Download Growth physiology and fate of diatoms in the ocean: a review

Journal of Sea Research 53 (2005) 25 – 42
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Growth physiology and fate of diatoms in the ocean: a review
Géraldine Sarthou a,*, Klaas R. Timmermans b, Stéphane Blain a, Paul Tréguer a
a
UMR6539/LEMAR/IUEM, CNRS/UBO, Place Nicolas Copernic, Technopôle Brest-Iroise, F-29280 Plouzané, France
Royal Netherlands Institute for Sea Research (NIOZ), P.O. Box 59, NL-1790 AB Den Burg, Texel, The Netherlands
b
Received 1 November 2003; accepted 6 January 2004
Available online 30 October 2004
Abstract
Diatoms are a major component of phytoplankton community. They tend to dominate under natural high-nutrient
concentrations, as well as during artificial Fe fertilisation experiments. They are main players in the biogeochemical cycle of
carbon (C), as they can account for 40% of the total primary production in the Ocean and dominate export production, as well as
in the biogeochemical cycles of the other macro-nutrients, nitrogen (N), phosphorus (P), and silicon (Si). Another important
nutrient is Fe, which was shown to have a direct or indirect effect on nearly all the biogeochemical parameters of diatoms. In the
present paper, an inventory is made of the growth, physiology and fate of many diatom species, including maximum growth
rate, photosynthetic parameters (maximum specific rate of photosynthesis, photosynthetic efficiency and light adaptation
parameter), nutrient limitation (half-saturation constant for growth/uptake), cellular elemental ratios, and loss terms (sinking
rates, autolysis rates and grazing rates). This is a first step for improvement of the parameterisation of physiologically based
phytoplankton growth and global 3D carbon models. This review is a synthesis of a large number of published laboratory
experiments using monospecific cultures as well as field data. Our compilation confirms that size is an important factor
explaining variations of biogeochemical parameters of diatoms (e.g. maximum growth rate, photosynthesis parameters, halfsaturation constants, sinking rate, and grazing). Some variations of elemental ratios can be explained by adaptation of
intracellular requirements or storage of Fe, and P, for instance. The important loss processes of diatoms pointed out by this
synthesis are (i) sinking, as single cells as well as through aggregation which generally greatly increases sinking rate, (ii) cell
autolysis, which can significantly reduce net growth rates, especially under nutrient limitation when gross growth rates are low,
and (iii) grazing by both meso- and micro-zooplankton. This review also defines gaps concerning our knowledge on some
important points. For example, we need to better know which iron species is available for phytoplankton, as well as the impact
of Fe on the variation of the elemental ratios, especially in terms of assimilation and regeneration of C and N. A better
quantification of prey selection by microzooplankton and mesozooplankton in natural environments is also needed, including
preference for the various phytoplankton and zooplankton species as well as for aggregates and faecal pellets.
D 2004 Elsevier B.V. All rights reserved.
Keywords: Diatoms; Biogeochemistry; Growth physiology; Nutrient limitation; Iron; Elemental ratios; Losses
1. Introduction
* Corresponding author. Fax: +33-2-98-49-86-45.
E-mail address: [email protected] (G. Sarthou).
1385-1101/$ - see front matter D 2004 Elsevier B.V. All rights reserved.
doi:10.1016/j.seares.2004.01.007
Diatoms are one of the predominant contributors
to global carbon fixation. They account for 40% of
the total primary production in the Ocean (Nelson
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G. Sarthou et al. / Journal of Sea Research 53 (2005) 25–42
et al., 1995; Tréguer et al., 1995; Mann, 1999;
Smetacek, 1999; Tréguer and Pondaven, 2000).
Evidence from sediment traps (Honjo, 1982; Smetacek, 1985; Takahashi, 1986) and in situ photographs of the sea floor (Billet et al., 1983) testifies
that significant vertical export of primary production
from the upper ocean to the deep sea occurs as
episodic, seasonal events following phytoplankton
blooms. Simultaneous aggregation of an entire phytoplankton population community and its subsequent sedimentation was shown to occur on a
time-scale of 24 hours (Alldredge and Gotschalk,
1989). A high enrichment of micro-organisms in
marine snow aggregates relative to the surrounding
waters was reported by many investigators (cf.
Riebesell, 1991); this rapidly sinking phytoplankton
is mainly dominated by diatoms, which sink in the
form of large, quickly settling flocs of marine
snow, amorphous aggregates 0.5 mm or greater in
diameter (Smetacek, 1985; Takahashi, 1986; Alldredge and Silver, 1988; Kranck and Milligan,
1988; Riebesell, 1991). Diatoms are main players
in the biogeochemical cycles of carbon (C), nitrogen (N), phosphorus (P), silicon (Si), and iron (Fe),
and tend to dominate export production (Buesseler,
1998). Nevertheless, their relatively low surface to
volume ratios will need nutrient-rich conditions for
growth in contrast to smaller phytoplankton, such
as nano- or pico-plankton, with higher surface to
volume ratios, which allow a more efficient exploitation of low nutrient concentrations (Chisholm,
1992). Therefore, diatoms will dominate phyto-
Table 1
Summarised parameters for diatoms (for references, see text and Appendixes 1 – 3 (www.nioz.nl/projects/ironages))
Parameter
Values
Units
Photosynthesis and growth
chl
Maximum specific rate of photosynthesis Pm
chl
Photosynthetic efficiency: a
chl chl
Light adaptation parameter: Ek = Pm
/a
Maximum specific growth rate: A
V = cell volume
2.6 F 1.0 (n = 10)
0.021 F 0.005 (n = 10)
95 F 40 (n = 10)
0.4 – 3.3
A = 3.4 V 0.13
gC gChl a 1 h 1
gC gChl a 1 h 1m2 s Amol 1
Amol m 2s 1
d 1
3.9 F 5.0 (n = 25)
Ks(Si) = 0.64 (S/V) 3.66
S/V in Am 1
1.6 F 1.9 (n = 35)
Ks(N) = 0.61 (S/V) 0.58
S/V in Am 1
0.24 F 0.29 (n = 14)
0.35 F 0.44 (n = 12)
KA(Fe) = 12 10 3 (S/V) 1.77
S/V in Am 1
AM
Nutrient limitation
Ks(Si)
Ks(N)
Ks(P)
KA(Fe)
AM
AM
nM
Elemental composition
C:N
N:P
Si:C
Si:N
Si:P
Fe:C
7.3 F 1.2 (n = 86)
10 F 4 (n = 27)
0.11 F 0.04 (n = 47)
0.8 F 0.3 (n = 50)
5.9 F 1.3 (n = 5)
35 F 25 (n = 21)
mol/mol
mol/mol
mol/mol
mol/mol
mol/mol
mol/mol
Loss terms
Sinking rate (individual cells) Fe-replete
Sinking rate (aggregates/flocs)
Grazing rate
Cell lysis
0.1 – 1.5
184 – 175
0.2 – 1.8
0.005 – 0.24
m d 1
m d 1
d 1
d 1
G. Sarthou et al. / Journal of Sea Research 53 (2005) 25–42
plankton communities under high-nutrient concentrations. The dominance of (large) diatoms is also
observed in man-made perturbations (iron additions) in so-called High-Nutrient, Low-Chlorophyll
(HNLC) regions. In-situ iron fertilisations, in the
Equatorial Pacific, the Southern Ocean, the Subarctic Pacific, as well as natural fertilisations, all
induced a shift in the natural phytoplankton assemblage towards a predominance of (larger) diatom
species, when Si does not become limiting (Martin
et al., 1994; De Baar et al., 1995; Coale et al.,
1996b, 2004; Boyd et al., 2000; Landry et al.,
2000b; Blain et al., 2001; Bucciarelli et al., 2001;
Gall et al., 2001; Smetacek, 2001; Takeda et al.,
2002; Boyd et al., 2004). In spite of so many
studies on diatoms, the real contribution of diatoms
to carbon export, as well as the impact on Fe on
this important phytoplankton group and on the
global carbon cycle still needs to be assessed.
One tool to answer these questions is the use of
physiologically based phytoplankton growth models
(e.g. SWANCO model, Lancelot et al., 2000) and
global 3D carbon models (e.g. PISCES model,
Aumont et al., 2003). These models may also help
to better understand why diatom species dominate
in some environments. In recent years, planktonic
ecological models have become increasingly complex and the parameter estimation becomes more
and more difficult. The aim of this review is then
to compile and synthesise the existing data on the
27
growth physiology and fate of diatom in the ocean
and the effect of Fe on these parameters (Table 1).
We define the gaps in our knowledge concerning
these parameters and give some recommendations
for additional laboratory experiments in order to
improve/extend our knowledge on this important
group of autotrophs.
2. Growth and photosynthesis
Maximum specific growth rates (Amax), obtained
under conditions of saturating light and nutrient
sufficiency, range from 0.2 d 1 to 3.3 d 1 with an
average value of 1.5 F 0.8 d 1 (n = 67, see Fig. 1).
Values vary by more than one order of magnitude, but
they can be related to cell size, which has long been
recognised as an important cause of interspecific
variability of Amax, the smallest cells having the
highest growth rates (see e.g. Geider et al., 1986;
Raven, 1986; Langdon, 1988; Tang, 1995; Raven and
Kübler, 2002). When plotting Amax (in d 1) vs. cell
volume (in Am3) of 67 diatom species obtained from
literature (Fig. 1), the size dependence of Amax was
described by the following allometric relation:
Amax ¼ 3:4 V0:13
ð1Þ
The magnitude of the exponent has been the
subject of some discussions (Chan, 1978; Banse,
Fig. 1. Variation of maximum growth rates (d1) vs. cell volume (Am3) (Blasco et al., 1982; Eppley and Sloan, 1966; Kudo et al., 2000; Milligan
and Harrison, 2000; Schöne, 1982; Williams, 1964).
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G. Sarthou et al. / Journal of Sea Research 53 (2005) 25–42
1982). Although the correlation coefficient remains
low (r2 = 0.48) when considering a range of variation
from 13 Am3 to 7 105 Am3, it appears that size
dependence of growth rate becomes statistically more
significant when considering this large range of sizes
(Geider et al., 1986).
The reduction of Amax with increasing cell size
implies that small cells have a distinct catalytic
advantage over large ones and should out-compete
them (Raven, 1986). The increase in cell size
induces a decrease in the capacity of solute influx
or efflux on a volume basis, due to a thicker
diffusion boundary layer and a smaller area of
membrane lipid and number of transporters allowing solute fluxes (Raven and Kübler, 2002). Moreover, the increase in cell size decreases the
effectiveness of increased pigmentation in harvesting light, the so-called ‘package effect’ (Kirk,
1994; Finkel and Irwin, 2000). The energy used
to synthesise pigment-protein complexes takes longer to repay in terms of absorbed energy in a
given external radiation field on larger cells (Raven, 1984). In other terms, assuming a constant
concentration of chlorophyll (Chl) per cell volume
and a constant spherical geometry, the ‘package
effect’ implies that each individual Chl molecule
has a lower probability of absorbing photons in a
given radiation field in a large cell than in a small
one, the Chl-a specific absorption cross-section
coefficient increasing with cell size (Geider et al.,
1986; Raven and Kübler, 2002). On the other
hand, intracellular concentration Chl-a of diatoms
tends to decrease with cell size, resulting in a
moderation in the increase in the package effect
with cell size (Finkel, 2001). Clearly, the quantification of the influence of the ‘package effect’ in
algae of different sizes and shapes, as well as for
cells exposed to low irradiance, is of great importance in mechanistic interpretations of rates of
growth and photosynthesis in natural conditions
(Raven and Kübler, 2002).
