Temporal and spatial changes in plankton respiration and biomass in the Canary Islands region: the...

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Journal of Marine System

Temporal and spatial changes in plankton respiration and biomass

in the Canary Islands region: the effect of mesoscale variability

Javier Arıstegui*, Marıa F. Montero

Facultad de Ciencias del Mar, Universidad de Las Palmas de Gran Canaria, Las Palmas de Gran Canaria, 35017 Las Palmas, Spain

Received 28 February 2002; accepted 1 July 2004

Available online 27 September 2004

Abstract

The temporal and spatial variabilities in the abundance and respiratory activity of plankton communities (b200 Am) were

studied during three seasonal cruises around Gran Canaria Island (Canary Islands), a region of high mesoscale variability.

Marked seasonal changes in respiratory activity, plankton community structure, and the ratio of heterotrophic to autotrophic

biomass can be largely explained by hydrographic changes at the mesoscale level. Wind/current shearing at the flanks of the

island enhances plankton respiration, presumably as the consequence of an increase in turbulence. Counter-paired cyclonic and

anticyclonic eddies generated downstream of the island act as a two-way biological pump, increasing plankton production by

nutrient pumping into the euphotic zone and accelerating the transport of organic matter into the aphotic zone, respectively.

Coastal upwelling waters invading the Canary region in the form of filaments can transport either water with low plankton

respiration and large phytoplankton cells or water with high respiratory rates associated with small cells. Plankton respiration

was closely related to the abundance of Synechococcus type cyanobacteria and heterotrophic nanoflagellates during the three

periods, but was only correlated with chlorophyll during the most fertile season, suggesting that respiration was mainly linked to

microbial food web processes. Size-fractionated studies showed that 51–67% of the respiratory activity was due to picoplankton

cells (b2 Am). Respiration rates (average values: 113F18 to 187F87 mmol C m�2 d�1) matched primary production rates

during the fertile period, but were up to one order of magnitude higher during the rest of the year. Substantial inputs of organic

matter from the coastal upwelling would be necessary to balance the large annual heterotrophic deficit in the region of study.

D 2004 Elsevier B.V. All rights reserved.

Keywords: Plankton respiration; Plankton abundance; Mesoscale variability; Island eddies; Upwelling filaments; Canary Islands region

0924-7963/$ - see front matter D 2004 Elsevier B.V. All rights reserved.

doi:10.1016/j.jmarsys.2004.07.004

* Corresponding author. Fax: +34 9 28 454490.

E-mail address: [email protected] (J. Arıstegui).

1. Introduction

Respiration is a key process in global marine

biogeochemical cycles. Most of the organic matter

synthesized in the ocean is respired in the surface

waters by microbial organisms (Williams, 1981) and

s 54 (2005) 65–82

J. Arıstegui, M.F. Montero / Journal of Marine Systems 54 (2005) 65–8266

lost to the atmosphere as carbon dioxide. A small

amount of organic matter is however preserved from

oxidation in the euphotic zone, and either made

available to the upper trophic levels or transported

into the dark ocean. The balance between primary

production (P) and plankton respiration (R), the P/R

ratio, sets, therefore, the potential of an ecosystem to

pump organic carbon into the ocean interior where it

is sequestered for extended periods of time. Although

R is widely accepted as being a critical process to

understand the ocean carbon cycle, a limited data set

on R, compared to P, is available (Williams, 2000),

and very few studies exist regarding the temporal

(e.g., Robinson et al., 1999) and/or spatial (e.g.,

Arıstegui and Montero, 1995a) variability of R at

regional or local scales. The urgent need to expand

our database on R runs up against the methodological

limitations of the traditional oxygen method to

estimate respiration rates at sea, which allows the

securing of accurate but few daily rates during regular

field samplings. This precludes in most studies the

possibility of analyzing the spatial and temporal

variability of community respiration, unless a huge

effort is solely dedicated to this task.

By studying the enzymatic respiratory electron

transport system (ETS) activity (Packard, 1971) of

plankton organisms b200 Am collected and preserved

on filters, we may however estimate R, provided that

the enzymatic measurements are correlated with actual

rates. Arıstegui and Montero (1995b) found a robust

correlation (r2=0.75; pb0.001) between plankton ETS

activity and R, from polar to subtropical waters, and

suggested the combined use of the calculated ETS–R

algorithm along with measurements of ETS activity to

estimate R in order to address metabolic studies in the

ocean. This approach allows us to perform denser

sampling grids and extends our knowledge of oceanic

respiration over larger temporal and spatial scales than

previously possible.

In this paper, we present results from three

oceanographic cruises around Gran Canaria Island

(Canary Islands), where plankton abundances and

respiratory ETS activity rates were measured. The aim

of our work was 2-fold: first to characterize and

quantify the variability of plankton biomass and

respiration in the Canary region, and second to show

that this variability responds to a large extent to

hydrographic changes at the mesoscale level. The

waters around Gran Canaria represent a natural marine

laboratory where ocean-wide mesoscale processes,

like wind shearing, fronts, eddies, and upwelling

filaments, coexist in a small sea region. The results

of this study can be therefore extended to any other

oceanic region where mesoscale variability governs

plankton distribution and metabolism.

