Biogeosciences, 7, 1075–1097, 2010
© Author(s) 2010. This work is distributed under
the Creative Commons Attribution 3.0 License.
Iron biogeochemistry across marine systems – progress from the
E. Breitbarth1,2, E. P. Achterberg3, M. V. Ardelan4, A. R. Baker5, E. Bucciarelli6,7, F. Chever6,7, P. L. Croot8,
S. Duggen9, M. Gledhill3, M. Hassell¨ ov2, C. Hassler10, L. J. Hoffmann1,11, K. A. Hunter1, D. A. Hutchins12, J. Ingri13,
T. Jickells5, M. C. Lohan14, M. C. Nielsd´ ottir3, G. Sarthou6,7, V. Schoemann15, J. M. Trapp16, D. R. Turner2, and
1Department of Chemistry, University of Otago, Dunedin, New Zealand
2Department of Chemistry, University of Gothenburg, Gothenburg, Sweden
3National Oceanography Center Southampton, University of Southampton, Southampton, UK
4Norwegian University of Science and Technology, Department of Chemistry, Trondheim, Norway
5School of Environmental Sciences, University of East Anglia, Norwich, UK
6Universit´ e Europ´ eenne de Bretagne, France
7Universit´ e de Brest, CNRS, IRD, UMR 6539 LEMAR, IUEM, Plouzan´ e, France
8IFM-GEOMAR, Leibniz-Institute of Marine Sciences, Division Marine Biogeochemistry, Kiel Germany
9IFM-GEOMAR, Leibniz-Institute of Marine Sciences, Division Dynamics of the Ocean Floor, Kiel, Germany
10Centre for Australian Weather and Climate Research (CAWCR), Hobart, TAS, Australia
11Department of Plant and Environmental Sciences, University of Gothenburg, Gothenburg, Sweden
12Department of Biological Sciences, University of Southern California, Los Angeles, CA, USA
13Lule˚ a University of Technology, Division of Applied Geology, Lule˚ a, Sweden
14Marine Institute, University of Plymouth, Plymouth, UK
15Ecologie des Syst` emes Aquatiques, Universit´ e Libre de Bruxelles, Bruxelles, Belgium
16University of Miami, Rosenstiel School of Marine and Atmospheric Science, Department of Marine and Atmospheric
Chemistry, Miami, USA
17Alfred Wegener Institute for Polar and Marine Research, Bremerhaven, Germany
Received: 31 May 2009 – Published in Biogeosciences Discuss.: 7 July 2009
Revised: 20 January 2010 – Accepted: 31 January 2010 – Published: 19 March 2010
Abstract. Based on an international workshop (Gothenburg,
14–16 May 2008), this review article aims to combine in-
terdisciplinary knowledge from coastal and open ocean re-
search on iron biogeochemistry. The major scientific find-
ings of the past decade are structured into sections on natural
and artificial iron fertilization, iron inputs into coastal and
estuarine systems, colloidal iron and organic matter, and bio-
logical processes. Potential effects of global climate change,
particularly ocean acidification, on iron biogeochemistry are
discussed. The findings are synthesized into recommenda-
tions for future research areas.
Correspondence to: E. Breitbarth
An international workshop addressing the biogeochemistry
of iron in the context of global change across marine ecosys-
tems was held in Gothenburg, Sweden (14–16 May 2008).
Largely driven by geographic separation, iron biogeochem-
istry in the open ocean and in coastal seas are often addressed
as two distinct fields and the workshops organized over the
past two decades have normally either been system- or task-
specific. This has led to the development of system-specific
expertise and research approaches, with potential separation
of know-how. The aim of this workshop was to conduct
a broader cross-system review of marine iron biogeochem-
istry by bringing together scientists from a wide range of
coastal, shelf and deep-ocean environments to merge their
system-specific knowledge into a truly cross-disciplinary and
cross-system synthesis. This lead article is an attempt to
Published by Copernicus Publications on behalf of the European Geosciences Union.
1076 E. Breitbarth et al.: Iron biogeochemistry across marine systems – progress from the past decade
summarize the scientific milestones of the past 10 years dis-
cussed during the workshop.
The Gothenburg workshop was convened almost ten years
after a workshop meeting in Amsterdam, sponsored by
SCOR and IUPAC which formed the basis for the book “The
Biogeochemistry of Iron in Seawater” (Turner and Hunter,
2001). The Gothenburg workshop revisited the topics listed
in the “Summary and Recommendations” of this book and
took up two further cross-cutting aspects: (A) What can
we learn from comparing Fe biogeochemistry in coastal and
open ocean systems? And (B), how are global change pro-
cesses expected to affect Fe biogeochemistry?
This article aims to synthesize the cross-system and inter-
disciplinary knowledge from atmospheric, chemical, biolog-
ical, and geological angles discussed during the Gothenburg
workshop and ties the manuscripts of the special issue “Iron
biogeochemistry across marine systems at changing times”
into this overall context. Due to this wide range of topics,
it is not intended to be a comprehensive, in-depth review on
all aspects of marine iron biogeochemistry. We follow the
structure of the workshop topics, which were: Natural Fe
fertilization (Sect. 2, articles: Ardelan et al., 2010; Chever et
al., 2010; Duggen et al., 2010; Ye et al., 2009); artificial Fe
fertilization (3: Bucciarelli et al., 2010; Chever et al., 2010);
Fe inputs into coastal and estuarine systems (4: Gelting et
al., 2009; Breitbarth et al., 2009); Colloidal iron and organic
matter (5); Linking biological processes to iron chemistry (6:
Breitbarth et al., 2009; Bucciarelli et al., 2010; Hassler and
Schoemann, 2009; Steigenberger et al., 2010); and Iron and
ClimateChange(7: Breitbarthetal., 2010; Roseetal., 2009).
