Progress in Oceanography 79 (2008) 83–94
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Progress in Oceanography
journal homepage: www.elsevier.com/locate/pocean
Microbial plankton abundance and heterotrophic activity across the Central
Atlantic Ocean
Evaristo Vázquez-Domínguez a,*, Carlos M. Duarte c, Susana Agustí c, Klaus Jürgens b, Dolors Vaqué a,
Josep M. Gasol a
a
Departament de Biologia Marina i Oceanografia, Institut de Ciències del Mar, CSIC Passeig Marítim de la Barceloneta, 37-49, E-08003 Barcelona, Spain
Institut für Ostseeforschung Warnemünde (IOW), 18119 Rostock-Warnemünde, Germany
c
Institut Mediterrani d’Estudis Avançats (CSIC-UIB), E-07190 Esporles, Illes Balears, Spain
b
a r t i c l e
i n f o
Article history:
Received 17 March 2008
Received in revised form 14 August 2008
Accepted 19 August 2008
Available online 6 September 2008
Keywords:
Auto- and heterotrophic picoplankton
Heterotrophic nanoflagellates
Bacterial production
Grazing
Central Atlantic Ocean
a b s t r a c t
The role of microorganisms in the transfer of carbon of marine systems is very important in open oligotrophic oceans. Here, we analyze the picoplankton structure, the heterotrophic bacterioplankton activity,
and the predator–prey relationships between heterotrophic bacteria and nanoflagellates during two large
scale cruises in the Central Atlantic Ocean (29°N to 40°S). Latitud cruises were performed in 1995
between March–April and October–November. During both cruises we crossed the regions of different
trophic statuses; where we measured different biological variables both at the surface and at the deep
chlorophyll maximum (DCM). The concentration of chlorophyll a varied between 0.1 and 0.8 mg m3,
the abundance of heterotrophic bacteria varied between <1.0 105 and >1.0 106 cells ml1, and that
of heterotrophic nanoflagellates between <100 and >1.0 104 cells ml1. The production of heterotrophic
bacteria varied more than three orders of magnitude between <0.01 and 24 lgC L1 d1; and the growth
rates were in the range <0.01–2.1 d1. In the Latitud-II cruise, Prochlorococcus ranged between <103 and
>3 105 cells ml1, Synechococcus between <100 and >1.0 104 cells ml1, and picoeukaryotes between
<100 and >104 cells ml1.
Two empirical models were used to learn more about the relationship between heterotrophic bacteria
and nanoflagellates. Most bacterial production was ingested when this production was low, the heterotrophic nanoflagellates could be controlled by preys during Latitud-I cruise at the DCM, and by predators
in the surface and in the Latitud-II cruise. Our results were placed in context with others about the structure and function of auto- and heterotrophic picoplankton and heterotrophic nanoplankton in the Central
Atlantic Ocean.
Ó 2008 Elsevier Ltd. All rights reserved.
1. Introduction
Prokaryotes are key components of planktonic food webs: autotrophic prokaryotes can dominate the primary producers’ compartment (Buck et al., 1996; Campbell et al., 1997; Li et al.,
1992), and contribute to a large percentage of total primary production (Li, 1994; Vaulot et al., 1995). Concomitantly, heterotrophic bacteria (HB) contribute to total plankton biomass in a
similar or higher way than the primary producers (Fuhrman
et al., 1989; Gasol et al., 1997; Li et al., 1992, 2004; Simon et al.,
1992) and they are a significant fraction of planktonic heterotrophic activity (Azam and Hodson, 1977). Autotrophic and heterotrophic bacteria are more relevant to the whole ecosystem structure
and metabolism in the oligotrophic regions of the ocean (Legendre
and Rassoulzadegan, 1995). Cyanobacteria are responsible for most
* Corresponding author. Tel.: +34 932 216 416; fax: +34 932 217 340.
E-mail address: [email protected] (E. Vázquez-Domínguez).
0079-6611/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.pocean.2008.08.002
chlorophyll a and primary production (i.e. Li, 1995), and the heterotrophic bacterial fraction in total plankton biomass is larger
than that of autotrophs as compared to eutrophic regions (Gasol
et al., 1997). In addition, the heterotrophic bacterial production
peaks there as a fraction of primary production (Cole and Caraco,
1993), and the bacterial consumption of organic carbon is high because heterotrophic bacterial growth efficiency tends to be low in
such systems (del Giorgio and Cole, 1998). Thus, it is in these oligotrophic oceanic regions where it is very important to ascertain the
importance of heterotrophic prokaryotes as secondary producers.
Regional variations of pico- and nanoplankton abundance
should reflect changes in the nutrient conditions of the ecosystems,
and the seasonal variability would reflect the differences in temperature and stratification. The pycnocline acts as a boundary layer
generating ecological conditions (nutrients, salinity, temperature,
etc.) that should differ above, below, and within this layer (i.e.
Longhurst, 1998). Although some studies have clearly revealed
large differences in the community composition and physiology
E. Vázquez-Domínguez et al. / Progress in Oceanography 79 (2008) 83–94
of the phytoplankton and zooplankton assemblages thriving in the
pycnocline (e.g. Longhurst and Harrison, 1989; Venrick, 1988), only
a handful of studies have concentrated in the differences in activity
and production between surface and deep-living microorganisms
(i.e. Li and Wood, 1988).
Closely coupled to the populations of auto- and heterotrophic
picoplankton develop the heterotrophic nanoflagellates (Andersen
and Fenchel, 1985), the tiniest but most abundant predators on
aquatic systems (between 102 and 103 cells ml1). Heterotrophic
nanoflagellates (HNFs) are recognized as the regulators of bacterial
abundance in aquatic systems (Berninger et al., 1991; Gasol and
Vaqué, 1993; Vaqué et al., 1994). They play a central role in the
transfer and nutrients within microbial food webs by channeling
the picoplankton carbon to higher trophic levels, such as microand mesozooplancton (Azam et al., 1983; Sherr and Sherr, 1988),
and they ingest an important fraction of the bacterial production
of oligotrophic environments (i.e. Vázquez-Domínguez et al.,
2005). Thus, our understanding of the function of open oceanic
ecosystems depends on the comprehension of the role of heterotrophic nanoflagellates within the microbial food webs of these
ecosystems.
During 1995, we crossed two times the Central Atlantic Ocean
(between 30°N and 40°S). The aim of both Latitud cruises was to
study (i) to what extend the microbial abundances and the heterotrophic bacterial activity varied with latitude, depths, and seasons
and (ii) the role of heterotrophic nanoflagellates in open oceanic
ecosystems. The latter objective was addressed by the use of two
ecological models: the model of Vaqué et al.(1994) that determines
the impact of protists as bacterial predators, and the model of
Gasol (1994) that analyzes the control by preys (bottom-up) or predators (top-down) of heterotrophic nanoflagellates. Finally, our results are compared to a bibliographic compilation of 64 studies,
integrating different aspects of the structure and function of the
microbial plankton communities in the Central Atlantic Ocean.
