Seasonal variations in upwelling and in the grazing impact of copepods on phytoplankton off A Coruña (Galicia, NW Spain

www.elsevier.com/locate/jembe

Journal of Experimental Marine Biology and Ecology

297 (2003) 85–105

Seasonal variations in upwelling and in the grazing

impact of copepods on phytoplankton off A Coruna

(Galicia, NW Spain)

A. Bode*, M.T. Alvarez-Ossorio, S. Barquero1,J. Lorenzo, A. Louro, M. Varela

Centro Costero de A Coruna, Instituto Espanol de Oceanografıa, Apdo. 130, 15080 A Coruna, Spain

Received 21 February 2003; received in revised form 16 July 2003; accepted 23 July 2003

Abstract

The impact of grazing by copepods on phytoplankton was studied during a seasonal cycle on the

Galician shelf off A Coruna (NW Spain). Grazing was estimated by measuring the chlorophyll gut

content and the evacuation rates of copepods from three mesh-size classes: 200–500 (small), 500–

1000 (medium), and 1000–2000 Am (large). Between February 1996 and June 1997, monthly

measurements of water temperature, chlorophyll concentration, primary production rates, and

copepod abundance, chlorophyll gut content, and evacuation rates were taken at an 80-m-deep, fixed

shelf station. Additionally, the same measurements were collected daily during two bloom events in

March and in July 1996. Small copepods were the most abundant through the seasonal cycle. The

highest grazing impact, however, was due to the medium and large size classes. Grazing by small

copepods exceeded grazing by medium and large copepods only during phytoplankton spring

blooms. The impact of copepod grazing (considering all size fractions) was generally low. On

average, 2% of the phytoplankton biomass and 6% of the primary production were removed daily by

the copepod community. Maximum grazing impact values (9% of the phytoplankton biomass and

39% of the primary production) were found in mid-summer. These results suggest that most of the

phytoplankton biomass would escape direct copepod grazing in this upwelling area.

D 2003 Elsevier B.V. All rights reserved.

Keywords: Zooplankton; Grazing; Copepods; Upwelling; Phytoplankton; NW Spain

0022-0981/$ - see front matter D 2003 Elsevier B.V. All rights reserved.

doi:10.1016/S0022-0981(03)00370-8

* Corresponding author. Tel.: +34-981205362; fax: +34-981229077.

E-mail address: [email protected] (A. Bode).1 Present address: Plymouth Marine Laboratory, Prospect Place, The Hoe, Plymouth PL1 3DH, UK.

A. Bode et al. / J. Exp. Mar. Biol. Ecol. 297 (2003) 85–10586

1. Introduction

Plankton dynamics in northeastern Atlantic waters show a seasonal cycle typical

of temperate latitudes, determined by alternating periods of mixing and stratification

in the water column (e.g., Colebrook, 1979). During the spring, phytoplankton

blooms are favoured by higher irradiance and lower turbulence in the upper water

layers (Smetacek and Passow, 1990) and by the scarce numbers of mesozooplankton

(>200 Am) grazers that survived the winter (Dam et al., 1993; Lenz et al., 1993;

Barquero et al., 1998). During the autumn, blooms may be produced at the

expenses of deep-water nutrients when the water overturns (Holligan, 1987).

Following the bloom of phytoplankton, the mesozooplankton usually shows two

annual maxima of abundance in late spring and autumn (Colebrook, 1979).

Although earlier models considered that zooplankton grazing was the ultimate cause

for bloom control and termination (e.g., Evans and Parslow, 1985), later experiments

carried out at sea revealed that other factors, such as nutrient depletion (Rees et al.,

1999) or water transport (Varela et al., 1991; Barquero et al., 1998), were more

effective than grazing in the removal of the phytoplankton biomass accumulated

during blooms.

In shelf waters of Galicia (northwestern Spain), these typical seasonal patters are

largely modified by the influence of coastal upwelling, which favours episodic blooms

between March and October (e.g., Valdes et al., 1991; Varela, 1992; Casas et al.,

1997). The high primary productivity induced by upwelling events sustains subsequent

maxima of mesozooplankton abundance and biomass (Braun et al., 1990; Valdes et al.,

1990a,b, 1991), which in turn support important fisheries (Tenore et al., 1995).

