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Deep-Sea Research II 53 (2006) 1593–1610
www.elsevier.com/locate/dsr2
Phytoplankton carbon fixation, chlorophyll-biomass and
diagnostic pigments in the Atlantic Ocean
Alex J. Poultona,, Patrick M. Holligana, Anna Hickmana, Young-Nam Kima,
Tim R. Adeya, Mark C. Stinchcombea, Claire Holetonb,
Sarah Roota, E. Malcolm S. Woodwardc
a
National Oceanography Centre, University of Southampton, Southampton SO14 3ZN, UK
b
Department of Plant Ecology, Uppsala University, Uppsala SE-752 36, Sweden
c
Plymouth Marine Laboratory, Plymouth PL1 3DH, UK
Received 26 August 2005; received in revised form 15 December 2005; accepted 15 May 2006
Available online 14 August 2006
Abstract
We have made daily measurements of phytoplankton pigments, size-fractionated (o2 and 42-mm) carbon fixation and
chlorophyll-a concentration during four Atlantic Meridional Transect (AMT) cruises in 2003–04. Surface rates of carbon
fixation ranged from o0.2-mmol C m3 d1 in the subtropical gyres to 0.2–0.5-mmol C m3 d1 in the tropical equatorial
Atlantic. Significant intercruise variability was restricted to the subtropical gyres, with higher chlorophyll-a concentrations
and carbon fixation in the subsurface chlorophyll maximum during spring in either hemisphere. In surface waters,
although picoplankton (o2-mm) represented the dominant fraction in terms of both carbon fixation (50–70%) and
chlorophyll-a (80–90%), nanoplankton (42-mm) contributions to total carbon fixation (30–50%) were higher than to total
chlorophyll-a (10–20%). However, in the subsurface chlorophyll maximum picoplankton dominated both carbon fixation
(70–90%) and chlorophyll-a (70–90%). Thus, in surface waters chlorophyll-normalised carbon fixation was 2–3 times
higher for nanoplankton and differences in picoplankton and nanoplankton carbon to chlorophyll-a ratios may lead to
either higher or similar growth rates. These low chlorophyll-normalised carbon fixation rates for picoplankton may also
reflect losses of fixed carbon (cell leakage or respiration), decreases in photosynthetic efficiency, grazing losses during the
incubations, or some combination of all these. Comparison of nitrate concentrations in the subsurface chlorophyll
maximum with estimates of those required to support the observed rates of carbon fixation (assuming Redfield
stoichiometry) indicate that primary production in the chlorophyll maximum may be light rather than nutrient limited.
r 2006 Elsevier Ltd. All rights reserved.
Keywords: Phytoplankton; Carbon fixation; Picoplankton; Nanoplankton; Chlorophyll-a; Atlantic Meridional Transect
1. Introduction
Corresponding author. Tel.: +44 2380592262;
fax: +44 2380593564.
E-mail address: [email protected] (A.J. Poulton).
0967-0645/$ - see front matter r 2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.dsr2.2006.05.007
The size structure and taxonomic composition of
the phytoplankton community in the open ocean
are important factors in regulating organic carbon
export to the deep ocean (Azam et al., 1983;
Tremblay and Legendre, 1994). Phytoplankton
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may be classified by cell size (e.g. Sieburth, 1979) to
include small picoplankton (0.2–2 mm in diameter;
e.g. prochlorophytes, Synechococcus spp., small
eukaryotes), medium-sized nanoplankton (2–20 mm;
e.g. prymnesiophytes, pelagophytes, small diatoms
and dinoflagellates), and larger microplankton
(420–200 mm; e.g. diatoms and dinoflagellates).
Factors that influence the composition and
dynamics of the phytoplankton community (nutrient and light availability, turbulence and predation)
vary in time and space, leading to significant
variability in phytoplankton diversity and growth
rates. Typically, the upper ocean is regarded as
composed of an upper light-rich and nutrientlimited surface layer, and a deep light-limited and
nutrient-rich layer (e.g. Dugdale, 1967).
Within the Atlantic Ocean the main ecological
regimes include regions with relatively high chlorophyll-a at high latitudes (4401; temperate zones)
and in the equatorial Atlantic (101S—201N) and
coastal upwelling, and regions with relatively low
chlorophyll-a around the central subtropical gyres
(10–401) of the northern and southern hemispheres.
Despite low biomass and primary production,
which characterise the central subtropical gyres
(Karl, 1999), their large spatial extent means that
they account for a significant fraction (30–50%) of
global oceanic primary productivity and export
production (Karl et al., 1996). Although picoplankton represent the dominant component of the
phytoplankton in terms of primary productivity,
chlorophyll-a and cell densities within nutrient poor
subtropical waters (Marañón et al., 2000; Zubkov
et al., 1998, 2000), a significant proportion of the
primary productivity can be attributed to the nanoand microphytoplankton (Marañón et al., 2000,
2001; Fernández et al., 2003).
In the equatorial Atlantic, elevated phytoplankton biomass and primary productivity are found
throughout most of the year (Pérez et al., 2005a, b).
The community remains dominated by picoplankton (Herbland et al, 1987; Zubkov et al., 1998, 2000;
Pérez et al., 2005b), although Synechococcus spp.
and picoeukaryotes become relatively abundant
(Zubkov et al., 1998, 2000), and compared to the
subtropical gyres, increases in nanoflagellates (Tarran et al., 2006) and pigments diagnostic of diatoms
and dinoflagellates (Gibb et al., 2000; Barlow et al.,
2002, 2004) are also observed. Primary productivity
measurements from the equatorial Atlantic show a
similar size structure to those from the central
subtropical gyres with a dominance of picoplankton
and greater nano- and microplankton contributions
to primary production than to total chlorophyll-a
(Marañón et al., 2000, 2001; Pérez et al., 2005b).
High primary productivity and chlorophyll-a concentrations are also found in association with areas
of coastal upwelling, although in this case there are
significant changes in the size structure of the
community, with increases in the abundance of
diatoms and dinoflagellates (Gibb et al., 2000;
Barlow et al., 2002, 2004) and nano- and microplankton dominate both production and biomass
(Marañón et al., 2000, 2001; Tarran et al., 2006).
The main objective of this study is to investigate
the spatial and temporal variability of phytoplankton community composition and carbon fixation in
tropical equatorial and subtropical central gyre
waters of the Atlantic Ocean. To address this
objective we have made depth-resolved measurements of daily particulate carbon fixation, chlorophyll-a
concentration
and
phytoplankton
diagnostic pigments (DP) during four basinscale
cruises in the Atlantic Ocean (2003–04) as part of
the recent phase of the Atlantic Meridional Transect
programme (see http://www.amt-uk.org); ‘gyre’focused cruises AMT-12 (May, 2003) and AMT-14
(May, 2004), and the ‘upwelling’-focused cruises
AMT-13 (September, 2003) and AMT-15 (September, 2004) (Fig. 1). Measurements of carbon fixation
and chlorophyll-a were size-fractionated into two
fractions: 0.2–2 mm, picoplankton, and 42 mm,
nanoplankton and microplankton (herein termed
nanoplankton). Rates of particulate carbon fixation
were determined from dawn to dusk incubations
and dissolved organic production was not measured. As spatial and temporal variability of
respiration rates (photorespiration, dark respiration) will determine the balance between daily rates
of carbon fixation and primary productivity (Falkowski and Raven, 1997), and are outside the scope
of this paper, we retain the rates of carbon fixation
as a proxy of daily phytoplankton community
production and growth.
