fitoplancton es el típico de un mar templado, con algunas peculiaridades. En invierno la columna de agua está bien mezclada, y la luz es el principal factor que controla la producción primaria. Durante la primavera, la estratificación del agua previo el desarrollo del bloom tiene un origen salino, en contraste con otras áreas en que la estratificación tiene un origen térmico. En verano, se produce una estratificación térmica con un máximo de clorofila subsuperficial (SCM) asociado a la
nitraclina. El máximo de producción primaria esta por encima del SCM. Esta situación puede asociarse a la estructura tropical típica. Sin embargo, el patrón básico del ciclo del fitoplancton se ve modificado por dos procesos importantes: La intrusión de aguas salinas (ENAWt) durante invierno-primavera que cuando es fuerte produce un descenso en la biomasa del
fitoplancton y los pulsos de afloramiento de verano asociados al afloramiento de Galicia, que causan una elevación del SCM.
La típica cadena trófica, dominada por procesos autótroficos predomina en periodos de alta productividad. Sin embargo,
durante la estratificación e intrusión salina la cadena trófica, basada en bucles microbianos, prevalece, siendo este sistema
de gran eficiencia en la regeneración de nutrientes. Los procesos hidrográficos, en particular los frentes, juegan un papel
crucial como barreras para el transporte de huevos y larvas. El éxito del reclutamiento de los peces pelágicos depende en
gran manera de que la puesta tenga lugar en áreas en las que las larvas recién eclosionadas encuentren el tipo y tamaño de
alimento apropiado. Las diferentes cadenas alimentarias que caracterizan ambas partes del frente son explotadas por diferentes especies durante la reproducción.
Palabras clave: Fitoplancton, frentes, afloramiento, cadenas tróficas, mar Cantábrico, Golfo de Vizcaya.
*Received June 20, 1995. Accepted March 20, 1996.
PHYTOPLANKTON ECOLOGY IN THE BAY OF BISCAY 45
INTRODUCTION
The Bay of Biscay is located between 43.5° and
48.5° N and between 3° and 8° W. The Bay can be
defined as an open Bay with the Spanish coast in the
southern part oriented W-E and the French coast in
the eastern part oriented SE-NW. The physical and
hydrological features of the Bay of Biscay are of
great complexity (Le Cann, 1982). The Bay is characterized by a strong influence of climatic conditions, important seasonal variations and a spatial and
temporal heterogeneity. In this sense, the structure
and functioning of the pelagic ecosystem are influenced by several processes acting on regional and
even local scales.
Despite its location and the economic importance
of various fisheries in the area, there seems to be a
dramatic lack of basic ecological knowledge, phytoplankton basic studies included, that makes it
impossible to associate together physical and biological processes. Some strange biological characteristics in the Bay (Quero et al., 1989) related to the
distribution of some fish species would probably be
explained if some information on hydrography and
biology at low trophic levels were available.
According to the situation in the Bay of Biscay,
the seasonal cycle of phytoplankton which we might
expect is that of temperate seas. This is characterized by a mixing period in winter followed by a
clear stratification phase during summer as well as
phytoplankton blooms during the transition periods
between mixing-stratification (spring) and stratification-mixing (autumn).
The first studies on phytoplankton succesion in
the Bay have been carried out in the southern part,
in the East Cantabrian Sea (Arias et al. , 1980; Estrada, 1982; Flos, 1982) and confirm this initial
appraisal. However, in recent years the influence of
some hydrological features, such as the Poleward
Current (Frouin et al., 1990) have been detected.
This water mass of high salinity flows especially
during spring time and causes the development of
density fronts across the shelf in the south part of the
Bay. Another effect related to the Poleward Current
are the anticyclonic eddies (SWODDIES) off the
shelf edge, at mesoscale level (50 -100 km), and relatively persistent in time (up to 1 year) (Pingree and
Le Cann, 1992).
The effect of hydrography on phytoplankton
dynamics along the Asturias Coast (Central
Cantabrian Sea), especially in relation to the slope
density currents, above mentioned, has been the
46 M. VARELA
matter of several papers (Botas et al., 1988; Bode,
1990; Bode et al., 1990; Botas et al., 1990; Fernández, 1990a; Fernández, 1990b; Fernández and Bode,
1991; Fernández et al., 1991a,b; Bode and Fernández, 1992a,b; Bode et al., 1993; Fernández et al.,
1993; Fernández and Bode, 1994). There is also
some extensive information on biomass distribution
and species composition in the Cantabrian Sea
(Varela, 1992; Robins et al., 1993; SARP, 1993).
On the other hand, the existence of a coastal
upwelling first predicted by Mateo (1955), has been
later confirmed by Ríos et al. (1987).