The rate of photosynthesis is controlled by the
efficiency of light utilisation to drive the overall
photosynthetic reactions to carbon fixation (Falkowski
and Raven, 1997). Photosynthesis vs. light can be
represented by a P-E curve (Webb et al., 1974), which
is now widely accepted as a useful relationship for
examining the photosynthesis physiology of micro-
algae, despite the uncertainties introduced by differences in methodology (Henley, 1993). Indeed, the
shape and the magnitude of the P-E curve reflect the
underlying biophysical, biochemical, and metabolic
processes that regulate photosynthesis (Falkowski
and Raven, 1997). Typically the P-E curve can be
divided into light-limited, light-saturated and photoinhibition regions. In nature pronounced photoinhibition in P-E curve is commonly observed only in
samples collected below the surface-mixed layer (Platt
et al., 1980). For a recent review on photoacclimation
of photosynthesis, see MacIntyre et al. (2002).
We compiled values for the maximum specific
rate of photosynthesis (Pm), the photosynthetic efficiency (a), which represents the initial slope of the
P-E curve, and the light adaptation parameter (Ek)
defined as the ratio between Pm and a. Values
(normalised to Chl-a content for Pmchla and achla)
are reported in Appendix 1 (www.nioz.nl/projects/
ironages). Pm chla ranges from 1.2 to 11.4 gC
gChla 1 h 1, with an average value of 2.6 F 1.0
gC gChla 1 h 1 (n = 10). achla ranged from 0.013 to
0.087 gC gChla 1 h 1 Amol 1 m2 s, with an
average value of 0.021 F 0.005 gC gChla 1 h 1
Amol 1 m2 s (n = 10). Finally, Ek varied between 46
and 498 Amol photons m 2 s 1, with an average
value of 95 F 120 Amol photons m 2 s 1 (n = 10).
The three extremely large values as shown in Appendix 1 (www.nioz.nl/projects/ironages) were excluded for the calculation of the average values.
Variability in the P-E curve, together with variability in the Chla:C ratio is used to assess photoacclimation, which involves changes in the macromolecular
composition and ultrastructure of the photosynthetic
apparatus (Durnford and Falkowski, 1997; Falkowski
and Raven, 1997). There is much work on the change
in Chl-a quota as a function of irradiance (e.g. Geider,
1987), with general agreement that this can be from 2
to 10 times. Thus the ‘down-regulation’ of the photosynthetic apparatus mostly occurs in response to irradiance. Next to the photon flux density, varying the
cellular chlorophyll-a quota up to one order of magnitude (Geider, 1987; Sosik et al., 1989; Veldhuis and
Kraay, 2004), iron also induces major changes in the
photosynthetic characteristics (Greene et al., 1991;
Sosik and Olson, 2002). Indeed, iron is essential for
many major biogeochemical processes, including photosynthesis (Geider and La Roche, 1994). Raven
G. Sarthou et al. / Journal of Sea Research 53 (2005) 25–42
(1990) estimated that 80% of the iron required by
phytoplankton is in the photosynthetic electron transfer. The high Fe requirement of the photosynthetic
apparatus makes photosynthesis a principal target of
Fe deficiency. In the marine diatom Phaeodactylum
tricornutum, Fe limitation induces a 2-fold reduction
of maximum photosynthesis rate and a 1.3-fold increase of the photosynthesis efficiency with Fe limitation (Greene et al., 1991). The decrease in the
maximum photosynthesis rate was explained by the
decrease in the minimal turnover time required for an
electron to pass from water to CO2 (Greene et al.,
1991). The increase in the photosynthetic efficiency
was explained by a decrease in light-harvesting pigment content, reducing the package effect related to the
optical properties of a heterogeneous suspension of
particles (Berner et al., 1989; Greene et al., 1991).
There is universal agreement that a reduction in
photosynthetic pigment content (chlorosis) accompanies Fe limitation (Greene et al., 1991; Geider and La
Roche, 1994). Fe limitation may either directly induce
chlorosis by influencing the formation of protochlorophyllide (Spiller et al., 1982), or indirectly, simply by
reduction of the cellular abundance or activity of
enzymes that require Fe and that are involved in the
Chl biosynthesis pathway (Davey and Geider, 2001).
3. Nutrient limitation: half-saturation constants
for growth/uptake
For a given nutrient (Nut), the specific uptake rate
(VNut) and the specific growth rate (A) follow Michaelis-Menten (Eq. 3) and Monod (1942) (Eq. 4) saturation functions, respectively:
VNut ¼ Vmax½Nut=ð½Nut þ KsÞ
ð3Þ
A ¼ Amax½Nut=ð½Nut þ KAÞ
ð4Þ
where Vmax and Amax represent the maximum rates
of uptake and growth, respectively, at infinite substrate concentration, Ks the concentration of the
nutrient that limits VNut to 0.5Vmax and KA the
concentration of the nutrient that limits A to 0.5Amax.
max. [Nut] is the concentration of the added nutrient.
At steady state, the specific growth rate and the
specific uptake rate are in balance and thus equiv-
29
alent. The large difference which exists between the
half-saturation constants for growth KA and shortterm uptake Ks is due to acclimation capabilities of
the organisms. Over the acclimation range, KA to
Ks, the algae can maintain maximum growth rates
by modulating both their internal nutrient quotas
and their maximum short-term nutrient uptake rates
in response to variations in external nutrients concentrations (Morel, 1987).
Half-saturation constants for nitrate (Ks(N)),
phosphate (Ks(P)), orthosilicic acid (Ks(Si)) and
iron (KA(Fe)) have been reported in Appendix 2
(www.nioz.nl/projects/ironages). For iron, KA(Fe) is
generally expressed using inorganic Fe concentrations (FeV) when adding an artificial chelator, ethylenediaminetetraacetate (EDTA) as a metal buffer
(Morel et al., 1979; Sunda et al., 1991; Sunda and
Huntsman, 1995), but total concentrations of dissolved Fe (Fediss) are chosen as master variable,
when no EDTA is added (Coale et al., 1996a;
Timmermans et al., 2001b). The form of Fe that
is available for phytoplankton growth is not yet
known. It was primarily thought that only FeV was
bioavailable (cf. Maranger et al., 1998). However,
more than 99% of dissolved Fe is organically
complexed in seawater (Gledhill and Van den Berg,
1994, 1995; Rue and Bruland, 1995). The corresponding FeV is then far too low for sustaining
growth of even the small phytoplankton species
(Timmermans et al., 2001b), and some Fe organic
complexes may be a source of available Fe for
phytoplankton growth (Soria-Dengg and Horstmann,
1995; Hutchins et al., 1999; Maldonado and Price,
1999). When concentrations of natural organic
ligands in the diatom cultures and their conditional
stability constants with Fe are known, or considering a theoretical percentage of organically complexed Fe in seawater (Timmermans et al., 2001b),
KA(Fediss) can be calculated from KA(FeV) (Gledhill and Van den Berg, 1994; Rue and Bruland,
1995). However, it is then hard to judge whether
the differences of KA(Fe) are caused by the physiological differences between the species, or whether
calculation of the concentration of FeV plays a role.
In this review, KA(Fe) refers to inorganic Fe concentrations when EDTA is added to culture medium
and to dissolved Fe concentrations when incubations
are performed in natural seawater. This assumes that
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G. Sarthou et al. / Journal of Sea Research 53 (2005) 25–42
FeV and dissolved Fe are the fractions that are
bioavailable in the former and latter cases, respectively. This hypothesis clearly shows that more
studies are needed to better know which iron
species is available for phytoplankton.
Ks(N) values ranged from 0.02 AM to 10.2 AM,
with an average value of 1.6 F 1.9 AM (n = 35). Ks(P)
ranged from 0.01 AM to 8.9 AM, with an average value
of 1.2 F 2.5 AM (n = 18). Ks(Si) values range from 0.2
to 22 AM, with an average value of 3.9 F 5.0 AM
(n = 25). Values of KA(Fe) varied between 0.59 pM to
1.12 nM, with an average value of 0.35 F 0.44 nM
(n = 12).
The range of variations of half-saturation constants
is very wide and the absolute values of the average half
saturation values indicate that generally these are well
above the annual sea surface concentrations (Levitus et
al., 1993; Johnson et al., 1997). Therefore, diatoms
may dominate phytoplankton community only under
conditions of high-nutrient concentrations. Such conditions are found in spring and early summer blooms in
open ocean waters (Ragueneau et al., 2000). This
implies that at the beginning of the growth season the
diatoms should not experience nutrient limitation. This
is what is seen in the spring development of the
phytoplankton, where the diatoms belong to the groups
with a rapid development. Only after the depletion of
nutrients (mainly silicate), do other phytoplankton
species take over.
On the other hand, diatoms can adapt to low
nutrient concentrations by reducing their size. Small
cells are more proficient (have a smaller half-saturation constant) than large cells (Eppley et al., 1969).
They have greater surface to volume (S/V) ratio,
which increases the exchanges of gases and solutes
across the cell surface, then decreasing the diffusion
limitation of nutrient uptake (Morel et al., 1991a).
Comparing half-saturation constants of macro- and
micro-algae, Hein et al. (1995) determined a power
law relationship between Ks(N) values and surface to
volume (S/V) ratios:
KsðNÞ ¼ 0:61ðS=VÞ0:58
ð5Þ
with Ks(N) in AM and S/V in Am 1, r2 = 0.4, n = 32.
Similarly, very recently, Leynaert et al. (2004)
observed a strong relationship between S/V ratios
and Ks(Si) for one diatom species, whose size was
reduced by Fe limitation:
KsðSiÞ ¼ 0:64ðS=VÞ3:66
ð6Þ
with Ks(Si) in AM and S/V in Am 1, r2 = 0.9, n = 5.
For Ks(P), Smith and Kalff (1982) showed little
evidence of significant variations of Ks(P) among a
group of eight co-occurring phytoplankton species
(diatom and non-diatom species). On the other hand,
Donald et al. (1997) showed that Thalassiosira weissflogii was able to use two phosphate uptake systems
depending on P concentrations, with each phase
possessing very different Ks(P) values. The phase I
uptake could occur in the oligotrophic ocean where
phosphate concentrations are low. The organisms
would acquire phosphate at very low concentration
without being able to acquire it quickly into the cell
(Donald et al., 1997). The phase II uptake could occur
in microscale phosphate-enriched patches and allows
for rapid uptake (Rivkin and Swift, 1982; Donald et
al., 1997). The range of variation found in the
literature may then be related to the existence of these
two phase uptake systems. However, when not considering the extreme values, Ks(P) values average
0.24 F 0.29 AM (n = 14).
For KA(Fe), using data reported in Appendix 2
(www.nioz.nl/projects/ironages), we also established a
power law relationship between KA(Fe) and S/V:
KAðFeÞ ¼ 12 103 ðS=VÞ1:77
ð7Þ
with KA(Fe) in nM and S/V in Am 1, r2 = 0.7, n = 9.
The very low value of KA(Fe) for the small oceanic
Antarctic species Chaetoceros brevis indicates that
this species has adapted to very low Fe concentrations
and would never experience Fe limitation in the
Southern Ocean, whereas the large chain-forming
diatom species Chaetoceros dichaeta will only bloom
following an Fe input (Timmermans et al., 2001b).
4. Elemental ratios
Elemental ratios for 47 different diatom species at
nutrient-replete conditions are reported in Appendix 3
(www.nioz.nl/projects/ironages).
G. Sarthou et al. / Journal of Sea Research 53 (2005) 25–42
31
Fig. 2. Frequencies of the elemental ratios (C:N, C:P, Si:C, Si:N, Si:P, Fe:C) of diatom species. Values and references are reported in Appendix 3
(www.nioz.nl/projects/ironages).