2. Methods
2.1. Sampling
Water samples were collected during daily predawn (0200–0400 h, local time) and mid-morning
(1100–1200 h) deployments of a 24 20 l SeaBird
CTD rosette sampler. Sampling depths were
determined by in situ fluorescence (WetLabs
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maximum was absent, the base of the surface
chlorophyll-rich layer (i.e. mixed layer). Incident
downwelling irradiance (400–700 nm, photosynthetically available radiation, PAR) was measured with
ship-mounted scalar irradiance sensors (Kipp &
Zonen ParLite 0348900, Skye Instruments SK3) and
integrated from dawn to dusk to estimate daily
irradiance (W m2 d1).
Stations were classified into biogeochemical
provinces as defined by Longhurst et al. (1995)
and Longhurst (1998) based on station positions
and characteristics of the chlorophyll-a distribution
(surface concentration, depth of the chlorophyll-a
maximum) to account for seasonal shifts in the
province boundaries. Provinces sampled in this
study are the North Atlantic Drift (NADR), North
Atlantic Subtropical Gyre (NATL), Canary Current
Coastal (CNRY), Western Tropical Atlantic
(WTRA), South Atlantic Subtropical Gyre (SATL)
and the Southern Subtropical Convergence (SSTC)
(Fig. 1). Within this analysis sub-provinces of the
Northern subtropical gyre (i.e. North Tropical
Atlantic, NATR, Eastern North Atlantic Subtropical Gyre, NAST-E, and Western North Atlantic
Subtropical Gyre, NAST-W) are all included in the
NATL to allow statistical analysis of intercruise
differences (Fig. 1).
Fig. 1. Cruise tracks and station positions for 2003–04 Atlantic
Meridional Transect (AMT) programme overlayed on biogeochemical provinces (see text). Cruises are AMT-12 (K; May,
2003), AMT-13 (J; September, 2003), AMT-14 (’; May, 2004),
and AMT-15 (&; September, 2004). Biogeochemical provinces
are North Atlantic Drift (NADR), North Atlantic Subtropical
Gyre (NATL), Canary Current Coastal upwelling (CNRY),
Western Tropical Atlantic (WTRA), SATL (South Atlantic
Subtropical Gyre), and South Subtropical Convergence (SSTC).
fluorometer), temperature and salinity (SeaBird)
profiles. Mixed layer depths (MLD) were identified
as an increase of 0.5 1C from surface (10 m)
temperatures (after Hooker et al., 2000). During
the pre-dawn cast, measurements of carbon fixation,
DP and size-fractionated chlorophyll-a were determined from 5–6 light depths, while total chlorophyll-a and nutrients were measured on up to 10
depths. DP (3–5 depths), total chlorophyll-a (5–10
depths) and nutrients (10–12 depths) were also
measured on the midday cast. Light depths were
estimated on the basis that the 1% isolume
corresponds to the depth of the subsurface
chlorophyll (fluorescence) maximum (Agustı́ and
Duarte, 1999) or, when the subsurface chlorophyll
2.2. Carbon fixation
Daily rates of carbon fixation (mmol C m3 d1)
were estimated from the incorporation of radiolabelled sodium bicarbonate (NaH14CO3) into particulate material. Three light and three dark 125 ml
polycarbonate bottles from 5–6 light depths (97%,
55%, 33%, 14%, 1% and 0.1% of surface
irradiance) were spiked with 18–20 mCi under dim
light and incubated from local dawn until dusk
(10–16 h) in deck incubators. The underwater light
field was reproduced using a combination of blue
and neutral density light filters. Incubators for the
upper 4 light levels were flushed with surface
seawater and incubators for the deep light depths
(1 and 0.1%) were flushed with chilled freshwater
regulated to 73 1C of in situ temperature. Incubations were terminated by filtration (o200 mbar)
through 47 mm 0.2 mm polycarbonate filters (Fileder
Filter Systems, UK). The filters were then rinsed
with filtered (o0.7 mm) seawater and fumed over
hydrochloric acid for 30–40 min. Size-fractionated
carbon fixation was determined for the 55% and
1% light levels by gravity filtering through 47 mm
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2 mm polycarbonate filters before filtering onto
0.2 mm filters. Therefore, size fractionation within
this study refers to the o2 mm (picoplankton) and
42 mm (nano- and micro-plankton, which we term
nanoplankton) cells.
After fuming, filters were placed in 6 ml pony
vials with 5 ml of Optiphase HiSafe-3 liquid
scintillation cocktail, and samples counted on a
TriCarb 3900TR liquid scintillation counter. Daily
spikes were prepared in fresh filtered (o0.7 mm)
seawater and spike activity checked by addition of
100 ml (10 mCi) of the seawater spike solution to
9.9 ml CarboSorb and subsamping 5 replicate 100 ml
sub-samples into 6 ml pony vials to which 5 ml
PermaFluor E+ was added. Daily spike activities
were 710% of the calculated spike activity of
18–20 mCi. Replicate measurements of daily rates of
carbon fixation had a relative standard deviation of
o30%. Relative standard deviations increased with
depth as rates of carbon fixation decreased.
2.3. Fluorometric chlorophyll-a
Fluorometric measurements of total chlorophylla were made by filtration of 250 ml of seawater
through Whatman GF/F (nominal pore size 0.7 mm)
glassfibre filters, extraction of the filters in 10 ml
90% acetone (HPLC grade) for 18–20 h (dark, 4 1C)
and determination of chlorophyll fluorescence with
a TD-700 (Turner Designs) fluorometer (after
Welschmeyer, 1994) calibrated with pure chlorophyll-a standards (Sigma, UK). Size-fractionated
chlorophyll-a measurements (AMT-13, AMT-14,
AMT-15) were made by sequential filtering through
10, 5, 2 and 0.2 mm polycarbonate filters (Fileder
Filter Systems, UK), and extraction as with GF/F
filters. Chlorophyll-a measurements from glassfibre
and polycarbonate filters (summed) were in good
agreement for all AMT cruises (AMT-13–AMT-15;
y ¼ 0:8620:015, r2 ¼ 0:84, po0.001, n ¼ 240). In
this study a comparison is made between picoplankton (o2 mm) and nanoplankton (42 mm;
2+5+10 mm filters) fluorometric chlorophyll-a.
2.4. HPLC pigment measurements
Duplicate 1–4.2 l water samples (stored at 60 to
80 1C) were filtered under positive pressure
through Whatman GF/F (0.7 mm) glass fibre filters.