2. Materials and methods
2.1. Sampling strategy
Two cruises sailed in the Atlantic Ocean in 1995 on board research vessel BIO Hespérides. The Latitud-I cruise was established
between March and April and the Latitud-II cruise between October and November (Fig. 1). The Latitud-I cruise started in the Rio
de la Plata Estuary (Argentina) and ended in the Canary Islands,
and the Latitud-II cruise started in the Canary Islands and ended
in the Mar del Plata (Argentina). Both cruises followed similar
tracks in the Southern hemisphere; however, they followed different routes in the northern hemisphere. The Latitud-I cruise followed the 29°W meridian, while the Latitud-II cruise sailed
closer to the NW African coast. We took samples at the surface
(5 m) and at the depth of the deep chlorophyll maximum (DCM)
for a total of 86 stations in Latitud-I cruise and 46 stations in Latitud-II cruise. In each station, the depth of the DCM was determined
after the deployment of a CTD that had attached a fluorometer. All
the stations were on oceanic waters with depths over 2000 m, and
they were located across different Atlantic regions including the
southern subtropical region (SST, 35°S–22°S), the southern tropical
region (ST, 22°S–10°S), equatorial waters (Eq, 10°S–5°N), the
northern tropical region (NT, 5°N–18°N), the northern subtropical
region (NST, 24°N–30°N), and the African upwelling region
(U, 18°N–24°N). Samples were collected with 12 L Niskin bottles
attached to a rosette sampler. Subsamples were either immediately preserved for microorganism counts, or kept less than
30 min in polyethylene bottles in an opaque box with in situ water
until posterior use for 3H-leucine uptake measurements. Chloro-
40
20
Latitude
84
0
-20
-40
-60
-50
-40
-30
-20
-10
0
10
Longitude
Fig. 1. Positions of the stations sampled in 1995 in the Latitud-I cruise (April–May,
open symbols) and the Latitud-II cruise (October–November, grey symbols).
phyll a concentration was measured fluorometrically as described
elsewhere (Agustí and Duarte, 1999).
2.2. Microorganisms abundance
In Latitud-I, we fixed 100 mL subsamples from each depth with
cold glutaraldehyde (1%, final concentration). Fifteen to twenty
milliliters of sample was filtered through 0.2 lm black polycarbonate filters to collect bacteria, while 50 mL of samples was filtered
onto 0.6 lm black polycarbonate filters for nanoflagellate counting. All filtration was performed in the same day of collection or
the next day. Heterotrophic bacteria and nanoflagellates were
stained for 5 min with DAPI (40 ,6-diamidino-2-fenilindol) at
5 lg mL1 final concentration (Porter and Feig, 1980), according
to the considerations of Sieracki et al. (1985). Filters were mounted
on microscope slides with non-fluorescent oil and were frozen
until counting. Epifluorescence microscopy inspection occurred
within two months after sampling. When it was possible, at least
200–400 cells were counted in each filter. For heterotrophic
bacteria we inspected random fields, while for nanoflagellates we
surveyed all the cells in three transects of 10 mm. Aplastidic
flagellates were assumed to be heterotrophic and plastidcontaining cells were assumed not to feed on bacteria.
In Latitud-II, heterotrophic nanoflagellates were processed as in
the Latitud-I cruise, while prokaryotes were analyzed by flowcytometry. We preserved 1.2 mL of sample with 1% paraformaldehyde + 0.05% glutaraldehyde (final concentration). Samples were
frozen in liquid nitrogen and later stored at 20° C to determine
the abundance and relative size of heterotrophic bacteria and the
concentration of picoautotrophs. Back in the laboratory, the samples
were thawed, stained for a few minutes with 2.5 lM of Syto13 (final
concentration) (del Giorgio et al., 1996), and run through a flow
cytometer (FACScalibur, Becton&Dickinson). Samples were approximately run at 12 lL min1, and 10,000 events were acquired in log
mode. In each sample, we added yellow–green latex beads (0.92 lm,
Polysciences) as internal standard. Bacteria were detected by their
signature in a plot of side scatter (SSC) vs. green fluorescence (FL1)
(del Giorgio et al., 1996). The average fluorescence of the bacterial
population, as normalized to that of the beads, was a rough approximation of bacterial size (Gasol and Del Giorgio, 2000).
E. Vázquez-Domínguez et al. / Progress in Oceanography 79 (2008) 83–94
Size ðlm3 Þ ¼ 7:5 103 þ 0:11 Relative FL1; N ¼ 20; R2 ¼ 0:66:
Bacterial size was converted to weight using the carbon to volume relationship derived by Norland (1993)
pgC cell
1
1
¼ 0:12 ðlm3 cell Þ0:7 :
In a plot of green vs. red fluorescence (FL1 vs. FL3), we could differentiate photosynthetic picoplankton. We were able to detect
Synechococcus by their red fluorescence (FL3) and orange fluorescence (FL2), Prochlorococcus with lower FL3 than Synechococcus
and no FL2, and ‘‘picoeukaryotes” with similar or higher FL3 than
Synechococcus and no FL2. In the equatorial surface waters Prochlorococcus could not be completely resolved because of their low
fluorescence. Approximate concentrations were computed by multiplying by two the cell number in the right part of the population
red fluorescence distributions, assumed to be log normal
(Partensky et al., 1996). In the case of autotrophic prokaryotes, biomasses were obtained by multiplying the abundance of Synechococcus by 39 fgC cell1, that of Prochlorococcus by 82 fgC cell1
and Picoeukaryotes by 530 fgC cell1 (Worden et al., 2004). Prochlorococcus were removed from flow-cytometry heterotrophic
bacterial counts in Latitud-II cruise.
2.3. Bacterial production
We estimated bacterial production from radioactive 3H-leucine
incorporation by using two small modifications of the method described by Kirchman et al.(1985). In Latitud-I we used the filtration
method as described in Kirchman (1993), while in the Latitud-II
cruise we used microcentrifuge vials as suggested by Smith and
Azam (1992). Commercial 3H-leucine solution was brought to
1 lM with 0.2 lm filtered autoclaved milliQ water, and this
solution was mixed with nonradioactive leucine at a ratio of 10%
radioactive to 90% nonradioactive leucine. Between 20 and 40 nM
of 3H-leucine was inoculated to triplicate vials in Latitud-I, a concentration that was found saturating in five concentration-dependent incorporation experiments performed in both cruises. In
Latitud-I we used one formalin-killed sample as control and two
experimental replicates, while in Latitud-II we used four experimental replicates and two killed controls. The inoculated vials
were placed in whirl-pack bags, and incubated in the dark at temperatures as close as possible to the in situ conditions by using
either running surface water or thermostatic baths. In accordance
with the results of linearity experiments incubations lasted 90–
200 min. After incubation, samples were killed with formalin and
processed as described in the references cited above in Latitud-I
cruise, while in Latitud-II cruise controls and incubations were terminated with a 5% final concentration of trichloroacetic acid (Sigma). We did not rinse with ethanol. The samples were counted
on board with a Beckman scintillation counter after 48 h of having
added the cocktail (Ultima Gold, Perkin Elmer). 3H-leucine incorporation (DPM) was calculated by the scintillation counter software
by using the H number. The filtration and microcentrifuge methods
were compared previously with Mediterranean waters, and we did
not find significant differences between both methods.
Heterotrophic bacterial production was calculated as leucine
incorporation rate (DPM) times a conversion factor (CF). We performed seven conversion factor experiments, which consisted of
sample water filtrated through 0.6 polycarbonate filters, diluted
1:9 with 0.2 lm filtered seawater, and incubated in acid-clean
glass Pyrex bottles. Subsamples were taken for heterotrophic bacterial biomass and leucine incorporation measurements at every
12 h. Data were computed following the cumulative method
(Kirchman and Ducklow, 1993), and the conversion factors varied
between 0.13 and 2.2 kgC mol Leu1, without any apparent latitu-
85
dinal pattern. Thus, we use an average conversion factor of
0.6 kgC mol Leu1.