Each section concludes with recommendations for future re-
2 Natural iron fertilization
The past decade brought major advances in the understand-
ing of natural iron fertilization processes to the open ocean.
The field is generally subdivided into two major areas: at-
mospheric deposition with the main focus on dust deposition
from the continents and more recently addressing volcanic
ash and pumice depositions; and marine processes, where
particular areas of interest have been ice melting, hydrother-
mal vents, continental margins, and the island mass effects.
2.1 Atmospheric deposition – dust
Over the last 10 years, the importance of dust transport and
deposition within the Earth System has become clear (Jick-
ells et al., 2005). This includes the role of dust in transport-
ing iron to the oceans, but also the transport of nutrients to
land and impacts on albedo. Dust supply is episodic and pre-
dominantly from desert regions, and satellite advances have
allowed these sources to be better characterized (Prospero
et al., 2002). These satellite advances also allow some im-
provement in understanding of dust transport and deposition,
but this is still limited to high dust regions where the total
aerosol is dominated by dust (Mahowald et al., 2005). In re-
gions remote from the desert sources, aerosols may be dom-
inated by sea and acid salts. Furthermore close to a source
region, particularly over the ocean off North Africa, the dust
is transported at altitude, so the satellite detection of a dust
plume, does not necessarily imply deposition to the oceans
at that location (Mahowald et al., 2005). Since dust trans-
port is episodic, field data to validate models and provide di-
rect estimates of dust loading should ideally cover periods of
months to years. Obviously though, shorter campaign style
measurements can be useful for studying processes, and if
repeated can provide long term average concentrations. The
number of long-term dust monitoring stations is still very
limited and broadly the same as identified in Jickells and
Spokes (2001). This data set is dominated by the Prospero
network (e.g. Ginoux et al., 2004), and the lack of data in the
low dust regions, where ocean euphotic zone iron limitation
is evident, is notable. Recent campaigns in some of these re-
gions (Baker et al., 2006; Planquette et al., 2007; Wagener et
al., 2008) do provide some confidence in the dust transport
models, but the uncertainties in parameterizations within the
models are still considerable and hence the uncertainties in
flux estimates are still substantial. The work of Measures
and colleagues (e.g. Han et al., 2008) has demonstrated the
validity of a novel indirect approach of using surface water
Al as a tracer of atmospheric deposition which provides data
averaged over long time scales (months to years) in remote
regions. Again this approach has significant uncertainties,
but the broad agreement between this, long term field data,
campaign data and models provides reassurance that the esti-
mates of total dust deposition to the oceans and the regional
patterns are realistic.
A major continuing source of uncertainty in estimating
dust deposition to the oceans is associated with the param-
eterisation of wet and dry deposition, except in the few cases
where wet deposition has been measured directly. The con-
gruence of data and models noted above does provide some
confidence that, at the global scale, the average deposition
parameterization is approximately correct. This does not
mean that the resultant dust flux from these averages is es-
timated correctly at the regional scale, or in the low dust re-
gions of water column iron limitation. Duce et al. (1991)
estimated uncertainties of a factor of three in the deposi-
tion flux and this uncertainty largely remains. Jickells et
al. (1998) demonstrated that the use of ocean sediment trap
data can provide a valuable constraint on the uncertainties in
deposition fluxes and Mahowald et al. (2005) considered this
further. However, the use of this technique in low dust re-
gions does require high quality measurements of a dust tracer
such as Al in the sediment traps and this is not always avail-
able. If this became routine it would offer a mechanism to
significantly reduce uncertainties in deposition parameteriza-
tion. Such an improvement would allow dust and iron mass
Biogeosciences, 7, 1075–1097, 2010 www.biogeosciences.net/7/1075/2010/
E. Breitbarth et al.: Iron biogeochemistry across marine systems – progress from the past decade1077
balance in individual regions and comparison to productivity
The conversion of dust deposition to soluble iron fluxes
requires the solubility of iron from dust to be known. This
is required ideally over the timescale of the residence times
of dust in the water column (tens of days, see Jickells et al.,
2005) and at realistically low dust loadings, although this is
very difficult in practice and more pragmatic short term sim-
ple aerosol leaching schemes are usually applied (Baker and
Considerable effort has been put into studies of aerosol
dust solubility over the last 10 years and this has tended to
confirm that on a global average Fe solubility is low (Jick-
ells et al., 2005; Mahowald et al., 2005), but also demon-
strated that the use of a single solubility estimate is probably
inappropriate and there does appear to be a systematic in-
crease in solubility from high to low dust regions (Baker and
Croot, 2009; Baker and Jickells, 2006). There is still consid-
erable debate surrounding the drivers of this variation in sol-
ubility with four main possibilities; (i) atmospheric chemical
processing during dust transport (Fan et al., 2006; Jickells
and Spokes, 2001), (ii) systematic changes in aerosol particle
size leading to changes in surface area and solubility (Baker
and Jickells, 2006), (iii) an additional source of iron beside
crustal dust (Jickells et al., 2005; Schroth et al., 2009); (iv)
active biological acquisition and uptake mechanisms such as
siderophores and grazing that can circumvent abiotic disso-
lution limitations (Barbeau and Moffett, 2000; Yoshida et al.,
2002; Frew et al., 2006).