One replicate was analysed following the highperformance liquid chromatography (HPLC) method of Barlow et al. (1997a, b) on a 3 mm Hypersil
MOS2 C8 column using a ThermoFinnigan Spectra
HPLC system with Thermo Separations AS3000
autosampler, Thermo Separations UV6000 diode
array absorbance detector, and PC1000 and
ChromQuest chromotography software. Standards
for chlorophyll-a were purchased from Sigma (UK),
and for other pigments from the DHI Institute for
Water and Environment, Denmark. Detection
limits were 0.002 mg3 or less for all pigments.
Analysis of replicates gave relative standard deviations between samples of o20% (for chlorophyll-a)
to o40% (for total pigments). Chlorophyllide-a
was not resolved in this study, and thus HPLC
chlorophyll-a (TChl-a) measurements include only
mono-vinyl (Chl-a) and divinyl- (DvChl-a) chlorophyll-a. Good agreement was found between
fluorometric and HPLC chlorophyll-a measurements for all AMT cruises (AMT-12–AMT-15;
y ¼ 1:4320:001, r2 ¼ 0:64, po0.001, n ¼ 811).
Due to fluorometer problems during AMT-12,
fluorometric chlorophyll-a results were calibrated
using a subset of the HPLC TChl-a. Thus, fluorometric chlorophyll-a values for AMT-12 are closer
to HPLC TChl-a values and are significantly lower
than fluorometric chlorophyll-a from the other
cruises.
In order to assess the size and taxonomic
composition of the phytoplankton community, a
diagnostic pigment index (Vidussi et al., 2001;
Barlow et al., 2004) was defined as the total of
seven pigments selected for their taxonomic and
associated size affinity:
DP ðmg m3 Þ ¼ Zea þ Chlb þ Allo þ 190 hex
þ 190 but þ Fuco þ Per;
ð1Þ
where zeaxanthin (Zea) is indicative of cyanobacteria (including prochlorophytes), chlorophyll-b
(Chl-b) of prochlorophytes, alloxanthin (Allo) of
cryptophytes, 190 -hexanoyloxyfucoxanthin (190 -hex)
of prymnesiophytes, 190 -butanoyloxyfucoxanthin
(190 -but) of pelagophytes, fucoxanthin (Fuco) of
diatoms, and peridinin (Per) of dinoflagellates.
Following Vidussi et al. (2001), the proportion of
DP attributable to each of the size categories of
phytoplankton is defined as
Picoplankton or PicoDPð%Þ
¼ Zea þ Chlb=DP 100,
ð2Þ
Nanoplankton or NanoDPð%Þ
¼ Allo þ 190 hex þ 190 but=DP 100.
ð3Þ
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Microplankton or MicroDPð%Þ
¼ Fuco þ Per=DP 100.
ð4Þ
The use of such an index must be viewed with
caution as (i) eukaryotic picoplankton are placed in
the nanoplankton rather than the picoplankton, (ii)
small (o20 mm) oceanic diatoms and dinoflagellates
are placed in the microplankton rather than the
nanoplankton, and (iii) Chl-b is regarded as being
solely derived from low-light-adapted prochlorophytes rather than from prasinophytes or chlorophytes. Within this study we have summed the DP
of the nanoplankton (NanoDP) and microplankton
(MicroDP) to represent the 42 mm fraction for
which we have measured fluorometric chlorophyll-a
and carbon fixation. Thus, further reference to
nanoplankton in terms of DP includes all cells
42 mm (i.e. NanoDP+MicroDP).
2.5. Nutrient measurements
Micromolar (mmol kg1) nitrate and phosphate
concentrations were measured on a 5-channel
Technicon segmented flow colorimetric autoanalyser (Bran+Luebbe, AAII). Nanomolar (nmol kg1)
concentrations of nitrate and phosphate were
measured using a colourimetric segmented flow
analytical system with liquid waveguide capillary
cell (World Guide Precision). Detection limits were
0.1 mmol kg1 for micromolar measurements and
2 nmol kg1 for nanomolar measurements. Further
details may be found in Rees et al. (2006) and Krom
et al. (2005). Within this study, the nitracline was
defined as the depth below which nitrate concentrations exceeded 1 mmol N kg1.
3. Results
3.1. General hydrography
On all four AMT cruises, shallow MLD (o75 m)
were found in equatorial waters (WTRA;
101S–101N), in the Canary upwelling off NW
Africa (CNRY; 101N–201N) and in temperate
waters of both the northern (NADR; 435–401N)
and southern hemisphere (SSTC; 4351S—401S)
(Fig. 2). During AMT-12 and -14, the MLD in the
southern subtropical gyre was 50–75 m compared
with 4100 m during AMT-13 and 15 (Fig. 2). In the
northern subtropical gyre MLD was 50–75 m during
AMTs-12, -13 and -15 with only a few stations
during AMT-14 showing MLD 4100 m (Fig. 2).
1597
The nitracline (1 mmol N kg1 contour) was relatively deep (4100–150 m) in both the NATL and
SATL, and shallow (o100 m) in the WTRA,
CNRY, NADR and SSTC (Fig. 2). Thus, surface
waters (o50 m) are depleted in nitrate below
1 mmol N kg1 throughout the tropical (WTRA)
and subtropical (NATL, SATL) Atlantic Ocean,
with only surface waters of the CNRY and high
latitudes (4351N) showing nitrate concentrations
41 mmol N kg1 (Fig. 2). There is no clear intercruise pattern of variability in depth of the nitracline
(Fig. 2) other than the differences in cruise track, in
particular sampling of the CNRY on AMTs 13 and
-15 (Fig. 1). Daily incident irradiance (PAR) shows
clear seasonal differences (Fig. 3) with PAR levels
higher in each hemisphere during spring (AMT-12
and -14 in northern hemisphere, AMT-13 and -15 in
southern hemisphere). The least intercruise variability in incident irradiance is found in the WTRA
with incident PAR levels consistently around
120 W m2 d1 during all four cruises (Fig. 3).
3.2. Latitudinal patterns of chlorophyll-a, carbon
fixation and DP
Total chlorophyll-a concentrations were generally
o0.1 mg m3 in surface waters, especially in the
NATL and SATL, and increased at depth to form a
basinscale subsurface chlorophyll-a maximum
(Fig. 2). The depth of the subsurface chlorophyll-a
maximum was closely related to the depth of the
nitracline (Fig. 2). Relatively high chlorophyll-a
(40.1–0.2 mg m3) in surface waters was found in
the WTRA during all four cruises (Fig. 2A–D) and
associated with a relatively shallow (o60 m) and
intense (40.4 mg m3) subsurface chlorophyll maximum. During AMT-13 and -15, high-surface
chlorophyll-a (42 mg m3) and shallow chlorophyll
maxima were observed within the CNRY (Fig.
2B,D). An inverse relationship exists between the
depth of the subsurface chlorophyll maximum and
its intensity (Herbland and Voituriez, 1979), so that
shallowing of the chlorophyll maximum from the
extreme depths of the subtropical gyres (SATL,
NATL; 100–150 m) to the relatively shallow depths
(50–75 m) around the equator (WTRA) and CNRY
upwelling is accompanied by increases in the total
amount of chlorophyll-a (Fig. 2). No consistent
relationship was found between the depth of the
subsurface chlorophyll-a maximum and the MLD
(Fig. 2).