2. Methods and regional hydrography

2.1. Hydrographic data and sampling

With the aim of addressing seasonal variability,

three oceanographic cruises were carried out during

three distinct periods of the seasonal production cycle

in the Canary region: (i) the season of strongest wind

intensity in June 1990, (ii) the end of the late winter

bloom in March 1991, and (iii) the period of greatest

stratification of the water column and least wind in

October 1991. Wind data were obtained from the

airport on the east coast of GranCanaria Island supplied

by the Spanish Instituto Nacional de Meteorologıa.

The cruises consisted of a grid of 42–64 stations,

separated at a distance of 20–25 km. At each station,

Conductivity–Temperature–Depth (CTD) and bottle

casts were made down to 500 m (see Arıstegui et al.,

1997 for details). Water samples for the analysis of

chlorophyll, plankton cell counts, and the respiratory

activity of the Electron Transport System (ETS) in

plankton b200 Amwere obtained at six depths from the

upper 150 m in March and June. In October, the

samples were collected from only two depths: the

mixed layer (ML, 5 m) and the depth of the chlorophyll

maximum (DCML, from 50 to 90 m). Chlorophyll a

(Chl), plankton ETS activity, and the abundances of

heterotrophic bacteria (HB) and Synechococcus type

cyanobacteria were estimated for all the cruises. The

abundances of autotrophic and heterotrophic nano-

flagellates were estimated at all stations in October and

at several stations crossing the cyclonic and anti-

cyclonic eddies during the March cruise.

2.2. Chlorophyll a, plankton cell counts, and con-

versions to carbon biomass

Chlorophyll a (Chl) was measured fluorometri-

cally by means of a Turner Designs bench fluor-

J. Arıstegui, M.F. Montero / Journal of Marine Systems 54 (2005) 65–82 67

ometer, calibrated with pure chlorophyll a (Sigma),

following the recommendations of Yentsch and

Menzel (1963), as described in Arıstegui et al.

(1997). Water (500 ml) was filtered through 25-mm,

Whatman GF/F fiber glass filters and extracted

overnight in 10 ml of 90% acetone at 4 8C in the

dark. Total autotrophic biomass was derived from

chlorophyll concentrations by assuming a carbon to

chlorophyll a conversion factor (C/Chl) of 50. A

similar factor has been widely used by many authors

(e.g., Li et al., 1992; Gasol et al., 1997; Bode et al.,

2001), although it probably represents a minimum

threshold, since the ratio may be close to 100 in

oligotrophic open-ocean systems (Welschmeyer and

Lorenzen, 1984; Hewes et al., 1990; Verity et al.,

1996; Buck et al., 1996). Size fractionation studies

for Chl and respiratory activity (see below) were

carried out in the upper 150 m of the cyclonic and

anticyclonic eddies during March and at the ML and

the DCML during October. For size fractionation of

Chl, the same volume was filtered through 25-mm,

2-Am Nuclepore polycarbonate filters. Picoplankton

Chl was computed as the difference between total

Chl (collected on GF/F filters) and N2 Am Chl

(collected on Nuclepore filters).

Samples (20 ml) for estimating the abundance of

heterotrophic bacteria (HB) were fixed with 0.5 ml of

40% formaldehyde (2% final concentration) and

preserved in the dark at 4 8C. Cells were counted

following the method of Porter and Feig (1980) with

slight modifications. Two milliliters of each sample

was poured into the filtration tower, stained with 4V-6-diamidino-2-phenylindole (DAPI; 0.5 Ag ml�1 final

concentration) for 5–10 min, and filtered onto a 0.2-

Am black polycarbonate, membrane filter placed over

a Whatman GF/C backing filter. The filter was

mounted on a microscope slide with low-fluorescence

paraffin oil. At least 300 cells, or 20 fields, were

counted employing an epifluorescence Zeiss Axiovert

35 microscope under UV excitation (excitation filter

BP 365/12, chromatic divisor FT 395, suppressor

filter LP 397) at a magnification of �1000. Daily

blanks were systematically counted to check for

contamination sources. Blanks were never higher than

1% of the total cell numbers. The error of the method

(b10%) was determined from random replicate

samples. HB abundances were converted to biomass

using a factor of 20 fg C cell�1 (Lee and Fuhrman,

1987; Cho and Azam, 1990; Bode et al., 2001). The

weak autofluorescence of Prochlorococcus type cya-

nobacteria was not readily visible under epifluores-

cence microscopy, and therefore some of these cells

were presumably included in the counts of bacteria

(see below).

For the enumeration of Synechococcus type

cyanobacteria (CB), 40-ml samples were frozen on

board immediately after being collected following the

recommendations of Kuuppo-Leinikki and Kuosa

(1989). We checked that cells preserved in this way

were kept in perfect condition for at least 2 months

after being frozen. In the lab, 20 ml of the de-frosted

sample was filtered onto a 0.2-Am black polycar-

bonate, membrane filter over a Whatman GF/C

backing filter and mounted on a microscope slide

with low-fluorescence paraffin oil. Orange cells,

under green light (excitation filter BP 546/12,

chromatic divisor FT 580, suppressor filter LP 590),

were counted (at least 300 or 20 fields) at a

magnification of �1000. Synechococcus cell num-

bers were converted to biomass by using a con-

version factor of 250 fg C cell�1 (Kana and Glibert,

1987; Li et al., 1992). This factor should, however,

be interpreted as merely an approximation, since as

Sieracki et al. (1995) observed it depends on the size

of the cells that increases with depth through the

water column.