However, available estimates of the grazing impact on the Galician shelf give

contradictory results with respect to the actual importance of mesozooplankton (mostly

copepods) within the food web in this upwelling region. Some studies concluded that

copepods grazed daily most of the primary production during upwelling events (Braun

et al., 1990; Valdes et al., 1990b; Varela et al., 1991; Tenore et al., 1995), while

recently, it has been shown that grazing losses due to copepods are of minor

importance during blooms following upwelling phenomena (Barquero et al., 1998;

Batten et al., 2001; Halvorsen et al., 2001a,b). As in other areas, it is likely that the

amount of phytoplankton biomass consumed by mesozooplankton varies through the

annual cycle as a consequence of the uncoupling between phytoplankton and

mesozooplankton at short time scales (Colebrook, 1979), thus affecting the determi-

nation of the importance of grazing. To date, there have been no seasonal studies of

grazing in shelf waters of the Galician upwelling, although Miranda et al. (1991)

concurrently measured primary and secondary production in plankton of the Rıa de

Vigo inlet.

The objective of this study is to evaluate the impact of grazing by copepods on

the phytoplankton during the seasonal cycle in the shelf waters off Coruna and

relate that impact to the size composition of the copepod community. The study site

is regularly sampled since 1988 as part of the Oceanographic Time-Series Program

of the Instituto Espanol de Oceanografıa (Valdes et al., 1991, 2002; Casas et al.,

1997).

A. Bode et al. / J. Exp. Mar. Biol. Ecol. 297 (2003) 85–105 87

2. Methods

Between February 1996 and June 1997, monthly samples were collected at Station 2

(43j25.3’N, 8j26.3’W, 80 m deep) off A Coruna (Galicia, NW Spain) (Fig. 1). Two series

of daily samples were also taken during two bloom episodes in 1996 between 11 and 18

March and between 23 and 30 July. At each sampling date, vertical distribution of water

temperature and chlorophyll fluorescence were determined with a CTD Seabird SBE-25,

and irradiance was measured with a LiCor spherical light sensor. Water samples for

chlorophyll analysis and primary production incubations were collected with Niskin

bottles at depths equivalent to 100%, 50%, 25%, 10%, and 1% of surface irradiance.

The concentration of chlorophyll a and phaeopigments were analyzed in acetone extracts

of phytoplankton collected onto glass-fibre Whatman GF/F filters in a Turner-Designs

fluorimeter (UNESCO, 1994; Bamstedt et al., 2000). Primary production was measured

following the 14C method (UNESCO, 1994): triplicate water samples from each depth

were incubated for 2–3 h around noon in simulated natural conditions of light and

temperature (Bode et al., 1994; Bode and Varela, 1998). Daily rates of primary production

were estimated by multiplying hourly rates by the photoperiod. In this study, both

Fig. 1. Map of sampling site off A Coruna (NW Spain).


phytoplankton pigment and primary production data were reported as integrated values in

the whole water column. Mesozooplankton samples were collected by vertical hauls from

75 m depth to surface with a Bongo-type net of 200-Am mesh size. All samples were

collected between dawn and noon and were gently sieved on board through 2000-, 1000-,

500-, and 200-Am meshes. Each size fraction of zooplankton was divided into two

aliquots: one was collected onto glass-fibre filters and frozen to later analyse the pigment

gut content, and the second one was preserved in formalin for counting and identification

of species. For the purpose of this paper, only copepod species able to consume

phytoplankton, but which probably act as omnivores (e.g., Halvorsen et al., 2001a), were

considered. Species with potentially carnivorous diets (Greene, 1985), namely, Aetideus

armatus, Paraeuchaeta hebes, Metridia lucens, Pleuromamma gracilis and Candacia

armata, were excluded. Biomass of copepods (W, Ag C individual� 1) was estimated in 20

samples collected between September 1996 and September 1997. The samples were size-

fractionated as described above, and the herbivorous copepods isolated and counted and

finally dried (60 jC, 24 h) and weighted. The carbon content per copepod was determined

by assuming an average carbon content of 41.5% of dry weight (Parsons et al., 1984).