There is good evidence that solubility of iron from anthro-
pogenic aerosol is higher than from soil dust (Schroth et al.,
2009; Journet et al., 2008) but the significance of this high
solubility anthropogenic dust to the global iron cycle is un-
certain, and in particular it seems unlikely to be responsible
for high iron solubilities in aerosols in remote regions seen
for instance by Baker and Jickells (2006). However, recent
measurements of iron speciation from African dust collected
in the Trade Winds at Barbados support the case for anthro-
pogenic iron controls over iron solubility. Trapp et al. (2010)
show that Fe3+dominates the iron solubility over the en-
tire range of particle sizes. However, at low mineral dust
concentrations Fe2+, believed to be largely derived from an-
thropogenic sources, becomes increasingly important. Air-
mass back trajectories indicate biomass burning in southern
Africa and potentially also South America as the source of
this anthropogenic iron and dust samples had an Fe2+/Fe3+
ratio twice that measured in dust-laden aerosols from North
Africa. (Trapp et al., 2010).
In their contribution to this special issue, Ye et al. (2009)
aim to improve the understanding of the impact of dust de-
position on Fe bioavailability and marine primary produc-
tivity in modeling iron speciation and biogeochemistry at
TENATSO (Tropical Eastern North Atlantic Time-series Ob-
servatory). Based on recent studies on Fe speciation and the
existing model for the Bermuda Atlantic Time-series Study
(BATS) (Weber et al., 2007), this model aims at studying the
role of dust particles in Fe removal and providing a better
description of the sources and fate of organic Fe-binding lig-
Dry deposition probably dominates dust and iron deposi-
tion over some regions of the ocean, particularly those where
winds flow off the land including areas downwind of major
deserts such as the Sahara. Wet deposition is probably partic-
ularly important for total deposition in remote regions of the
ocean. The data set for dust and soluble iron in wet deposi-
tion in the marine atmosphere is very small, and this requires
improvement. To date, this discussion has largely consid-
ered only dust and iron deposition. However, atmospheric
deposition delivers significant amounts of iron (Jickells et
al., 2005) and nitrogen (Duce et al., 2008) and relatively
small amounts of phosphorus (Mahowald et al., 2008) rel-
ative to phytoplankton requirements. Assorted trace metals
that may play a role in phytoplankton productivity, including
some that are potentially inhibitory, will also be deposited
(e.g. Paytan et al., 2009). It is important that we evaluate
the impacts of atmospheric deposition holistically, and not
artificially separate the contributions of individual nutrients.
2.2 Other atmospheric and marine processes of natural
All short-term artificial Fe fertilization experiments unequiv-
ocally showed the importance of Fe on the carbon cycle,
in particular on the food web structure and functioning
(e.g. Boyd, 2004; Boyd et al., 2007, 2000; Coale et al., 1996,
2004; Gervais et al., 2002; Tsuda et al., 2003; de Baar et
al., 2005, see Sect. 2). However, it is difficult to reliably
assess the magnitude of carbon export to the ocean interior
using such methods (Blain et al., 2007). Recent natural Fe
fertilization experiments carried out in the Southern Ocean
showed that the efficiency of fertilization was at least 10 to
20 times greater than that of a phytoplankton bloom induced
artificially by adding iron, (KEOPS and CROZEX, Blain et
al., 2007; Pollard et al., 2009). Large losses of purposefully
added iron can explain the lower efficiency of the induced
bloom, as well as the mode of iron addition and the require-
ment of concomitant supply with major nutrients (Pollard et
al., 2009; Blain et al., 2007). In the open ocean, a large vari-
ety of naturally iron-fertilized sites exist, which could allow
for improved forecasting of the oceanic response to Fe fer-
tilization and a better knowledge of Fe sources to the open
ocean. Chever et al. (2010) provide a Fe budget for the natu-
rally fertilized area above the Kerguelen Plateau, using total
dissolvable Fe as an additional tracer to better constrain the
Fe cycle in this area. They show that horizontal advection of
water from South of the Plateau seems to be the predominant
source of apparent particulate and dissolved iron above the
plateau, over atmospheric and vertical inputs. Further, Arde-
lan et al. (2010) illustrate natural Fe enrichment processes
from the South Shetland Islands-Antarctic Peninsula region.
www.biogeosciences.net/7/1075/2010/ Biogeosciences, 7, 1075–1097, 2010
1078 E. Breitbarth et al.: Iron biogeochemistry across marine systems – progress from the past decade
As discussed in Sect. 2.1, aeolian inputs may have differ-
ent origins, such as (i) the arid and semi-arid regions (Jickells
et al., 2005), (ii) combustion sources (fossil fuel burning, in-
cinerator use, biomass burning; (Spokes and Jickells, 2002;
Guieu et al., 2005; Sedwick et al., 2007; Luo et al., 2008),
but also by (iii) meteoritic material and extraterrestrial dust
(Johnson, 2001), and (iv) volcanic origin (Benitez-Nelson et
al., 2003; Duggen et al., 2007; Boyd et al., 1998). All atmo-
spheric input may have an effect on biological productivity
in the ocean (Schroth et al., 2009), in particular on bacterial
activity (Pulido-Villena et al., 2008), although the causative
link is not always obvious as shown by (Boyd et al., 2009).