Seawater samples (20 ml) for autotrophic (NAF)

and heterotrophic (NHF) nanoflagellate enumeration

were preserved following Haas (1982). Immediately

after collection, the sample was fixed with gluta-

raldehyde (0.3% final concentration). After 30 min, a

10-ml subsample was placed into the filtration tower

and fixed with proflavine (6.6 mg ml�1 final

concentration) for 3–5 min. The stained sample

was later filtered through a 0.2-Am black polycar-

bonate, membrane filter over a Whatman GF/C

backing filter and finally mounted on a microscope

slide with low-fluorescence paraffin oil. NAFs were

distinguished from NHF by their chloroplasts, which

emitted red fluorescence when observed under blue

light (excitation filter BP 450–490, chromatic divisor

FT 510, suppressor filter LP 520). At least 50 cells

or 20 fields were counted at a magnification of�1000. NAF and NHF numbers were converted to

biomass assuming a mean biovolume of 20 Am3

cell�1 for NAF and of 10 Am3 cell�1 for NHF


(values estimated for North Atlantic flagellates; J.M.

Gasol personal communication), and a conversion

factor of 220 fg C Am�3 (Borsheim and Bratbak,

1987).

2.3. Heterotrophic to autotrophic carbon ratio

In spite of the uncertainties associated with

transforming measured variables (like chlorophyll

or cell counts) into carbon values using conversion

factors that may vary according to environmental

conditions (e.g., Sieracki et al., 1995), the ratio be-

tween autotrophic and heterotrophic biomasses (H/A)

may give us a useful index of the functioning of

plankton communities (Gasol et al., 1997). In our

study, the index was calculated from average values

in the ML during March and October, the periods

when flagellates estimations were available. The

plankton heterotrophic biomass (H) was computed

as the sum of the HB and NHF biomasses. The

autotrophic biomass was both calculated for the

whole autotrophic community (AChl), by deriving it

from chlorophyll a, and for the pico- and nano-

plankton components (A), computed as the sum of

the CB and NAF biomasses. H and A biomasses

were corrected for unaccounted Prochlorococcus

cells, since otherwise the H/A indexes would be

overestimated. Assuming an average Prochlorococ-

cus cell concentration of 5�104 cells ml�1 in the

ML (Arıstegui, unpublished data for the Canary

region), an average biovolume for the ML of 0.1

Am3 (Sieracki et al., 1995), and a conversion factor

of 220 fg C Am�3 (Christian and Karl, 1994; Zubkov

et al., 2000), the Prochlorococcus biomass would

amount to 1 mg C m�3. This value is comparable to

other published results from the subtropical North

Atlantic (e.g., Sieracki et al., 1995) and would

represent an overestimation of 5–13% in the H

biomass and an underestimation of 9–12% in the A

biomass.

2.4. Respiratory Electron Transport System (ETS)

activity

Samples (5 l) for ETS analysis were pre-filtered

through a 200-Am mesh and poured into acid-cleaned

plastic carboys before being filtered through 47-mm

Whatman GF/F filters (or through 47-mm, 2-Am

Nuclepore polycarbonate filters for size-fractionation

studies) at a low vacuum pressure (b1/3 atm). The

filters were immediately stored in liquid nitrogen until

assayed within a few weeks. ETS determinations were

carried out according to the Kenner and Ahmed

(1975) modification of the tetrazolium reduction

technique proposed by Packard (1971) as described

in Arıstegui and Montero (1995b). An incubation time

of 20 min at 18 8C was selected from a previous time

and temperature kinetic study. ETS activities meas-

ured at 18 8C were converted to activities at in situ

temperatures by using the Arrhenius equation. A

calculated mean activation energy of 16 kcal mol�1

was used. This activation energy value is similar to

the activation energy values obtained from other

studies in oceanic regions (Arıstegui and Montero,

1995b).

Plankton respiration was estimated from the respi-

ratory ETS activity using the general equation log

R=0.357+0.750 log ETS (r2=0.75; n=197) obtained

by Arıstegui and Montero (1995b) for surface oceanic

waters. This equation yields a mean error in the

prediction of F34%. A respiratory quotient=0.8 (the

average value obtained by conventional stoichiometry

of heterotrophic respiration; Robinson and Williams,

1999, and references therein) was used to convert

oxygen values to carbon units.

Picoplankton ETS was computed as the differ-

ence between total ETS (measured from samples

collected on GF/F filters) and N2 Am ETS

(measured from samples collected on Nuclepore

filters).

2.5. Regional oceanographic setting

The hydrographical conditions as well as the

variability in the mesoscale chlorophyll field during

the three cruises were described in detail in

Arıstegui et al. (1997). The cruises of March and

June were carried out under moderate to high wind

intensity (30–40 km h�1), with northerly winds

blowing during March and north-easterly winds

during June (Fig. 1). The deepest mixed layer (75–

100 m) was found in March as a result of winter

cooling and wind stress, while the shallowest mixed

layer (b50 m) was observed in October, the period

of warmest surface temperatures and lowest wind

intensity (b15 km h�1).

