Microb Ecol (2002) 44:217±223
DOI: 10.1007/s00248-002-1026-z
Ó 2002 Springer-Verlag New York Inc.
Dissolved Primary Production and the Strength of Phytoplankton±
Bacterioplankton Coupling in Contrasting Marine Regions
X.A.G. MoraÂn,1 M. Estrada,2 J.M. Gasol,2 C. PedroÂs-AlioÂ2
1
Instituto EspanÄol de OceanografõÂa, Centro Oceanogra®co de XixoÂn, Avda. PrõÂncipe d'Asturies, 70 bis,
E-33212 XixoÂn, Asturies, Spain
2
Dept. Biologia Marina i Oceanogra®a, Institut de CieÁncies del Mar, CSIC Pg. Joan de BorboÂ, s/n, E-08039
Barcelona, Catalunya, Spain
Received: 21 February 2002; Accepted: 3 July 2002; Online Publication: 6 September 2002
A
B S T R A C T
We analyzed the strength of phytoplankton±bacterioplankton coupling by comparing the rate of
particulate (PPP) and dissolved primary production (DPP) with bacterial carbon demand (BCD)
in four contrasting marine regions: offshore and coastal waters of the Southern Ocean, a coastal
area of the NE Atlantic, and a coastal±offshore transect in the NW Mediterranean. We measured
bacterial heterotrophic production (BHP) and estimated BCD from a literature model. Average
phytoplanktonic percent extracellular release [PER = DPP/(DPP + PPP)] was 18±20% in the
Antarctic (offshore and coastal, respectively), 16% in the NW Mediterranean, and 7% in the NE
Atlantic. A signi®cant inverse relationship was found between PER and total system productivity
with pooled data. On average BHP amounted to <5% of total primary production in all regions.
However, the strength of phytoplankton±bacterioplankton coupling, estimated as the potential
importance of DPP in meeting BCD, differed greatly in the four regions. DPP was highly correlated to BCD in offshore Antarctic waters and was suf®cient to meet BCD. In contrast, BCD
exceeded DPP and bore no signi®cant relationship in the remaining regions. The data suggest
that a strong dependence of bacteria on algal extracellular production is only expected in openocean environments isolated from coastal inputs of DOC.
Introduction
The release of photosynthate in dissolved form by phytoplankton (dissolved primary production, DPP) is relatively low when compared with particulate primary
production (PPP), which frequently exceeds 80% of total
Correspondence to: Xose Anxelu G. MoraÂn; E-mail: [email protected]
production [3, 24]. DPP is often disregarded in budgets of
oceanic primary production because of its low contribution to total rates. However, it constitutes one of the most
important sources of labile organic molecules for heterotrophic bacterial growth [26] and may in part contribute
to explain the general covariation between algal and bacterial production in the ocean [12]. A trophic dependence
of bacteria on algae via DPP would be characteristic of
X.A.G. MoraÂn et al.
218
Table 1. Ranges of selected hydrographical and biological characteristics of the stations sampled in the four regionsa
Region
Antarctic offshore
Antarctic coastal
NE Atlantic
NW Mediterranean
a
Temperature
(°C)
)1.6±7.2
)0.8±0.6
15.0±18.7
13.9±19.7
Salinity
(psu)
Chl a
(mg m)3)
BN ´ 105
(cells mL)1)
TPP
(mg C m)3 h)1)
33.4±34.4
33.7±34.0
34.6±35.9
37.8±38.3
0.11±3.56
1.35±17.79
0.23±5.48
0.09±0.96
1.8±10.7
1.9±7.7
6.8±35.4
0.9±7.7
0.13±14.58
1.11±38.54
1.06±21.52
0.49±5.57
Chl a, Chlorophyll a; BN, bacterial abundance; TPP, total primary production.