The information that I will try to summarize, on
phytoplankton ecology in the Bay of Biscay is
essentially related to the southern part, especially in
the Cantabrian Sea, where most of work has been
carried out. The information on this matter in other
areas of the Bay (English and French coasts), is
scarce (Le Corre and Treguer, 1976; Pingree et al.,
1976; Holligan and Harbour, 1977; Treguer et al.,
1979; Le Fèvre, 1986).
THE ANNUAL CYCLE OF PHYTOPLANKTON
IN THE CANTABRIAN SEA
The annual cycle of phytoplankton in the
Cantabrian Sea shows the typical pattern of a temperate sea (Fernández, 1990 a,b), with some special
peculiarities.
Winter mixing: There are no differences in water
density so the masses mix throroughly. The mixing
layer is deeper than the euphotic layer, so that even
the nutrients are present in high concentrations. The
low irradiance levels and the permanence of phytoplankton for a long time out of the photic zone results
in low biomass and production of phytoplankton.
Spring bloom: During spring, surface layers
receive increasing irradiance and heat giving rise to
a relative stabilization of the water column and the
spring outburst of phytoplankton; Smetaceck and
Passow (1990) have recently revised the criticaldepth model by Sverdrup (1953) and suggested that
the existence of a well-defined mixing layer is not
strictly necessary for phytoplankton development as
is a certain degree of stability in the upper meters of
water column. This hypothesis seems to be confirmed in the Cantabrian Sea and in the area near the
Galician shelf (NW of Spain) (Fernández and Bode,
1991; Valdés et al., 1991; Casas, 1995).
Summer stratification: Solar radiation increases
during summer and thewater column clearly strati-
Fig. 1.– Circulation pattern of surface waters in the Cantabrian Sea during winter-spring.
fies. The photic layer is deeper than the mixing
layer. Phytoplankton growth exhausts nutrients, and
phytoplankton biomass become very low. The existence of the thermocline acting as a physical barrier
prevents the supply of nutrients from deep layers to
surface layers. In this season, and under certain circumstances, episodies of red tides can occur. Even
though this is a poorly documented event in the
Cantabrian, some data suggest that this could take
place (Estrada, 1982). In any case according to
available information this seems to be an exception
more than a general feature.
Autumn mixing: Surface layers cool and sink, and
the thermocline is destroyed. The water column
mixes thoroughly and nutrients become available. A
phytoplankton bloom occurs when mixing is moderate. This outburst of phytoplankton is less important
and persistent than that of spring, but some evidence
of its existence exist (Estrada, 1982; Fernández,
1990a).
PECULIARITIES OF SEASONAL CYCLE OF
PHYTOPLANKTON
The annual cycle outlined above presents some
particular aspects in contrast to other temperate
areas.
During spring, the stratification of the water column previous to the phytoplankton outburst has
essentially a saline origin, in contrast to other areas
of Bay of Biscay where the stratification is of thermal origin (Fernández, 1990a). In the Cantabrian
Sea the stratification of coastal waters may originate
as a result of the eastern surface currents, which prevailed during this season (Fig. 1). The water masses
transported by these currents had a higher salinity
than typical surface waters from the Bay of Biscay.
In addition, the flow helps to retain low salinity
water close to the coast (Botas et al., 1989). Therefore the saline stratification is the mechanism generating the relative stability neccesary for development of phytoplankton spring blooms.
During the period of stratification, the most
important feature of stratified waters is the existence
of a subsurface chlorophyll maximum (SCM)
(Longhurst and Harrison, 1989; Fernández and
Bode, 1991). This SCM in the Cantabrian Sea is
related to the nitracline (Fernández and Bode, 1991).
This relationship is different to that found in northern areas of the Bay of Biscay where the SCM is
related to a thermocline (Holligan et al., 1984). This
apparent mistmatch resuls from the different vertical
structure between the two areas. In the weak tidal
regions of the Western English Channel, the seasonal thermocline is very sharp, with a gradient of c.a
1°C m-1 (Pingree et al., 1976). On the contrary, in
the Cantabrian Sea, as in the frontal areas of the
northern Bay of Biscay, the vertical distribution of
temperature shows a gradual decrease from 0 to 50
m (Botas et al., 1989).
The higher values of primary production during
the stratified period are measured at subsurface layers just above the SCM. The different vertical position of both maxima and the coupling between the
nitracline and the SCM define a vertical structure
similar to that found in the western Mediterranean
Sea (Estrada, 1985), and can be adscribed to the typical tropical structure as defined by Herbland and
Voituriez (1979) and Cullen (1982). Even though
passive accumulation is one of the main mechanisms accounting for the maintenance of SCM, the
relatively high estimated doubling time (0.8-3
turnover days), the close relation between SCM and
PHYTOPLANKTON ECOLOGY IN THE BAY OF BISCAY 47
nitracline as well as the species composition dominated by diatoms (Fernández, 1990a), suggest that
active growth is the most likely cause of SCM formation in the Central Cantabrian Sea (Fernández
and Bode, 1991).