While the meteoritic contribution is difficult to assess due
to the sporadic events, the amount of soluble (presumably
bioavailable) iron input into the ocean from extraterrestrial
dust is estimated to be 7×109gyear−1(Johnson, 2001) and
is thus not insignificant. More so, volcanic eruptions can
transport volcanic ash up to several tens of kilometres high
into the atmosphere and fine ash may encircle the globe for
years, thereby reaching even the remotest and most iron-
starved oceanic areas (Schmincke, 2004). The implication
of volcanism for the marine biogeochemical iron-cycle is
poorly constrained so far. Recent studies demonstrate that
volcanic ash from volcanoes worldwide quickly releases sol-
uble and bio-available iron on contact with water (e.g. Jones
and Gislason, 2008; Duggen et al., 2007; Frogner et al.,
2001). Drill core data from scientific ocean drilling show
that volcanic ash layers and dispersed ash particles are fre-
quently found in marine sediments and that volcanic ash
deposition and therefore iron-injection into the oceans took
place throughout much of the Earths history (Straub and
Schmincke, 1998). It may thus well be possible that the con-
tribution of volcanic ash to the marine biogeochemical iron-
cycle is generally underestimated. A review paper (Duggen
et al., 2010) summarises the development and the knowledge
in a fairly young research field covering a wide range of
chemical and biological issues and gives recommendations
for future directions. The approach by Duggen et al. (2010)
contributes to understanding of the role of volcanic ash for
the marine biogeochemical iron-cycle, marine primary pro-
ductivity and the ocean-atmosphere exchange of CO2 and
other gases relevant for climate throughout the Earths’ his-
Melting of sea ice, icebergs and glacial inputs may con-
tribute as Fe sources in polar regions. Estimates of these
sources’ magnitudes are poorly constraint. Recent studies
have highlighted the importance of these sources (Lannuzel
et al., 2008; Lannuzel et al., 2007; Statham et al., 2008;
Aguilar-Islas et al., 2008; Raiswell et al., 2008, 2006; Smith
et al., 2007; Croot et al., 2004). Iron accumulates in sea ice
with concentrations one to two orders of magnitude higher
than the underlying seawater. Atmospheric iron can be one
source but flux estimates by Lannuzel et al. (2008, 2007)
seem to indicate that iron must come mostly from below.
The exact mechanism remains unclear, but recent evidence
suggests that organic matter could play an essential role in
trapping Fe in the sea ice not only during sea ice formation
but also during ice algae proliferation in the bottom ice af-
ter its formation (Schoemann et al., 2008). Its release into
the seawater during ice melting can occur in short time spans
such as weeks. For example, Lannuzel et al. (2008) showed
that 70% of the accumulated Fe in the sea ice could be re-
leased due to brine drainage in a 10 days period, while the
sea ice cover was still present. This represents a significant
Fe flux to the surface ocean that may be instrumental in sus-
taining springtime ice edge blooms in the marginal ice zone
and polynias. Dense phytoplankton blooms have been ob-
shelf areas (e.g. Smith and Nelson, 1985; Holm-Hansen et
al., 1989). Moreover, both sea ice and icebergs may consti-
tute vectors of Fe transport far away from its initial source
(Smith et al., 2007; Lancelot et al., 2009). Further to this,
Edwards and Sedwick (2001) addressed the contribution of
snow bound aerosol iron in the Antarctic seasonal sea ice
The continental margins may also play a key role as a Fe
source (Elrod et al., 2004; La¨ es et al., 2003, 2007; Chase
et al., 2005; Blain et al., 2008). As an example, Lam and
Bishop (2008) clearly showed that the continental margin
was a key source of Fe to the HNLC (high nutrient low
chlorophyll) North Pacific Ocean, since the lateral source
of Fe is shallow enough to be accessible to phytoplankton
by winter mixing and Fe can be transported at distance over
900km from the continental shelf.
Our current challenge in regions where natural iron fer-
tilization occurs is to have a better knowledge and quantifi-
cation of these various Fe sources. For example, the global
atmospheric iron fluxes are reasonably well known, but the
fluxes to remote low iron regions are rather uncertain. More-
over, the aerosol iron solubility varies systematically, but the
underlying causes of this are uncertain. In the deep waters,
Fe can be transported far away from the source, especially
in waters with anoxic conditions (Blain et al., 2008). Local
and remote sources of Fe may not have the same impact on
carbon cycle. We also need to understand how (i) the differ-
ent sources of Fe influence its speciation and bioavailability;
(ii) they contribute to the global Fe budget; (iii) they will
be affected by global change, and (iv) what are the physical
mechanisms that allow long distance Fe transport: advection
(strong currents, ACC, EUC, de Baar et al., 1995; Mackey
et al., 2002; Lam and Bishop, 2008; Loscher et al., 1997),
internal waves and slope circulation (La¨ es et al., 2003), and
eddies (Johnson et al., 2005). Finally, the physical mecha-
nisms that allow Fe to be accessible for the food web should
also be better understood and quantified (upwelling, diapyc-
nal mixing, winter mixing, Blain et al., 2007).
To assesthese challenging
a crucialneed for(i)
proaches, such as the one promoted by the international
(ii) multi-proxy ap-
Biogeosciences, 7, 1075–1097, 2010 www.biogeosciences.net/7/1075/2010/
E. Breitbarth et al.: Iron biogeochemistry across marine systems – progress from the past decade1079
GEOTRACES program, including oceanic sections and
intercalibration experiments for seawater and aerosols; (iii)
the development of biogeochemical models that correctly
take into account the various Fe sources and their impact on
Fe speciation and bioavailability, and (iv) the development
of regional iron budgets.
3 Artificial iron fertilization
The largest source of iron for the HNLC surface waters
comes from deep water supply (Watson, 2001). However,
the Fe:N or Fe:P ratio of the upwelled deep waters is often
not high enough for optimum phytoplankton growth (Moore
et al., 2006). Consequently, an additional source of iron is
required, which could be derived from suboxic or anoxic
sediments (Las et al., 2007) or dust inputs (Jickells et al.,
2005). Fertilization of the Southern Ocean with dust has
been suggested as an explanation for past glacial periods
(Martin, 1990). During these periods iron dust inputs to the
oceans were strongly enhanced, with the Southern Ocean re-
ceiving up to 10 times more dust-derived iron (Wolff et al.,
2006), and consequent stimulation of phytoplankton growth
and the biological carbon pump. Nevertheless, it has been
estimated that the increase in iron stimulated productivity
could have contributed perhaps 15–25% of the 80–100ppm
drawdown in atmospheric CO2observed during glacial max-
ima by enhancing the biological carbon pump (Sigman and
Boyle, 2000; Bopp et al., 2003).