C:N ratios have an averaged value of 8.0 F 3.5
mol/mol (n = 101), ranging from 2.7 to 29.7 mol/mol
(Fig. 2). This range of variation is very wide but we
observed that more than 85% of diatom species have
C:N varying from 5.0 to 9.7 (Fig. 2). Three diatom
species have very high C:N ratios (>19.4, see Appendix 3 (www.nioz.nl/projects/ironages)). When not considering these three very high values, which may be
the result of some peculiarity of the culture conditions
(Brzezinski, 1985), C:N ratios have an averaged value
of 7.3 F 1.2 mol/mol (n = 86), which is close to the 6.6
C:N ratio reported by Redfield et al. (1963). N:P ratios
have an average value of 10 F 4 (n = 27) and are
widely distributed from 5 to 18 mol/mol (Fig. 2).
More than 90% of the values are lower than the
Redfield ratio of 16. Revisiting the C:N:P ratios for
several phytoplankton groups, Geider and La Roche
(2002) also observed in nutrient-replete cultures that
the C:N ratio, although variable, has a typical value
close to that of the Redfield ratio and that the N:P ratio
fall below the Redfield ratio. Using mass balance
calculations based on the physiologically achievable
range of the dominant macromolecules in the cell, they
could only explain the low N:P ratios by an intracellular storage of P.
Si:C ratios have an averaged value of 0.14 F 0.13
mol/mol (n = 54), ranging from 0.04 to 0.95 mol/mol.
More than 88% of diatom species have Si:C ratios
between 0.05 and 0.19 mol/mol (Fig. 2), which means
a factor 4 of variation. One diatom species, the giant
diatom Ethmodiscus (Villareal et al., 1999a), has a
very high Si:C ratio (0.95 mol/mol), due to a low C
content per cell volume (Villareal et al., 1999a). When
not considering the extreme values, Si:C ratios have an
averaged value of 0.11 F 0.04 mol/mol (n = 47). Si:N
ratios have an average value of 1.0 F 1.0 mol/mol
(n = 57), ranging from 0.17 to 7.24. The very high
value (7.24) is also observed for the giant diatom
Ethmodiscus, and is also due to a low N content per
cell volume (Villareal et al., 1999a). 88% of diatoms
species have values ranging from 0.4 to 1.55 mol/mol,
which means a factor 4 of variation, as for Si:C ratios.
When not considering the extreme values, Si:N ratios
have an average value of 0.8 F 0.3 mol/mol (n = 50).
Si:P had an average value of 10.0 F 7.1 (n = 7), varying between 3.8 and 21. The number of measurements
is much less than for the other elemental ratios. It
seems that two diatom species have higher ratios than
the five others do: 19.5 mol/mol (Stephanopyxis palmeria; Goldman et al., 1992) and 21 mol/mol (Nitzschia sp.; Takeda, 1998). When not considering these
two very high values, Si:P ratios have an average value
of 5.9 F 1.3 mol/mol (n = 5).
Fe:C ratios had an average value of 65 F 91 Amol/
mol (n = 25), ranging over more than 2 orders of
magnitude, from 2.3 to 370 Amol/mol. As seen in
Fig. 2, Fe:C ratios are widely distributed. 84% of
diatom species had Fe:C ratios between 2.3 and 89
Amol/mol, corresponding to an average value of
35 F 25 Amol/mol (n = 21). The Fe:C ratios of diatom
32
G. Sarthou et al. / Journal of Sea Research 53 (2005) 25–42
species are highly dependent on iron concentration in
the medium (Sunda et al., 1991; Sunda and Huntsman,
1995; Maldonado and Price, 1996). Bruland et al.
(2001) showed that the variation of Fe:C ratio with
Fe availability has to be taken into account for the
prediction of iron depletion or nitrate depletion in
upwelling systems. Oceanic species, which are growing in seawater with very low Fe concentrations (100 –
1000 times lower than in the coastal waters) have
lower Fe:C ratios than related estuarine species (Sunda
and Huntsman, 1995).
Reduction of size cell is not the only strategy for
adaptation to low-iron oceanic conditions (see
above). Another strategy for the adaptation to low
Fe concentrations is reducing their Fe requirement
for growth (thus reducing their Fe:C ratios; Sunda
et al., 1991; Sunda and Huntsman, 1995; Maldonado and Price, 1996; Muggli et al., 1996; Muggli
and Harrison, 1997; Schmidt et al., 1999). The
mechanism is still unknown. It could be a more
efficient exchange of iron within intracellular pools
during Fe starvation (Sunda et al., 1991), a minimisation of metabolic pathways that requires large
amount of Fe (Stefels and Van Leeuwe, 1998), or a
replacement of Fe-containing proteins by non-Fecontaining proteins possessing other metal catalysts
(La Roche et al., 1996). Under low Fe conditions,
flavodoxin replaces the Fe-containing electron transfer catalyst ferrodoxin as a means of decreasing the
cellular Fe requirement (Entsch et al., 1983; Raven,
1988; La Roche et al., 1993, 1996, 1999; McKay et
al., 1999). On the other hand, during periods of
high Fe availability, some coastal diatoms are able
to accumulate excess Fe, having Fe:C ratios 20 –30
times higher than those needed for maximal growth
(Sunda and Huntsman, 1995). Diatoms could then
out-compete other species if Fe became limiting
(Bruland et al., 2001).
Recent seawater and culture experiments showed an
increase in Si:C and Si:N ratios of diatoms under Fe
limitation (Martin and Fitzwater, 1988; Hutchins and
Bruland, 1998; Hutchins et al., 1998; Takeda, 1998; De
la Rocha et al., 2000; Franck et al., 2000; Bucciarelli et
al., ms in review; Brzezinski et al., 2003). Iron-stressed
diatoms should therefore deplete surface waters of
orthosilicic acid before nitrate, driving the system
towards Si limitation of the phytoplankton community.
The effect of Fe on the uncoupling between Si, C, and
N uptake and assimilation is currently not well understood. It may be due to the different ways Fe is involved
in intracellular mechanisms (Stefels and Van Leeuwe,
1998; Bucciarelli et al., ms in review) and to the
differences between silicon, carbon and nitrogen
cyclings (Martin-Jézéquel et al., 2000; Claquin et al.,
2002). Fe is essential to many metabolic processes
that require electron transfer reactions, such as photosynthesis, respiration and nitrogen assimilation inducing that C and N assimilations are directly affected
by Fe limitation. On the other hand, Si is mainly
linked to the growth rate and the duration of the cell
wall synthesis phase (Martin-Jézéquel et al., 2000;
Claquin et al., 2002). Si assimilation may be indirectly affected by Fe limitation through a reduction of
growth rate (Bucciarelli et al., ms in review). By
examining gross and net utilisation of carbon, nitrogen and silicon in the Southern Ocean, Brzezinski et
al. (2003) hypothesised that the main effect of Fe
limitation on nutrient uptake is the Antarctic Circumpolar Current is to diminish the relative use of new
nitrogen, i.e. to increase reliance on regenerated
nitrogen by inhibiting nitrate uptake, rather than to
alter the stoichiometry of gross nutrient uptake by
phytoplankton. Clearly more experimental work is
needed to better understand and quantify the different
processes involved in this positive feedback of Fe
limitation on the ‘silicate pump’ (Dugdale et al.,
1995).
5. Losses
5.1. Sinking rates of diatom cells
Sinking rate of a diatom cell is not only a function
of its size and shape but is also strongly dependent on
the physiological state of the cell (Brzezinski and
Nelson, 1988). In healthy, non-aggregated cells, sinking and ascent rates are generally described by
Stokes’ equation (Hutchinson, 1967). Increasing senescence of a population is accompanied by an
increasing sinking rate. The means of this control
was in part found to be through the selective exchange of heavier ions for lighter ions in the vacuole,
the so-called ionic pump, which is an energy-requiring process (Anderson and Sweeney, 1978). Nutrient
(N, P, Si, and Fe) and energy limitations increase cell
G. Sarthou et al. / Journal of Sea Research 53 (2005) 25–42
sinking rates several fold (Smayda, 1970; Bienfang et
al., 1982; Bienfang and Harrison, 1984; Harrison et
al., 1986; Waite et al., 1992; Muggli et al., 1996).
Muggli et al. (1996) observed a 5-time increase from
Fe-replete to Fe-stress conditions in the sinking rate
of the oceanic diatom Actinocyclus sp., from 0.17 m
d 1 to 0.93 m d 1. Fe limitation may affect phytoplankton sinking rates by stressing the energy-producing pathways needed by the cell to maintain their
buoyancy. Furthermore, the higher silicification of
diatoms under Fe-stress (Martin and Fitzwater,
1988; Hutchins and Bruland, 1998; Hutchins et al.,
1998; Takeda, 1998; De la Rocha et al., 2000; Franck
et al., 2000; Bucciarelli et al., ms in review) may
increase the sinking rate via thicker siliceous frustules. Recently, during the Southern Ocean RElease
Experiment (SOIREE, in Feb. 1999), Watson et al.
(2000) observed a two-fold decrease of Si:C ratio
inside the patch as opposed to outside the patch and
Waite and Nodder (2001) noted a four-fold decrease
in the sinking rate inside the patch as opposed to
outside the patch, on day 8. This decrease may be in
agreement with the hypothesis of a lower sinking rate
due to thinner frustules when Fe was added. However, the sinking rate response was very rapid, with
almost a three-fold increase in 24 h, on days 11 and
12 when algae were again Fe stressed due to Fe
complexation by organic ligands (Maldonado et al.,
2001). This fast response is then more consistent with
ionic changes in cell protopolast (Waite and Nodder,
2001).
Some large-sized diatoms adopted a strategy of
buoyancy-mediated vertical migration to access nutrient-enriched waters located below the nutricline
(Villareal, 1992; Villareal et al., 1993, 1999b; Moore
and Villareal, 1996; McKay et al., 2000). These species
are able to grow under low-light conditions (Goldman
and McGillicuddy, 2003) and, although there are virtually no data on nutrient uptake by large diatoms for
extremely low light environments, large diatoms may
play a major role in primary and export production
(Kemp et al., 2000; Goldman and McGillicuddy,
2003).
5.2. Aggregation
Aggregation processes generally increase sinking
rates (Alldredge and Silver, 1988). In theory, the
33
combined effect of cell sinking rates increases and
aggregation should have the largest effect on the
magnitude of diatom export flux (Jackson and
Lochmann, 1992). Diatom aggregates are the primary
source of marine snow aggregates, which were shown
to sink at a mean rate of f 50 – 100 m d 1 (Billet et
al., 1983; Alldredge and Silver, 1988; Mann, 1999).
For a detailed review on diatom aggregation in the sea,
see Thornton (2002). Both biological and physical
processes are responsible for the formation of large,
rapidly sinking aggregates (McCave, 1984). The
repackaging of particulate material into faecal pellets
through the feeding activities of animals is the biologically mediated aggregation and dominates when primary productivity is directly consumed by grazers
(McCave, 1984; Kiørboe et al., 1996; Wassmann et
al., 1999). On the other hand, physical mechanisms
dominate during intense phytoplankton blooms, when
an uncoupling between primary and secondary productivity occurs (Jackson, 1990; Riebesell and WolfGladrow, 1992). The rate of physical formation of algal
flocs depends on biomass accumulation and concentration, cell size and shape, including setae, the abundance of chain-forming species, stickiness, and
whether the cells are solitary or chain-forming, and
the mechanisms responsible for particle collision,
such as Brownian motion, differential settlement and
shear (Jackson, 1990; Jackson and Lochmann, 1992;
Riebesell and Wolf-Gladrow, 1992; Kiørboe et al.,
1998). Another important agent of diatom aggregation
is the presence of transparent exopolymer particles
(TEP) (Riebesell, 1991; Alldredge et al., 1993; Passow
et al., 1994, 2001; Engel, 2004) For a recent review on
TEP, see Passow (2002). TEP are probably generated
abiotically from dissolved extracellular polysaccharides (Passow et al., 1994), which are released by
phytoplankton, especially diatoms, and bacteria (Hama
and Handa, 1987; Decho, 1990; Williams, 1990). The
major importance of TEP for aggregation of diatom
blooms appears to be the much higher sticking coefficients of TEP compared to diatom cells (Kiørboe et
al., 1990; Kiørboe and Hansen, 1993; Passow et al.,
1994; Logan et al., 1995).