Grazing was estimated by measuring the content of chlorophyll a in the gut of

copepods from each size class (Mackas and Bohrer, 1976; Pasternak, 1994; Bamstedt et

al., 2000) as described in Barquero et al. (1998). The gut content (GC) is expressed in

chlorophyll a equivalents following Bamstedt et al. (2000). To determine GC, copepods

from herbivorous species were individually picked up from frozen aliquots under a

binocular microscope and transferred to vials containing 90% acetone to analyse fluori-

metrically the content of chlorophyll a in their guts (UNESCO, 1994). The procedure was

carried out in dim light and at low ambient temperature to avoid the degradation of the

pigments.

The rates of gut evacuation of copepods (k) were determined during on board

experiments in March and July 1996. The animals for the experiments were collected

from slow net hauls and immediately placed in a tank of filtered seawater (Whatman GF/F)

and kept at sea-surface temperature. To measure the decrease in the gut content with time

(t), samples of animals were collected from the tank at intervals of 0, 5, 10, 20, 40, 60, and

90 min to measure their GC. The evacuation rates were calculated from the equation:

GCt ¼ GC0 � e�kt

where GC0 is the gut content at the beginning of the experiment and GCt is the gut content

at the interval time t (Bamstedt et al., 2000). Separate experiments were run for copepods

in each of the size fractions.

Finally, the ingestion rate of phytoplankton by copepods (I) was estimated from the

product of chlorophyll a concentration in the gut contents of individual copepods, the gut

evacuation rate, and the abundance of herbivorous copepods species (A):

I ¼ GC� k � A

Grazing rates were converted to carbon units using the equivalence 50 g C (g Chl a)� 1.

Grazing by the community of copepods was estimated as the total sum of grazing rates by

each of the three size classes.

Fig. 2. Variations of temperature at the surface and at 70 m depth (a), water column-integrated chlorophyll a and

phaeopigment concentrations (b) and daily primary production during the study (c).



The contribution of herbivorous grazing to the carbon requirements of copepods was

determined as in Halvorsen et al. (2001a). First, we estimated the respiration of an average

copepod from each size fraction (R, Al O2 h� 1) from the empirical model by Mauchline

(1998):

log R ¼ 0:787 log ðW=1000Þ þ 0:245

Next, minimum (only respiration) and mean (respiration plus net growth) daily carbon

requirements were computed by assuming a constant relationship between respiration and

ingestion, a respiratory quotient of 0.97, and assimilation and gross growth efficiency

values of 70% and 30%, respectively.

Table 1

Mean abundance (individuals m� 3) of herbivorous copepod species during the study

Species Mean S.E. n

Copepodites 670.0 114.3 8

Oncaea spp. 386.1 103.7 8

Clausocalanus spp. 319.0 102.3 8

Paracalanus parvus (Claus, 1863) 279.8 110.9 8

Acartia clausi (Giesbrecht, 1889) 234.0 63.3 8

Oithona spp. 153.8 30.7 8

Temora longicornis (Muller, 1792) 87.9 35.2 7

Calanus spp. (young) 72.3 34.4 8

Acartia spp. (young) 63.3 17.0 8

Centropages spp. (young) 57.0 22.5 8

Calanus helgolandicus (Claus, 1863) 49.8 20.8 8

Calanoides carinatus (Kroyer, 1848) 46.9 19.6 8

Pseudocalanus elongatus (Boeck, 1865) 40.1 16.7 8

Ctenocalanus vanus (Giesbrecht, 1889) 39.9 10.2 8

Temora stylifera (Dana, 1849) 36.8 15.3 6

Calocalanus styliremis (Giesbrecht, 1888) 29.3 12.1 7

Centropages chierchiae (Giesbrecht, 1889) 27.0 9.7 7

Copepod nauplii 24.6 11.5 8

Diaxis durani (Corral, 1792) 23.3 8.0 6

Euterpina acutifrons (Dana, 1852) 13.4 7.1 8

Microcalanus pusillus (Giesbrecht, 1888) 10.5 1.5 2

Diaxis hibernica (A. Scott, 1896) 6.4 1.8 7

Isias clavipes (Boeck, 1864) 6.2 2.7 5

Scolecithricella dentata (Giesbrecht, 1892) 3.0 2.0 2

Shapphirina angusta (Dana, 1849) 3.0 – 1

Mesocalanus tenuicornis (Dana, 1849) 2.3 0.5 4

Centropages typicus (Kroyer, 1849) 2.3 0.6 4

Subeucalanus crassus (Giesbrecht, 1888) 2.0 0.4 4

Clytemnestra rostrata (Brady, 1883) 2.0 0.7 7

Microsetella rosea (Dana, 1852) 2.0 – 1

Corycaeus spp. 1.7 0.3 3

Ischnocalanus tenuis (Farran, 1926) 1.5 0.3 4

Nannocalanus minor (Claus, 1863) 1.0 – 1

Harpacticoidea 0.7 0.3 3

S.E.: standard error.