Fig. 1. Canary Islands region showing the sampling grids around Gran Canaria Island, overlying temperature (8C) contour maps at 100 m depth,

during the three periods of study. Arrows on the top of the maps indicate average wind speed and direction during cruises. Sections S–SV are

represented in Figs. 3 and 6. Circled stations at cyclonic and anticyclonic eddies in June and March are represented in Figs. 4 and 5.


Cold-core cyclonic eddies were observed down-

stream of the island during the three cruises (Fig. 1),

although in October the strong stratification of the

surface waters almost overrode the effect of the

cyclonic dome in the upper 100 m. Warm-core

anticyclonic eddies were found during March (in an

early stage of cyclogenesis) and June (Fig. 1). The

horizontal temperature map in June does not illustrate,

however, the anticyclonic eddy clear enough due to a

lag of 3 days in the sampling between stations

adjacent to each other.

Coastal waters upwelled in the northwest African

coast invaded the eastern and southeastern sectors of

the island during March and October, as evidenced by

the temperature and salinity fields (Arıstegui et al.,

1997). The intrusion of surface upwelling water was

more pronounced during March. This is clearly

observed in Sea Surface Temperature (SST) images

derived from High Resolution Picture Transmission

(HRPT) data recorded during the days previous to the

March cruise (Arıstegui et al., 1997).

3. Results and discussion

3.1. Seasonal variation in plankton abundance and

respiratory activity

Substantial temporal variabilities in respiratory

activity and plankton abundance were found when

comparing the three periods of study. Mean concen-

trations of Chl and mean abundance of HB and CB

cells (Table 1) were highest in March, when primary

production is known to peak after the erosion of the

seasonal thermocline (De Leon and Braun, 1973;

Basterretxea, 1994; Arıstegui et al., 1997; Barton et

Table 1

Mean volumetric values (Fstandard deviation, SD) of chlorophyll a (Chl), plankton ETS activity (ETS), and heterotrophic bacteria (HB) and

cyanobacteria type Synechococcus (CB) abundance during the three periods of study

Depth March June October

MeanFSD n MeanFSD n MeanFSD n

Chl mg m�3 ML 0.39F0.15 56 0.10F0.05 32 0.14F0.05 45

DCML 0.47F0.17 56 0.30F0.12 36 0.39F0.13 45

0–150 m 0.31F0.19 320 0.15F0.11 206

ETS Amol O2 m�3 h�1 ML 93.9F44.7 55 62.6F17.9 35 89.4F26.8 45

DCML 93.9F40.2 55 49.2F17.9 35 58.1F22.4 45

0–150 m 76.0F44.7 316 49.2F22.4 203

HB cells ml�1�105 ML 8.7F2.6 33 3.7F1.5 26 2.6F0.7 44

DCML 7.8F1.4 96 3.9F3.9 54 2.5F1.1 43

0–150 m 7.7F3.4 239 4.8F2.4 161

CB cells ml�1�104 ML 2.9F1.4 39 0.6F0.2 24 1.1F0.8 45

DCML 2.4F1.0 94 0.1F0.1 40 0.6F0.8 43

0–150 m 1.9F1.7 242 0.3F0.3 132

n=number of data; ML=mixed layer; DCML=deep-chlorophyll maximum layer.


al., 1998; Arıstegui et al., 2001). Opposite trends in

HB and CB were observed, however, when compar-

ing the other two periods. Mean HBs were more

abundant in June than in October, while CBs were up

to six times higher in October than in June. These

patterns of distribution applied both for the whole

water column and when comparing data from the

Mixed Layer (ML) and the Deep Chlorophyll

Maximum Layer (DCML) separately (Table 1).

Respiratory ETS activity also showed a large (about

2-fold) temporal variation, with overall highest values

in March and lowest in June, although ETS in the

ML was about the same in March and in October

(Table 1).

The seasonal changes in chlorophyll, plankton

abundance, or metabolic rates cannot however be

explained only by seasonal variability in the water-

column stability in the open ocean. Arıstegui et al.

(1997) showed that the temporal variability in the

chlorophyll field was largely influenced by the

intrusion of cold, chlorophyll-rich water from the

NW Africa upwelling system. Similarly, upwelling

waters invading the eastern sector of the sampling

grid largely affected the composition and metabolism

of plankton communities. Indeed, in March, an

increasing east–west gradient in plankton abundances

and metabolism was apparent, with lower HB and

CB numbers and ETS activity coinciding with the

high-chlorophyll waters of the upwelling filament

(Fig. 2). An opposite gradient was observed in

October. In this case, the upwelling waters invading

the southeastern sector of the island presented

slightly higher chlorophyll concentrations than the

oceanic waters, but marked increases in HB and CB

numbers, with respect to the western region, a fact

that could only be explained by allochthonous inputs

of organic matter into the region of study. In June,

the smaller grid of stations sampled, particularly for

plankton abundances, precluded to infer the demon-

stration of any east–west gradient, although bacteria,

like in March, tended to accumulate in the frontal

waters between the cyclonic and the anticyclonic

eddy (Figs. 2 and 3).