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Fig. 2. Sections of total fluorometric chlorophyll-a (left column; mg m3) and daily rates of carbon fixation (right column;
mmol C m3 d1) for (A) AMT-12 (May, 2003), (B) AMT-13 (September, 2003), (C) AMT-14 (May, 2004), and (D) AMT-15 (September,
2004). Solid lines on left panels indicate mixed layer depth (MLD; m) (defined after Hooker et al., 2000) and solid lines on right panels
indicate depth of the 1-mmol kg1 nitrate contour.
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Fig. 3. Incident PAR (W m2 d1) for AMT-12 (May, 2003),
AMT-13 (September, 2003), AMT-14 (May, 2004), and AMT-15
(September, 2004).
Temperate waters of the NADR and SSTC
provinces show elevated chlorophyll-a concentrations (Fig. 2D; Table 1) dependent on the season
sampled. High chlorophyll-a concentrations were
seen in the NADR during AMT-12 and -14 (northern spring), and in the SSTC during AMT-13 and
-15 (southern spring) (Fig. 2). The boundaries of the
subtropical gyres in both hemispheres vary seasonally, with southward movement of the boundary
between the NADR and NATL during northern
spring (40–361N), northward movement of the
boundary between SSTC and SATL during southern spring (37–331S) and opposite trends during the
autumn (Fig. 2).
Daily rates of carbon fixation were generally
highest in surface waters and decreased with depth
(Fig. 2) as irradiance decreased. Therefore, the
subsurface chlorophyll maximum makes only a
small contribution to water-column carbon fixation
(Marañón et al., 2000), except where it shallows in
the equatorial Atlantic (WTRA), CNRY upwelling,
SSTC and NADR (Fig. 2A–D). In surface waters of
the NATL and SATL, rates of carbon fixation were
low (o0.2 mmol C m3 d1) compared to those
(40.3–0.5 mmol C m3 d1) in surface waters of
the WTRA, CNRY upwelling and NADR and
SSTC during spring (Fig. 2A–D; Table 1).
In surface waters of the tropics and subtropics,
nanoplankton DP (NanoDP+MicroDP; Fig. 4)
represented o50% of the total DP which highlights
the importance of cyanophytes and picoplankton to
chlorophyll-biomass and production (Zubkov et al.,
1998, 2000; Gibb et al., 2000; Marañón et al., 2000).
Microplankton (MicroDP; not shown) DP were
o10% of total DP throughout the tropical and
subtropical Atlantic Ocean, except in association
with upwelled waters off NW Africa during AMT-
1599
13 and -15, and in temperate waters during spring
(NADR on AMT-12 and AMT-14, SSTC on AMT13 and -15). In the northern section of the NATL
(301N) during both AMT-12 and -14, nanoflagellate DP represented 450% of DP in upper waters
(o50–80 m) but were less important in the SATL on
AMTs 13 and 15 (Fig. 4). Within the subtropics and
tropics, deeper communities (especially in the
subsurface chlorophyll maximum) showed a more
even mixture of cyanophyte and nanoflagellate DP
(Fig. 4; see also Table 2). As the subsurface
chlorophyll maximum shallows in the WTRA
(Fig. 4), cyanophytes were dominant in subsurface
waters (450%; Table 2) while nanoflagellates were
more important at depth (450 m) in the water
column (Fig. 4; Barlow et al., 2002).
3.3. Temporal patterns of chlorophyll-a, carbon
fixation and DP
3.3.1. NATL
Within the NATL, euphotic zone parameters
describing chlorophyll-a distribution and carbon
fixation rates were variable (Table 1). In particular,
chlorophyll-a concentrations were relatively high
during AMT-14 within both the surface and chlorophyll maximum layers (Table 1). Though these high
chlorophyll-a concentrations were accompanied by
slightly higher euphotic zone production (significant at
a lower level due to high variability within the cruise
measurements), no significant differences were found
in surface and deep rates of carbon fixation (Table 1).
The subsurface chlorophyll maximum was relatively
shallow during both AMT-13 and -15 (although only
significant during the latter; Table 1). These differences may be related to variability in cruise track, with
AMT-12 and -14 further offshore than AMT-13 and 15 (Fig. 1). Intercruise differences in DP in the NATL
were observed in surface waters only and relate to
lower nanoplankton DP (mean 23.075.1%) during
AMT-15 than during the other cruises (Table 2).
3.3.2. SATL
In the SATL, chlorophyll-a concentrations were
relatively high during AMT-14 in both surface
waters and the subsurface chlorophyll maximum,
and rates of carbon fixation were relatively high
during AMT-13 (Table 1). Chlorophyll-a in the
chlorophyll maximum was also lower during AMT12 than later cruises (Table 1; Fig. 2), which is due
to calibration differences (see Section 2.4). Significantly higher rates of carbon fixation were seen within
[6]
[3]
[12]
[8]
[11]
[11]
[20]
[18]
po0:001
12,13514b15
10.272.1
13.271.6
16.373.8
12.472.4
po0:005
12,13514b15
11.972.7
11.572.5
20.175.3
14.072.0
po0:001
12,13o14,15
[16]
[9]
[18]
[14]
[12]
[4]
[12]
[10]
[11]
[12]
[20]
[22]
po0:001
12,13514b15
0.0670.03
0.0570.02
0.1070.06
0.0470.02
po0:001
12, 13514b15
0.1170.02
0.1070.02
0.1970.06
0.1170.02
po0:001
12,13514,15
0.0470.01
0.0670.02
0.0970.05
0.0970.03
Csur (mg m3)
[16]
[9]
[18]
[14]
[12]
[3]
[12]
[10]
[11]
[11]
[19]
[19]
po0:001
12o13o14b15
0.1770.03
0.2170.04
0.2670.04
0.2070.04
po0:001
12,13514b15
0.3270.08
0.2870.05
0.5770.13
0.4070.09
po0:001
12,13514,15
0.2170.05
0.2770.11
0.4470.12
0.3470.10
Ccmax (mg m3)
[16]
[9]
[18]
[14]
ns
—
107.8719.7
130.4722.2
107.6722.0
129.8738.1
ns
—
[11]
[11]
[20]
[19]
72.4712.7 [12]
72.576.6 [4]
65.4715.6 [12]
67.5717.5 [10]
po0:01
12,13,14 415
113.8727.1
85.6725.9
106.9728.8
81.0728.3
Zcmax (m)
[5]
[4]
[8]
[2]
[5]
[8]
[7]
[4]
po0:001
12513b14,15
10.472.4
23.877.7
12.572.8
16.773.7
ns
—
23.773.9 [2]
7.1 [1]
30.876.7 [5]
26.875.7 [3]
po0:05
12,13o 14,15
18.873.8
12.378.1
25.078.0
15.172.8
Pzeu (mmol C m2 d1)
[5]
[5]
[8]
[2]
ns
—
0.1370.02
0.2270.11
0.1670.04
0.1370.05
ns
—
[5]
[8]
[8]
[4]
0.4570.17 [3]
0.20 [1]
0.6370.19 [5]
0.4870.20 [3]
ns
—
0.1970.06
0.1670.06
0.3570.16
0.2670.16
Psur (mmol C m3 d1)
[8]
[5]
[8]
[2]
[5]
[8]
[7]
[4]
po0:001
12513b14o15
0.0470.02
0.1370.04
0.0470.02
0.0870.02
ns
—
0.1270.06 [3]
0.07 [1]
0.1470.09 [5]
0.2270.07 [3]
ns
—
0.1270.03
0.1070.07
0.1470.08
0.1270.11
Pcmax (mmol C m3 d1)
Parameters include euphotic zone chlorophyll-a (Czeu) and carbon fixation (Pzeu), surface (55% PAR level) chlorophyll-a (Csur) and carbon fixation (Psur), chlorophyll maximum
chlorophyll-a (Ccmax) and carbon fixation (Pcmax), and depth of the chlorophyll maximum (Zcmax). Biogeochemical provinces included are the North Atlantic Subtropical Gyre
(NATL), Western Tropical Atlantic (WTRA), and South Atlantic Subtropical Gyre (SATL). [n] indicates number of measurements. One-way ANOVA and paired Student T-tests are
used to analyse intercruise differences; p values are given for significant ANOVAs and T-tests (o/4 indicates significant at po0:05, 5/b indicates significant at po0:005, ns indicates
not significant).