3. Results

3.1. Seasonal variations of phytoplankton and zooplankton

The temporal distribution of temperature reflected the summer warming of the surface

and also showed very clearly the effect of upwelling events during 1996, as deep cool

water from the ocean (below 13 jC) washed the bottom layers at Station 2 in March and

again in July (Fig. 2a). Chlorophyll biomass reached the highest values in spring both

years and was generally lower during winter (Fig. 2b). However, very low concentrations

of chlorophyll were also measured in July 1996, when maximum differences between

surface and bottom temperature indicated the development of an upwelling pulse.

Phaeopigments varied in parallel with chlorophyll except during bloom development (as

in March 1996). The temporal variation of primary production values (Fig. 2c) was

parallel to that of chlorophyll and the two variables were significantly correlated

(r = 0.832, p < 0.0001, n = 30).

Fig. 3. Variations in the abundance of herbivorous copepods (a) and chlorophyll gut content of herbivorous

copepods (b) in the 200–500-, 500–1000-, and 1000–2000-Am size classes during the study.


A total of 31 taxa of omnivorous copepods were identified in the zooplankton samples,

of which Oncaea, Clausocalanus, Paracalanus, Acartia, Oithona, and Temora had mean

abundances exceeding 100 individuals m� 3 and made up nearly 75% of the copepod

community (Table 1). In addition, copepodites and nauplii (mostly from these genera) also

reached high abundances. Herbivorous copepods were more abundant during summer and

autumn, although had secondary maxima in spring (Fig. 3a). The lowest numbers were

found in winter. The abundance of the three size classes of copepods varied similarly,

although the number of small copepods (200–500 Am) increased earlier in the season than

larger species. In particular, rapid changes in the abundance of copepods were seen during

the blooms in March and July 1996. The content of chlorophyll in the gut of medium

(500–1000 Am) and large copepods (1000–2000 Am) increased in summer, thus

paralleling their general increase in abundance, but other peaks in gut content during

spring and autumn were not clearly related to abundance (Fig. 3b). Compared to larger

Fig. 4. Daily variations of water column-integrated chlorophyll a during phytoplankton blooms in March (a) and

July 1996 (b).


copepods, the small copepods had uniformly low chlorophyll gut content for most of the

year with peaks in spring and summer.

3.2. Daily changes during blooms

The two blooms studied in 1996 differed in their state of development. In the case of

the March bloom, chlorophyll increased rapidly after 14 May, and on 17 May, the

concentration reached over 100 mg Chl a m� 2, more than five times the initial

concentration (Fig. 4a). At the same time, phaeopigments only showed a slight increase.

During this bloom, water temperature at Station 2 remained approximately constant, with

both surface and bottom values ranging between 12.43 and 12.74 jC (Fig. 2a). These

characteristics are typical of the early, active stage of a bloom, typical of the spring (e.g.,

Casas et al., 1997). In contrast, the situation found in July represented a period in-between

blooms. Chlorophyll concentration decreased at the beginning, reached a minimum on 27

Fig. 5. Daily variations in the abundance of herbivorous copepods in the 200–500-, 500–1000-, and 1000–2000-

Am size classes during phytoplankton blooms in March (a) and July 1996 (b).


July, and increased thereafter at a steady rate until the end of the study (Fig. 4b). In

addition, the differences between chlorophyll and phaeopigment concentrations first

decreased and later increased, indicating the change in growth state of the phytoplankton

population. However, due to the large variability found in March, the average values of

integrated chlorophyll and primary production were not significantly different between the

two blooms (Mann–Whitney test, p>0.05).

3.3. Abundance and chlorophyll gut content of copepods during blooms

The abundance of the three size classes of copepods in the July bloom was significantly

higher than abundance in March (Fig. 5a and b, Mann–Whitney test, p < 0.01). In contrast,

the chlorophyll gut content of large copepods did not show significant differences between

the bloom in March and the bloom in July (Fig. 6a and b). Medium-sized copepods,

however, had a significantly higher mean gut content of chlorophyll in July than in March

Fig. 6. Daily variations of chlorophyll gut content of herbivorous copepods in the 200–500-, 500–1000-, and

1000–2000-Am size classes during phytoplankton blooms in March (a) and July 1996 (b).