From the estimates of bacterial production (BP) and those of
heterotrophic bacterial biomass (BBM), we obtained growth rates
(l) and turnover times (Td) as
l ¼ BP=BBM; Td ¼ lnð2Þ=l:
2.4. Ecological models
In order to ascertain the grazing rates (G, HB mL1 h1) of heterotrophic nanoflagellates (HNFs) on heterotrophic bacteria (HB),
we used the model of Vaqué et al.
(1994), log G = 3.21 +
0.99 log HNF + 0.028T + 0.55 log HB. This model assumes that the
grazing rates of protists on the heterotrophic bacteria could be
estimated from the abundance of the prey and their main predators. Besides, the abundance of heterotrophic bacteria and nanoflagellates was compared with the model presented by Gasol (1994).
Briefly, the model compares the abundance of heterotrophic bacteria and nanoflagellates to infer whether heterotrophic nanoflagellates are mainly controlled by resources or by predation. The
model has several theoretical assumptions, and is based on a plot
of the abundance of heterotrophic bacteria and protists. If the
abundance of heterotrophic nanoflagellates is close to their maximal abundance attained for a certain concentration of heterotrophic bacteria, which is depicted in the model by a line called
maximum attainable abundance (MAA), log HNF = 2.47 +
1.07 log HB, the protists are limited by resources and not by predation. However, if the abundance of bacteria is higher than the average abundance for a certain level of heterotrophic nanoflagellates,
which is depicted in the model by a line called mean realized abundance (MRA), log HNF = 1.67(±1.2) + 0.79(±0.19) log HB, the protists are mainly controlled by the predation of larger organisms.
2.5. Statistics
Statistical analyses, Pearson product–moment correlation coefficients and regression equations (Model II), were done with the
JMP statistical package (SAS Institute Inc.).
3. Results
3.1. Salinity, temperature, and chlorophyll a
Surface salinity varied between maxima of 37.5 psu in the
southern tropical region and minima of 35.5 psu in the northern
tropical region (Fig. 2A). Salinity values differed in the African
upwelling (U) and northern tropical (NT) regions, showing the
great influence of the waters affected by the upwelling of the African coast.
Surface water temperatures strongly reflected seasonality
(Fig. 2B and C), the maximum temperatures (>27 °C) were found
between 0°S and 20°S in Latitud-I cruise and between 0°N and
20°N in Latitud-II cruise. The temperatures at the DCM oscillated
between 19 and 24 °C in Latitud-I cruise and between 14 and
26 °C in Latitud-II cruise, with maximum values near the Equator.
The maximum difference between temperatures at the surface and
at the DCM was found in the autumn season (shaded area in Figs.
2–5), which corresponded to the southern regions in the first cruise
and the northern in the second.
The depth of the deep chlorophyll maxima (DCM) in the southern hemisphere attained near150 m at 20°S, and shoaled to near
50 m at 35°S (Fig. 2B and C). In the northern hemisphere, there
were different patterns in spring and fall, as the cruise sailed in
different routes: in the Latitud-I cruise the DCM was around
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E. Vázquez-Domínguez et al. / Progress in Oceanography 79 (2008) 83–94
season of the year, the chlorophyll a was high near the African
upwelling region and low near the northern subtropical region.
38
A
37.5
3.2. Heterotrophic bacteria and nanoflagellates
Salinity
37
36.5
35.5
SST
ST
Eq
NT
AU
B
25
0
20
50
15
100
10
150
DCM (m)
Temperature (°C)
30
NST
36
C
25
0
20
50
15
100
10
150
5
-30
-20
-10
0
10
20
Latitude (°)
Fig. 2. Surface salinity (A) in the different stations occupied in the Latitud-I cruise
(open symbols) and the Latitud-II cruise (grey symbols). Temperature at the surface
(dark circles) and at the deep chlorophyll maximum (open circles) during the
Latitud-I (B) and the Latitud-II (C) cruises. The dotted line corresponds to the deep
chlorophyll maximum, and the other two lines (straight and slashed) correspond to
the smoothed line of the data. The grey shading corresponds to the autumn season.
100 m near 28°N, and in the Latitud-II cruise it rises below 50 m
near 22°N due to the African upwelling.
Quite similar chlorophyll a was found in both cruises, except for
maximum values near the African upwelling area (Table 1, Fig. 3A
and B). The Latitud-I cruise use to be bellow 0.2 mg m3 at the surface, although values of 0.7 mg m3 were reached in several stations. The DCM was around 0.2 mg m3 in the southern
hemisphere and between 0.4 and 1 mg m3 in the northern
hemisphere. In the Latitud-II, cruise the chlorophyll a was near
0.2 mg m3 at the surface, with a tendency for higher values in
the northern hemisphere and reaching a value of 2 mg m3 close
to the African coast. The DCM was close to 0.2 mg m3 in the
southern hemisphere and between 0.5 and 2.4 mg m3 in the
northern hemisphere.
Regionally, the chlorophyll a at the surface in the Latitud-I
cruise was >0.2 mg m3 in the African upwelling area and
<0.2 mg m3 in the remaining regions, with minimum values in
the northern subtropical regions (Table 2). At the DCM, the chlorophyll a was between two and three times more concentrated than
at the surface. In the Latitud-II cruise, the chlorophyll a showed a
similar pattern both at the surface and at the DCM. In addition,
the chlorophyll a was nearly 3-fold more concentrated in the African upwelling region than in the first cruise. Independently on the
In the Latitud-I cruise, the heterotrophic bacteria ranged between
5.0 105 and 1.0 106 HB mL1 in the southern hemisphere and
they were close to 1.0 105 HB mL1 from 10°N to 28°N (Fig. 3C).
In Latitud-II, the heterotrophic bacteria reached 1.0 106 HB mL1
in the vicinity of the Canary Islands and they were close to
2.0 105 HB mL1 near the Argentinean coast, and there was a slight
decrease on concentration going southwards (Fig. 3D). Overall, there
was a tendency for heterotrophic bacteria to be more concentrated
at the surface and in the Latitud-II cruise (Table 1).
Regionally, the heterotrophic bacteria in the Latitud-I cruise and
at the surface were near 0.2 106 HB mL1 in the northern regions
and reached 0.9 106 HB mL1 in the Equatorial region (Table 2).
The DCM was <0.3 106 HB mL1 in the northern regions and near
0.5 106 HB mL1 in the southern. In the Latitud-II cruise at the
surface they were below 0.63 106 HB mL1 in the southern regions and between 0.7 and 1.6 106 HB mL1 in the northern regions. The DCM varied between 0.4 106 in the southern
tropical region and 1.7 106 HB mL1 in the African upwelling region. The higher concentrations of heterotrophic bacteria were
found near the equator in the Latitud-I cruise and in the African
upwelling area in the Latitud-II cruise, while the lower abundances
were found in the northern subtropical regions in the first cruise
and in the southern subtropical regions in the second cruise.
During the Latitud-I cruise, the abundance of heterotrophic bacteria was not correlated with the concentration of chlorophyll a,
neither at the surface nor at the DCM. Conversely, there was a significant correlation between both variables during the Latitud-II
cruise, both at the surface (log HB vs. log Chl. a, n = 45, r = 0.41,
p < 0.01) and at the DCM (log HB vs. log Chl. a, n = 44, r = 0.48,
p < 0.01).
The size of heterotrophic bacteria in the Latitud-II cruise varied
between 0.038 and 0.076 lm3, averaging 0.054 lm3. Thus, the
average cellular biomass was estimated to be 14.7 fgC HB1. The
average heterotrophic bacterial biomass in the Latitud-I cruise
was slightly higher near the surface, 9.13 lgC L1, than at the
DCM, 7.46 lgC L1, particularly in the southern regions (Tables 1
and 3). In Latitud-II, the average bacterial biomass was also slightly
higher at the surface, 12.7 lgC L1, than at the DCM, 10.7 lgC L1;
except in the southern subtropical and African upwelling regions.