systems where bacteria are carbon limited. The existence
of phytoplankton±bacterioplankton coupling should lead
to a signi®cant correlation between the rates of DPP and
bacterial heterotrophic production (BHP). Nonetheless,
very seldom is dissolved primary production compared to
bacterial carbon demand (BCD). If BCD is much higher
than DPP, then bacteria must have other sources of carbon
for maintenance and growth. Conversely, if DPP covers
BCD, and given that DPP is usually composed of easy-todegrade molecules [1], we would expect bacteria to preferentially use DPP over other carbon sources (i.e., degradation of particulate matter, semilabile DOC) and we can
consider that phytoplankton and bacterioplankton are well
coupled. The term ``coupling'' has been widely used in
aquatic microbial ecology to designate somewhat different
concepts, such as a high ratio of bacterial to primary
production [e.g., 6] or a signi®cant correlation between
their respective biomasses or production rates [e.g., 8]. We
de®ne here strength of coupling as the extent to which
DPP meets BCD, being thus independent of the proportion
of total photosynthate that ¯ows through bacteria. Unlike
other common uses of ``coupling,'' which are indirect ways
of approaching the transfer of carbon from primary producers to bacteria, our de®nition intends to identify the
variables responsible for a direct and concurrent dependence of bacteria on phytoplankton. The aim of this work
is to compare the relative importance of DPP and PPP and
the ability of DPP to ful®ll BCD, in four regions of fundamentally different ecological characteristics: offshore
and coastal waters of the Southern Ocean, upwelling-in¯uenced coastal waters of the NE Atlantic, and a coastal
transition zone in the NW Mediterranean. These regions
cover a wide range in the relative contribution of autochthonous vs allochthonous DOC supply; i.e., allochthonous inputs of dissolved organic matter are frequent and
important in the NE Atlantic [11] and negligible in Antarctic offshore waters [5], providing a suitable context for
the assessment of the variability of the trophic link between planktonic algae and bacteria. The same empirical
model of del Giorgio and Cole [10] was used for the estimation of BCD from bacterial production data in order to
avoid biases in the choice of the bacterial growth ef®ciencies (BGE) applicable for each region.
Methods
The analyzed data set was collected in two oceanographic cruises
in the Southern Ocean, one in the Brans®eld and Gerlache Straits
(Dec 1995±Jan 96) and one in the Weddell and Scotia Seas (Jan±
Feb 1998); two cruises in the NE Atlantic coastal waters off the
NW Iberian Peninsula (Apr±May 1997 and Sep 1998); and one
cruise in the NW Mediterranean (Jun 1995). These regions presented different hydrographical and biological conditions (Table
1). In the ®rst Antarctic cruise both offshore (Brans®eld Strait)
and coastal (Gerlache Strait) waters, characterized by notably
different productivities [21], were sampled, whereas the second
cruise was carried out in low-productivity open-ocean waters.
During the ®rst NE Atlantic cruise stable downwelling conditions
were met, while a sequence of upwelling±upwelling relaxation±
resumption of upwelling occurred during the second one. This
hydrographical variability was of greater importance in determining biological rates than the exact location of the stations in
the coastal±offshore gradient [23]. The three stations sampled in
the NW Mediterranean were also located along a coastal±offshore
gradient that did not show signi®cant differences in phytoplankton biomass and total production, in accordance with the
results of a 4-year study of the region [27].
Phytoplanktonic PPP and DPP rates were estimated by kinetic
experiments of 14C incorporation and subsequent compartmental
analysis described in detail in MoraÂn and Estrada [21] and
MoraÂn et al. [22]. The justi®cation of the use of kinetic rather
than end-point incubations is that they allow for the correction of
bacterial removal of DOC during the incubation, which results in
a nonlinear time-course evolution of labeled DOC [17, 21].
Brie¯y, experiments lasted for ca 6 h and 70 mL samples (duplicate clear and dark bottles) were taken at intervals of 30 to 60
min for measurements of labeled POC and DOC production after
®ltration through membrane ®lters of 0.22 lm pore size. Glass®ber (GF/F) ®lters were used in the ®rst Antarctic cruise and in
the Mediterranean. Membrane ®lters prove better than GF/F ones
for DPP and PPP partitioning since a variable amount of labeled
DOC can be adsorbed on the latter ®lter type [14, 20]. However,
any difference in DPP estimates due to the ®lter used were much
14
61
176
240
‹
‹
‹
‹
a
The average percentage of BHP to total primary production (TPP = DPP + PPP), and of BCD to TPP and DPP (BHP:TPP, BCD:TPP, BCD:DPP, respectively) are also given.