3.2. Island shearing effect on respiratory activity

Patches of high ETS activity at surface were

observed at the flanks of the island during March

and June (Fig. 2), the periods of highest wind stress

(N8 m s�1; Fig. 1). The position of these maxima

varied depending on wind direction, and therefore the

shearing sites (either of the wind field and/or the main

flow) with the island. They coincided with patches of

chlorophyll, particularly during March when phyto-

plankton was more abundant, and presumably con-

tributed more to seawater respiration.

The presence of these patches in the wind/current

shearing sites with the flanks of the island during the

windy periods (June and March) suggests that

turbulence plays a key role in enhancing plankton

Fig. 2. Near-surface (5 m) maps of chlorophyll a (mg m�3), respiratory ETS activity (ml O2 m�3 h�1), and abundance of Synechococcus type

cyanobacteria (�104 cells ml�1) and heterotrophic bacteria (�105 cells ml�1) during the three periods of study.


Fig. 3. Vertical sections (S–SV) showing temperature (8C), chlorophyll a (mg m�3), respiratory ETS activity (ml O2 m�3 h�1), and abundance of

Synechococcus type cyanobacteria (�104 cells ml�1) and heterotrophic bacteria (�105 cells ml�1) during June and March. C: position of the

cyclonic eddy; AC: position of the anticyclonic eddy.



respiration around the island. Laboratory experiments

have demonstrated that turbulence increases the

metabolic activity of microorganisms, either directly

or indirectly (Peters and Marrase, 2000, and refer-

ences therein). Some of these studies suggest that an

increase in turbulence favors the ingestion of particles

and the uptake of dissolved organic matter by leading

to a grazing shift from smaller to larger prey sizes,

lowering the grazing pressure on bacteria and accel-

erating nutrient recycling (Peters et al., 1998). Our

results do not provide any direct field evidence to

support the bgrazing-shift hypothesisQ. However, ourdata clearly indicate that plankton respiratory activity

increases at the shearing sites of the island, where it is

known that primary production is enhanced (Arıstegui

et al., 1989; Basterretxea et al., 2002) and zooplank-

ton tends to accumulate (Arıstegui et al., 1989),

presumably by having the opportunity of feeding on

larger phytoplankton cells. Other authors (e.g., Simp-

son et al., 1982; Wolanski and Hamner, 1988) have

also described enhancements in primary production

associated with island effects; although the cause of

these effects could be different (see discussion in

Arıstegui et al., 1997).

3.3. Island eddies: a two-way biological pump

Cyclonic and anticyclonic eddies were observed

during the three periods of study, since there are

recurrent features of the mesoscale field downstream

of the Canary Islands (Arıstegui et al., 1994). The

effect of these eddies on the distribution of HB, CB,

and ETS activity can be better viewed through vertical

sections crossing the main hydrographic features (Fig.

3). A section crossing the eddy field in June shows a

steep depression of isotherms in the anticyclonic eddy

center, clearly paralleled by a depression of isolines in

Chl, CB, and ETS activity. In March, the section

illustrates the westward intrusion of high-chlorophyll

upwelling water with low numbers of CB and low

respiratory rates, as well as the high Chl and ETS at

the boundary of the cyclonic eddy. Along both

sections, it is noticeably the distribution of HB that

accumulates in the frontal regions between eddies or

filament and oceanic waters.

Vertical profiles of Chl, HB, and CB at eddy

stations from June and March (see Fig. 1 for station

positions) and of NAF and NHF from the March

eddies are depicted in Figs. 4 and 5, respectively.

Although the cyclonic eddies showed relatively high

volumetric numbers and activities in the upper 50 m,

the anticyclonic eddies presented higher integrated

values of Chl, ETS, CB, and HB due to the more

uniform distributions in the upper 150 m (Table 2).

Cyclonic eddies in their early formation stages may

increase primary production by pumping high-nutrient

water into the euphotic zone (e.g., Basterretxea,

1994). This situation favors a close coupling between

the different plankton groups, which may be bpackedQin the upper 50 m as occurred in March (Figs. 4 and

5). However, during other periods (e.g., October), the

effect of eddies on surface plankton communities may

be overridden by the strong surface stratification,

which restricts nutrient diffusion to the euphotic zone.

Anticyclonic eddies may downwell organic matter

in their cores, increasing water column respiration.

This is clearly observed in the anticyclone sampled

during June, where the isolines of chlorophyll,

cyanobacteria, and ETS activity follow the same

downward trend as the isotherms. These eddies may

act as effective organic carbon pumps, sequestering

dissolved and particulate organic carbon from the

nearby waters and sinking it below the euphotic zone.

As satellite color images show, the anticyclones may

entrain high-chlorophyll water from upwelling fila-

ments with which they interact. Overall, when

counter-paired cyclonic and anticyclonic eddies occur

together, the biological pump, i.e., the production and

downward flux of organic carbon in the ocean due to

the biological activity, may work faster than in the

surrounding waters.