Not all diatom flocs settle immediately from surface waters. Large marine snow aggregates were
observed to be retained in the surface layer for several
days, including the floating mats of Rhizisolenia spp.
(Villareal, 1988; Kemp et al., 2000) and marine snow
34
G. Sarthou et al. / Journal of Sea Research 53 (2005) 25–42
aggregates with neutral buoyancy or even slow ascending rates, related to gas bubble formation within
the flocs (Stachanowitsch et al., 1990; Riebesell,
1992). Turbulence may help retain some large aggregates in the mixed layer for many days where they
age and dissociate (Alldredge and Cohen, 1987).
Aggregate feeders may capture aggregates and prevent them from sinking to the sea-floor, resulting in
increased remineralisation rates in the euphotic zone
(Jackson, 1993; Green and Dagg, 1997).
5.3. Cell lysis
Lysis of phytoplankton cells is increasingly recognised as a potentially important factor in phytoplankton population dynamics (Brussaard et al.,
1995; Augusti et al., 1998, 2001; Kirchman, 1999;
Augusti and Duarte, 2000). One type of cell lysis is
the viral lysis, but diatoms appear to be relatively
well protected against viruses. In Ross Sea habitats,
of over 29 700 diatom cells examined none was
infected by large viruses (Gowing, 2003). Another
type of cell lysis is death due to nutrient stress.
Brussaard et al. (1997) first studied the autolysis
kinetics of a marine diatom under nutrient stress.
Although the autolysis rates in their study do not
seem very high (mostly lower than 0.13 d 1), these
loss rates can significantly reduce net growth rates,
especially under nutrient limitation when gross
growth rates are low. Veldhuis et al. (2001) published detailed results of viability and cell death of,
amongst others, Chaetoceros calcitrans. They
showed that, even in apparently uniform populations, distinct differences in viability could exist.
The exact consequences of loss of membrane integrity used in the Veldhuis et al. (2001) study as the
indicator of viability are yet unknown. Similarly,
data on the Antarctic diatom Chaetoceros brevis
seemed to show that increased mortality could occur
after relief from iron limitation (Timmermans et al.,
2001b).
5.4. Grazing
In the last decade there has been considerable
debate about whether grazing pressure or Fe supply
control algal stock in HNLC regions (Cullen, 1991;
Frost, 1991; Morel et al., 1991b; Banse, 1992; Price
et al., 1994; Landry et al., 1997). Current opinion
suggests that both are important and that they form
the basis for the ecumenical Fe hypothesis (Cullen
et al., 1992). In the NE subartic Pacific, the findings of Boyd et al. (1996), from in-vitro Fe enrichments
in which representative number of mesozooplankton
were present, indicate that Fe supply rather than
grazing pressure exerts the ultimate control over
the magnitude of diatom stocks in this region. Invitro experiments at Ocean Station Papa, where
mesozooplankton stock was increased in order to
increase grazing pressure, showed that more than
five times ambient grazing pressure is required to
prevent the accumulation of algal biomass following an episodic Fe supply (Boyd et al., 1999). On
the contrary, during monsoons, in the Arabian
Sea, which is a typical HNLC area where Fe
concentrations are not likely to be limiting (Measures and Vink, 1999), grow-out experiments
showed that diatoms were the only group capable
of blooming in the absence of mesozooplankton,
i.e. their abundance in situ was more likely to be
controlled by mesozooplankton grazing than by Fe
availability.
The most common grazers of diatoms are large
organisms such as copepods (Smetacek, 1999). Some
studies question the role of diatoms as a key food
and for reproductive success in copepods (Klepplel
et al., 1991; Klepplel, 1993; Poulet et al., 1994,
1995; Uye, 1996; Ban et al., 1997; Ianora et al.,
1999; Miralto et al., 1999; Tang and Dam, 2001).
Even if diatoms do not always show a negative
effect on egg production and hatching (Starr et al.,
1999; Irigoien et al., 2000; Shin et al., 2003), some
inhibitory compounds that block female copepod
embryogenesis (Poulet et al., 1995; Uye, 1996)
may represent a defence mechanism by diatoms
against grazing by copepods, thereby prolonging
diatom blooms (Ban et al., 1997). Grazing impacts
of copepods vary between values lower than 1% and
values around 45% of primary productivity (e.g.
Dam et al., 1995; Verity et al., 1996b; Dubischar
and Bathmann, 1997; Roman et al., 2000; UrbanRich et al., 2001; Zeldis, 2001; Cabal et al., 2002).
Some studies contradict the paradigm that microzooplankton are constrained to diets of nanoplankton
and strongly suggest that they feed on phytoplankton
larger than themselves (e.g. Hansen and Calado,
G. Sarthou et al. / Journal of Sea Research 53 (2005) 25–42
1999, and references herein). Heterotrophic dinoflagellates, for example, achieve that either by engulfing prey in a membrane extruded from the
dinoflagellate cell (Jacobson and Anderson, 1986)
or by drawing in chains and compressing them in
food vacuoles (Buck and Newton, 1995). In coastal,
as well as open ocean environments, 45 –110% of
the standing stock of diatoms can be removed each
day by microzooplankton grazing (Verity et al.,
1996a; Nejstgaard et al., 1997; Landry et al.,
2000a; Calbet, 2001; Strom et al., 2001; Olson and
Strom, 2002; Suzuki et al., 2002). A predictive
understanding of diatoms grazing losses must then
take into account microzooplankton as important and
sometimes dominant consumers of bloom-forming
diatoms. However, a better quantification of prey
selection by microzooplankton and mesozooplankton
in natural environments is needed, including preference for the various phytoplankton and zooplankton
species as well as for aggregates and faecal pellets.
6. Conclusions and recommendations
Diatoms are the most important phytoplankton
group in marine environments and are the key players
in the ocean carbon cycle. In spite of so much research
on diatoms, the real contribution of diatoms to carbon
export, as well as the impact on Fe on this important
phytoplankton group and on the global carbon cycle
still needs to be assessed. The biochemical parameters
vary among the species and size can account for much
of interspecific variability of maximum growth rate,
optical absorption cross-section, half-saturation constants for nitrate, orthosilic acid, and iron, and sinking
rate of individual cells. However, so far very few
studies have investigated the variations of these
parameters, as well as the impact of Fe limitation on
the very large diatom species, which significantly
contribute to annual new production (Goldman et
al., 1992; Goldman, 1993; Pudsey and King, 1997;
Gersonde and Barcena, 1998; Timmermans et al.,
2001b; Goldman and McGillicuddy, 2003; Timmermans et al., in press). There is then an obvious need
for more studies on the biogeochemical parameters of
isolated, ecologically relevant, open ocean, bloom
forming large diatoms, in particular for a better
constrain of the allometric relationships. However,
35
these species might be not easy to grow and maintain
for longer periods in the laboratory.
The elemental ratios, the C:N, Si:C, Si:N ratios,
although variable, have typical values close to Redfield/Brzezinski ratios. The largest difference is observed for N:P and Si:P, and could be explained by an
intracellular storage of P (Geider and La Roche,
2002). Fe:C ratio could also be explained by a
reduction of Fe requirement, through a more efficient
use of intracellular pools (Sunda et al., 1991), a
minimisation of metabolic pathways (Stefels and
Van Leeuwe, 1998), and/or a replacement of Fecontaining proteins by non Fe-containing proteins
(La Roche et al., 1996). A luxury uptake of Fe can
also happen when Fe availability is high (Sunda and
Huntsman, 1995) and may explain part of the variability in Fe:C ratios if Fe concentrations in culture
media are different from one experiment to another
one. Recent studies showed the strong impact on Fe
limitation on the elemental ratios Si:N and Si:C
(Marin and Fitzwater, 1988; Hutchins and Bruland,
1998; Hutchins et al., 1998; Takeda, 1998; De La
Rocha et al., 2000; Franck et al., 2000; Bucciarelli et
al., ms in review; Brzezinski et al., 2003). However,
the mechanisms underlying this impact are still not
clear and need more studies including the effect on
the cell cycle, and on the assimilation and regeneration of C and N.
Concerning the losses, diatoms can sink quite
rapidly because of their large size and because they
form aggregates which generally increase sinking
rates. Diatoms are also subject to cell lysis by
autolysis (Brussaard et al., 1997; Veldhuis et al.,
2001) as they seem to be relatively well protected
against viruses (Gowing, 2003). Diatom cells are
commonly grazed by mesozooplankton species such
as copepods; however, one cannot ignore that microzooplankton species are sometimes dominant consumers of bloom-forming diatoms. However, a better
quantification of prey selection by microzooplankton
and mesozooplankton in natural environments is
needed.
Acknowledgements
We acknowledge the support from the European
Commission’s Marine Science and Technology
36
G. Sarthou et al. / Journal of Sea Research 53 (2005) 25–42
Programme under contract EVK2-1999-00227 (IRONAGES, ‘‘Iron Resources and Oceanic Nutrients—
Advancement of Global Environment Simulations’’).
This is contribution Nj911 of the IUEM, European
Institute for Marine Studies (Brest, France).
References
Alldredge, A.L., Cohen, Y., 1987. Can microscale patches persist in
the sea? Microelectrode study of marine snow, faecal pellets.
Science 235, 601 – 689.
Alldredge, A.L., Gotschalk, C.C., 1989. Direct observations of the
mass floculation of diatom blooms: characteristics, settling velocities and formation of diatom aggregates. Deep-Sea Res. 36,
159 – 171.
Alldredge, A.L., Silver, W., 1988. Characteristics, dynamics and
significance of marine snow. Prog. Oceanogr. 20, 41 – 82.
Alldredge, A.L., Passow, U., Logan, B.E., 1993. The abundance
and significance of a class of large, transparent organic particles
in the ocean. Deep-Sea Res. I 40, 1131 – 1140.
Anderson, L.W.J., Sweeney, B.M., 1978. Role of inorganic ions in
controlling sedimentation rate of a marine centric diatom Dytilum brightwellii. J. Phycol. 14, 204 – 214.
Augusti, A., Duarte, C.M., 2000. Strong seasonality on phytoplankton cell lysis in the NW Mediterranean littoral. Limnol. Oceanogr. 45, 940 – 947.
Augusti, A., Satta, M.P., Mura, M.P., Benavent, E., 1998. Dissolved
esterate activity as a tracer of phytoplankton lysis: Evidence of
high phytoplankton lysis rates in the NW Mediterranean. Limnol. Oceanogr. 43, 1836 – 1849.
Augusti, A., Duarte, C.M., Vaqué, D., Hein, M., Gasol, J.M., Vidal,
M., 2001. Food-web structure and elemental (C, N, and P)
fluxes in the eastern tropical North Atlantic. Deep-Sea Res. II
48, 2295 – 2321.
Aumont, O., Maier, R.E., Blain, S., Monfray, P., 2003. An ecosystem model of the global ocean including Fe, Si, P co-limitations.
Global Biogeochem. Cycles 17, 1 – 26.
Ban, S., Burns, C., Castel, J., Chaudron, Y., Christou, R., Escribano,
R., Umani, S.F., Gasparini, S., Ruiz, F.G., Hoffmeyer, M., Ianora,
A., Kang, H.K., Laabir, M., Lacoste, A., Miralto, A., Ning, X.,
Poulet, S., Rodriguez, V., Funge, J., Shi, J., Starr, M., Uye, S.,
Wang, Y., 1997. The paradox of diatom-copepod interactions.
Mar. Ecol. Prog. Ser. 157, 287 – 293.
Banse, K., 1982. Cell volumes, maximal growth rates of unicellular
algae and ciliates, the role of ciliates in the marine pelagial.