Fig. 7. Time-course variation of chlorophyll gut content of herbivorous copepods (GCt) in the 200–500- (a),

500–1000- (b), and 1000–2000-Am (c) size classes. The regression line fitted to each data set is indicated.



Table 2

Contribution of copepod size classes to the estimates of total ingestion rates

Variance component r df SS % SStotal

I500 0.946 1 91.08 89.5

I1000 0.936 1 8.47 8.3

I200 0.848 1 2.25 2.2

Total – 24 101.80 100.0

Total ingestion was related by a linear ANOVA model to ingestion rates computed for each size class entered

sequentially according to their correlation values (r) with the predicted variable. I200, I500, and I1000 stand for

ingestion rates in 200–500-, 500–1000-, and 1000–2000-Am size classes, respectively. The variance

contribution of each size class (% SStotal) was expressed as the percentage of total sum of squares (SS). df:

degrees of freedom.


(Mann–Whitney test, p < 0.05). In the case of small copepods, no statistical difference was

detected, although the chlorophyll content increased towards the end of the March bloom

(Fig. 6a).

3.4. Evacuation rates

The evacuation rates of the gut content of copepods determined during the onboard

experiments were 0.01, 0.02, and 0.03 min� 1, for the small, medium, and large size

classes, respectively (Fig. 7). These values, however, were not statistically different

(ANCOVA, p < 0.05), and thus, a constant evacuation rate of 0.02 min� 1 was used for

all size fractions.

3.5. Copepod grazing rates

Ingestion of phytoplankton by copepods reached maximum values in late summer, with

secondary peaks appearing in spring and autumn (Fig. 8a). The seasonal pattern of grazing

followed that observed for copepod abundance (Fig. 3a). On average, medium-sized

copepods contributed to ca. 90% of the total annual ingestion of phytoplankton. The

contribution of large copepods was < 10%, and that of small copepods was only marginal

(Table 2). However, during the March 1996 bloom and again in March 1997, small

copepods were the most active grazers (Fig. 8a and b).

During the March bloom in 1996, grazing by small copepods increased exponentially

(Fig. 8b) following the growth of phytoplankton (Fig. 4a). The ingestion rate by the

medium-sized copepods also seemed to increase slightly at the end of the study. In

contrast, the rate of grazing by large copepods slowly decreased during the bloom (Fig.

8b). Because of these changes in the feeding pattern, the ingestion of phytoplankton was

dominated by large copepods at the start of the bloom, but at the end, it was the smaller

copepods that had a major impact. In the July bloom, the situation changed, and the

Fig. 8. Daily chlorophyll ingestion rates by herbivorous copepods in the 200–500-, 500–1000-, and 1000–2000-

Am size classes during the study (a) and during March (b) and July 1996 (c). Note that the ingestion rates for the

whole study period are represented in a logarithmic scale while those for March and July are reported in

arithmetic scales.


medium-sized copepods generally had the largest contribution to total ingestion (Fig. 8c).

At the same time, the ingestion by the larger copepods was very irregular.

3.6. Grazing impact on phytoplankton

All the described variations in phytoplankton and grazing rates were summarized for a

typical annual cycle (Fig. 9). The daily grazing impact of copepods on phytoplankton

biomass was low through spring, rarely reaching 1% between February and June (Fig. 9a).

The highest impact, 9%, occurred during the bloom in July 1996, but decreased again later

and stayed very low during the winter (ca. 0.1% in January and December). The seasonal

pattern of the impact of grazing on primary production was very similar but with higher

values than the impact on the biomass. For instance, copepods consumed on average 39%

of primary production in July (Fig. 9a). From these results, we estimate that the annual

mean of the daily grazing impact on phytoplankton is equivalent to 1.6% of the biomass

and 5.8% of primary production.

Fig. 9. Mean (F S.E.) impact of daily copepod ingestion rates on (a) chlorophyll (%Chl a) and primary

production (%PP) during an annual cycle. The mean grazing impact during blooms in March and July 1996 are

also shown (b). The number of samples averaged is indicated above bars.