ANOVA
T-tests
SATL
AMT-12
AMT-13
AMT-14
AMT-15
ANOVA
T-tests
WTRA
AMT-12
AMT-13
AMT-14
AMT-15
ANOVA
T-tests
11.471.6
10.371.7
19.675.2
13.471.9
Province/cruise
NATL
AMT-12
AMT-13
AMT-14
AMT-15
[8]
[9]
[18]
[14]
Czeu (mg m2)
Parameter/ (Units)
Table 1
Average values (7standard deviation) for parameters describing the distribution of carbon fixation and chlorophyll-a in the euphotic zone for the different AMT cruises and
biogeochemical provinces
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Fig. 4. Sections of nanoplankton diagnostic pigments (NanoDP+MicroDP) as a proportion (%) of total diagnostic pigments for (A)
AMT-12 (May, 2003), (B) AMT-13 (September, 2003), (C) AMT-14 (May, 2004), and (D) AMT-15 (September, 2004). Solid lines
represent the depth of maximum chlorophyll-a concentration.
the subsurface chlorophyll maximum on both AMT13 and -15 (Table 1; Fig. 2), but only within the
euphotic zone on AMT-13. DP varied between cruises
in both surface waters and the chlorophyll maximum
(Table 2), being significantly higher in surface waters
during AMT-13 compared to AMT-12, and in the
subsurface chlorophyll maximum on AMT-14 compared to either AMT-13 or -15.
3.3.3. WTRA
Significant intercruise differences in the WTRA
were only observed for chlorophyll-a, with higher
surface and subsurface chlorophyll maximum concentrations during AMT-14 (Table 1; Fig. 2). No
significant differences were found between the
cruises in terms of DP (Table 2).
3.4. Pico- and nanoplankton contributions to
chlorophyll-a and carbon fixation
Picoplankton and nanoplankton contributions to
chlorophyll-a and carbon fixation are presented for
surface waters and the subsurface chlorophyll
maximum from AMT-14 in Fig. 5 and are
summarised in Table 3 for all four AMT cruises.
Within surface waters of the NATL and SATL,
nanoplankton contributions to carbon fixation are
typically higher than their contributions to chlorophyll-biomass (Fig. 5; Table 3). In the subsurface
chlorophyll maximum, nanoplankton represent
similar levels of both carbon fixation and chlorophyll-a (Fig. 5; Table 3). In the WTRA, there is
evidence of a similar pattern, with higher nanoplankton surface contributions to carbon fixation
than to chlorophyll-a and similar levels of both
chlorophyll-a and carbon fixation in the subsurface
chlorophyll maximum (Fig. 5; Table 3).
Estimates of the chlorophyll-normalised rate of
carbon fixation (Pchl) for the different size fractions
show different relative patterns in surface waters
and the chlorophyll maximum (Table 3). In surface
waters, estimates of Pchl (Table 3) are generally
much higher for nanoplankton than for picoplankton
(80–125 mg C
(mg chl-a)1 m3 d1
and
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Table 2
AMT cruise averages (7 standard deviation) for picoplankton (o2 mm; PicoDP) and nanoplankton (42 mm; NanoDP+MicroDP)
diagnostic pigments in surface waters and the chlorophyll maximum within biogeochemical provinces
Surface
Province/cruise
NATL
AMT-12
AMT-13
AMT-14
AMT-15
[n]
o2 mm
42 mm
[n]
o2 mm
42 mm
[16]
[8]
[15]
[13]
54.9710.8
61.878.1
67.673.3
76.875.1
45.2710.8
37.977.2
45.4714.1
23.075.1
[16]
[8]
[16]
[11]
38.479.3
39.8712.4
45.8714.1
35.679.8
61.679.3
60.2712.4
54.2714.1
64.479.8
po0:001
12,13,14515
Po0:001
12,13,14b15
ns
—
ns
—
66.377.0
59.4725.8
63.2718.0
71.2720.3
33.777.0
40.6725.8
36.8718.0
28.8720.4
33.6713.1
39.5712.7
44.174.5
32.175.3
66.4713.2
60.6712.7
55.974.5
68.075.3
ns
—
ns
—
ns
—
ns
—
58.7710.0
66.076.1
62.678.4
67.977.5
41.4710.0
34.176.1
37.478.4
32.077.4
43.2710.5
43.975.7
56.178.4
42.479.5
56.8710.5
56.175.7
45.279.5
57.679.5
po0:05
12o13,14,15
Po0:05
12413,14,15
po0:001
12,13514b15
po0:001
12,13b14515
ANOVA
T-tests
WTRA
AMT-12
AMT-13
AMT-14
AMT-15
[10]
[1]
[12]
[5]
ANOVA
T-tests
SATL
AMT-12
AMT-13
AMT-14
AMT-15
ANOVA
T-tests
Chlorophyll maximum
[11]
[8]
[16]
[18]
[10]
[4]
[9]
[6]
[13]
[11]
[16]
[17]
Biogeochemical provinces included are the North Atlantic Subtropical Gyre (NATL), Western Tropical Atlantic (WTRA), and South
Atlantic Subtropical Gyre (SATL). One-way ANOVA and pair-wise Student T-tests are used to analyse intercruise differences; p values
are given for significant ANOVAs and T-tests (o/4 indicates significant at po0:05, 5/b significant at po0:005, ns not significant). [n]
indicates number of measurements.