Additional evidence of entrainment by anticy-

clones is supplied by the size fractionation studies

of Chl and ETS in cyclonic and anticyclonic eddies

during March and October. Picoplankton (b2 Am)

contributed an average 60% to Chl and 51% to ETS

activity in the cyclonic eddy in March. In the

anticyclonic eddy, however, most (73%) of the Chl

belonged to cells N2 Am, although ETS activity was

largely (67%) due to small cells. This apparent

controversy can be explained by the anticyclonic

entrainment of coastal upwelled waters, presumably

bearing high-chlorophyll, large phytoplankton cells,

with low respiratory rates. In October, picoplankton

increased its contribution to Chl (73% in the ML and

75% in the DCML), while the contribution to ETS

Fig. 4. Vertical distribution of chlorophyll a, respiratory ETS activity, and abundance of Synechococcus type cyanobacteria and heterotrophic

bacteria at selected stations (see Fig. 1) inside cyclonic and anticyclonic eddies during June and March.


activity (55% in both layers) remained approximately

the same, despite the differences found in plankton

composition between the two sampling layers. Com-

paratively, the ML presented similar abundances of

HB, but higher numbers of CB and NHF, and lower

numbers of NAF than the DCML (Fig. 6).

The frontal region between cyclonic and anti-

cyclonic eddies, or between eddies and surrounding

Fig. 5. Vertical distribution of autotrophic and heterotrophic nanoflagellates at selected stations (see Fig. 1) inside cyclonic and anticyclonic

eddies during March.


waters, may constitute sites of water convergence

where dissolved and particulate organic matter accu-

mulates. This would explain the higher numbers of

bacteria found at these sites (Fig. 3) that presumably

would be oxidizing the organic compounds. Our

results agree with previous works by other authors

who described accumulations of bacteria abundances

at diverse frontal regions (Floodgate et al., 1981;

Pomeroy et al., 1983; Lochte and Turley, 1984;

Nelson et al., 1985; Peele et al., 1985; Ducklow,

1988; La Ferla and Crisafi, 1991).

3.4. The unequal effects of upwelling filaments

The waters around the eastern islands of the

archipelago are frequently invaded by filaments of

cold and high chlorophyll water, stretching from the

NW Africa coastal upwelling system, as occurred

Table 2

Integrated (0–150 m) values of chlorophyll a (Chl), plankton ETS activity (E

heterotrophic bacteria (HB) from stations in cyclonic and anticyclonic edd

March

Cyclonic An

Chl (mg m�2) 24 3

ETS (mmol O2 m�2 h�1) 11.8 1

CB (cells cm�2�104) 126 17

HB (cells cm�2�105) 992 140

during March and October (Van Camp et al., 1991;

Hernandez-Guerra et al., 1993; Arıstegui et al., 1994,

1997; Barton et al., 1998; Navarro-Perez and Barton,

1998). The island of Gran Canaria constitutes the

western boundary of some of these filaments and

therefore represents the most offshore extension of the

upwelling into the oceanic domain. South of the

island, newly generated anticyclonic island eddies

may interact with the filaments, entraining upwelling

water into their cores. At the time of the March cruise

little—but still apparent—entrainment was produced

from the upwelling filament into the core of the

anticyclone, since the latter was starting to develop.

As discussed above, the size fractionation studies of

chlorophyll at two stations placed in the anticyclonic

and the cyclonic eddy, respectively, indicated a higher

contribution of large cells in the anticyclone, which

would presumably have arrived with the upwelling

TS), and abundance of cyanobacteria type Synechococcus (CB) and

ies during June and March (see Fig. 1 for station positions)

June

ticyclonic Cyclonic Anticyclonic

6 14 31

2.7 3.5 7.2

7 36 57

8 640 758

Fig. 6. Horizontal distribution of chlorophyll a (mg m�3), respiratory ETS activity (ml O2 m�3 h�1), and abundance of Synechococcus type

cyanobacteria (�104 cells ml�1), heterotrophic bacteria (�105 cells ml�1), and heterotrophic and autotrophic nanoflagellates (�102 cells ml�1)

at the mixed layer (ML) and the deep-chlorophyll maximum layer (DCML) during October (section S–SV).



waters. Indeed, AVHRR sea surface temperature

images obtained for the days following the cruise

(Arıstegui et al., 1997) showed a track of cold

filament water entrained by the anticyclone as the

eddy drifted southwards.

The biological effects of upwelling filaments on

the oceanic system were unequal. In March, the cold

upwelling waters transported larger cells, with higher

chlorophyll concentrations, but lower CB and HB

cells than the oceanic waters. Phytoplankton cells in

the filament presented low assimilation numbers

(Basterretxea, 1994) while seawater respiration was

considerably lower than in the open ocean. Con-

versely, the upwelling waters invading the south-

eastern sector of Gran Canaria in October presented

higher HB and CB cell abundance, and a similar

contribution of picoplankton to chlorophyll than the

oceanic waters. These contrasting differences in the

composition and metabolism can be explained by a

different origin of the filament waters and the time

that these waters take to be advected offshore. The

lower wind intensity in October with respect to March

would presumably slow down the offshore advection

Table 3

Pearson pairwise correlation coefficients (R) between chlorophyll a (CHL

bacteria (HB), Synechococcus type cyanobacteria (CB), and heterotrophic (

study

March CHL ETS

ETS 0.53** (313)

HB 0.33** (237) 0.13* (234)

CB 0.72** (239) 0.54** (237)

NHF 0.61** (34) 0.59** (34)

NAF 0.75** (29) 0.45* (34)

June CHL ETS

ETS 0.32** (186)

HB 0.30** (149) 0.41** (149)

CB 0.33** (123) 0.82** (125)

October CHL ETS

ETS NS (124)

HB 0.36** (122) 0.47** (122)

CB 0.28* (120) 0.75** (120)

NHF NS (40) 0.63** (40)

NAF 0.63** (40) NS (40)

All data were previously log transformed. Values in parenthesis are numb

NS: not significant.