Limnol. Oceanogr. 27, 1059 – 1071.
Banse, K., 1992. Grazing, the temporal changes of phytoplankton
concentrations, and the microbial loop in the open sea. In:
Falkowski, P., Woodhead, A.D. (Eds.), Primary Production
and Biogeochemical Cycles in the Sea. Plenum, New York,
pp. 409 – 440.
Berner, T., Dubinsky, K., Wyman, K., Falkowski, P.G., 1989. Photoadaptation and the ‘‘package’’ effect in Dunaliella tertiolecta
(Chlorophyceae). J. Phycol. 25, 70 – 78.
Bienfang, P.K., Harrison, P.J., 1984. Sinking rate response of natural assemblages of temperate and subtropical phytoplankton to
nutrient depletion. Mar. Biol. 83, 293 – 300.
Bienfang, P.K., Harrison, P.J., Quamrby, L., 1982. Sinking rate
response to depletion of nitrate, phosphate and silicate in four
marine diatoms. Mar. Biol. 67, 295 – 302.
Billet, D.M., Lampitt, A.L., Rice, A.L., Mantoura, R.F.C., 1983.
Seasonal sedimentation of phytoplankton to the deep sea benthos. Nature 302, 520 – 522.
Blain, S., Tréguer, P., Belviso, S., Bucciarelli, E., Denis, M., Desabre,
S., Fiala, M., Martin-Jézéquel, V., Le Fèvre, J., Myzaud, P.,
Marty, J.-C., Razouls, S., 2001. A biogeochemical study of the
island mass effect in the context of the iron hypothesis: Kerguelen
Islands, Southern Ocean. Deep-Sea Res. I 48, 163 – 187.
Blasco, D., Packard, T.T., Garfield, P.C., 1982. Size dependence
of growth rate, respiratory electron transport system activity
and chemical composition in marine diatoms in the laboratory.
J. Phycol. 18, 58 – 63.
Boyd, P.W., Muggli, D.L., Varela, D.E., Chretien, R., Goldblatt,
R.H., Orians, K.J., Harrison, P.J., 1996. In vitro iron enrichment and herbivory experiments in the NE subarctic Pacific.
Mar. Ecol. Prog. Ser. 136, 179 – 193.
Boyd, P.W., Goldblatt, R.H., Harrison, P.J., 1999. Mesozooplankton
grazing manipulations during in vitro iron enrichment studies in
the NE subarctic Pacific. Deep-Sea Res. II 46, 2645 – 2668.
Boyd, P.W., Watson, A.J., Law, C.S., Abraham, E.R., Trull, T.,
Murdoch, R., Bakker, D.C.E., Bowie, A., Buesseler, K.O.,
Chang, H., Charette, M., Croot, P., Downing, K., Frew, R., Gall,
M., Hadfield, M., Hall, J., Harvey, M., Jameson, G., LaRoche, J.,
Liddicoat, M., Ling, R., Maldonado, M.T., McKay, R.M.,
Nodder, S., Pickmere, S., Pridmore, R., Rintoul, S., Safi, K.,
Sutton, P., Strzepek, R., Tanneberger, K., Turner, S., Waite, A.,
Zeldis, J., 2000. A mesoscale phytoplankton bloom in the polar
Southern Ocean stimulated by iron fertilization. Nature 407,
695 – 702.
Boyd, P.W., Law, C.S., Wong, C.S., Nojiri, Y., Tsuda, A., Levasseur,
M., Takeda, S., Rivkin, R., Harrison, P.J., Strzepek, R., Gower, J.,
McKay, R.M., Abraham, E., Arychuk, M., Barwell, C.J.,
Crawford, W., Crawford, D., Hale, M., Harada, K., Johnson,
K., Kiyosawa, H., Kudo, I., Marchetti, A., Miller, W., Needoba,
J., Nishioka, J., Ogawa, H., Page, J., Robert, M., Saito, H., Sastri,
A., Sherry, N., Soutar, T., Sutherland, N., Taira, Y., Whitney,
F., Wong, S.K.E., Yoshimura, T., 2004. The decline and fate
of an iron-induced subarctic phytoplankton bloom. Nature
428, 549 – 553.
Bruland, K.W., Rue, E.L., Smith, G.J., 2001. Iron and macronutrients in California coastal upwelling regimes: Implications for
diatom blooms. Limnol. Oceanogr. 46, 1661 – 1674.
Brussaard, C.P.D., Riegman, R., Noordeloos, A.A.M., Cadée, G.C.,
Witte, H., Kop, A.J., Nieuwland, G., Van Duyl, F.C., Bak,
R.P.M., 1995. Effects of grazing, sedimentation, and phytoplankton cell lysis on the structure of a coastal pelagic foodweb.
Mar. Ecol. Prog. Ser. 123, 259 – 271.
Brussaard, C.P.D., Noordeloos, A.A.M., Riegman, R., 1997. Autolysis kinetics of the marine diatom Ditylum brightwellii (Bacillariophyceae) under nitrogen and phosphorus limitation and
starvation. J. Phycol 33, 980 – 987.
G. Sarthou et al. / Journal of Sea Research 53 (2005) 25–42
Brzezinski, M.A., 1985. The Si:C:N ratio of marine diatoms: interspecific variability and the effect of some environmental variables. J. Phycol. 21, 347 – 357.
Brzezinski, M.A., Nelson, D.M., 1988. Differential cell sinking as a
factor influencing diatom species competition for limiting
nutrients. J. Exp. Mar. Biol. Ecol. 119, 179 – 200.
Brzezinski, M.A., Dickson, M.-L., Nelson, D.M., Sambrotto, R.,
2003. Ratios of Si, C, and N uptake by microphytoplankton in
the Southern Ocean. Deep-Sea Res. II 50, 619 – 633.
Bucciarelli, E., Blain, S., Tréguer, P., 2001. Iron and manganese in
the wake of the Kerguelen Islands (Southern Ocean). Mar.
Chem. 73, 21 – 36.
Buck, K.R., Newton, J., 1995. Fecal pellet flux in Dabob Bay
during a diatom bloom: contribution of microzooplankton. Limnol. Oceanogr. 40, 306 – 315.
Buesseler, K.O., 1998. The decoupling of production and particulate export in the surface ocean. Global Biogeochem. Cycles 12,
297 – 310.
Cabal, J.A., Alvarez-Marqués, F., Acuña, J.L., Quevedo, M.,
Gonzalez-Quiros, R., Huskin, I., Fernandez, D., Rodriguez del
Valle, C., Anadon, R., 2002. Mesozooplankton distribution and
grazing during the productive season in the Northwest Antarctic
Peninsula (FRUELA cruises). Deep-Sea Res. II 49, 869 – 882.
Calbet, A., 2001. Mesozooplankton grazing effect on primary production: A global comparative analysis in marine ecosystems.
Limnol. Oceanogr. 46, 1824 – 1830.
Chan, A.T., 1978. Comparative physiological study of marine diatoms and dinoflagellates in relation to irradiance and cell size.
I. Growth under continuous light. J. Phycol. 14, 396 – 402.
Chisholm, S.W., 1992. Phytoplankton size. In: Falkowski, P.G.,
Woodhead, A.D. (Eds.), Primary Production and Biogeochemical Cycles in the Sea. Plenum, New-York, pp. 213 – 237.
Claquin, P., Martin-Jézéquel, V., Kromkamp, J.C., Veldhuis, M.,
Kraay, G., 2002. Uncoupling of silicon compared to carbon
and nitrogen metabolisms, and role of the cell cycle, in continuous cultures of Thalassiosira pseudonana (Bacillariophyceae),
under light, nitrogen, and phosphorus control. J. Phycol. 38,
922 – 930.
Coale, K.H., Fitzwater, S.E., Gordon, R.M., Johnson, K.S., Barber,
R.T., 1996a. Control of community growth and export production by upwelled iron in the equatorial Pacific Ocean. Nature
379, 621 – 624.
Coale, K.H., Johnson, K.S., Fitzwater, S.E., Gordon, R.M., Tanner,
S., Chavez, F.P., Ferioli, L., Sakamoto, C., Rogers, P., Millero,
F., Steinberg, P., Nightingale, P., Cooper, D., Cochlan, W.P.,
Landry, M.R., Constantinou, J., Rollwagen, G., Trasvina, A.,
Kudela, R., 1996b. A massive phytoplankton bloom induced
by an ecosystem-scale iron fertilization experiment in the equatorial Pacific Ocean. Nature 383, 495 – 501.
Coale, K.H., Johnson, K.S., Chavez, F.P., Buesseler, K.O., Barber,
R.T., Brzezinski, M.A., Cochlan, W.P., Millero, F.J., Falkowski,
P.G., Bauer, J.E., Wanninkhof, R.H., Kudela, R.M., Altabet,
M.A., Hales, B.E., Takahashi, T., Landry, M.R., Bidigare,
R.R., Wang, X.J., Chase, Z., Strutton, P.G., Friederich, G.E.,
Gorbunov, M.Y., Lance, V.P., Hilting, A.K., Hiscock, M.R.,
Demarest, M., Hiscock, W.T., Sullivan, K.F., Tanner, S.J., Gordon, R.M., Hunter, C.N., Elrod, V.A., Fitzwater, S.E., Jones,
37
J.L., Tozzi, S., Koblizek, M., Roberts, A.E., Herndon, J., Brewster, J., Ladizinsky, N., Smith, G., Cooper, D., Timothy, D.,
Brown, S.L., Selph, K.E., Sheridan, C.C., Twining, B.S., Johnson, Z.I., 2004. Southern ocean iron enrichment experiment:
Carbon cycling in high- and low-Si waters. Science 304
(5669), 408 – 414.
Cullen, J.J., 1991. Hypotheses to explain high-nutrient conditions in
the open sea. Limnol. Oceanogr. 36, 1578 – 1599.
Cullen, J.J., Lewis, M.R., Davis, C.O., Barber, R.T., 1992. Photosynthesis characteristics and estimated growth rates indicate
grazing is the proximate control of primary production in the
Equatorial Pacific. J. Geophys. Res. 97, 639 – 654.
Dam, H.G., Zhang, X., Butler, M., Roman, M.R.R., 1995. Mesozooplankton grazing and metabolism at the equator in the Central Pacific: Implications for carbon and nitrogen fluxes. DeepSea Res. II 42, 735 – 756.
Davey, M., Geider, R.J., 2001. Impact of iron limitation on the
photosynthetic apparatus of the diatom Chaetoceros muelleri
(Bacillariophyceae). J. Phycol. 37, 987 – 1000.
De Baar, H.J.W., De Jong, J.T.M., Bakker, D.C.E., Löscher, B.M.,
Veth, C., Bathmann, U., Smetacek, V., 1995. Importance of iron
for plankton blooms and carbon dioxide drawdown in the
Southern Ocean. Nature 373, 412 – 415.
De la Rocha, C.L., Hutchins, D.A., Brzezinski, M.A., Zhang, Y.,
2000. Effects of iron and zinc deficiency on elemental composition and silica production by diatoms. Mar. Ecol. Prog. Ser.
195, 71 – 79.
Decho, A.W., 1990. Microbial exopolymer secretions in ocean
environments: their role in food webs and marine processes.
Oceanogr. Mar. Biol. Ann. Rev. 28, 73 – 153.
Donald, K.M., Scanlan, D.J., Carr, N.G., Mann, N.H., Joint, I.,
1997. Comparative phosphorus nutrition of the marine cyanobacterium Synechococus WH7803 and the marine diatom Thalassiosira weissflogii. J. Plankton Res. 19, 1793 – 1814.
Dubischar, C.D., Bathmann, U.V., 1997. Grazing impact of copepods and salps on phytoplankton in the Atlantic sector of the
Southern Ocean. Deep-Sea Res. 44, 415 – 433.