When trace metal clean techniques became available in
the late 1980s it was possible to directly test the effect of
iron additions on phytoplankton growth in HNLC regions.
Ship-board iron-addition bottle experiments clearly showed
that these additions stimulated phytoplankton growth (e.g. de
Baar et al., 1990). However, the potential for bottle-effects
during these experiments led researchers to plan and un-
dertake mesoscale Lagrangian-type oceanic experiments to
study the influence of iron additions on primary produc-
tivity, and investigate the consequences for nutrient utiliza-
tion, ecosystem dynamics and carbon export. More than a
dozen of these large scale (typically 10×10km grid) iron ad-
dition experiments have been conducted to date in HNLC
regions and were reviewed by de Baar et al. (2005) and
Boyd et al. (2007). Recent experiments involved conduct-
ing iron, carbon, nutrient, climatically active gasses, and
ecosystem observations, the latest being Lohafex (January–
March, 2009; Editorial Nature Geoscience, Editorial, 2009)
following a 300km2iron addition in a stable Southern Ocean
mesoscale eddy for >7 weeks. The longer time scale allowed
a thorough examination of biogeochemical and ecosystem
changes and carbon export.
In summary, all artificial iron experiments have confirmed
that iron supply limits primary production and has impact on
phytoplankton species composition and bloom dynamics in
tropical as well as in polar HNLC waters (Boyd et al., 2007;
de Baar et al., 2005). Iron limitation also induces a decou-
pling in the use of macronutrients by phytoplankton, likely
to influence the cycling of the major biogeochemical cycles
(C, N, P, Si, S) over geological time scales (de Baar and La
Roche, 2003). In addition to iron, light has been shown to
ductioninHNLCregions(Mooreetal., 2007a, b; Maldonado
etal., 1999; Boydetal., 2001; Hoffmannetal., 2008; deBaar
et al., 2005; Bucciarelli et al., 2010). Overall, in situ iron fer-
tilization experiments have greatly enhanced our knowledge
about iron solubility, organic iron complexation, and the im-
portance of iron redox states (e.g. Rue and Bruland, 1995;
Croot et al., 2001; Rue and Bruland, 1997), which apply to
Fe biogeochemistry in the ocean in general.
Large scale iron oceanic addition has been suggested as an
option for mitigating the present day increasing atmospheric
CO2concentrations (Kintisch, 2007). The Southern Ocean is
the HNLC region where iron stimulation of CO2sequestra-
tion would be most efficient and yield long-term carbon stor-
age in deeper waters (Sarmiento and Orr, 1991). Currently
there are a number of uncertainties surrounding intentional,
large-scale, ocean iron fertilization, which will require fur-
ther research for clarification. These have already been crit-
ically assessed by Chisholm et al. (2001) as well as more
recently by Buesseler et al. (2008). Potential side effects in-
clude that the mineralization of the enhanced sinking phyto-
plankton biomass could result in local anoxia and consequent
negative effects to oceanic ecosystems and the production
of the harmful greenhouse gases nitrous oxide and methane
(Cullen and Boyd, 2008; Furman and Capone, 1991). Other
climate active gases, like dimethylsufide (DMS) might in-
crease following Fe fertilisation (Liss et al., 2005). Direct
ecosystem shifts resulting in for example proliferation of jel-
lyfish have also been suggested. Furthermore, purposeful
iron fertilization may result in a reduced nutrient inventory
and consequently reduced productivity and potentially fish-
eries in oceanic systems downstream of the fertilization areas
(Gnanadesikan et al., 2003).
A further key unknown is the efficiency of carbon re-
moval. The amount of carbon sequestered per unit addition
of iron is crucial to the effectiveness of iron fertilization (de
Baar et al., 2008). The artificial experiments have indicated
an efficiency of biological carbon export into deeper water
(100–250m) ranging from 650 (SERIES, Boyd et al., 2004)
to 3300(molC/molFe) (SOFEX – south, Buesseler et al.,
2004). The seasonal sequestration efficiencies estimated for
natural Fe fertilization are much higher, 8640 for CROZEX
(Pollard et al., 2009) and 154000 for KEOPS (Chever et
al., 2010). The discrepancies in effectiveness between nat-
ural and purposeful fertilizations might be partly due to the
∼75% immediate loss of added Fe in artificial fertilisations
(de Baar et al., 2008). These values will need to be much
more tightly constrained to allow a thorough assessment of
the potential success of iron fertilization as a means to re-
www.biogeosciences.net/7/1075/2010/ Biogeosciences, 7, 1075–1097, 2010
1080 E. Breitbarth et al.: Iron biogeochemistry across marine systems – progress from the past decade
(Boyd, 2008). The success of the large scale oceanic addi-
tions of iron has furthermore been put into doubt by mod-
eling studies. Recent work by Dutkiewicz et al. (2005) and
Aumont and Bopp (2006) suggests that large scale iron addi-
tions would only reduce atmospheric CO2concentrations by
ca. 10ppm, as other limiting factors such as light and zoo-
plankton grazing become more important. It appears that
large uncertainties remain with respect to the efficiency of
iron fertilization that require further investigations using ob-
servation and models. For a recent in depth assessment of
the topic see Boyd et al. (2007), as well as Boyd (2008) and
associated publications. From a marine trace-metal research
perspective, the attendants of the workshop came to the con-
clusion, that priority should be given to small scale open
ocean Fe biogeochemistry studies that are specifically de-
signed to address clearly defined research questions of trace-
4 Fe inputs into coastal and estuarine systems
where the brackish water environment changes the physico-
chemical speciation, and thus mobility, of river-introduced
iron via aggregation, sedimentation and redox processes.