In the Latitud-I cruise, the concentration of heterotrophic nanoflagellates averaged 200 HNF mL1 at the surface and were close to
600 HNF mL1 at the DCM (Fig. 3E and Table 1). Conversely, in the
Latitud-II cruise there was roughly the same amount of protists at
the surface than at the DCM, averaging 500 HNF mL1 (Fig. 3F).
Regionally, the highest concentrations of heterotrophic nanoflagellates in the Latitud-I cruise at the surface were in the tropical regions (Table 2), 0.3 103 HNF mL1, while at the DCM they were
more abundant in the upwelling, northern tropical and subtropical
regions, >0.9 103 HNF mL1 (ANOVA, F = 9.5, p < 0.01, Tukey-Kramer HSD). In the Latitud-II cruise, heterotrophic nanoflagellates
tended to be more concentrated at the surface than at the DCM,
and in the upwelling and northern regions (ANOVA, F = 6.6,
p < 0.01, Tukey-Kramer HSD). Taking into account both cruises,
there was a significant relation between the concentration of bacteria and its predators, log HNF = 0.01(±0.6) + 0.41(±0.1)log HB
(r2 = 0.10, n = 139, p < 0.001).
3.3. Autotrophic picoplankton
In the Latitud-II cruise, prochlorophytes were more abundant at
the surface than at the DCM (Fig. 4A, Table 1). Values of
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-3
Chlorophyll a (mg m )
1
2.5
B
A
0.8
2
0.6
1.5
0.4
1
0.2
0.5
D
C
-1
Bacteria (106 cells ml )
0
1.0
1.0
0.1
0.1
F
-1
HNF (103 cells ml )
E
1.5
1.5
1.0
1.0
0.5
0.5
0
0
-30
-20
-10
0
10
20
Latitude (°)
-30
-20
-10
0
10
20
Latitude (°)
Fig. 3. Chlorophyll a concentration and abundance of heterotrophic bacteria and nanoflagellates (HNF) in the Latitud-I cruise (A, C, E) and the Latitud-II cruise (B, D, F). The
values correspond to the surface data (dark circles) and to the deep chlorophyll maximum data (open circles).
2.0 105 cells mL1 were common at the surface and they were
close to 7.0 104 cells mL1 at the DCM. Synechococcus were also
more concentrated at the surface in most regions, although the
average concentration was 1.3 104 cells mL1 in the surface and
in the DCM (Table 1, Fig. 4B), with values varying between
1.0 103 and >1.0 105 cells mL1. Picoeukaryotes varied between 1.0 102 and 2.8 104 cells mL1 at the surface, and they
could often reach 2.0 104 cells mL1 in the DCM (Fig. 4C). The
average concentration of picoeukaryotes was found to be near 2fold lower at the surface than at the DCM (Table 1).
Regionally, the higher concentrations of Prochlorococcus in the
surface were found near the Equator, 2.3 105 cells mL1, while
the lower abundances were reached near the African upwelling
area, 0.4 105 cells mL1. Prochlorococcus varied at the DCM between 0.6 105 cells mL1 in the southern subtropical region and
1.2 105 cells mL1 in the Equator. Conversely, Synechococcus
were more concentrated near the African upwelling area both at
the surface and at the DCM, and the lower concentrations were
found in the northern subtropical region. Picoeukaryotes were
more concentrated in the vicinity of the African upwelling region,
>10.0 103 cells mL1, and the lower abundances were found in
the southern tropical region, <1.0 103 cells mL1. Thus, Prochlorococcus were more abundant at the surface when the concentration of chlorophyll a was low, while Synechococcus were more
abundant at the same depth when the concentration of chlorophyll
a was high. Picoeukaryotes were more abundant in eutrophic
places and they developed better in the DCM.
3.4. Bacterial production
In Latitud-I cruise, bacterial production rates were similar at the
surface and at the DCM, averaging, respectively, 0.31 and
0.49 lgC L1 d1 (Fig. 5A, Table 1). The average production rates
were significantly higher in the Latitud-II cruise (T-test’s, n > 39,
p < 0.01), near 10-fold at the surface and 3-fold at the DCM
(Fig. 5B, Table 3). In the Latitud-I cruise, the growth rates of heterotrophic bacteria averaged 0.04 d1 at the surface and 0.09 d1 at
the DCM. Thus, they were lower than the >0.2 d1 measured in
the Latitud-II cruise (Table 1, Fig. 5C and D). The average turnover
times were on the order of >30 days in Latitud-I, and between 22
and 39 days in Latitud-II (Table 1, Fig. 5E and F).
Regionally, the maximum bacterial productions in the Latitud-I
cruise were measured at the surface and at the DCM near the
northern tropical region, 1 lgC L1 d1 (Table 3). The growth
rates were above 0.06 d1 in the northern regions and below
0.04 d1 in the Equator and the southern regions. In the LatitudII cruise, the maximal bacterial productions at the surface and at
the DCM were reached in the northern tropical and African upwelling regions, up to 10 lgC L1 d1. The higher growth rates were
measured in the northern tropical region, >0.4 d1, and the lower
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6
A
-1
Prochlorococcus (cells ml )
10
10
5
4
10
6
10
5
10
4
10
3
5
10
2
10
4
10
3
10
2
C
-1
Picoeukaryotes (cells ml )
10
Synechococcus (cells ml -1 )
10
B
subtropical and the African upwelling regions and 0.73 lgC L1 d1
in the southern tropical region. The grazing rates at the DCM varied
between 0.21 lgC L1 d1 in the southern subtropical region and
0.67 lgC L1 d1 in the northern tropical region. In the Latitud-II
cruise, the grazing rates at the surface were higher, varying between 0.26 lgC L1 d1 in the southern subtropical region and
2.88 lgC L1 d1 in the African upwelling region, while at the
DCM varied between 0.13 and 7.9 lgC L1 d1 in the same regions.
Thus, in most regions of Latitud-I cruise the grazing rates were
higher than the production rates, while in Latitud-II cruise most regions have higher production rates than grazing rates (Table 3).
The concentration of heterotrophic nanoflagellates in Latitud-I
cruise at the surface was below the average concentration of protists found in marine waters for a given concentration of bacteria,
what is called in the model of Gasol (1994) the mean realized abundance (MRA, Fig. 6C). This means that the abundance of heterotrophic bacteria surpasses the feeding requirements of the population
of heterotrophic nanoflagellates, and that the protists do not reach
higher numbers because they could be controlled by predators.
However, the concentration of heterotrophic nanoflagellates at
the DCM was closer to the maximum expected for the concentration of heterotrophic bacteria, or what is called in the same model
the maximum attainable abundance (MAA, Fig. 6C). Thus, the
abundance of bacteria at the DCM meets the demands of its main
predators. Finally, in Latitud-II cruise the concentrations of heterotrophic bacteria and nanoflagellates were distributed slightly below the MRA both at the surface and at the DCM (Fig. 6D), and
there was a significant correlation between the heterotrophic bacteria and the nanoflagellates (log HB = 1.48(± 0.72) + 0.69(± 0.12)
log HNF (r2 = 0.29, n = 77, p < 0.001), which means a better coupling
between predators and preys.