Dugdale, R.C., Wilkerson, F.P., Minas, H.J., 1995. The role of a
silicate pump in driving new production. Deep-Sea Res. I 42,
697 – 719.
Durnford, D.G., Falkowski, P.G., 1997. Chloroplast redox regulation of nuclear gene transcription during photoacclimation. Photosyn. Res. 52, 229 – 241.
Engel, A., 2004. Distribution of transparent exopolymer particles
(TEP) in the northeast Atlantic Ocean and their potential significance for aggregation processes. Deep-Sea Res. 51, 83 – 92.
Entsch, B., Sim, R.G., Hatcher, B.G., 1983. Indications from photosynthetic components that iron is a limiting nutrient in primary
producers on coral reefs. Mar. Biol. 73, 17 – 30.
Eppley, R.W., Sloan, P.R., 1966. Growth rates of marine phytoplankton: correlation with light absorption by cell chlorophyll
a. Physiol. Plant. 19, 47 – 59.
Eppley, R.W., Rogers, J.N., McCarthy, J.J., 1969. Half-saturation
constants for uptake of nitrate and ammonium by marine phytoplancton. Limnol. Oceanogr. 14, 912 – 920.
Falkowski, P.G., Raven, J.A., 1997. Aquatic Photosynthesis Blackwell Science, Malden, Massachussetts.
38
G. Sarthou et al. / Journal of Sea Research 53 (2005) 25–42
Finkel, Z.V., 2001. Light absorption and size scaling of light-limited
metabolism in marine diatoms. Limnol. Oceanogr. 46, 86 – 94.
Finkel, Z.V., Irwin, A.J., 2000. Modeling size-dependent photosynthesis: Light absorption and the allometric rule. J. Theor. Biol.
204, 361 – 369.
Franck, V.M., Brzezinsky, M.A., Coale, K., Nelson, D., 2000. Iron
and silicic acid availability regulate Si uptake in the Pacific
sector of the Southern Ocean. Deep-Sea Res. II 47, 3315 – 3338.
Frost, B.W., 1991. The role of grazing in nutrient-rich areas of the
open sea. Limnol. Oceanogr. 36, 1616 – 1630.
Gall, M.P., Boyd, P.W., Hall, J., Safi, K.A., Chang, H., 2001. Phytoplankton processes: Part 1 Community structure in the Southern Ocean and changes associated with the SOIREE bloom.
Deep-Sea Res. II 48, 2551 – 2570.
Geider, R.J., 1987. Light and temperature dependence of the carbon
to chlorophyll a ratio in microalgae and cyanobacteria: Implications for physiology and growth of phytoplankton. New Phytol.
106, 1 – 34.
Geider, R.J., La Roche, J., 1994. The role of iron in phytoplankton
photosynthesis, and the potential for iron-limitation of primary
productivity in the sea. Photosynthesis Research 39, 275 – 301.
Geider, R.J., La Roche, J., 2002. Redfield revisited: variability of
C:N:P in marine microalgae and its biochemical basis. Eur. J.
Phycol. 37, 1 – 17.
Geider, R.J., Platt, T., Raven, J.A., 1986. Size dependence of
growth and photosynthesis in diatoms: a synthesis. Mar. Ecol.
Prog. Ser. 30, 93 – 104.
Gersonde, R., Barcena, M.A., 1998. Revision of the upper Pliocene-Pleistocene diatom biostratigraphy for the northern belt of
the Southern Ocean. Micropaleontology 44, 84 – 98.
Gledhill, M., van den Berg, C.M.G., 1994. Determination of complexation of iron(III) with natural organic complexing ligands in
seawater using cathodic stripping voltammetry. Mar. Chem. 47,
41 – 54.
Gledhill, M., van den Berg, C.M.G., 1995. Measurement of the
redox speciation of iron in seawater by catalytic cathodic stripping voltammetry. Mar. Chem. 50, 51 – 62.
Goldman, J.C., 1993. Potential role of large diatoms in new primary
production. Deep-Sea Res. I 40, 159 – 168.
Goldman, J.C., McGillicuddy, D.J.J.R., 2003. Effect of large marine
diatoms growing at low light on episodic new production. Limnol. Oceanogr. 48, 1176 – 1182.
Goldman, J.C., Hansell, D.A., Dennett, M.R., 1992. Chemical characterization of three large oceanic diatoms: potential impact on
the water column chemistry. Mar. Ecol. Prog. Ser. 88, 257 – 270.
Gowing, M.M., 2003. Large viruses and infected microeukaryotes in Ross Sea summer pack ice habitats. Mar. Biol.
142, 1029 – 1040.
Green, E.P., Dagg, M.J., 1997. Mesozooplankton associations with
medium to large marine snow aggregates in the northern Gulf of
Mexico. J. Plankton Res. 19, 435 – 447.
Greene, R.M., Geider, R.J., Falkowski, P.G., 1991. Effect of iron
limitation on photosynthesis in a marine diatom. Limnol. Oceanogr. 36, 1772 – 1782.
Hama, T., Handa, N., 1987. Pattern of organic matter production by
natural phytoplankton population in a eutrophic lake: Extracellular products. Arch. Hydrobiol. 109, 227 – 243.
Hansen, P.J., Calado, A.J., 1999. Phagotrophy mechanisms and
prey selection in free-living dinoflagellates. J. Eukaryot. Microbiol. 46, 382 – 389.
Harrison, P.J., Turpin, D.H., Bienfang, P.K., Davis, C.O., 1986.
Sinking as a factor affecting phytoplankton species succession:
the use of selective loss semi-continuous cultures. J. Exp. Mar.
Biol. Ecol. 99, 19 – 30.
Hein, M., Pedersen, M.F., Sand-Jensen, K., 1995. Size-dependent
nitrogen uptake in micro- and macroalgae. Mar. Ecol. Prog. Ser.
118, 247 – 253.
Henley, W.J., 1993. Measurements and interpretation of photosynthesis light-response curves in algae in the context of photoinhibition and diel changes. J. Phycol. 29, 729 – 745.
Honjo, T., 1982. Seasonality and interaction of biogenic and
lithogenic particulate flux at the Panama Basin. Science
218, 883 – 884.
Hutchins, D.A., Bruland, K.W., 1998. Iron-limited diatom growth
and Si:N uptake ratios in a coastal upwelling regime. Nature
393, 561 – 564.
Hutchins, D.A., DiTullio, G.R., Zhang, Y., Bruland, K.W., 1998.
An iron limitation mosaic in the California upwelling regime.
Limnol. Oceanogr. 43, 1037 – 1054.
Hutchins, D.A., Witter, A.E., Butler, A., Luther III, G.W., 1999.
Competition among marine phytoplankton for different chelated
iron species. Nature 400, 858 – 861.
Hutchinson, G.E., 1967. A Treatise on Limnology. Introduction to
Lake Biology and Limnoplankton. John Wiley and Sons, New
York.
Ianora, A., Miralto, A., Poulet, S.A., 1999. Are diatoms good or
toxic for copepods? Reply to comment by Jònasdòttir et al. Mar.
Ecol. Prog. Ser. 177, 305 – 308.
Irigoien, X., Head, R.N., Harris, R.P., Cummings, D., Harbour, D.,
Meyer-Harms, B., 2000. Feeding selectivity and egg production
of Calanus helgolandicus in the English Channel. Limnol. Oceanogr. 45, 44 – 54.
Jackson, G.A., 1990. A model of the formation of marine algal
flocs by physical coagulation processes. Deep-Sea Res. I 37,
1197 – 1211.
Jackson, G.A., 1993. Flux feeding as a mechanism for zooplankton
grazing and its implication for vertical flux. Limnol. Oceanogr.
38, 1328 – 1331.
Jackson, G.A., Lochmann, S.E., 1992. Effect of coagulation on
nutrient and light limitation of an algal bloom. Limnol. Oceanogr. 37, 77 – 89.
Jacobson, D.M., Anderson, D.M., 1986. Thecate heterotrophic
dinoflagellates: feeding behavior and mechanisms. J. Phycol.
22, 249 – 258.
Johnson, K.S., Gordon, R.M., Coale, K.H., 1997. What controls
dissolved iron concentrations in the world ocean? Mar. Chem.
57, 137 – 161.
Kemp, A.E.S., Pike, J., Pearce, R.B., Lange, C.B., 2000. The ‘‘fall
dump’’: a new perspective on the role of a ‘‘shade flora’’ in the
annual cycle of diatom production and export flux. Particle flux
and its preservation in deep-sea sediments. Deep-Sea Res. II 47,
2129 – 2154.
Kiørboe, T., Hansen, J.L.S., 1993. Phytoplankton aggregate formation: Observations of patterns and mechanisms of cell sticking
G. Sarthou et al. / Journal of Sea Research 53 (2005) 25–42
and the significance of exopolymeric material. J. Plankton Res.
15, 993 – 1018.
Kiørboe, T., Andersen, K.P., Dam, H.G., 1990. Coagulation efficiency and aggregate formation in marine phytoplankton. Mar.
Biol. 107, 235 – 245.
Kiørboe, T., Hansen, J.L.S., Alldredge, A.L., Jackson, G.A., Passow, U., Dam, H.G., Drapeau, D.T., Waite, A., Garcia, C.M.,
1996. Sedimentation of phytoplankton bloom during a diatom
bloom: rates and mechanisms. J. Mar. Res. 54, 1123 – 1148.
Kiørboe, T., Tiselius, P., Mitchell-Innes, B., Hansen, J.L.S., Visser,
A.W., Mari, X., 1998. Intensive aggregate formation with low
vertical flux during an upwelling-induced diatom bloom. Limnol. Oceanogr. 43, 104 – 116.
Kirchman, D.L., 1999. Phytoplankton death in the sea. Nature 398,
293 – 294.
Kirk, J.T.O., 1994. Light and Photosynthesis in Aquatic systems
Cambridge University Press, Cambridge, UK.
Klepplel, G.S., 1993. On the diets of calanoid copepods. Mar. Ecol.
Prog. Ser. 99, 183 – 195.
Klepplel, G.S., Holliday, D.V., Pieper, R.E., 1991. Trophic interactions between copepods and microplankton: a question about the
role of diatoms. Limnol. Oceanogr. 36, 172 – 178.
Kranck, K., Milligan, T.G., 1988. Macroflocs from diatoms: in situ
photography of particles in Bedford basin, Nova Scotia. Mar.
Ecol. Prog. Ser. 44, 183 – 189.
Kudo, I., Miyamoto, M., Noiri, Y., Maita, Y., 2000. Combined
effect of temperature and iron on the growth and physiology
of the marine diatom Phaeodactylum tricornutum (Bacillariophyceae). J. Phycol. 36, 1096 – 1102.
La Roche, J., Geider, R.J., Graziano, L.M., Murray, H., Lewis, K.,
1993. Induction of specific proteins in eukaryotic algae grown
under iron-, phosphorus-, or nitrogen-deficient conditions. J.
Phycol. 29, 767 – 777.
La Roche, J., Boyd, P.W., McKay, M.L., Geider, R.J., 1996. Flavodoxin as an in situ marker for iron stress in phytoplankton.
Nature 382, 802 – 805.
La Roche, J., McKay, R.M.L., Boyd, P., 1999. Immunological and
molecular probes to detect phytoplankton responses to environmental stress in nature. Hydrobiologia 401, 177 – 198.
Lancelot, C., Hannon, E., Becquevort, S., Veth, C., De Baar, H.J.W.,
2000. Modeling phytoplankton blooms and carbon export production in the Southern Ocean: dominant controls by light and
iron in the Atlantic sector in Austral spring 1992. Deep-Sea Res.
47, 1621 – 1662.