The coastal waters also are a highly dynamic transition zone,
resulting in very diverse temporal and spatial chemical and
biological changes. Total concentrations of iron in coastal
waters though are generally several orders of magnitude
higher than open ocean values and at a first glance, iron lim-
itation of primary production in coastal areas seems not very
likely. However, temporal growth limitation by iron can oc-
cur in some coastal upwelling regions (Bruland et al., 2001;
Hutchins and Bruland, 1998) and fjord systems (¨Ozt¨ urk et
The world’s largest estuary, the Baltic Sea, serves as an ex-
cellent large scale laboratory to study trace metal chemistry
over a wide salinity gradient. Here the total iron concen-
tration decreases by more than an order of magnitude from
the low salinity north-east (Bothnian Bay), via the Bothnian
Sea to its central part (Baltic Proper), thus forming a nat-
ural well defined iron concentration gradient for studying
physicochemical speciation of iron and the role of iron for
primary production at different total (unfiltered) iron concen-
trations (Gelting et al., 2009). The authors observed signifi-
cant variations in the physicochemical speciation, including
the iron isotopes, at high temporal resolution from the eu-
photic zone. Other large river systems such as the Columbia
River and Mississippi also show large gradients in iron con-
centrations but also act as significant sources of Fe to coastal
regions (Powell and Wilson-Finelli, 2003; Lohan and Bru-
In addition to photochemical processes and organic com-
plexation it is the cycling of iron between particles, colloids
and the truly dissolved fraction (<1kD), rather than the to-
tal concentration, that determines the bioavailability of iron
in coastal surface water. The truly dissolved fraction can
rapidly be consumed during bloom conditions if this frac-
tion is small and exchange processes between particulate-
colloidal matter and the truly dissolved fraction are slow.
Hence, knowledge about distribution and cycling of iron be-
tween these phases in the coastal zone is fundamental for
predictions about iron limitation for plankton growth, and is
key to understanding iron export pathways to the open ocean.
For the Baltic Sea, Gelting et al. (2009) show that iron in
the <1kDa fraction never reached critical low levels during
summer phytoplankton bloom conditions. Further, Fe(II) is
generally not considered as an abundant source of bioavail-
able iron due to its short residence time in oxygenated water.
However, a relatively high standing concentration of Fe(II),
large enough to cover the demand for iron by cyanobacteria
in Baltic Sea waters, was observed by Breitbarth et al. (2009)
in a study paralleling Gelting et al. (2009).
Measurements of the physicochemical speciation of iron
in freshwater during the last five years suggest that iron trans-
port in rivers is associated with two types of carrier phases
(besides detrital particles), an oxyhydroxide phase with as-
sociated CDOM (chromophoric dissolved organic matter,
mostly consisting of humic acids) and an organic carbon
(fulvic) phase (e.g. Lyv´ en et al., 2003; Andersson et al.,
2006). Much of this fulvic phase is present as small col-
loids and in the truly dissolved fraction (<1kD). When these
phases reach the saline coastal water substantial aggregation
of the Fe-oxyhydroxide fraction with associated CDOM is
observed, whereas iron associated to the fulvic fraction show
little aggregation (Stolpe and Hassell¨ ov, 2007) and survives
the sequential sequestration from the water column during
gradual mixing with seawater (Krachler et al., 2005). It is
possible that this land-derived fraction can reach the open
ocean, as indicated by recent data (Laglera and van den Berg,
2009). With fulvic acid as one important carrier mecha-
nism for riverine Fe, the influence of this Fe source reaches
further out to sea than previously expected. Tovar-Sanchez
et al. (2006) for example, suggested based on metal com-
position, that riverine and not dust born material was the
main source of trace metal accumulation in a diazotroph (Tri-
chodesmium sp.) dwelling the surface waters of the subtrop-
ical and tropical North Atlantic Ocean.
Back at the river-seawater interface, Gerringa et al. (2007)
argue that particularly the weak iron ligand groups (L2) may
impede the precipitation of Fe in the Scheldt Estuary upon
mixing with seawater and that the strong ligand (L1) gener-
ally observed in the open ocean, albeit also present, were in-
sufficient in concentration. Powell and Wilson-Finelli (2003)
though point out that the latter is of crucial importance for Fe
transport in the Mississippi river plume. Likewise, Buck et
al. (2007) demonstrated the predominant importance L1type
ligands for Fe transport into the sea from the Columbia River
and San Francisco Bay plumes. The stability constants of
these strong L1ligands are very similar to those reported by
Biogeosciences, 7, 1075–1097, 2010 www.biogeosciences.net/7/1075/2010/
E. Breitbarth et al.: Iron biogeochemistry across marine systems – progress from the past decade1081
indicating the importance of these ligands in controlling the
solubility of dissolved iron in riverine and coastal systems.
Clearly, Fe speciation in estuarine and near-shore waters can
not be addressed in a generalized manner and systems may
differ depending on watershed characteristics (e.g., pristine
versus anthropogenically impacted) as well as the level and
type of riverine input (¨Ozt¨ urk and Bizsel, 2003; Krachler et
al., 2005) (see Sect. 5 for colloidal matter).