MODIFICATIONS TO THE GENERAL
PATTERN OF ANNUAL CYCLE
Even though the spring and autumn blooms (the
later to a lesser extent), are observed year after year,
the general pattern of seasonal cycle of phytoplankton outlined above, can be modified by the effects of
two main oceanographic processes characteristic of
this area: a) the intrusions of high salinity waters during transition periods mixing-stratification; and b)
the coastal upwelling during summer stratification.
Saline intrusions: The water mass related to
saline intrusions shows characteristics of ENAWt
(Eastern North Atlantic Central Water of subtropical
origin; Ríos et al., 1992). This water originates in
the Northern Azores and flows poleward along the
Portuguese and Galician slopes (Frouin et al., 1990).
This slope current gives rise to a convergence front,
localized in the boundary zone between the stratified
coastal water and the off shelf well mixed oceanic
water. This frontal structure is of great importance in
(A)
(B)
Fig. 2.– Vertical profiles of salinity (A) and chlorophyll (B) in three transects inshore-offshore in March 1987 in the Cantabrian Sea. Early
stage of phytoplankton seasonal cycle. Adapted from Fernández et al. (1993)
48 M. VARELA
(A)
(B)
Fig. 3.– Vertical profiles of salinity (A) and chlorophyll (B) in three transects inshore-offshore in April 1987 in the Cantabrian Sea. Period
of Spring diatom bloom. Adapted from Fernández et al. (1991b)
determining the distribution, standing stocks,
growth rates, species composition and functioning
of various compartments of the planktonic system
during periods of vertical mixing.
The influence of slope current and associated
fronts on plankton dynamics is dependent on the seasonal stage of phytoplankton development. When a
convergent front develops in a very early stage, prior
to the typical spring diatom bloom (Fig. 2), this
results in an outburst of small flagellates (Fernández
et al., 1993). As far as I am aware there are not pub-
lished references about such high densities of
microflagellates during periods of strong vertical
mixing previous to the typical diatom bloom in the
North Atlantic. However this is a recurrent feature
arising from models on phytoplankton succesion at
47°N latitude (Taylor et al., 1993), and therefore the
lack of information on this type of bloom is probably
the result of an inadequate sampling coverage.
Sometimes the saline intrusion can present the
form of a well defined wedge across the shelf producing two fronts, on the shelf and at the outer shelf,
PHYTOPLANKTON ECOLOGY IN THE BAY OF BISCAY 49
Fig. 4.– Group of stations defined by multivariate analysis during a saline intrusion in the period of
Spring bloom in April 1987 in the Cantabrian Sea. Adapted from Fernández et al. (1991b)
separating three water mass bodies: coastal, saline
and oceanic waters (Figs. 3 and 4). Fernández et al.
(1991a) have studied the influence of this type of
saline intrusion in the Cantabrian Sea during the
diatom spring bloom. The species composition of
phtyoplankton in coastal stations is the typical
spring bloom, and is dominated by diatoms, as
described in other regions of the Bay of Biscay
(Holligan and Harbour, 1977; Treguer et al., 1979;
Estrada, 1982). Microflagellates dominated the
saline water body. Probably most of these microflagellates are heterotrophs (Fernández et al., 1991a).
Chemically the water body is characterized by high
nitrite and inorganic nutrient concentrations and low
values of dissolved oxygen, suggesting the predominance of regeneration over uptake processes (Botas
et al., 1988). The microbial loop (Azam et al.,
1983), is the dominant trophic web in this water. In
oceanic stations, nutrients are present in high concentrations and the ratios nitrate/phosphorus and
nitrate/silicate were close to Redfield’s ratio (Botas
et al., 1988). This feature implies an equilibrium
between uptake and regeneration or input of nutrients from advection processes in oceanic waters.
Microplankton composition was represented by a
mixed diatom-small dinoflagellate community, and
their abundances seem to be the result of passive
accumulation. Mixing of waters with different densities at the frontal margin would give rise to a
downward circulation, and therefore retention
50 M. VARELA
processes (Fernández et al., 1991a) such as those
proposed by Heywood and Pridle (1987) in an eddy
system.