20–70 mg C (mg chl-a)1 m3 d1, respectively),
whereas chlorophyll maximum estimates of Pchl
are similar for the two fractions (6–14 mg C (mg chla)1 m3 d1 and 3–8 mg C (mg chl-a)1 m3 d1,
respectively). These differences between pico- and
nanoplankton Pchl are significantly different in all
cases in surface waters, whereas only around half of
the cases are significantly different in the subsurface
chlorophyll maximum (Table 3).
4. Discussion
4.1. Spatial and temporal variability
The chlorophyll-a concentrations and rates of
carbon fixation observed in this study are in general
agreement with measurements from previous AMT
cruises and other studies in low nutrient areas of the
Atlantic and Pacific Ocean (Table 4). At the
basinscale, low rates of carbon fixation and low
chlorophyll-a biomass are observed in the subtropical gyres, increasing in proximity to the equator,
to coastal upwelling off NW Africa and to spring in
temperate waters in either hemisphere (Fig. 2).
During earlier AMT cruises (AMT-1–4,
1995–99), evidence of temporal variability was
observed by Marañón et al. (2000) with four-fold
or greater differences in primary production in both
the NATL and SATL (Table 4). Marañón et al.
(2000) also observed an opposing pattern in the
SATL and WTRA, with much higher rates (4–5
times) of primary production during AMT-1 and -2
(Marañón et al., 2000). Within this study (AMT12–15), such large-scale intercruise variability was
not observed and typical rates of carbon fixation for
the NATL, SATL and WTRA within the range
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Fig. 5. Percentage contributions of picoplankton and nanoplankton to total fluorometric chlorophyll-a and to daily rates of carbon
fixation in surface waters (A) and the subsurface chlorophyll maximum (B) for the NADR, NATL, WTRA and SATL during AMT-14
(May, 2004).
10–30 mmol C m2 d1 (Table 1). These values are
at the lower range of those found by Marañón et al.
(2000) and other studies in low nutrient open-ocean
settings (Table 4). A possible reason for these
differences may relate to the cruise tracks of earlier
AMTs, which were relatively close to the basin
margins whereas the tracks for AMT-12–15
sampled the mid-ocean gyres (see Fig. 1 in
Robinson et al., 2006). The intercruise variations
observed by Marañón et al. (2000) in primary
productivity were not associated with any detectable
variability in phytoplankton biomass (chlorophylla, microscope counts) or community composition
(microscope counts, flow cytometer), but were
interpreted as being related to changes in the
chlorophyll-normalised carbon fixation rate (Marañón and Holligan, 1999; Behrenfeld et al., 2002).
In contrast, the spatial and temporal variability
found within this study are associated with differences in the phytoplankton biomass and community
composition. In the NATL, the AMT-14 stations
were characterised by high surface and deep
chlorophyll-a concentrations and high euphotic
zone rates of carbon fixation, while the AMT-15
stations were characterised by significantly higher
picoplankton DP (Tables 1 and 2; Section 3.3.1).
These differences in between cruises are mainly
attributable to a number of stations at the northern
(35–401N) and southern (14–181N) boundaries of
the province (Fig. 2; Table 1). However, high
chlorophyll-a in the subsurface chlorophyll maximum during AMT-14 is observed over the entire
NATL (Fig. 2; Table 1) and these combined signals
may reflect a spring signal in the northern portion of
the gyre (see Fig. 2) (see also Letelier et al., 2004).
In the SATL, some of the AMT-14 stations close
to the southern boundary (30–401N) were characterised by high-surface chlorophyll-a concentrations, while high chlorophyll-a in the subsurface
chlorophyll maximum was observed over the entire
province (Fig. 2; Table 1). Stations in the SATL
during AMT-13 and -15 were characterised by high
rates of carbon fixation within the subsurface
chlorophyll maximum (Fig. 2), and in the case of
AMT-13 are associated with higher nanoplankton
DP relative to AMT-14 (Tables 1 and 2; Section
3.3.2). These differences may relate to the spring
signal in the oligotrophic ocean where winter mixing
supplies nitrate to the subsurface chlorophyll
maximum and there are basinscale changes in
[n]
[7]
[2]
[8]
[2]
[2]
—
[4]
[4]
[2]
[8]
[9]
[4]
Parameter
Province/cruise
NATL
AMT-12
AMT-13
AMT-14
AMT-15
WTRA
AMT-12
AMT-13
AMT-14
AMT-15
SATL
AMT-12
AMT-13
AMT-14
AMT-15
47.273.9
44.678.3
45.4716.4
53.0712.5
36.8714.6
nd
32.476.1
36.673.5
55.1714.9
46.371.2
49.1713.0
41.571.6
42 mm% Prod
nd
47.2715.7
20.477.3
39.6732.2
nd
nd
55.173.0
69.3733.8
nd
69.5714.9
45.675.2
29.4732.8
o2 mm Pchl
nd
113.6727.7
116.8791.5
90.0711.9
nd
nd
124.9740.3
125.2720.1
nd
78.2721.3
118.3733.3
125.4773.8
42 mm Pchl
—
po0:001
po0:01
po0:05
—
—
po0:05
po0:05
—
—
po0:001
—
T-tests
[2]
[8]
[9]
[4]
[2]
—
[4]
[4]
[7]
[1]
[8]
[2]
[n]
nd
15.371.4
9.072.2
22.274.1
nd
nd
13.073.4
16.976.6
nd
12
16.477.3
28.277.3
42 mm % Chl
Chlorophyll maximum
19.677.6
22.874.6
17.978.0
24.171.2
23.8713.5
nd
23.171.3
26.675.8
23.6710.5
37
22.676.6
25.578.4
42 mm% Prod
nd
8.473.0
3.071.9
4.270.8
nd
nd
3.772.3
6.470.8
nd
9.2
6.174.0
7.673.2
o2 mm Pchl
nd
13.474.1
7.476.2
9.073.3
nd
nd
7.672.6
13.774.4
nd
38.7
8.872.9
6.572.4
42 mm Pchl
—
po0:05
ns
po0:05
—
—
ns
po0:05
—
—
ns
—
T-tests
nd indicates not determined. Results from Student T-tests comparing differences between Pchl for pico- and nanoplankton are shown with appropriate significance (p) levels (ns
indicates non-significant). [n] indicates the number of measurements.