Table 3

Estimated carbon requirements and herbivorous grazing expressed as percentage of mean copepod body carbon

(B)

Size class (Am) B (Ag C individual� 1) % Cmin % Cmean % Iherb

200–500 2.0F 0.8 (n= 20) 11.8 39.4 15.7F 26.5 (n= 24)

500–1000 10.3F 5.7 (n= 20) 8.3 27.7 5.6F 4.9 (n= 24)

1000–2000 27.8F 15.5 (n= 20) 6.7 22.3 7.2F 6.9 (n= 24)

% Cmin and % Cmean: minimum and mean percent daily requirements of carbon, respectively, computed from the

respiration estimated from the empirical model of Mauchline (1998). The assumptions included a constant

relationship between ingestion and respiration, a respiratory quotient of 0.97, an assimilation efficiency of 70%,

and a gross growth efficiency of 30%. % Iherb: measured phytoplankton-carbon ingested by copepods expressed

as percentage of mean copepod body carbon. Standard errors and number of determinations (n) for B and % Iherbare indicated.


The grazing impact of copepods was significantly different for the two blooms studied

(Mann–Whitney test, p < 0.05, Fig. 9b). Copepod grazing daily removed less than 1% of

phytoplankton biomass during March, but nearly 7% in July. Similarly, the impact of

grazing on primary production increased from 3% during the March bloom to 30% in July.

3.7. Herbivory and carbon requirements

Average values of daily herbivorous grazing by small, medium-sized and large

copepods were equivalent to 16%, 6%, and 7% of individual body carbon, respectively

(Table 3). These values are slightly higher than the minimum metabolic requirements for

each size class, also expressed as percent of body weight. However, daily phytoplankton

consumption was, on average, between three (small and large copepods) and five times

lower (medium-sized copepods) than the estimated mean daily carbon requirements

including net growth of copepods.

4. Discussion

The estimations of copepod grazing from their pigment gut content are comparable to

those obtained from other experimental methods (Peterson et al., 1990; Pasternak, 1994;

Bamstedt et al., 2000; Calbet, 2001). The gut fluorescence method has the advantage of

causing minimal disturbance of the animals because incubation is only required in order

to experimentally determine gut evacuation rates. It also allows for the measurement of

grazing in specimens of different body size, which is very important, as grazing rates are

largely size dependent (Barquero et al., 1998; Halvorsen et al., 2001a). The three

variables needed to estimate grazing rates, evacuation rates, gut content, and abundance

of copepods, vary with the size of the animal. In this study, gut evacuation rates increased

from small to large copepods, as found previously by Barquero et al. (1998) in the same

region. In addition, the evacuation rates computed in this study are within the range

0.01–0.05 min� 1 measured in the Atlantic Ocean (Huskin et al., 2001). Some studies

have found a linear relationship between evacuation rates and temperature (e.g., Irigoien,

1998) that can be used to estimate these rates without experimental data (Halvorsen et al.,


2001a). According to the empirical model of Irigoien (1998) and considering a mean

water temperature of 15 jC, the expected evacuation rate for this study would be 0.04

min� 1, which is slightly higher than the rate determined experimentally for large

copepods (0.03 min� 1). No significant differences were found between the evacuation

rates measured in March and in July (ANCOVA, p>0.05), which suggests that the

variations of water temperature during the experiments did not affected the gut

evacuation of the copepods.

Day to night variations in the gut content of copepods has previously been reported.

The highest values generally appeared at night and occasionally doubled those at daytime

(Barquero et al., 1998; Halvorsen et al., 2001a). The samples for this study were always

taken between dawn and noon; however, it is not likely that the impact of grazing has been

significantly underestimated. First, gut content values were within the range reported for

the Galician shelf. Second, even if we consider an increase by a factor of two in our

estimates, herbivorous grazing will still be far from controlling phytoplankton in most

cases. Similarly, if we account for pigment degradation inside copepod guts (Bamstedt et

al., 2000), the recalculated grazing impact on phytoplankton would amount on average

11% of standing stock and 41% of primary production, which are equivalent to values

estimated by Halvorsen et al. (2001a).