* pb0.05.

** pb0.0001.

of upwelling water, allowing nutrient exhaustion in

surface waters, the growth of small picoplankton cells

and their grazers, and therefore an increase in

plankton respiration, as in the oceanic domain. In

fact, the strong surface warming in October caused by

the weak wind intensity precluded the identification of

any filament structure by satellite imagery, although

the temperature/salinity signature allowed the identi-

fication of the origin of the upwelled water (Arıstegui

et al., 1997). Large differences in nutrient concen-

trations and phytoplankton composition and chloro-

phyll have previously been described for similar

filaments in the California Current upwelling system

(Chavez et al., 1991; Jones et al., 1991). In these

cases, the origin of the upwelled water along the

coastal jet as well as the local dynamic of the filament

(Brink and Cowles, 1991) was used to interpret the

chemical and biological differences.

3.5. Picoplankton contribution to plankton respiration

From the analysis of paired correlations between

variables (Table 3), the strong correlation between the

), respiratory ETS activity (ETS), and abundance of heterotrophic

NHF), and autotrophic (NAF) nanoflagellates for the three periods of

HB CB NHF

0.46** (226)

0.39** (34) 0.61** (34)

0.56* (34) 0.58* (34) 0.56* (34)

HB

0.32** (132)

HB CB NHF

0.54** (120)

0.48* (40) 0.45* (40)

0.30* (40) NS (40) NS (40)

er of data.

Table 4

Mean values of autotrophic (A) and heterotrophic (H) biomasses

and H/A ratios for the mixed layer during March and October

AChl CB NAF A HB NHF H H/AChl H/A

March 19.5 7.3 2.6 9.9 17.4 0.9 18.3 0.9 1.8

October 7.0 2.8 4.4 7.2 5.2 2.2 7.4 1.1 1.0

A was calculated as the sum of the biomasses of Synechococcus

type cyanobacteria (CB) and autotrophic nanoflagellates (NAF)

H was calculated as the sum of the biomasses of heterotrophic

bacteria (HB) and heterotrophic nanoflagellates (NHF). AChl was

calculated from chlorophyll using a C/Chl ratio=50. All units are in

mg C m�3 (see Methods and regional hydrography for details).


ETS activity and the CB abundance during the three

periods, increasing towards the less productive peri-

ods, are apparent. Similarly, the weak correlation

between ETS and HB in March strengthens during the

more oligotrophic conditions of June and October,

suggesting that picoplanktons, and particularly CB,

play a major role in seawater respiration during the

whole year, but mainly during the most unproductive

periods. A multiple regression analysis between ETS

activity and all the biological variables measured

during October reveals that the association between

CB and HB explains 78% of the ETS variance,

increasing to 81% when the NHF component is

included:

logETS ¼ 0:32logHBþ 0:18logCBþ 0:14logNHF

� 6:17;

r2 ¼ 0:81; n ¼ 40;F ¼ 49:9

The key role of picoplankton in seawater respira-

tion is also supported by size fractionation studies of

chlorophyll and ETS activity in October, which

indicate that picoplankton contributes on average

55% to ETS activity.

NHF, the picoplankton grazers, shows a sig-

nificant relationship with their potential prey (HB

and CB), as well as a strong correlation with ETS

activity. Whether this is a direct or indirect cause–

effect is not clear. NHFs are thought to contribute

not only largely to the release of dissolved

organic carbon used by bacteria (Nagata, 2000;

Teira et al., 2001), but also to the plankton

respiration of organic matter (Nagata, 2000). Our

results show a strong link between picoplankton,

NHF, and plankton respiration, although the contri-

bution of each of the groups to the overall respiration

cannot be ascertained with our data. Bode et al.

(2001) concluded from a study on bacteria and

phytoplankton in the Canary islands that HBs were

able to consume dissolved organic carbon in excess

of that produced locally by the phytoplankton

community. This allochthonous carbon could be

remineralized directly by the bacterial community

or channeled through the flagellates community. The

latter hypothesis seems more plausible, providing the

strong relationship obtained between NHF and ETS

activity.

3.6. Changes in the ratio of heterotrophic to auto-

trophic biomass

According to the carbon conversion factors used

(see Methods and regional hydrography), the ratio of

heterotrophic to autotrophic (H/AChl) biomasses was

~1 in March and October, when A was computed from

chlorophyll (Table 4). Following the analysis on H/A

ratios of Gasol et al. (1997), our results would indicate

an intermediate situation between coastal and open-

ocean systems. Nevertheless, in our calculations, we

did not include large protozoans (e.g., ciliates) or

zooplankton, which could represent a considerable

fraction of the H biomass (Bode et al., 2001) and

produce H/A indexes N1. According to Li et al.