nd
25.478.8
14.074.1
29.274.8
nd
nd
17.277.8
20.777.4
nd
43.7710.8
29.2713.0
11.377.6
42 mm% Chl-a
Surface
Depth
Table 3
AMT cruise averages (7standard deviation) for nanoplankton (42 mm) contributions to fluorometric chlorophyll-a (% Chl-a) and to carbon fixation (% Prod), and for chlorophyllnormalised rates of carbon fixation (Pchl; mg C (mg chl-a)1 m3 d1) for both size fractions surface and chlorophyll maximum samples
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Table 4
Comparison of euphotic zone chlorophyll-a concentration (Czeu; mg m2) and carbon fixation rates (Pzeu; mmol C m2 d1) from this
study with measurements from previous studies in the Atlantic and Pacific Ocean
Region
Czeu (mg m2)
Pzeu (mmol C m2 d1)
Source
(a) Subtropical Gyres
SATL
AMT-1
AMT-2
AMT-3
AMT-4
AMT-5
AMT-12–15
3673
3172
2672
2372
2872
1374
25712
1675
3378
Marañón et al. (2000)
NATL
AMT-1
AMT-2
AMT-3
AMT-4
AMT-5
AMT-6
AMT-12–15
2672
2775
1372
38710
2072
2172
1575
26717
2078
Robinson et al. (2002)
This study
1771
2172
Teira et al. (2005)
16–80
Steinberg et al. (2001)
González et al. (2002)
1777
This study
672
3678
2475
Marañón et al. (2000)
González et al., (2002)
NATL
1992–2001
NATL (BATS)
1989–1997
NPSG (HOTS)
1989–1993
20–27
13–25
Letelier et al. (1996)
(b) Equatorial waters (WTRA)
AMT-1
AMT-2
AMT-3
AMT-11
AMT-12–15
3272
3472
3073
17–108
1675
972
1676
4774
18–22
2679
Marañón et al. (2000)
incident irradiance, which allow the growth of
larger eukaryotic phytoplankton (DuRand et al.,
2001; Letelier et al., 2004).
Variability of chlorophyll-a in the WTRA is seen
in both surface waters and the chlorophyll maximum but appears not to be linked to changes in DP
for picoplankton in surface waters or for nanoplankton in the subsurface chlorophyll maximum
(Tables 1 and 2; Section 3.3.3). Seasonal shifts in the
trade winds, in the depth of the thermocline, and in
the strength of the equatorial currents and countercurrents are all thought to affect phytoplankton
distribution and growth in this region (Pérez et al.,
2005a, b).
Basinscale spatial (and temporal) variability of
primary productivity, community structure and
photophysiology is thought to be related to depth
variability of the nitracline (here defined as the
depth of the 1 mmol N kg1 contour) and nitrate
Pérez et al. (2005b)
This study
supply to the euphotic zone (Marañón and Holligan, 1999; Marañón et al., 2000; Behrenfeld et al.,
2002). The subsurface chlorophyll maximum acts as
a barrier to nutrients diffusing into the upper ocean
(Letelier et al., 2004) and is generally found above
the nitracline with basinscale variability in the depth
of the chlorophyll maximum closely related to the
nitracline (Fig. 2). Only in equatorial waters is the
subsurface chlorophyll maximum found at a similar
depth to the nitracline (Fig. 2). Upper ocean carbon
fixation rates are also related to the depth of the
nitracline on the basinscale, however, intercruise
differences in carbon fixation rates are not associated with changes in nitracline depth (Fig. 2).
Rather, intercruise differences in carbon fixation in
the subtropical gyres appear to be related to
seasonal variability in incidental irradiance (Fig. 3).
The supply of nitrate to the euphotic zone
increases from the subtropical gyres to equatorial
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waters (Planas et al., 1999). Nitrate concentrations
in the subsurface chlorophyll maximum are significantly higher than those estimated to be required
to support the rates of carbon fixation observed
(Fig. 6A,C), although the N:P ratio in most cases is
much lower than 15 (Fig. 6B,D). This apparent
excess of nitrate at depth indicates that carbon
fixation in the subsurface chlorophyll maximum is
controlled by light availability. Thus, new production in the subsurface chlorophyll maximum is likely
to be a transient feature fuelled by seasonal changes
in light availability (Letelier et al., 2004) or localised
physical instability (Dandonneau et al., 2003). As
the subsurface chlorophyll maximum represents
only a small fraction of water column productivity
(Marañón et al., 2000), variability in nutrient supply
over the upper portion of the water-column is likely
to have a greater effect on phytoplankton community structure (Mills et al., 2004) and rates of carbon
fixation (Letelier et al., 2004) within the water
column as a whole.
4.2. Picoplankton and nanoplankton contributions
Several other studies have reported greater
nanoplankton contributions to carbon fixation than
to chlorophyll-biomass in tropical and subtropical
waters (Marañón et al., 2000, 2001; Fernández
et al., 2003). This observation implies that chlorophyll-normalised carbon uptake (Pchl) is significantly higher for nanoplankton than for
picoplankton (Marañón et al., 2000, 2001; Fernández et al., 2003). Previous studies (e.g. Marañón et
al., 2000, 2001) have concentrated on euphotic zone
measurements rather than resolving the phytoplankton of the upper and lower portions of the
euphotic zone which differ in community composition (Barlow et al., 2002), nutrition (Dugdale, 1967;
Moore et al., 2002) and seasonal trends (DuRand et
al., 2001; Letelier et al., 2004). Our division of the
water column shows that the differences between
pico- and nanoplankton contributions to chlorophyll-a and carbon fixation appear to follow
different patterns in surface waters and in the
chlorophyll maximum (Fig. 5; Section 3.4).
Higher photosynthetic efficiency of nanoplankton
than picoplankton appears contrary to the accepted
paradigm that small cells are more efficient at light
harvesting (lower ‘package effect’) and nutrient
uptake (Raven, 1998; Veldhuis et al., 2005). Average
surface values for chlorophyll-normalised carbon
fixation (Pchl) in Table 3 indicate that Pchl is
significantly higher for nanoplankton than for
picoplankton (80–125 and 20–70 mg C (mg chla)1 m3 d1, respectively). If the two components
have a similar carbon to chlorophyll-a ratio (e.g.
150, as proposed by Marañón, 2005) nanoplankton
growth rates will be higher than those of picoplankton (0.6–0.8 and 0.2–0.3 d1, respectively). Lower
carbon to chlorophyll-a ratios, or significant losses
of photosynthetically fixed carbon, are required to
increase surface Pchl and growth rates for picoplankton.
Within the subsurface chlorophyll maximum,
average Pchl are more similar for the two fractions
(3–8 mg C (mg chl)1 m3 d1 for the picoplankton
and 6–14 mg C (mg chl)1 m3 d1 for the nanoplankton; Table 3). In this case, if the carbon to
chlorophyll-a ratios were similar for the two
fractions (e.g. 50 as used in Karl, 1999) then the
two would have similar growth rates (0.1–0.2 and
0.1–0.3 d1). However, due to the lower package
effect in small cells (Raven, 1998) and utilisation of
organic growth compounds (Zubkov et al., 2003),
picoplankton may be able to maintain lower carbon
to chlorophyll-a ratios and attain higher growth
rates in the subsurface chlorophyll maximum.
The lower efficiency and growth rates of picoplankton in surface waters could be explained by
significant losses of photosynthetically fixed carbon,
cells or photosynthetic efficiency relative to larger
nanoplankton cells. Increased loss rates of picoplankton relative to nanoplankton during incubations have not been found so far (e.g. Fernández
et al., 2003). Although loss of photosynthetically
fixed carbon is higher for small cells (Raven, 1998),
estimated losses required to balance Pchl rates are
significantly higher than present estimates of losses
of fixed carbon (20%; Teira et al., 2003).