Landry, M.R., Barber, R.T., Bidigare, R.R., Chai, F., Coale, K.H.,
Dam, H.G., Lewis, M.R., Lindley, S.T., McCarthy, J.J., Roman,
M.R., Stoecker, D.K., Verity, P.G., White, J.R., 1997. Iron and
grazing constraints on primary production in the central equatorial Pacific: an EqPac synthesis. Limnol. Oceanogr. 42, 405 – 418.
Landry, M.R., Constantinou, J., Latasa, M., Brown, S.L., Bidigare,
R.R., Ondrusek, M.E., 2000a. Biological response to iron fertilisation in the eastern equatorial Pacific (IronEx II). III. Dynamics
of phytoplankton growth and microzooplankton grazing. Mar.
Ecol. Prog. Ser. 207, 57 – 72.
Landry, M.R., Ondrusek, M.E., Tanner, S.J., Brown, S.L., Constantinou, J., Bidigare, R.R., Coale, K.H., Fitzwater, S., 2000b.
Biological response to iron fertilisation in the eastern equatorial
39
Pacific (IronEx II). I. Microplankton community abundances
and biomass. Mar. Ecol. Prog. Ser. 201, 27 – 42.
Langdon, C., 1988. On the causes of interspecific differences in the
growth-irradiance relationship of three marine phytoplankton
species: Skeletonema costatum, Olisthodiscus luteus, Gonyaulax
tamarensis. J. Plankton Res. 10, 1291 – 1312.
Levitus, S., Conkright, M.E., Reid, J.L., Najjar, R.G., Mantyla, A.,
1993. Distribution of nitrate, phosphate and silicate in the world
ocean. Prog. Oceanogr. 31, 245 – 273.
Leynaert, A., Bucciarelli, E., Claquin, P., Dugdale, R.C., MartinJézéquel, V., Pondaven, P., Ragueneau, O., 2004. Effect of iron
deficiency on diatom cell size and silicic acid uptake kinetics.
Limnol. Oceanogr. 49, 1134 – 1143.
Logan, B.E., Passow, U., Alldredge, A.L., Grossart, H.-P., Simon,
M., 1995. Rapid formation and sedimentation of large aggregates is predictable from coagulation rates (half-lives) of transparent exopolymer particles (TEP). Deep-Sea Res. II 42, 203 – 214.
MacIntyre, H.L., Kana, T.M., Anning, J., Geider, R., 2002. Photoacclimation of photosynthesis irradiance response curves
and photosynthetic pigments in microalgae and cyanobacteria.
J. Phycol. 38, 17 – 38.
Maldonado, M.T., Price, N.M., 1996. Influence of N substrate on Fe
requirements of marine centric diatoms. Mar. Ecol. Prog. Ser.
141, 161 – 172.
Maldonado, M.Y., Price, N.M., 1999. Utilization of iron bound to
strong organic ligands by plankton communities in the subarctic
Pacific Ocean. Deep-Sea Res. II 46, 2447 – 2473.
Maldonado, M.T., Boyd, P.W., La Roche, J., Strezepek, R., Waite,
A.M., Bowie, A.R., Croot, P.L., Frew, R.D., Price, N.M., 2001.
Iron uptake and physiological response of phytoplankton during
a mesoscale Southern Ocean iron enrichment. Limnol. Oceanogr. 46, 1802 – 1808.
Mann, D.G., 1999. The species concept in diatoms. Phycologia 38,
437 – 495.
Maranger, R., Bird, D.F., Price, N.M., 1998. Iron acquisition by
photosynthetic marine phytoplankton from ingested bacteria.
Nature 396, 248 – 251.
Martin, J.H., Fitzwater, S.E., 1988. Iron deficiency limits phytoplankton growth in the north-east Pacific subarctic. Nature 331,
341 – 343.
Martin, J.H., Coale, K.H., Johnson, K.S., Fitzwater, S.E., Gordon,
R.M., Tanner, S.J., Hunter, C.N., Elrod, V.A., Nowiicki, J.L.,
Coley, T.L., Barber, R.T., Lindley, S., Watson, A.J., Van Scoy,
K., Law, C.S., Liddicoat, M.I., Ling, R., Stanton, T., Stockel, J.,
Collins, C., Anderson, A., Bidigare, R., Ondrusek, M., Latasa,
F.J., Millero, F.J., Lee, K., Yao, W., Zhang, J.Z., Friederich, G.,
Sakamoto, C., Chavez, F., Buck, K., Kolber, Z., Greene, R.,
Falkowski, P., Chisholm, S.W., Hoge, F., Swift, R., Yungel, J.,
Turner, S., Nightingale, P., Hatton, A., Liss, P., Tindale, N.W.,
1994. Testing the iron hypothesis in ecosystems of the equatorial
Pacific Ocean. Nature 371, 123 – 129.
Martin-Jézéquel, V., Hildebrand, M., Brzezinski, M., 2000. Silicon
metabolism in diatoms: implications for growth. J. Phycol. 36,
1 – 20.
McCave, I.N., 1984. Size spectra and aggregation of suspended
particles in the deep ocean. Deep-Sea Res. 31, 329 – 352.
McKay, R.M.L., La Roche, J., Yakunin, A.F., Durnford, D.G.,
40
G. Sarthou et al. / Journal of Sea Research 53 (2005) 25–42
Geider, R.J., 1999. Accumulation of Ferrodoxin and Flavodoxin
in a marine diatom in response to Fe. J. Phycol. 35, 510 – 519.
McKay, R.M.L., Villareal, T.A., La Roche, J., 2000. Vertical migration by Rhizosolenia spp. (Bacillariophyceae): Implications
for Fe acquisition. J. Phycol. 36, 669 – 674.
Measures, C.I., Vink, S., 1999. Seasonal variations in the distribution of Fe and Al in the surface waters of the Arabian Sea. DeepSea Res. II 46, 1597 – 1622.
Milligan, A.J., Harrison, P.J., 2000. Effects of non-steady-state iron
limitation on nitrogen assimilatory enzymes in the marine diatom Thalassiosira weissflogii (Bacillariophyceae). J. Phycol. 36,
78 – 86.
Miralto, A., Barone, G., Romano, G., Poulet, S.A., Ianora, A.,
Russo, G.L., Buttino, I., Mazzarella, G., Laabir, M., Cabrini,
M., Giacobbe, M.G., 1999. The insidious effect of diatoms on
copepod reproduction. Nature 402, 173 – 176.
Monod, J., 1942. Recherche sur la croissance des cultures bactériennes. Actualités scientifiques et industrielles. Annu. Rev.
Micriobiol. 3, 3 – 71.
Moore, J.K., Villareal, T.A., 1996. Size-ascent rate relationships in
positively buoyant marine diatoms. Limnol. Oceanogr. 41,
1514 – 1520.
Morel, F.M.M., 1987. Kinetics of nutrient uptake and growth in
phytoplankton. J. Phycol. 23, 137 – 150.
Morel, F.M.M., Rueter, J.G., Anderson, D.M., Guillard, R.L.L.,
1979. Aquil: a chemically defined phytoplankton culture medium for trace metal studies. J. Phycol. 15, 135 – 141.
Morel, F.M.M., Hudson, R.J.M., Price, N.M., 1991a. Limitation of
productivity by trace metals in the sea. Limnol. Oceanogr. 36,
1742 – 1755.
Morel, F.M.M., Rueter, J.G., Price, N.M., 1991b. Iron nutrition of
phytoplankton and its possible importance in the ecology of
ocean regions with High Nutrient and Low Biomass. Oceanography 4, 56 – 61.
Muggli, D.L., Harrison, P.J., 1997. Effects of iron on two oceanic
phytoplankters grown in natural NE subarctic pacific seawater
with no artificial chelators present. J. Exp. Mar. Biol. Ecol. 212,
225 – 237.
Muggli, D.L., Lecourt, M., Harrison, P.J., 1996. Effects of iron and
nitrogen source on the sinking rate, physiology and metal composition of an oceanic diatom from the subarctic Pacific. Mar.
Ecol. Prog. Ser. 132, 215 – 227.
Nejstgaard, J.C., Gismervik, I., Solberg, P.T., 1997. Feeding and
reproduction by Calanus finmarchicus, and microzooplankton
grazing during mesocosm blooms of diatoms and the coccolithophore Emiliania huxleyi. Mar. Ecol. Prog. Ser. 147,
197 – 218.
Nelson, D.M., Tréguer, P., Brzezinski, M.A., Leynaert, A., Quéguiner, B., 1995. Production and dissolution of biogenic silica
in the ocean. Revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Global Biogeochem. Cycles 9, 359 – 372.
Olson, M.B., Strom, S.L., 2002. Phytoplankton growth, microzooplankton herbivory and community structure in the southeast Bering Sea: insight into the formation and temporal
persistence of an Emiliania huxleyi bloom. Deep-Sea Res. II
49, 5969 – 5990.
Passow, U., 2002. Transparent exopolymer particles (TEP) in aquatic environments. Prog. Oceanogr. 55, 287 – 333.
Passow, U., Alldredge, A.L., Logan, B.E., 1994. The role of particulate carbohydrate exudates in the flocculation of diatom
blooms. Deep-Sea Res. I 41, 335 – 357.
Passow, U., Shipe, R.F., Murray, A., Pak, D.K., Brzezinski, M.A.,
Alldredge, A.L., 2001. The origin of transparent exopolymer
particles (TEP) and their role in the sedimentation of particulate
matter. Cont. Shelf Res. 21, 327 – 346.
Platt, T., Gallegos, C.L., Harrison, W.G., 1980. Photoinhibition of
photosynthesis in natural assemblages of marine phytoplankton.
J. Mar. Res. 38, 687 – 701.
Poulet, S.A., Ianora, A., Miralto, A., Meijer, L., 1994. Do diatoms
arrest embryonic development in copepods? Mar. Ecol. Prog.
Ser. 111, 79 – 86.
Poulet, S.A., Laabir, M., Ianora, A., Miralto, A., 1995. Reproductive response of Calanus helgolandicus. Abnormal embryonic
and naupliar development. Mar. Ecol. Prog. Ser. 129, 85 – 95.
Price, N.M., Ahner, B.A., Morel, F.M.M., 1994. The equatorial
Pacific Ocean: Grazer-controlled phytoplankton population in
an iron-limited ecosystem. Limnol. Oceanogr. 39, 520 – 534.
Pudsey, C.J., King, P., 1997. Particle fluxes, benthic processes and
the paleoenvironmental record in the Northern Weddell Sea.
Deep-Sea Res. I 44, 1841 – 1876.
Ragueneau, O., Tréguer, P., Leynaert, A., Anderson, R.F., Brzezinski, M.A., DeMaster, D.J., Dugdale, R.C., Dymond, J., Fischer,
G., Francois, R., Heinze, C., Maier-Reimer, E., Martin-Jézéquel,
V., Nelson, D.M., Quéguiner, B., 2000. A review of the Si cycle
in the modern ocean: recent progress and missing gaps in the
application of biogenic opal as a paleoproductivity proxy. Global Planet Change 26, 317 – 365.
Raven, J., 1986. Physiological consequences of extremely small
size for autotrophic organisms in the sea. In: Platt, T., Li,
W.K.W. (Eds.), Photosynthetic Picoplankton. Can. Bull. Fish.
Aq. Sci., vol. 214, pp. 1 – 70.
Raven, J.A., 1984. A cost-benefit analysis of photon absorption by
photosynthetic unicells. New Phytol. 98, 593 – 625.
Raven, J.A., 1988. The iron and molybdenum use efficiencies of
plant growth with different energy, carbon and nitrogen sources.
New Phytol. 109, 279 – 287.
Raven, J.A., 1990. Predictions of Mn and Fe use efficiencies of
plant growth with different energy, carbon and nitrogen sources.
New Phytol. 109, 279 – 287.
Raven, J.A., Kübler, J.E., 2002. New light on the scaling of metabolic rate with the size of algae. J. Phycol. 38, 11 – 16.