4. Discussion
-30
-20
-10
0
10
20
Latitude (°)
Fig. 4. Abundance of Prochlorococcus (A), Synechococcus (B) and autotrophic
picoeukaryotes (C) in the Latitud-II cruise. The values correspond to the surface
(dark circles) and to the deep chlorophyll maximum (open circles). The grey
shading corresponds to the autumn season.
growth rates were measured in the northern subtropical region,
<0.005 d1. Consequently, the longer turnover times were found
in the southern regions of the Latitud-I cruise and in the northern
tropical region of the Latitud-II cruise.
3.5. Grazing rates and prey-predator interactions
In Latitud-I cruise, the average grazing rate at the surface was
0.35 lgC L1 d1 and at the DCM was 0.51 lgC L1 d1 (Table 1),
which means that the 100% of the bacterial production could be
consumed by protists. However, the average grazing rate in Latitud-II cruise at the surface was 1.16 lgC L1 d1 while at the DCM
was 0.75 lgC L1 d1, thus between 2-fold and 4-fold lower than
the average production rates. Then, the biomass of bacteria grazed
per day was above bacterial production in Latitud-I cruise (Fig. 6A),
and close or lower than the bacterial production in Latitud-II cruise
(Fig. 6B). Pooling all the data together, the relation between both
variables was positive and significant, log G = 0.28(±0.04) +
0.34(±0.05)log BP (r2 = 0.19, n = 164, p < 0.001). The high intercept
and low slope of this relationship indicate that the fraction of bacterial production ingested by grazing was higher in the less productive areas of the Central Atlantic Ocean.
Regionally, the grazing rates during Latitud-I cruise varied at
the surface between values below 0.15 lgC L1 d1 in the southern
4.1. Methodological considerations
Epifluorescence microscopy is unable to account easily for Prochlorococcus, and thus, we ignore their abundance during the first
cruise. In Latitud-II cruise, Prochlorococcus averaged 20% of the total prokaryotic counts at the surface and 14% at the DCM. If we had
corrected the abundance of heterotrophic bacteria in Latitud-I
cruise accounting for Prochlorococcus, the bacterial growth rates
would increase up to a 20%, but they would still be far away from
the growth rates observed in Latitud-II cruise.
We measured several conversion factors in different stations of
the cruises to transform the leucine incorporation rates into bacterial biomass, and we obtained values ranging between 0.13 and
2.0 kgC mol Leu1 but without any clear latitudinal pattern. Thus,
we converted the leucine incorporation rates into bacterial production with an average conversion value of 0.6 kgC mol Leu1, which is
nearly five times lower than the conversion factor of
3.1 kgC mol Leu1 proposed by Smith and Azam, (1992). However,
this conversion factor is close to that reported in the Central Atlantic
Ocean, for example, Alonso-Saez et al. found empirical conversion
factors ranging between 0.012 and 1.29 kgC mol Leu1 (Alonso-Saez
et al., 2007), Moran et al. found 0.73 kgC mol Leu1 (Moran et al.,
2004), and Zubkov et al. 0.23 kgC mol Leu1 (Zubkov et al., 2000).
Thus, most variability found in the bacterial production rates between regions and cruises should be related with an intrinsic ecological feature of the system, and not to the conversion factor used to
transform the incorporation of 3H-leucine into bacterial biomass.
4.2. Photoautotrophic picoplankton
In the permanently stratified ocean, nutrient depletion occurs in
the upper layers and a deep chlorophyll maximum (DCM) develops
89
10
B
A
10
-1
-1
Production (µgC L d )
E. Vázquez-Domínguez et al. / Progress in Oceanography 79 (2008) 83–94
1
1
0.1
0.1
0.01
0.01
0.4
0.8
-1
µ (d )
C
D
0.3
0.6
0.2
0.4
0.1
0.2
0
0
F
Turnover time (d)
E
100
100
10
10
1
1
-40
-30
-20
-10
0
10
20
Latitude (°)
-30
-20
-10
0
10
20
30
Latitude (°)
Fig. 5. Bacterial production, growth rates, and biomass turnover times in the Latitud-I (A, C, E) and the Latitud-II (B, D, F) cruises. The values correspond to the surface (dark
circles) and to the deep chlorophyll maximum (open circles). The grey shading corresponds to the autumn season.
(Cullen, 1982; Herbland and Vouturiez, 1978). The depth of this
DCM often coincides with that of 1% surface light irradiance and
with the depth where the thermocline is strongest (Agustí and
Duarte, 1999). The chlorophyll a concentration was 5-fold higher
at the DCM than at the surface, which is within typical ratios for
the oligotrophic ocean (Jochem et al., 1993). Picoautotrophs were
present within usual values for the Central Atlantic Ocean (Table
4), and the differential response to light and trophic conditions acts
as an important structuring force of autotrophic picoplankton in
open oceanic regions (Longhurst, 1998). Prochlorococcus were the
dominant group at the surface in the oligotrophic conditions. Synechococcus were dominant at the surface in the mesotrophic regions, similar to what has been found in other studies (i.e. Li,
1995; Olson et al., 1990). Picoeukaryotes dominate where chlorophyll a was higher at the DCM and in the African upwelling region
(Buck et al., 1996; Zubkov et al., 1998). Thus, cyanobacteria were
better adapted to surface waters with high light levels and low
or medium nutrient conditions, while picoeukaryotes thrive better
near the bottom of the euphotic zone where the light is scarce but
the nutrient concentration is higher (Lindell and Post, 1995; Olson
et al., 1990; Partensky et al., 1996).
4.3. Heterotrophic bacteria: abundance, biomass, and production
In the Latitud-I cruise, heterotrophic bacteria reached
1.0 106 HB mL1 in many occasions and they were above these
concentrations in the northern and southern part of the Latitud-II
cruise, such concentrations are usually found in the Central Atlantic Ocean (Table 4). During the Latitud-I cruise, the heterotrophic
bacterial abundance was not correlated with the concentration of
chlorophyll a neither at the surface nor in the DCM; thus, the heterotrophic bacteria were probably unrelated to the recent episodes
of primary production (Sherr and Sherr, 1996). Conversely, during
the Latitud-II cruise the abundance of heterotrophic bacteria was
significantly correlated with the concentration of chlorophyll a
both at the surface and at the DCM, which suggest a better coupling between primary and secondary production. However, the
low regression coefficient indicates that the relation between both
variables is not straightforward. In this sense, a recent study in the
Central Atlantic Ocean has shown that there could be a 20-fold
change in the primary production of picophytoplankton with only
a 3-fold change in the chlorophyll a concentration (Marañon et al.,
2003), which may help to understand the low relation between the
bacterial abundance and the chlorophyll a concentration.