Respiratory losses (normalised to cell volume) of
photosynthetically fixed carbon are also higher for
smaller cells (Raven, 1998). Size specific differences
in grazing pressure may also explain a loss of
picoplankton fixed carbon due to higher grazing
rates on small cells (Veldhuis et al., 2005), however
changes in chlorophyll-a would accompany such
losses.
Reduction in the photosynthetic efficiency of
small cells relative to larger cells may also explain
lower Pchl. The lower package effect in small cells
may be disadvantageous in well-lit surface waters
of the tropics and subtropics as it implies that
lower light fluxes are required to saturate the photosynthetic machinery and induce photoinhibitory
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damage from both photosynthetically active radiation and UV (Raven, 1998). Recent laboratory
work has shown suppression of photosynthetic
efficiency in Prochlorococcus with around 60% of
the daily carbon fixation occurring before midday
(Bruyant et al., 2005). Diel variations in photosynthetic parameters of Prochlorococcus are regulated
by photoacclimation and the cell cycle, and thus
balanced growth is not achieved over a day as
different cellular processes occur during the light/
dark cycle (Bruyant et al., 2005). Diel variability
of cell fluorescence in Prochlorococcus (Bruyant
et al., 2005) also highlights that for this taxa Pchl will
vary over the day. The existence of similar diel
changes of cellular metabolism for nanoplankton in
the subtropical and tropical has not been reported,
but its absence may explain size specific differences
in Pchl.
Size-specific differences in the carbon to chlorophyll-a ratios could also resolve differences in Pchl
for picoplankton and nanoplankton. Several studies
have shown an increase in carbon to chlorophyll-a
ratios with cell size (e.g. Finkel, 2001), although
some have shown no trend with cell size (e.g. Geider
et al., 1986). However, field measurements taken by
Veldhuis and Kraay (2004) found highly variable
carbon to chlorophyll-a ratios for Prochlorococcus
spp. (450 in the surface to 15 at depth) in contrast to
relatively lower and more stable ratios for eukaryotic phytoplankton (30–80 in surface and at
depth). Therefore, until accurate estimates of the
cellular carbon to chlorophyll-a ratios are available
it is difficult to fully resolve the implications of high
Pchl for nanoplankton.
4.3. Implications for the biological pump
Currently, small photosynthetic cyanobacteria
and heterotrophic bacteria are thought to dominate
oligotrophic open ocean ecosystems and are involved in an efficient microbial loop which recycles
organic carbon within lower trophic groups (heterotrophic bacteria, nanoflagellates, ciliates, heterotrophic dinoflagellates) so that little is available to
higher trophic groups or for export (Azam et al.,
1983; Kiørboe, 1993). Increases in nutrient availability favours larger and faster-growing phytoplankton (e.g. diatoms), which may outgrow small
autotrophs and are available for predation by
higher trophic levels (e.g. zooplankton, fish larvae)
and for export through sedimentation (Kiørboe,
1993). The modern view of low nutrient open-ocean
1607
ecosystems includes both of these food webs (Karl,
1999), with a dominant picoplankton community
supporting the microbial food web which is
occasionally overshadowed by larger phytoplankton (Carpenter et al., 1999; Scharek et al., 1999)
during episodic nutrient events (Platt and Harrison,
1985).
Variability in the rates of primary production in
the Atlantic Ocean (Marañón et al., 2000) have
previously been related to changes in the chlorophyll specific rate of carbon fixation (Marañón and
Holligan, 1999; Behrenfeld et al., 2002). These
observations have led to the conclusion that open
ocean ecosystems tend to respond to instability in
the environment by changes in metabolic rates
rather than changes in the trophic organisation
(Marañón et al., 2001, 2003; Pérez et al., 2005a, b).
However, the variability in this study is associated
with a combination of changes in chlorophyll
specific carbon fixation and changes in the DP and
inferred community structure. The timescale of
environmental forcing is likely to control whether
the community responds metabolically or by
trophic reorganisation, with metabolic changes
leading to trophic ones as competitive mechanisms
become important.
In the tropical and subtropical open oceans, the
majority of carbon fixation occurs in surface waters
well removed from deep inorganic nutrient pools.
Thus, spatial and temporal variability of inorganic
and organic nutrient supply to the surface ocean
(e.g. Baker et al., 2003) regulate variability in upper
(o50 m) open ocean ecosystems. However, the
nitrate concentration in the subsurface chlorophyll
maximum appears to be sufficient to maintain the
rates of carbon fixation observed (Fig. 6; assuming
balanced carbon and nitrogen acquisition). These
deep nitrate concentrations appear to be in ‘excess’
of requirements which implies that carbon fixation
in the subsurface chlorophyll maximum is light
limited (Letelier et al., 2004). Although picoplankton dominance at depth appears paradoxical, due to
the lack of nitrate reductase by prochlorophytes
(Moore et al., 2002), their efficient light-harvesting
properties (Raven, 1998) may ensure their success at
depth. The utilisation of seasonal nitrate inputs into
the subsurface chlorophyll maximum will only
occur when sufficient light levels are present, and
thus new production and the export of material
from near the base of the euphotic zone will be
limited by the availability of light (Letelier et al.,
2004).
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Fig. 6. Subsurface chlorophyll maximum rates of carbon fixation (mmol C m3 d1), nitrate concentrations (A, C; mmol N kg1) and the
nitrate to phosphate ratios (B, D; mmol:mmol) for different biogeochemical provinces (A, B) and AMT cruises (C, D). Dotted lines
represent nitrogen uptake based on a C:N ratio of 6.6 (A, C), and a N:P ratio of 15 (B, D).
Greater rates of Pchl and estimated growth rates
for nanoplankton than for picoplankton imply a
greater role for large phytoplankton cells in the
turnover of organic carbon within low nutrient open
ocean environments than might be expected from
their relative contribution to total chlorophyll-a.
Such cells may include mineralising phytoplankton
which are important in carbon export (Klass and
Archer, 2002), and raises important questions over
its nutritional basis (e.g. Karl, 1999; Carpenter
et al., 1999; Singler and Villareal, 2005) and its
trophic fate (Azam et al., 1983; Kiørboe, 1993).
However, size-specific differences in carbon to
chlorophyll-a ratios may resolve size specific differences in Pchl and thus it remains important to
address the variability of carbon to chlorophyll-a
ratios in the open ocean.
Acknowledgments
We thank Katie Chamberlain for assistance with
nutrient analysis, Mike Lucas and Phil Warwick for
assistance with radiochemical methodology, Mark
Moore, Valesca Pérez, Tom Bell and Stuart Painter
for helpful discussions, and Claudia Castellani at
BODC for help with data access. We would also like
to thank 3 anonymous reviewers for their comments
and helpful suggestions. We thank the officers and
crew of the RRS James Clark Ross and RRS
Discovery, and the UKORS technical staff for their
support at sea. This study was supported by the UK
Natural Environment Research Council through
the Atlantic Meridional Transect consortium
(NER/O/S/2001/00680). This is contribution number 124 of the AMT programme.
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