There is some evidence that the amount of
ENAWt varies from year to year. In years of low
flow there is more chance for the formation of fronts
in the shelf and near the shelf-break. These fronts
provide favourable conditions for extensive blooms
(Varela, 1992). On the contrary, high flow of
ENAWt washes out surface waters and prevents the
formation of massive blooms (Bode et al., 1995)
When a saline front develops, different food
webs characterize both sides of the fronts. In the
saline area of the front, a regenerating system based
on the microbial food chain became dominant. On
the contrary, in the other part of front where different populations of chain-forming diatoms are the
bulk of phytoplankton biomass, the classical food
web prevailed.
Summer upwelling: During summer two mechanisms exist to modify the original stratified water
column: internal waves and advection of deep
upwelling water. We know about the existence of
internal waves in the Bay of Biscay (Holligan et al.,
1985; Pingree et al., 1986; New, 1988) even though
their periodicity and general influence on plankton
dynamics has not been studied, at least in the
Cantabrian Sea. This process affects the phytoplankton growth because it gives rise to an elevation
of pycnocline and therefore an elevation of SCM,
Fig. 5.– Circulation pattern of surface waters in the Cantabrian Sea during summer
causing an important increase in primary production
(Holloway and Denman, 1989).
The existence of a coastal upwelling in the western Cantabrian Sea was predicted by Mateo (1955)
on the basis of the frequency of dominant winds.
Later on, Dickson and Hughes (1981) pointed out
the existence of cold water in the vicinity of the
coast using satellite images. More recently Ríos et
al. (1987), obtain the first oceanographic data confirming the existence of a coastal upwelling that
occurs all summer round (Botas et al., 1990).
During summer the surface currents flow to the
west (Fig. 5) causing coastal upwelling. The stratification pattern during this season is modified by this
advection of deep nutrient-rich water. In such hydrographic conditions, the SCM and the primary production maxima were located at the same depth, thus giving rise to a vertical structure typical of temperate seas
Fig. 6.– Integrated values of chlorophyll and primary production
in upwelling and stratified stations during the upwelling period in
the Cantabrian Sea. Data relative to first 20 m. Adapted from
Fernández et al. (1990a)
(Cullen, 1982) and the highest rates of carbon incorporation of the year (Fernández and Bode, 1991).
The enrichment caused by nutrients, in the phase
of maximum intensity, and related to first 20 m of
water column, may account for an increase of 250%
of integrated Chl a and 170% in primary production
rates (Fig. 6) as compared to stratified stations (Fernández, 1990a).
THE INFLUENCE OF FRONTS IN FISHERIES
Hydrographic events, in particular fronts, play a
crucial role as barriers for eggs and larval transport.
The close association between spawning areas and
shelf-edge fronts have been established in many
areas of the Atlantic (Iles and Sinclair, 1985; Heath
and MacLachlan, 1987; Coombs et al., 1990).
The success of recruitment of pelagic fishes is
highly dependent on spawning taking place in areas
where the newly hatched larvae find the appropriate
food type and size. As reported in coastal jet frontal
regions (Fortier et al. , 1992), the different trophic
food webs which characterize both sides of the front
were exploited by different fish species for reproduction.
Sardine larvae (Fernández et al., 1993) were
more abundant in the part of the front where the
trophic food web based on the microbial loop prevailed. The density of sardine larvae was similar to
those previously reported (Chesney and AlonsoNoval, 1989) in the same period of the year when
maximum sardine spawning is likely to occur. On
the contrary, the larval stages of blue whiting mostly appeared in the oceanic side of the front (Fig. 7),
where the classical food web is dominant. The differences in the distributions of these larvae probably
PHYTOPLANKTON ECOLOGY IN THE BAY OF BISCAY 51
Fig. 7. – Abundances of three different fish larvae at both sides of a frontal zone in the Cantabrian
Sea in March 1987. Adapted from Fernández et al. (1993)
reflects the distinct adaptation to size and type of
preys. Anchovy larvae feed on particles between 4080 μm, and they do not feed on diatoms (Lasker
1978). Probably sardine larvae exhibit a similar
behaviour. Then, the area where the food web based
on microbial loop prevails would be more appropriate for feeding of these larvae because of the abundance of flagellate and ciliates of adequate size. On
the contrary, the zones of frontal area with a classical food web, where diatoms are dominant, would
not be suitable for larval feeding.
In summary, the timing of fish-recruitment and
the occurrence of these fronts may decide the success of the local populations since some of the most
important fishing species hatch during the spring.
Some study programs related to the recruitment of
local pelagic fisheries found a really complicated
distribution pattern of both eggs and larvae, suggesting a strong influence of local and regional
hydrographic processes (López-Jamar et al. 1991).
These interactions between regional hydrography,
planktonic productivity and fish larvae deserve further study in the Bay of Biscay
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