Medium-sized copepods (500–1000 Am) were the most effective grazers through the

year, followed by large (1000–2000 Am) copepods. In comparison, copepods smaller

than 500 Am must reach very high abundances (e.g., in March 1996) to have a

significant impact on phytoplankton standing stock or primary production values. These

findings agree with an earlier study during a spring bloom in the same area by Barquero

et al. (1998), while higher grazing rates by small copepods have been reported by

Halvorsen et al. (2001a) in an upwelling filament during summer to the south of the

Galician shelf. It is likely that the species and size of phytoplankton and zooplankton

affect the impact of grazing. For instance, several studies show that the impact of grazing

by copepods on phytoplankton biomass and production can increase notably when

considering only phytoplankton cells larger than 2 Am (Halvorsen et al., 2001a; Huskin

et al., 2001). In the present study, we have not size fractionated our measurements of

phytoplankton biomass and primary production. However, in a previous study in the

same area, we have shown that the average contribution of net phytoplankton (>12 Am)

to both total phytoplankton biomass and production was ca. 50% during blooms, while

its contribution during late summer and winter periods was < 30% (Bode et al., 1994;

Casas et al., 1997). Such dominance of relatively large-sized phytoplankton cells and

colonies (mostly diatoms), typical of upwelling areas, may explain the relatively higher

impact of medium and large copepods in total phytoplankton biomass or production

when compared to small copepods in the study area. Other studies showed the ability of

copepods to consume the cells that grow at faster rates within a large range of sizes (e.g.,

Poulet, 1978).

The daily variations in grazing rates observed during the two blooms emphasize the

relative uncertainty associated with seasonal cycles described with single monthly

observations. In addition, these variations indicate that the highest grazing impact occurs

when the phytoplankton bloom is in a late-development phase and when medium and large

copepods dominate (e.g., the July bloom in our study). Small-sized copepods, as those


dominating during early spring, have a limited capacity to consume significant amounts of

phytoplankton, because of their small guts compared to those of larger copepods. Their

high numbers do not compensate for these limitations. However, these small copepods are

known to consume significant amounts of microplankton (e.g., protozoa and other

crustacean plankton) in order to fulfil their metabolic requirements (Batten et al., 2001).

Variations in herbivorous grazing impact of a similar magnitude as those described here

were shown during Lagrangian studies following a recent upwelling in Galicia (Halvorsen

et al., 2001a). To date, all the studies about zooplankton grazing in the upwelling area off

Galicia covered periods from 1 to several weeks (Braun et al., 1990; Tenore et al., 1995;

Barquero et al., 1998; Batten et al., 2001; Halvorsen et al., 2001a,b). Only the seasonal

study of Miranda et al. (1991) in the Rıa de Vigo inlet, south of A Coruna, considered a

few monthly samples during spring and summer. The results of the present study provide

the first strong evidence of a low impact of copepod grazing over the entire seasonal cycle

in open waters of the Galician shelf.

Previous studies in the region using the gut fluorescence method have reported that

daily grazing impact rarely exceeded 10% of both biomass and production of the

phytoplankton (Barquero et al., 1998; Batten et al., 2001; Halvorsen et al., 2001a,b). In

contrast, other studies using 14C-labelled phytoplankton to measure feeding (Braun et al.,

1990; Miranda et al., 1991; Tenore et al., 1995) concluded that grazing losses accounted

for the total of phytoplankton biomass and more than 100% of primary production during

blooms induced by upwelling. It does not seem likely that the gut fluorescence method

underestimates grazing to such an extent compared to the 14C method. Rather, recent work

in this region suggests that earlier estimates of grazing impact on phytoplankton have been

biased by underestimated primary production rates and overestimated mesozooplankton

grazing. For instance, Braun et al. (1990) reported a maximum primary production rate of

169 mg C m� 2 day� 1 for coastal phytoplankton, which is lower than the maximum in

March 1996 in this study (>5000 mg C m� 2 day� 1). Another example is given by the

primary production values reported by Joint et al. (2002), which were greater than those

reviewed in Bode et al. (1994). In addition, it must be noted that the uncertainty in the

estimation of the grazing impact varies when either phytoplankton biomass or primary

production is considered. For instance, our estimations show that the mean grazing impact

in March and July varied daily by 47% and 37%, respectively, while the impacts relative to

primary production varied by more than 100%. This is particularly important in an area

where primary production values are generally high. Finally, the estimates of community

grazing by Tenore et al. (1995) were possibly too high because the biomass of

mesozooplankton was overestimated (Bode et al., 1998a).