Bacterial production rates in Latitud cruises varied between 1
and 2400 mgC m2 d1, which is within the range described for
the Central Atlantic Ocean (Table 5). The average bacterial productions recorded during the Latitud-II cruise were between three to
10-fold higher than those measured in the first cruise, which is
indicative of a high variability of production rates in the Central
Atlantic Ocean (Hoppe et al., 2002). There was a consistent pattern
in both Latitud cruises: higher bacterial production rates were
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E. Vázquez-Domínguez et al. / Progress in Oceanography 79 (2008) 83–94
Table 1
Averaged values (±standard error) and range of different variables measured during
the Latitud cruises
Latitud-I
Temperature (°C)
Chlorophyll a (mg m3)
Bacteria (105 cells mL1)
HNF (102 cells mL1)
Prochlorophytes
(105 cells mL1)
Synechococcus (104
cells mL1)
Picoeukaryotes (103
cells mL1)
Picoautotrophs biomass
(lgC L1)
Bacterial biomass (lgC L1)
Bacterial production
(lgC L1 d1)
Grazing rate (lgC L1 d1)
Growth rate (d1)
Biomass turnover time (d)
Latitud-II
Surface
DCM
Surface
DCM
25.9 ± 0.3
21–29
0.12 ± 0.01
0.02–0.72
6.2 ± 0.5
0.6–13.9
1.9 ± 0.2
0.2–11.0
–
21.9 ± 0.3
19–27
0.43 ± 0.04
0.05–0.98
5.1 ± 0.7
0.5–19.8
5.9 ± 0.7
0.9–15.7
–
–
–
–
–
–
–
9.13 ± 0.69
0.9–20.5
0.31 ± 0.06
0.04–1.83
0.35 ± 0.07
0.02–2.77
0.04 ± 0.01
0.004–
0.31
50.3 ± 6.2
2.2–166
7.46 ± 0.99
0.7–29.2
0.49 ± 0.10
0.01–2.06
0.51 ± 0.06
0.06–1.43
0.09 ± 0.02
0.004–
0.78
32.9 ± 5.8
0.9–161.6
24.9 ± 0.5
17–29
0.16 ± 0.05
0.02–2.0
7.9 ± 0.8
0.5–28.7
5.6 ± 0.7
0.3–22.8
1.4 ± 0.1
0.1–3.8
1.3 ± 0.4
0.1–14.1
2.67 ± 0.9
0.1–28.0
8.12 ± 1.36
0.45–27.0
12.7 ± 1.3
0.6–44.3
4.06 ± 0.87
0.03–24.3
1.16 ± 0.20
0.02–6.62
0.25 ± 0.06
0.001–1.6
21.0 ± 0.4
14–26
0.47 ± 0.07
0.2–2.4
6.8 ± 0.9
1.4–32.8
4.8 ± 1.1
0.5–39.4
0.8 ± 0.1
0.1–2.28
1.3 ± 0.5
0.1–16.8
5.51 ± 1.1
0.1–27.5
6.95 ± 0.89
1.5–26.7
10.7 ± 1.37
1.9–52.3
1.50 ± 0.37
0.04–10.3
0.75 ± 0.20
0.03–6.18
0.23 ± 0.06
0.003–2.1
39.4 ± 16.1
0.4–611.3
21.9 ± 7.8
0.3–263.2
Bacterial production was measured with the 3H-leucine incorporation method, and
a conversion factor of 0.6 kgC mol Leu1(see text for details).
HNF: heterotrophic nanoflagellates.
found north of the Equator or in the vicinity of the African upwelling waters (between 0°N and 20°N) where upward fluxes of nutrients are high (Vidal et al., 1999), spikes of high production were
observed in several southern locations, and the lower production
rates were associated with the oligotrophic regions north of
20°N, which maybe related to the low nutrient availability in this
region (Pastor et al., 2008). The average turnover times of more
than 10 days reinforce the generality of the low turnover of heterotrophic bacterial biomass found in the Central Atlantic Ocean (Table 5). Then, the heterotrophic bacteria grow in the oligotrophic
ocean at rates much smaller than those of autotrophs, which are
in the range 0.5–2 d1 (Landry et al., 1997; Laws et al., 1987; Worden et al., 2004). We have to consider, however, that the growth
rates were estimated with the total abundance of heterotrophic
bacteria, while the fraction of bacteria that is active in oligotrophic
waters is in the order of 5% (Sherr et al., 1999). If we had scaled the
production rates to the active fraction of the bacterial assemblage,
the growth rates should increase and the turnover times should
decrease considerably.
During both Latitud cruises, there was also an uncoupling between regions with maximum heterotrophic bacterial abundance
and production rates. This uncoupling could be related to different
mechanisms. For example, in the Latitud-I cruise the maximum
heterotrophic bacterial abundances were observed in the southern
locations, while the higher bacterial productions were slightly in
the north where the upward flux of nutrients can be high (Vidal
et al., 1999). In the Latitud-II cruise, the higher bacterial productions were observed in the northern tropical region, where the
nutrient fluxes were still high, and the abundance of heterotrophic
nanoflagellates was 2-fold lower than that observed in the African
upwelling region. Thus, the bacterial growth along both cruises
could be influenced by factors related to nutrient fluxes and not directly related to primary production. In addition, if there are regions where the bacterial production and grazing rates are high,
the biomass could be maintained in low or high levels, and the
same happens in the regions where the bacterial production and
mortality rates are low. Conversely, in the regions where the bacterial production is high and the grazing rates are low, the bacterial
biomass could be high. While in the regions where the bacterial
production is low and the grazing rates are high, the bacterial biomass could be maintained at low levels.
Table 2
Zone-averaged (±standard error) abundance of microorganisms measured during both Latitud cruises at the surface and deep chlorophyll maximum (DCM)
SST
35°S–22°S
ST
22°S–10°S
Eq
10°S–5°N
NT
5°N–18°N
U
18°N–24°N
NST
24°N–30°N
Chlorophyll a (mg m3)
Latitud-I
Surface
DCM
Latitud-II
Surface
DCM
0.13 ± 0.01
0.37 ± 0.04
0.08 ± 0.01
0.36 ± 0.05
0.16 ± 0.06
0.17 ± 0.02
0.03 ± 0.00
0.20 ± 0.02
0.10 ± 0.01
0.50 ± 0.10
0.10 ± 0.01
0.40 ± 0.05
0.15 ± 0.02
0.66 ± 0.06
0.24 ± 0.04
0.65 ± 0.12
0.22 ± 0.13
0.60 ± 0.19
0.68 ± 0.46
1.37 ± 0.50
0.06 ± 0.13
0.34 ± 0.08
0.06 ± 0.02
0.22 ± 0.01
Bacteria (106 cells mL1)
Latitud-I
Surface
DCM
Latitud-II
Surface
DCM
0.68 ± 0.07
0.51 ± 0.09
0.39 ± 0.06
0.46 ± 0.08
0.72 ± 0.06
0.53 ± 0.08
0.70 ± 0.17
0.41 ± 0.13
0.89 ± 0.08
0.90 ± 0.20
0.87 ± 1.40
0.62 ± 0.19
0.41 ± 0.11
0.28 ± 0.14
0.91 ± 0.13
0.71 ± 0.08
0.14 ± 0.04
0.11 ± 0.09
1.61 ± 0.47
1.67 ± 0.05
0.16 ± 0.04
0.09 ± 0.02
0.98 ± 0.24
0.88 ± 0.36
HNF (103 cells mL1)
Latitud-I
Surface
DCM
Latitud-II
Surface
DCM
0.08 ± 0.01
0.21 ± 0.05
0.27 ± 0.08
0.14 ± 0.04
0.33 ± 0.09
0.39 ± 0.09
0.40 ± 0.07
0.22 ± 0.03
0.19 ± 0.04
0.64 ± 0.13
0.29 ± 0.04
0.29 ± 0.06
0.31 ± 0.05
0.93 ± 0.19
0.88 ± 0.06
0.47 ± 0.08
0.15 ± 0.01
1.34 ± 0.07
1.16 ± 0.37
1.98 ± 0.72
0.17 ± 0.04
1.17 ± 0.10
0.71 ± 0.04
0.50 ± 0.11
Prochlorophytes (105 cells mL1)
Latitud-II
Surface
DCM
1.09 ± 0.20
0.66 ± 0.13
1.65 ± 0.28
0.56 ± 0.11
2.27 ± 0.32
1.20 ± 0.19
1.64 ± 0.36
0.82 ± 0.21
0.40 ± 0.12
0.80 ± 0.50
1.15 ± 0.53
0.76 ± 0.32
Synechococcus (104 cells mL1)
Latitud-II
Surface
DCM
0.70 ± 0.10
0.78 ± 0.36
0.58 ± 0.18
0.05 ± 0.02
0.66 ± 0.17
0.30 ± 0.13
2.18 ± 1.53
1.27 ± 0.50
4.62 ± 3.19
7.87 ± 3.99
0.61 ± 0.25
0.24 ± 0.12
Picoeukaryotes (103 cells mL1)
Latitud-II
Surface
DCM
1.73 ± 0.33
5.81 ± 0.36
1.07 ± 0.47
1.06 ± 0.20
1.47 ± 0.40
3.43 ± 0.84
1.24 ± 0.33
10.4 ± 2.16
15.0 ± 6.99
10.1 ± 4.34
1.26 ± 0.53
2.36 ± 0.64
Picophytoplankton data from cruise Latitud-II only.