Redfield, A.C., Ketchum, B.H., Richards, F.A., 1963. The influence
of organisms on the composition of seawater. In: Hill, M.N.
(Ed.), The Sea, vol. 2. The Composition of Seawater. Wiley,
New York, pp. 26 – 77.
Riebesell, U., 1991. Particle aggregation during a diatom bloom.
II. Biological aspect. Mar. Ecol. Prog. Ser. 69, 281 – 291.
Riebesell, U., 1992. The formation of large marine snow and its
sustained residence in surface waters. Limnol. Oceanogr. 37,
63 – 76.
Riebesell, U., Wolf-Gladrow, D.A., 1992. The relationship between
physical aggregation of phytoplankton and particle flux: a numerical model. Deep-Sea Res. I 38, 1085 – 1102.
G. Sarthou et al. / Journal of Sea Research 53 (2005) 25–42
Rivkin, R.B., Swift, E., 1982. Phosphate uptake by the oceanic
dinoflagellate Pyrocystis noctiluca. J. Phycol. 118, 113 – 120.
Roman, M., Smith, S., Wishner, K., Zhang, X., Gowing, M., 2000.
Mesozooplankton production and grazing in the Arabian Sea.
The 1994 – 1996 Arabian Sea Expedition: Oceanic Response to
Monsoonal Forcing, Part 3. Deep-Sea Res. II 47, 1423 – 1450.
Rue, E.L., Bruland, K.W., 1995. Complexation of iron(III) by natural organic ligands in the Central North Pacific as determined
by a new competitive ligand equilibration/adsorptive cathodic
stripping voltammetric method. Mar. Chem. 50, 117 – 138.
Schmidt, M.A., Zhang, Y., Hutchins, D.A., 1999. Assimilation of
Fe and carbon by marine copepods from Fe-limited and Fereplete diatom prey. J. Plankton Res. 21, 1753 – 1764.
Schöne, H.K., 1982. The influence of light and temperature on the
growth rates of six phytoplankton species from the upwelling
area off nortwest Africa. Rapp. P.-V. Réun. Cons. Int. Explor.
Mer. 180, 246 – 253.
Shin, K., Jang, M.-C., Jang, P.-K., Ju, S.-J., Lee, T.-K., Chang, M.,
2003. Influence of food quality on egg production and viability
of the marine planktonic copepod Acartia omorii. Prog. Oceanogr. 57, 265 – 277.
Smayda, T.J., 1970. The suspension and sinking of phytoplankton
in the Sea. Oceanogr. Mar. Biol. A Rev. 8, 353 – 414.
Smetacek, V., 1985. Role of sinking in diatom life-history cycles:
ecological, evolutionary and geological significance. Mar. Biol.
84, 239 – 251.
Smetacek, V., 1999. Diatoms and the ocean carbon cycle. Protist
150, 25 – 32.
Smetacek, V., 2001. EisenEx: international team conducts iron experiment in Southern Ocean. US JGOFS Newsletter January,
11 – 14.
Smith, R.E.H., Kalff, J., 1982. Size-dependent phosphorus uptake
kinetics and cell quota in phytoplankton. J. Phycol. 18, 275 – 284.
Soria-Dengg, S., Horstmann, U., 1995. Ferrioxamines B and E as
iron sources for the diatom Phaeodactylum tricornotum. Mar.
Ecol. Prog. Ser. 127, 269 – 277.
Sosik, H.M., Olson, R.J., 2002. Phytoplankton and iron limitation
of photosynthetic efficiency in the Southern Ocean during late
summer. Deep-Sea Res. I 49, 1195 – 1216.
Sosik, H.M., Chisholm, S.W., Olsen, R.J., 1989. Chlorophyll fluorescence from single cells: interpretation of flow cytometric
signals. Limnol. Oceanogr. 34, 1749 – 1761.
Spiller, S.C., Castelfranco, A.M., Castelfranco, P.A., 1982. Effect of
iron and oxygen on chlorophyll biosynthesis I. In vivo observation of iron and oxygen-deficient plants. Plant Physiol. 69,
107 – 111.
Stachanowitsch, M., Fanuko, N., Richter, M., 1990. Mucus aggregates in the Adriatic Sea: An overview of types and occurrence.
Mar. Ecol. 11, 327 – 350.
Starr, M., Runge, A., Therriault, J.-C., 1999. Effects of diatom diets
on the reproduction of planktonic copepod Calanus finmarchicus. Sarsia 84, 379 – 389.
Stefels, J., Van Leeuwe, M.A., 1998. Effects of iron and light
stress on the biochemical composition of Antarctic Phaeocystis
sp. (Prymnesiophyceae). I. Intracellular DMSP concentrations.
J. Phycol. 34, 486 – 495.
Strom, S.L., Brainard, M.A., Holmes, J.L., Olson, M.B., 2001.
41
Phytoplankton blooms are strongly impacted by microzooplankton grazing in coastal North Pacific waters. Mar. Biol. 138,
355 – 368.
Sunda, W.G., Huntsman, S.A., 1995. Iron uptake and growth limitation in oceanic and coastal phytoplankton. Mar. Chem. 50,
189 – 206.
Sunda, W.G., Swift, D.G., Huntsman, S.A., 1991. Low iron requirement for growth in oceanic phytoplankton. Nature 351,
55 – 57.
Suzuki, K., Tsuda, A., Kiyosawa, H., Takeda, S., Nishioka, J.,
Saino, T., Takahashi, M., Wong, C.S., 2002. Grazing impact
of microzooplankton on a diatom bloom in a mesocosm as
estimated by pigment-specific dilution technique. J. Exp. Mar.
Biol. Ecol. 271, 99 – 120.
Takahashi, K., 1986. Seasonal fluxes of pelagic diatoms in the
subarctic Pacific, 1982 – 1983. Deep-Sea Res. 33, 1225 – 1251.
Takeda, S., 1998. Influence of iron availability on nutrient consumption ratio of diatoms in oceanic waters. Nature 393,
774 – 777.
Takeda, S., Tsuda, A., Saito, H., Nojiri, Y., Nishioka, J., Kudo, I.,
Shiomoto, A., Tsumune, D., 2002. Biogeochemical Processes
during the Subarctic Pacific Iron Experiment Dynamics Study
(SEEDS). AGU-ASLO Ocean Sciences Meeting, Abstract
OS31J-06.
Tang, E.P.Y., 1995. The allometry of algal growth rates. J. Plankton
Res. 17, 1325 – 1335.
Tang, K.W., Dam, H.G., 2001. Phytoplankton inhibition of copepod
egg hatching: test of an exudate hypothesis. Mar. Ecol. Prog.
Ser. 209, 197 – 202.
Thornton, D.C.O., 2002. Diatom aggregation in the sea: mechanisms and ecological implications. Eur. J. Phycol. 37,
149 – 161.
Timmermans, K.R., Gerringa, L.J.A., De Baar, H.J.W., Van der
Wagt, B., Veldhuis, M.J.W., De Jong, J.T.M., Croot, P.L.,
2001. Growth rates of large and small Southern Ocean diatoms
in relation to availability of iron in natural seawater. Limnol.
Oceanogr. 46, 260 – 266.
Timmermans, K.R., Van der Wagt, B., De Baar, H.J.W., in press.
Growth rates, half saturation constants, and silicate, nitrate and
phosphate depletion in relation to iron availability of four large,
open ocean diatoms from the Southern Ocean. Limnol. Oceanogr.
Tréguer, P., Pondaven, P., 2000. Silica control of carbon dioxide.
Nature 406, 358 – 359.
Tréguer, P., Nelson, D.M., van Bennekom, J.V., DeMaster, D.J.,
Leynaert, A., Quéguiner, B., 1995. The silica balance in the
world Ocean: a reestimate. Science 268, 375 – 379.
Urban-Rich, J., Dagg, M., Peterson, J., 2001. Copepod grazing on
phytoplankton in the Pacific sector of the Antarctic Polar Front.
Deep-Sea Res. II 48, 4223 – 4246.
Uye, S., 1996. Induction of reproductive failure in the planktonic
copepod Calanus pacificus by diatoms. Mar. Ecol. Prog. Ser.
133, 89 – 97.
Veldhuis, M.J.W., Kraay, G.W., 2004. Phytoplankton in the subtropical Atlantic Ocean: towards a better assessment of biomass
and composition. Deep-Sea Res. I 51 (4), 507 – 530.
Veldhuis, M.J.W., Kraay, G.W., Timmermans, K.R., 2001. Cell
death in phytoplankton: correlation between changes in mem-
42
G. Sarthou et al. / Journal of Sea Research 53 (2005) 25–42
brane permeability, photosynthetic activity, pigmentation and
growth. Eur. J. Phycol. 13, 167 – 177.
Verity, P.G., Stoecker, D.K., Sieracki, M.E., Nelson, J.R., 1996a.
Microzooplankton grazing of primary production at 140jW in
the Equatorial Pacific. Deep-Sea Res. II 43, 1227 – 1255.
Verity, P.G., Stoecker, D.K., Sieracki, T.M.E., Nelson, J.R., Murray,
J.W.E., 1996b. Microzooplankton grazing of primary production
at 140jW in the equatorial Pacific. A US JGOFS process study in
the equatorial pacific. Deep-Sea Res. II 43, 1227 – 1255.
Villareal, T.A., 1988. Positive buoyancy in the oceanic diatom Rhizosolenia debyana. Deep-Sea Res. I 35, 1037 – 1045.
Villareal, T.A., 1992. Buoyancy properties of the giant diatom Ethmodiscus. J. Plankton Res. 14 (3), 459 – 463.
Villareal, T.A., Altabet, M.A., Rymszak, C., 1993. Nitrogen transport by vertically migrating diatom mats in the North Pacific
Ocean. Nature 363, 709 – 712.
Villareal, T.A., Joseph, L., Brzezinski, M.A., Shipe, R.F., Lipschultz, F., Altabet, M.A., 1999a. Biological and chemical characteristics of the giant diatom Ethmodiscus (Bacillariophyceae)
in the central North Pacific Gyre. J. Phycol. 35, 896 – 902.
Villareal, T.A., Pilskaln, C., Brzezinski, M., Lipschultz, F., Dennett,
M., Gardner, G., 1999b. Upward transport of oceanic nitrate by
migrating diatom mats. Nature 397, 423 – 425.
Waite, A.M., Nodder, S.D., 2001. The effect of in-situ iron addition
on the sinking rates and export flux of Southern Ocean diatoms.
Deep-Sea Res. II 48, 2635 – 2654.
Waite, A.M., Thompson, P.A., Harrison, P.J., 1992. Does energy
control the sinking rates of marine diatoms? Limnol. Oceanogr.
37, 468 – 477.
Wassmann, P., Hansen, L., Andreassen, I.J., Riser, C.W., UrbanRich, J., 1999. Distribution and sedimentation of faecal pellets
on the Nordvestbanken shelf, northern Norway, in 1994. Sarsia
84, 239 – 252.
Watson, A.J., Bakker, D.C.E., Ridgwell, A.J., Boyd, P.W., Law,
C.S., 2000. Effect of iron supply on Southern Ocean CO2
uptake and implications for glacial atmospheric CO2. Nature
407, 730 – 733.
Webb, W.L., Newton, M., Starr, D., 1974. Carbon dioxide exchange
of Alnus rubra: A mathematical model. Oecologia 17, 281 – 291.
Williams, P.J., 1990. The importance of losses during microbial
growth: Commentary on the physiology, measurements and
ecology of the release of dissolved organic material. Mar.
Microb. Food Webs 4, 175 – 206.
Williams, R.B., 1964. Division rates of salt marsh diatoms in relation to salinity and cell size. Ecology 45, 877 – 880.
Zeldis, J., 2001. Mesozooplankton community composition, grazing, nutrition, and export production at the SOIREE site. DeepSea Res. II 48, 2615 – 2634.