There is increasing evidence that mesozooplankton grazing rarely exceeds 30% of

either phytoplankton biomass or production in temperate latitudes, even when taking into

account only phytoplankton fractions which are more likely consumed by copepods (Dam

et al., 1993; Huskin et al., 2001). Recent reviews indicate that the average impact of

grazers on primary production at a global scale is ca. 12%, with even lower values in areas

of high primary production (e.g., Calbet, 2001). Taking into account that the season of

high production of phytoplankton extends from March to October, and that most of this

production is due to net phytoplankton (Bode et al., 1994), we hypothesize that in this

upwelling ecosystem, the rates of accumulation of phytoplankton always exceed grazing


rates of copepods. Some studies in non-upwelling areas have suggested that zooplankton

can consume most of the primary production during periods when phytoplankton growth

decays and the abundance of zooplankton increase, thus contributing to terminate the

bloom (Lenz et al., 1993). However, in upwelling areas, grazing impact is generally low

(Landry and Lorenzen, 1989; Peterson et al., 1990; Verheye et al., 1992; Painting et al.,

1993), so other mechanisms can be invoked to explain bloom termination.

One mechanism of phytoplankton loss can be the transport of water from the coast

towards the shelf-break. For example, off Galicia, the rapid sinking of surface waters near

the shelf-break has been repeatedly cited as the cause of phytoplankton disappearance

(Varela et al., 1991; Barquero et al., 1998). In fact, export of surface waters by upwelling

dynamics appears as one of the most effective ways of reducing phytoplankton biomass

near the coast (Castro et al., 1994; Bode et al., 1998b). Recently, large upwelling-derived

filaments were reported to account for most of organic carbon export from the coast to

oceanic waters (Joint et al., 2001). Another mechanism can be sedimentation. Near the

coast, sedimentation of plankton debris (dead cells, faecal pellets, etc.) accounts for a small

fraction of the total particulate carbon export (Bode et al., 1998b; Hall et al., 2000; Riser et

al., 2001; Schmidt et al., 2002), but it may be of local importance near the shelf-break (De

Wilde et al., 1998). Finally, a third mechanism is grazing by microzooplankton ( < 200-Amsize), which was observed to be a major consumer of phytoplankton during summer

blooms on the shelf of this upwelling area (Bode and Varela, 1994; Fileman and Burkill,

2001; Halvorsen et al., 2001b).

The low impact of grazing found during this study suggests that copepods must rely on

other food sources in addition to phytoplankton, for example, smaller zooplankton or

detritus. The estimations in Table 3 indicate that, particularly, the medium-sized copepods

must complement their carbon intake with other food sources in order to fulfil their

metabolic requirements. This is supported by recent reviews (e.g., Calbet, 2001) and by

studies in Galician waters, in which microzooplankton accounted for up to 15% of the

daily carbon diet of copepods (Batten et al., 2001; Halvorsen et al., 2001a). In addition, the

ingestion of zooplankton faecal pellets has been estimated to be between 8% (Halvorsen et

al., 2001a) and 20% (Riser et al., 2001) of their daily carbon diet.

5. Conclusion

Grazing impact of herbivorous copepods on phytoplankton on the Galician shelf is

generally low for most of the year. Copepods can remove daily up to 9% of

phytoplankton biomass and ca. 40% of primary production during mid-summer, although

the annual impact is much lower with mean values around 2% of biomass and 6% or

production. The small size (200–500 Am) copepods were the most abundant, and they

were the most effective grazers during the spring bloom. However, medium and large-

sized copepods (500–2000 Am) dominated grazing for most of the year because of their

larger gut content and the dominance of relatively large phytoplanktonic particles. Taking

into account the metabolic requirements of copepods, herbivorous grazing probably needs

to be supplemented with the consumption of microplankton and other particles during

most of the year.


Acknowledgements

We are grateful to the crew of the R/V Lura and R/V Francisco de Paula Navarro for

their collaboration during sampling. We also acknowledge the collaboration of Isabel

Gonzalez in processing zooplankton samples. J.L., A.L., and S.B. were supported by

Training Fellowships of IEO-FSE, the FPII Programme of Xunta de Galicia, and the FPI

Programme of the Ministerio de Educacion y Ciencia (Spain), respectively. This study was

funded in part by project IEO-1007 and by project AMB1993-0014 of CICYT (Spain).

[RW]

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