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E. Vázquez-Domínguez et al. / Progress in Oceanography 79 (2008) 83–94
Table 3
Zone-averaged (±standard error) bacterial biomass production, grazing, growth, and turnover rates measured during both Latitud cruises at the surface and deep chlorophyll
maximum (DCM)
SST
35°S–22°S
ST
22°S–10°S
Eq
10°S–5°N
NT
5°N–18°N
U
18°N–24°N
Bacterial biomass (lgC l1)
Latitud-I
Surface
DCM
Latitud-II
Surface
DCM
9.98 ± 1.13
7.44 ± 1.26
5.86 ± 1.06
7.07 ± 1.29
10.5 ± 0.82
7.86 ± 1.11
11.7 ± 3.2
6.58 ± 1.82
13.1 ± 1.23
13.3 ± 2.81
12.7 ± 1.86
9.45 ± 2.59
6.08 ± 1.67
4.13 ± 2.04
14.7 ± 2.47
11.2 ± 1.33
2.13 ± 0.62
1.57 ± 0.13
26.5 ± 6.87
26.9 ± 8.48
2.31 ± 0.53
1.45 ± 0.26
16.3 ± 4.08
14.5 ± 5.81
Bacterial production (lgC l1 d1)
Latitud-I
Surface
DCM
Latitud-II
Surface
DCM
0.23 ± 0.07
0.43 ± 0.15
1.68 ± 0.82
0.36 ± 0.06
0.15 ± 0.02
0.25 ± 0.14
1.91 ± 0.78
0.69 ± 0.22
0.29 ± 0.12
0.46 ± 0.22
2.63 ± 0.83
2.92 ± 1.29
0.83 ± 0.23
1.14 ± 0.30
10.2 ± 1.79
2.68 ± 1.05
0.35 ± 0.04
0.23 ± 0.08
6.7 ± 5.9
1.61 ± 0.49
0.15 ± 0.10
0.12 ± 0.07
0.08 ± 0.02
0.09 ± 0.02
Grazing rate (lgC l1 d1)
Latitud-I
Surface
DCM
Latitud-II
Surface
DCM
0.13 ± 0.02
0.21 ± 0.05
0.26 ± 0.09
0.13 ± 0.03
0.73 ± 0.21
0.51 ± 0.14
0.59 ± 0.23
0.24 ± 0.04
0.41 ± 0.13
0.84 ± 0.10
0.6 ± 0.06
0.58 ± 0.25
0.31 ± 0.14
0.67 ± 0.18
2.15 ± 0.22
0.64 ± 0.14
0.08
0.58
2.88 ± 1.25
7.9 ± 4.1
0.11 ± 0.05
0.47 ± 0.11
1.53 ± 0.84
0.73 ± 0.23
Bacterial growth rate (d1)
Latitud-I
Surface
DCM
Latitud-II
Surface
DCM
0.03 ± 0.01
0.04 ± 0.01
0.18 ± 0.09
0.10 ± 0.05
0.02 ± 0.01
0.03 ± 0.01
0.14 ± 0.09
0.15 ± 0.06
0.02 ± 0.01
0.02 ± 0.01
0.14 ± 0.04
0.32 ± 0.12
0.15 ± 0.03
0.28 ± 0.10
0.64 ± 0.17
0.42 ± 0.21
0.17
0.17 ± 0.06
0.25 ± 0.23
0.16 ± 0.05
0.06 ± 0.04
0.09 ± 0.05
0.004 ± 00.01
0.005 ± 0.001
Bacterial turnover times (d)
Latitud-I
Surface
DCM
Latitud-II
Surface
DCM
62.0 ± 10.9
38.2 ± 9.0
15.5 ± 4.5
9.8 ± 6.3
60.9 ± 9.4
38.6 ± 7.3
13.8 ± 3.9
7.7 ± 2.3
54.3 ± 16.1
40.7 ± 9.5
11.3 ± 3.9
7.2 ± 3.2
5.6 ± 1.0
3.7 ± 0.7
1.6 ± 0.4
6.0 ± 2.1
4.1
4.5 ± 1.5
48.1 ± 22.9
7.9 ± 4.1
25.7 ± 9.7
50.9 ± 37.5
260.6 ± 118.9
150.11 ± 38.1
1.5
1
4.5
A
NST
24°N–30°N
C
4
0.5
3.5
0
3
-0.5
2.5
-1
2
Log HNF (cells ml-1)
log G (µg C L-1)
-1.5
-2
1
B
0.5
1.5
1
4.5
D
4
3.5
0
3
-0.5
2.5
-1
2
-1.5
1.5
-2
-2.5
-2.5
-2
-1.5
-1
-0.5
0
0.5
1
1.5
-1
log BP (µg C L )
1
4.5
5
5.5
6
6.5
7
Log HB (cells ml-1)
Fig. 6. Scatterplot of bacterial production (log BP) versus grazing on heterotrophic bacteria (log G) in the Latitud-I (A) and the Latitud-II (B) cruises. Depiction of Gasol model
(1994) in the Latitud-I (C) and the Latitud-II (D) cruises. The values correspond to the surface (dark circles) and to the deep chlorophyll maximum (open circles). In panels A
and B, the dotted lines are the 1 to 1 ratio. In panels C and D, the continuous line is the MAA (Maximum Attainable Abundance), and the slashed line is the Mean Realized
Abundance line (MRA, see text for further details).
4.4. Heterotrophic nanoflagellates: abundance and activity
The abundance of heterotrophic nanoflagellates in Latitud
cruises varied between 20 and 39,000 HNF mL1; thus, the maxi-
mum abundances were in the higher end of the concentration of
protists for the Central Atlantic Ocean (Table 4). The highest concentrations of heterotrophic nanoflagellates coincided with the
maxima of chlorophyll a, as they were attained at the DCM in
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Table 4
Range, average, median, and standard deviation of the abundance of different groups of microorganisms in the Atlantic Ocean (compilation of data published in 64 articles; see
Table 1 in supplementary information)
Range
Average
Median
Std. Dev.
N
Bacteria (105 cells mL1)
HNF (cells mL1)
Prochlorococcus (104 cells mL1)
Synechococcus (104 cells mL1)
Picoeukaryotes (104 cells mL1)
0.2–39
8.31
6.88
4.62
47
30–4200
925.17
569.90
834.14
10
0.001–50
8.43
8.76
5.14
22
0.002–62.2
2.61
1.80
2.71
27
0.0001–3.4
0.55
0.38
0.60
16
HNF: Heterotrophic nanoflagellates.
N = number of references where we find the data.
Table 5
Range, average, median, and standard deviation of different variables measured in the Atlantic Ocean (compilation of data published in 64 articles; see supplementary
information)
Range
Average
Median
Std. Dev.