91
182
790
453
3
18
10
21
‹
‹
‹
‹
14
44
45
48
0.05
0.09
0.26
0.11
‹
‹
‹
‹
0.20
1.33
1.60
0.59
0.0
0.2
1.6
0.1
Antarctic offshore
Antarctic coastal
NE Atlantic
NW Mediterranean
1.67
9.46
5.79
1.55
‹
‹
‹
‹
0.48
3.24
1.02
0.63
0.52
1.39
0.32
0.20
‹
‹
‹
‹
0.15
0.33
0.07
0.07
17.7
20.4
7.2
16.1
‹
‹
‹
‹
2.2
3.5
1.1
5.5
0.005
0.054
0.199
0.016
‹
‹
‹
‹
0.001
0.006
0.071
0.004
0.3
2.0
4.1
1.5
‹
‹
‹
‹
0.0
0.9
1.3
0.5
2.2
3.9
7.1
2.6
‹
‹
‹
‹
BCD:DPP
(%)
BCD:TPP
(%)
BCD
(mg C m)3 h)1)
BGE
(%)
BHP:TPP
(%)
BHP
(mg C m)3 h)1)
PER
(%)
DPP
(mg C m)3 h)1)
Particulate and dissolved primary production rates were
highest in Antarctic coastal waters (Table 2), which harbored diatom blooms at the time of sampling (mean 6.2
mg chlorophyll a m)3). Percent extracellular release
[PER = DPP/(DPP + PPP)] values were signi®cantly lower
in the NE Atlantic than in either Antarctic offshore or
coastal waters (Kruskal±Wallis test, P = 0.0004) but the
ranges of variation within the four regions were in accordance with the expectations of previous studies [3, 24],
suggesting that the low temperatures of the Southern
Ocean do not affect differentially the extent of photosynthate release by algal assemblages. Data obtained in the
®rst Antarctic cruise had showed that PER decreased with
increasing primary production rates [21]. We pooled here
all data obtained with membrane ®lters (the second Antarctic and the two NE Atlantic cruises) and found that the
slope of the log-log Model I linear regression between
dissolved and particulate primary production (Fig. 1A)
was signi®cantly lower than 1.0 (t-test, P < 0.001):
PPP
(mg C m)3 h)1)
Results and Discussion
Region
lower than the difference between DPP and bacterial heterotrophic production rates, rendering possible a cross-system
comparison of both variables. All labeled DOC produced during
the experiment was considered for estimating DPP rates since
our method could not distinguish between DOC released by algae
and that released by other processes such as lysis or grazing.
Although mesozooplankton grazing and lysis processes were
likely of minor importance because of the small volumes used
and the short duration of the experiments, microzooplankton
grazing could have contributed signi®cantly to the release of
recently synthesized DOC, especially at the less productive stations [24].
The rates of bacterial heterotrophic production (BHP) were
estimated from 3H-leucine incorporation in Eppendorf vials [32]
and empirically derived conversion factors. A constant 0.81 kg C
mol Leu)1 was used in the Southern Ocean, as obtained in the
®rst cruise [28], and different factors were used for each station
in the NE Atlantic, ranging from 0.62 to 3.55 kg C mol Leu)1
[PedroÂs-Alio et al., unpublished data] and the NW Mediterranean, 0.30 to 1.50 kg C mol Leu)1 [27]. BCD was estimated as
BHP/BGE with BGE values calculated from del Giorgio and Cole's
empirical model [10] relating bacterial respiration and production rates.
Variables were log-transformed in order to attain normality
and homogeneity of variances. Together with the more common
Model I, Model II linear regressions were also calculated since the
pairs of variables analyzed were equally subject to measurement
errors. When the slope of the equation is critical for the conclusion, results obtained with both models should be consistent
[3].
219
Table 2. Mean ‹ SE values of particulate (PPP) and dissolved (DPP) primary production, percent extracellular release (PER), bacterial heterotrophic production (BHP), and
carbon demand (BCD) calculated from bacterial growth ef®ciencies (BGE) estimated with del Giorgio and Cole's [10] model in the four regionsa
Phytoplankton±Bacterioplankton Coupling
X.A.G. MoraÂn et al.
220
Fig. 1. A. Relationship between dissolved and particulate primary production rates in experiments carried out in the second
Southern Ocean cruise (squares) and in the NE Atlantic (circles).
The ®tted line is Model I linear regression. B. Percent extracellular release (PER) vs. particulate primary production for the
same date set.
log DPP ˆ
1:03 ‡ 0:62…0:07† log PPP
…r2 ˆ 0:68; P < 0:000001; n ˆ 40†
The slope of the Model II regression (log DPP =)1.05 +
0.75 log PPP) was also signi®cantly lower than 1.0 (95%
con®dence limits 0.63±0.91) [29]. In other words, PER was
inversely related to total system productivity (Fig. 1B).