Ingri et al. (2006) suggest that iron isotopes could be used
to roughly identify the two major suspended fractions for
iron in river water, the oxyhydroxides phase, which shows
positive δ56values, and the fulvic fraction that has a more
negative signal. River water-seawater mixing experiments by
Bergquist and Boyle (2006) showed that aggregated Fe was
enriched in heavy isotopes. Hence, aggregation and sedi-
ing should remove heavy isotopes from surface suspended
matter, resulting in a more negative signal in the suspended
phase, as indicated by field data from the River Lena fresh-
water plume (J. Ingri, personal communication, 2009). Cy-
cling of iron in coastal areas appears to result in export of
a negative iron isotope signal in the truly dissolved fraction,
suggesting that open ocean water generally has a negative
dissolved isotope iron signal thus explaining the negative δ56
value in ferromanganese crusts in the deep-sea. However, re-
cent data indicate that bottom water in the open ocean has a
positive δ56value (Lacan et al., 2008), although it should be
noted that the dataset is limited to one depth profile.
Iron isotope data from surface water in the Baltic Sea re-
veal systematic temporal variations in the Fe-isotope signal.
For example, the δ56value changed from −0.1 to +0.25‰
during a diatom spring-bloom resulting in subsequent sedi-
mentation of iron with a negative isotope signal (Gelting et
al., 2009). During the summer a relatively stable positive
δ56value was measured in suspended matter at different lo-
cations. This was likely due to a combination of river intro-
duced aggregated oxyhydroxides and particulate iron formed
from oxidation of dissolved Fe(II) in surface water. In this
low salinity system, river introduced Fe-oxyhydroxides ag-
gregate, but may not sediment in the river estuaries due to
the lack of detrital sinking and flocculation processes and
hence can spread far into the Baltic Sea (Gustafsson et al.,
2000). This system is in sharp contrast to recently revised
very rapid aggregation and sedimentation processes for di-
rect river – seawater mixing (Nowostawska et al., 2008).
Recent advances suggest that iron isotope measurements
have a large potential to provide new information on iron cy-
cling and iron transport from coastal areas to the open ocean
(de Jong et al., 2007). Fe/Ti or Fe/Al ratios close to average
crust material do not necessarily indicate that the suspended
phase mainly reflects detrital particles. Both positive and
negative iron isotope values have been measured although
the sample has a Fe/Ti or Fe/Al ratio close to average crust
material. Furthermore, a δ56value around zero does not nec-
essarily mean that the sample consists of mainly detrital rock
fragments, as it usually is a mixture of iron particles with
positive and negative δ56values (Gelting et al., 2009). Rec-
ommendations for future work thus consist of a focus on this
field including continuing the characterization of the carrier
phase for Fe across the salinity gradient and into the open
5 Colloidal iron and organic matter
Ten years ago the focus of Fe biogeochemistry was on dis-
solved (filterable) iron speciation and quite specific iron
complexes. Once overlooked and neglected (Wells, 1998),
progress has been made in understanding the nature and im-
portance of organic colloidal material in seawater and coastal
systems and challenged the simple discrimination into par-
ticulate and dissolved iron (0.45 or 0.2µm filtered). Fur-
thermore, dynamic exchange between larger iron particles,
colloidal iron, and soluble iron (defined as passing either a
0.02µmora 1kDa filter)also directsinteresttowards thepar-
ticulate and soluble phase. The FeCycle study, a mesoscale
SF6 tracer release experiment without iron perturbation in
HNLC waters southeast of New Zealand (Boyd et al., 2005),
showed that iron recycling rates due to biological iron up-
take and regeneration exceeded input of new iron by 10-
fold. Further, particulate Fe would undergo a transformation
from lithogenic to biogenic iron during settling through the
mixed layer. Rapid biological processing (bacterivory and
herbivory, subsequent biological uptake) after dissolution of
dust deposited iron hydroxides and presumably also photoly-
sis of siderophore complexed Fe(III)-hydroxide (Borer et al.,
2005) resulted in exchange from the lithogenic particulate
phase via the soluble to the biogenic particulate phase (Frew
et al., 2006; Strzepek et al., 2005; Maldonado et al., 2005).
The rapid exchange with particulate iron phases provides
new insight into iron cycling and export dynamics since the
role of particulate iron in iron biogeochemistry appears more
important than previously assumed. During the Gothenburg
workshop however, the main center of attention was on col-
loidal iron and we therefore focus thereon hereafter.
Moran et al. (1996) measured iron, among other bioac-
tive trace metals, in colloidal matter obtained by cross-flow
filtration of seawater. The major proportion of the dis-
solved Fe in open ocean seawater (here defined as 0.4µm
filtered) was found to be in the colloidal form (here defined
as >0.02µm–0.4µm) (Wu et al., 2001), with continuing de-
bate about the bioavailability of this fraction.
Wang (2001) showed that freshly precipitated colloids were
available to phytoplankton but aging processes (15 days) re-
duced markedly their availability.
demonstrated that Fe availability from colloidal matter to
cyanobacteria (Synechococcus, Trichodesmium) is largely
dependent on the size and origin of the material, with the ten-
dency of Fe bound to smaller colloids and biogenic colloidal
Wang and Dei (2003)
www.biogeosciences.net/7/1075/2010/Biogeosciences, 7, 1075–1097, 2010
1082 E. Breitbarth et al.: Iron biogeochemistry across marine systems – progress from the past decade
material derived from the same species being more available.
The transfer from the soluble to the colloidal fraction ap-
pears rapid for iron in comparison to for example Zn, result-
ing in dynamic cycling including particle formation, and the
drawdown of colloidal Fe indicated uptake by phytoplankton
(Hurst and Bruland, 2007). Further, colloidal Fe is photore-
active and thus also contributes to the bioavailable pool of
Fe(II) in surface waters (Barbeau, 2006; Fan, 2008).
Dissolved organic matter (DOM, which contains the col-
loidal fraction) in seawater has previously been considered
to be old (∼6KY) and refractory (Bauer et al., 1992).