N
PPBM (mgC m2)
BBM (mgC m2)
BP (mgC m2 d1)
l (d1)
Td (d)
59–1772
555.20
450.95
405.03
28
30–5880
1143.29
933.40
669.95
47
8–5880
331.09
255.99
514.65
30
0.07 to 1.22
0.23
0.19
0.18
32
0.88–231
7.66
5.45
10.07
31
Picophytoplancton biomass (PPBM), bacterial biomass (BBM) and bacterial production (BP) were estimated on an areal basis assuming a 100 m depth layer.
l: bacterial growth rate; Td: bacterial turnover times.
N = number of references where we find the data.
the northern stations in the first cruise and throughout the entire
water column near the African upwelling in the second cruise,
which could be indicative of a direct trophic link between picoautotrophs and heterotrophic nanoflagellates. In addition, the
average concentration of heterotrophic nanoflagellates in the Latitud-I cruise was 3-fold higher in the DCM than in the surface. This
difference could be related to a higher predation by micro- and
mesozooplancton (including larger flagellates), because the abundance of heterotrophic bacteria was similar in both depths. Conversely, in the Latitud-II cruise the average concentration of
heterotrophic nanoflagellates in both depths was close to
500 HNF mL1, which is near the 569 HNF mL1 found as median
concentration in the Atlantic Ocean (Table 4) and could be indicative of a coupling between heterotrophic bacteria and
nanoflagellates.
The ability of different species of heterotrophic nanoflagellates
to ingest picoautotrophs is well known (i.e. Christaki et al.,
2005). The model of Vaqué et al. (1994) gives an estimation of
the biomass of heterotrophic picoplankton ingested by the heterotrophic nanoflagellates in the Central Atlantic Ocean, but it does
not account for the grazing rates on picoautotrophs. Thus, we could
have underestimated the grazing rates of heterotrophic nanoflagellates. However, the mortality rates of heterotrophic bacteria could
be considered conservative because, on the one hand, plastidic
nanoflagellates were abundant in both cruises and mixotrophic
nanoflagellates could be an important factor of bacterial mortality
in oligotrophic waters (Unrein et al., 2007) and, on the other hand,
the viral lysis is neglected as a source of mortality in the model,
although they could have an impact similar to heterotrophic nanoflagellates (i.e. Suttle, 2005). Our results show that the total
amount of bacterioplankton grazed daily was higher in the regions
with more protists, while more than all the bacterial production
was preyed in the regions where this production was very low.
These results are coincident with the direct estimates of grazing
on bacteria in the same area determined by the disappearance of
fluorescent-labeled bacteria (Vázquez-Domínguez et al., 2005).
Then, the heterotrophic nanoflagellates were exerting a high predation pressure on the heterotrophic bacteria in the most oligotrophic regions of the Central Atlantic Ocean.
The model of Gasol (1994) indicates that during the Latitud-I
cruise most samples at the surface were below the mean abundance of heterotrophic nanoflagellates found for a given abundance of heterotrophic bacteria (below the MRA line), which
could mean that the heterotrophic nanoflagellates were controlled
by the predation of micro- or mesozooplankton. In the same cruise
but at the DCM, the number of heterotrophic nanoflagellates for a
given amount of bacteria was close to the maximum attainable
abundance (MAA) line. Then, the heterotrophic nanoflagellates
could be ingesting picoautotrophs there to complete their diet.
During the Latitud-II cruise, most samples were close or slightly
below the mean realized abundance line and there was a significant correlation between heterotrophic bacteria and nanoflagellates, which means a better coupling between heterotrophic
bacteria and nanoflagellates as compared to the first cruise. We
have to keep in mind, however, that the correlation between the
abundance of heterotrophic bacteria and nanoflagellates can be
modulated by other circumstances, as heterotrophic bacteria is a
pool of cells with heterogeneous physiological states and heterotrophic nanoflagellates prey on active bacteria at higher rates than
on inactive cells (Gonzalez et al., 1993). Therefore, during the same
year we identified one situation in which heterotrophic bacteria
and nanoflagellates were uncoupled, and a different state with a
better coupling between preys and predators.
4.5. Ecological considerations
If we consider an integration depth of 100 m and an average
concentration of 1.0 105 Prochorococcus mL1, 1.0 104 Synechococcus mL1, and 4.0 103 picoeukaryotes mL1, the average biomass of picoautotrophs in the Central Atlantic Ocean would be
0.7 gC m2, thus close to the 0.56 gC m2 found in the literature
(Table 5). If the growth rates of picoautotrophs were near 1 d1
(Agawin and Agustí, 2005), the autotrophic picoplankton should
produce around 0.7 gC m2 d1. With a biomass of heterotrophic
bacteria close to 1 gC m2 and growth rates close to 0.2 d1 (this
study), the heterotrophic bacteria should be producing around
0.2 gC m2 d1. If we assume a conservative bacterial growth efficiency of 30% (del Giorgio and Cole, 1998), the heterotrophic
E. Vázquez-Domínguez et al. / Progress in Oceanography 79 (2008) 83–94
bacteria could require daily almost all the autotrophic picoplankton production. Obviously, these estimations do not consider the
large variability that can be found in the Central Atlantic Ocean.
As an example, a recent study of the gyre in the north Atlantic subtropical has found a picophytoplankton biomass close to 1 gC m2
that produced near 0.3 gC m2 d1, and a bacterial biomass near
0.4 g m2 that produced near 0.017 gC m2 d1. Meaning that under some circumstances primary production could meet all bacterial requirements in this region (Marañón et al., 2007). In any case,
as depicted in the same region by Karayanni et al. (2008), most of
this picoplanktonic primary and secondary productions will end up
consumed by heterotrophic nanoflagellates and recycled back to
the system as inorganic and organic nutrients.
Overall, there were large differences in the abundance and
activity of microorganisms between different regions of the Central
Atlantic Ocean. Picoplankton and heterotrophic nanoplankton
were more abundant in the eutrophic (e.g African upwelling) than
in the oligotrophic (e.g. northern subtropical) regions, and there
was no coincidence between the higher bacterial biomass and
growth rates. High bacterial abundances and low growth rates
could indicate a population that reached the carrying capacity of
the system (e.g. Wright, 1988). Conversely, low abundances and
high growth rates would be indicative of sites where bacteria are
kept well below the carrying capacity of the system by predators.
Most stations in the surface waters of Latitud-I cruise had low bacterial abundances and growth rates coupled to high grazing rates,
which is indicative of a high pressure of predation by protists. In
Latitud-II cruise, the bacterial growth rates were high even at large
bacterial abundances, indicating that the carrying capacity of the
system had not yet been reached in most stations. Compared to
the first cruise, then the larger bacterial productions in the second
cruise were translated into higher heterotrophic nanoflagellate
abundances with only slightly larger bacterial biomasses.
This study thus underlines the influence of the regional and
temporal variability on the abundance and biomass of bacteria,
the heterotrophic bacterial production, and the transfer of carbon
between the bacteria and the nanoflagellates in the Central Atlantic Ocean.
Acknowledgements
We acknowledge the help provided in both cruises by the crew
and all the scientists on board the research vessel BIO Hespérides.
Isabel Casamajor helped with the processing of the cytometry samples. This work was supported by grant AMB94-0739 to S. Agustí.
Final writing of the manuscript has been supported by an I3P fellow (CSIC) to E.V.-D.
Appendix A. Supplementary material
Supplementary data associated with this article can be found, in
the online version, at doi:10.1016/j.pocean.2008.08.002.
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