This new evidence of a decreasing contribution of dissolved primary production to total rates in more productive waters adds to several old [e.g., 4, 19] and recent [e.g.,
34] reports, but contradicts the conclusion obtained in the
literature review of Baines and Pace [3] that the average
13% PER encountered did not vary systematically across
the productivity range in marine systems. As pointed out
by Nagata [24], the lack of suf®cient data from open ocean
waters, but also the use of data sets obtained with different
methodologies, could have prevented the recognition of
such an inverse relationship in their analysis. In this regard, when Baines and Pace [3] divided their data set between studies that had and had not corrected for bacterial
uptake of DO14C during the experiments (as we did here),
their result approached ours. The slope of the log DPP vs
log PPP regression for corrected data was signi®cantly
lower than that for uncorrected data (see Fig. 3 in their
study), indirectly suggesting that bacteria remove more
algal DOC in oligotrophic conditions, but also supporting
the expectation of a higher PER at low productivities. DPP
has been understood as the ``unwanted'' outcome of
keeping the cellular machinery active when algae cannot
complete the synthesis of structural molecules [36]. Accordingly, a higher proportion of photosynthate should be
released in oligotrophic conditions, whereas most of the
®xed organic carbon would remain within the cells under
conditions of inorganic nutrient suf®ciency.
Average bacterial production spanned over two orders
of magnitude in the different regions (Table 2), being
signi®cantly higher in the NE Atlantic than in offshore
Antarctic waters (Kruskal±Wallis test, P < 0.0001). Yet,
BHP consistently amounted to a very low fraction of total
primary production in all regions (from 0.3% in the offshore Antarctic to 4.1% in the NE Atlantic). Low ratios of
BHP to total primary production have often been regarded
as evidence of uncoupling of the activities of both planktonic compartments [e.g., 5]. Although a signi®cant correlation between primary production (total or particulate)
and bacterial production is sometimes accepted as enough
evidence of phytoplankton±bacterioplankton coupling, a
direct and concurrent trophic dependence of heterotrophic bacteria on algae can only be mediated through
DPP, since PPP needs a variable lag phase before it is
available to bacterial uptake, for instance at the end of
phytoplankton blooms. In this study, we have addressed
the question of phytoplankton±bacterioplankton coupling
by means of the simultaneous determination of DPP and
its potential consumption by bacteria. BHP must re¯ect
the algal supply of DOC as a prerequisite for the consideration that both groups are coupled, but only when most
or all carbon processed by bacteria is met by DPP can we
conclude this trophic linkage to be strong.
The relationship between BCD and DPP was strongly
dependent on the location of the experiments either in
coastal or open-ocean waters. A high correlation (r = 0.93,
P < 0.001, n = 26) was found between DPP and BCD in
offshore waters of the Southern Ocean and, in most of the
Phytoplankton±Bacterioplankton Coupling
Fig. 2. Scatter plot of bacterial carbon demand vs dissolved
primary production for the four regions. The ®tted dashed line is
Model I linear regression for Antarctic offshore data [log
BCD = 0.41 + 0.69 ( ‹ 0.06) log DPP; r2 = 0.87, P < 0.001,
n = 26]. The Model II slope (0.74) is also signi®cantly lower than
1 [29] (95% con®dence limits: 0.64±0.86). The dotted line represents the Model I linear regression for the same original data
but using a BGE of 14% (see the text for details).
experiments (18 out of 26), dissolved primary production
was suf®cient to meet the estimated demand of carbon by
bacteria (Fig. 2), strongly suggesting that bacteria were
tightly dependent on algal DOC for growth and metabolism. Although the ratio of BCD to DPP tended to decrease
along the productivity gradient (Fig. 2), BCD was on average 91% of DPP in these Southern Ocean waters (Table
2), suggesting similar rates of photosynthate release by
phytoplankton and uptake by bacteria. If bacteria processed all algal-released DOC and had no other sources
available, the resulting mean estimate of BGE [i.e., DOC
incorporated as biomass (BHP) in relation to DOC produced (DPP)] would be 2%, equal to del Giorgio and
Cole's [10] modeled value (Table 2). Partially because of
the use of empirical leucine-to-carbon conversion factors,
all BGE values in the four regions (Table 2) were lower
than the median ocean value of 22% given by del Giorgio
and Cole [10], so the corresponding BCD estimates should
be viewed as the maximum amount of carbon potentially
processed by bacteria. Any higher BGEÐas hypothesized
by Rivkin and Legendre's [30] equation relating BGE and
temperatureÐwould yield a greater excess of DPP over
BCD, ®rmly supporting our conclusion of a strong coupling between algae and bacteria in offshore Antarctic
waters. For comparison, Fig. 2 also shows the regression
line that would result if BCD were calculated with a BGE of
14%, as measured by Carlson et al. [7] in the Ross Sea.
Whereas bacterial carbon demand could be almost
entirely explained by dissolved primary production in
221
Fig. 3. Mean (‹ SE) percentages of bacterial carbon demand to
dissolved primary production (BCD:DPP) with different values of
bacterial growth ef®ciency (BGE). Mean modeled BGE for each
region is given in Table 2.