(1993), the boundary below which a system can be

considered oligotrophic enough for bacteria to dom-

inate phytoplankton is between 1 and 2 g phytoplank-

ton C m�2. Yearly average phytoplankton biomass

from the Canary region (derived from integrated

chlorophyll, and a C/Chl ratio of 50) ranges from 1

to 1.5 g C m�2, close to the boundary of bacteria-

dominated systems.

Aside from the global value of the H/A index, it is

interesting to notice the temporal variability in each of

the groups that contribute to the H and A components

of the ratio. In March, AChl (autotrophic biomass

derived from chlorophyll) was significantly higher

than A (autotrophic biomass derived from individual

biomasses), while in October AChl and A were

approximately the same. In the latter period, the sum

of CB and NAF biomasses (7.2 mg C m�3) matched

the phytoplankton carbon (7 mg C m�3) derived from

chlorophyll. In March, however, the sum of CB and

NAF biomasses (9.9 mg C m�3) represented only 51%

of the phytoplankton carbon, indicating that large

.


eukaryotes contributed significantly to the autotrophic

biomass. Furthermore, in March, CBs were more

representative in biomass terms (7.3 mg C m�3) than

NAF (2.6 mg C m�3), in contrast to October, where

the biomass of NAF (4.4 mg C m�3) was significantly

higher than that of CB (2.6 mg C m�3). Similarly,

NHFs were more important in absolute and relative

(compared to bacteria) biomass terms during October

than during March. As discussed above, these shifts in

autotrophic and heterotrophic biomasses are strongly

dependent on the mesoscale variability of the region,

and particularly on the effect of upwelling filaments,

which intrude coastal upwelled waters with contrast-

ing biological properties, resulting from changes

during its offshore flow.

3.7. Metabolic balance in surface waters

The advection of upwelling waters into the Canary

region has important consequences not only by

prompting changes in plankton community structure,

but also by altering the metabolic balance of the

region. We have shown that upwelling waters trans-

porting higher chlorophyll concentrations than the

oceanic waters may either bear similar or lower

respiratory rates than the oceanic domain, in close

association with the abundance of CB and HB.

However, on a seasonal or annual scale, one would

Fig. 7. Distribution of integrated (0–150 m) plankton (b200 Am) respiration

sections of the sampling grid in March. P data were obtained from Basterr

obtained by Arıstegui and Montero (1995b) and applying a respiration qu

expect that the recurrent inputs of high-chlorophyll

waters would increase the community respiration of

the region and, at a lower extent, the photosynthesis,

by supplying bnewQ ammonium regenerated from the

allochthonous organic matter to autotrophs.

Average primary production measured during

March (N100 mmol C m�2 d�1) and October (b10

mmol C m�2 d�1) varied more than one order of

magnitude (Basterretxea, 1994) compared with the

lower variability in chlorophyll (2- to 3-fold) or CB

(6-fold) cell abundance, suggesting that phytoplank-

tons present not only high growth rates, but also fast

losses. Comparatively, the integrated (0–150 m)

plankton respiration rates ranged less than 2-fold,

from 113F18 mmol C m�2 d�1 in June to 187F87 18

mmol C m�2 d�1 in March. Thus, the average primary

production to plankton respiration (P/R) ratio calcu-

lated for these two periods shifted from an approx-

imate equilibrium (P/R=1) in March to strong

heterotrophy (P/Rb0.1) in other periods, when pri-

mary production is much lower (Basterretxea, 1994).

Since March corresponds to the time of the year when

phytoplankton blooms, one would expect to have a

net positive balance well over the equilibrium. This

situation is however only evident in the eastward

sector of the sampling grid, affected by the intrusion

of upwelling waters (Fig. 7). Although cyclonic

eddies may contribute to increase the primary

(R) and the primary production to respiration (P/R) ratio along three

etxea (1994). R was derived from ETS activity using the algorithm

otient of 0.8.


production (Barton et al., 1998; Basterretxea and

Arıstegui, 2000), and thus the amount of matter to be

respired by the plankton community, frequent load-

ings of organic matter from the nearby upwelling

region would be necessary to balance the high

respiration rates measured in the Canary region.

Satellite images show the yearly recurrence of high-

chlorophyll filaments invading the eastern waters of

the archipelago (Arıstegui et al., 1997; Pacheco and

Hernandez-Guerra, 1999) that would support the

advection hypothesis. These filaments would presum-

ably transport not only particulate but also dissolved

substances. Whether this organic matter is mostly

respired in the Canary region or exported to the

oligotrophic waters of the subtropical gyre is still a

matter of debate (e.g., Duarte et al., 2001).

Acknowledgements

We would like to thank the officers and crew of the

Research Vessels Garcıa del Cid and Ignat Pavlyu-

chenkov for their expert help with over-the-side

operations. We also thank S. Ballesteros for micro-

scope cell counting. Two anonymous reviewers con-

tributed to improve the paper. This work was funded

by projects 22/01.06.88 (GAC), PB88-0436 (CICYT),

AMB95-0731 (CICYT), and MAST-0031 (EC).

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