Antarctic offshore waters, no correlation was found between BCD and DPP either in coastal Antarctic waters
(P = 0.34, n = 11), the NE Atlantic (P = 0.37, n = 22) or
the Mediterranean (P = 0.87, n = 5). Moreover, BCD was
greater than the actual supply of dissolved compounds
from algae (Table 2, Fig. 2), ranging from 1.8-fold on average in Antarctic coastal areas to ca 8-fold in the NE
Atlantic, allowing us to conclude that bacteria and phytoplankton were uncoupled in these regions. As mentioned before, the choice of another, ®xed BGE instead of
the modeled values shown in Table 2 would in turn affect
the percentage of BCD to DPP. Figure 3 shows the mean
values that this percentage would attain in the four regions
if two higher BGE values (15% and 30%) were used for
estimating BCD. By comparing the three BCD:DPP estimates for each region we can safely conclude that BCD can
be entirely met by DPP in the offshore Antarctic, whereas
BCD would on average always exceed DPP in the NE
Atlantic, unless an unrealistically high BGE were used.
Although the modeled mean BCD:DPP percentage in
the NW Mediterranean was 453%, these experiments displayed a clear inshore±offshore gradient (Fig. 4). In parallel to an increase in PER from 3% at the shelf station to
28% offshore, DPP varied from accounting for as low as
7% of BCD to virtually meeting all (104%) bacterial needs
of organic carbon.
An excess of heterotrophic carbon demand over primary production does not necessarily imply the existence
of allochthonous sources [33]. However, additional DOC
inputs other than algal release were clearly needed to
X.A.G. MoraÂn et al.
222
Fig. 4. Coastal±offshore variability of the potential ful®llment
of bacterial carbon demand by dissolved primary production
(DPP:BCD ratio, gray bars) and percent extracellular release
(PER, striped bars) at the 3 NW Mediterranean stations sampled.
The value of BCD used was that of del Giorgio and Cole's [10]
model. Error bars show ‹1 SE.
sustain bacterial production and respiration in the coastal
areas examined here. DOC is produced by phytoplankton
direct release, but also by cellular lysis [13] or grazer activity, either protozoan [25] or metazoan [16]. Bearing in
mind that the contribution of microbial grazers could in
fact have been partially considered in our estimates of
DPP, these latter DOC sources, DOC previously accumulated in situ after upwelling episodes in the NE Atlantic
experiments [2] and/or allochthonous inputs, must surely
have supplemented the algal production of labile carbon.
Previous reports have shown DPP to amount to less
than one-third of BCD [3, 18, 24]. Most of the data in these
studies, however, were obtained in coastal, relatively eutrophic sites. Although our results have con®rmed a
marked excess of BCD over DPP in coastal sites, the
contribution of DPP to BCD could be substantially higher
in offshore waters, even ful®lling it (Fig. 2 and Fig. 3). It
appears from these results that a key factor in¯uencing the
strength of phytoplankton±bacterioplankton coupling is
distance to the coast, presumably associated with trophic
conditions. Heterotrophic bacteria in coastal waters would
not be controlled by local DPP but by other autochthonous
or allochthonous inputs of organic matter, making possible the existence of more complex, net heterotrophic food
webs [15]. Conversely, open-ocean environments isolated
from external DOC sources and hypothesized to be in
metabolic balance (gross primary production = community respiration, [31]) would present a strong coupling
between phytoplankton and bacteria, such as that demonstrated here for the Southern Ocean (Fig. 2).
In conclusion, the relationship depicted in Fig. 1B
shows that low PPP is associated with a relatively high
DPP. At the low primary productivities characteristic of
most open-ocean waters, this high PER would result in a
tight dependence of bacteria on substrates supplied by
algae (Figs. 2 and 4). Conversely, lower PER at the more
productive coastal sites would involve additional sources
of DOC to sustain bacterial growth, such as DOC that
accumulates after algal blooms, both in polar [9] and
temperate systems [35]. Although more experiments are
needed in order to generalize whether these Southern
Ocean and NW Mediterranean results can be representative of all other open-ocean regions, we suggest that a
strong phytoplankton±bacterioplankton coupling, expressed as a concurrent link between dissolved primary
production and its consumption by bacteria, should only
be expected in areas far from the in¯uence of coastal inputs of dissolved organic carbon.
Acknowledgments
We thank the scientists and crew of the R/Vs HespeÂrides
and Cornide de Saavedra for their assistance and the good
atmosphere during the cruises. This study was supported
by Spanish CICYT Grants ANT-92-1186, ANT-96-0866,
MAR95-1901, and AMB94-0853.
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