This refractory pool is also known to be rich in aromatic
chromophoric material therefore often called chromophoric
DOM (CDOM). However, in the last ten years the picture
has changed somewhat and now it is believed that in addi-
tion to the refractory pool seawater DOM also consists of
in situ biologically derived material, rich in proteic matter
and sacharides and saccharide derivatives as building blocks
(Aluwihare et al., 1997). In addition significant findings have
been made to understand that fractions of marine DOM pos-
sess a gel forming character, including spontaneous assem-
bling into microgels after filtration, where calcium bridging
is shown to be important (Chin et al., 1998). In addition, new
microscopy based techniques have shown that fibrillar type
materials, hypothesized to consist of acid polysaccharides,
are abundant in many open ocean regimes (Santschi et al.,
1998). This marine gel phase can be an important transfer
route from truly dissolved to particulate pool of matter (Ver-
dugo et al., 2004). These findings in the dissolved fraction
exopolymeric particles (TEP), which are important for car-
bon export (Engel et al., 2004), although direct experimental
evidence linking the fibrillar material to TEP and sedimenta-
tion has been lacking.
To what extent these processes and phase transfers in or-
ganic matter are controlling the physicochemical states and
vertical distributions of iron and other trace elements has pre-
viouslyonlybeenhypothesized. StolpeandHassell¨ ov(2010)
on-line “humic” fluorescence and UV-absorbance detectors,
and subsamples for Atomic Force Microscopy (AFM) to
fractionate and identify different colloidal size classes and
associated trace metals during phytoplankton bloom events
in a Fjord on the North Sea coast of Sweden. They found
both seasonal and vertical variations in the colloidal size dis-
tributions for iron and other trace elements and could use
these in order to explain the apparent iron solubility and
vertical distribution to a large extent (Stolpe and Hassell¨ ov,
2010). During the winter season colloidal size distribution
for iron (and many other elements) were only appearing in
the CDOM fraction (∼0.5–3nm), while during the spring
bloom and summer bloom in two consecutive seasons the
colloidal size distributions for iron were shifting dramati-
cally. In addition to the CDOM phase, iron partitioned into
two larger size classes. With AFM these two colloidal popu-
lations were identified to be semispherical (3–7nm) and fib-
rillar (∼0.5nm thick and 30–200nm long). From the parti-
tioning of other elements and their size and shape it was hy-
pothesized that the semispherical colloids were mainly thiol
rich proteic biopolymers, while the fibrillar materials were
polysaccharide rich exudates that could be the precursors of
the microgels proposed by Chin et al. (1998). The conclu-
sion that the seasonal variations of iron association with dif-
ferent colloidal phases to some extent control the apparent
iron solubility in estuarine water is in line with the find-
ings from Bergquist et al. (2007), implying that colloids in
the open ocean control iron solubility. Likewise, Boehme
and Wells (2006) and Floge and Wells (2007), using FlFFF
coupled to excitation emission matrix spectroscopy and a
UV-absorbance detector, observed a shift in colloidal size
class distribution between protein-like and humic-like fluo-
rescence of CDOM during phytoplankton blooms in an estu-
Progress has been made in studying the behavior of iron
oxide nanoparticles in different freshwater and salt matrixes
and drawing conclusions for the inorganic phase within the
filterable fraction (Hassell¨ ov and von der Kammer, 2008,
and references therein). Partly based on this work, the un-
derstanding of flocculation processes has improved and pre-
vious concepts (Sholkovitz, 1978; Sholkovitz et al., 1978)
have been confirmed. Mylon et al. (2004) using natural or-
ganic matter (NOM) coated synthesized hematite colloids,
show that the rate of colloid aggregation reaches a maximum
at a salinity of 12, resulting in a removal of 80–90% of dis-
solved iron in a process occurring on a time scale of sec-
onds (Nowostawska et al., 2008). The colloidal particles are
stabilized by NOM due to electrostatic and repulsive forces
(Mosley et al., 2003; Sander et al., 2004). Theoretically in
seawater the conditions would favor attachment, but low par-
ticle concentrations result in a low collision frequency. Fur-
ther, colloidal matter undergoes a transformation in size dis-
tribution and elemental composition upon introduction from
fresh water into a seawater system (Stolpe and Hassell¨ ov,
2007). The efficiency of transport through salinity gradients
needs more investigation and isotope studies may be of sig-
nificant importance to form a proper understanding of fluvial
iron inputs into the sea (see Sect. 4).
As aforementioned, recent methodological advancements
include the application of field flow fractionation (FFF),
in conjunction with size fractionation by membrane and/or
ultrafiltration techniques, to studies of the metal-colloidal
phase (Boehme and Wells, 2006; Stolpe et al., 2005).
FFF was generally applied to samples from coastal systems
and detection limits necessitate the use of pre-concentration
steps. While being a powerful tool to characterize size frac-
tionated material, FFF can also help in developing robust fil-
tering methods particularly at the lower end of the size range,
as results reveal artefacts from membrane filtration can re-
sult in unintended removal of undersized material (Howell
et al., 2006). The relevance of this for open ocean seawater
Biogeosciences, 7, 1075–1097, 2010www.biogeosciences.net/7/1075/2010/
E. Breitbarth et al.: Iron biogeochemistry across marine systems – progress from the past decade1083
requires further testing. Further, cross-flow ultra-filters are
defined as a molar cut-off, which may result in retention of
undersized components and permeation of oversized compo-
nents, as well as separation of size and chemical composi-
tion (Assemi et al., 2004). An intercalibration of cross-flow
filtration techniques was carried out previously (Buesseler
et al., 1996), but a new approach including classical mem-
brane filtration and utilizing FlFFF coupled to ICPMS may
yield valuable information about the robustness of different
filter membraneswith regard tofractionation of colloidal size
classes and their elemental composition.
We conclude that future research directions should encom-
pass further in depth characterizations of the different phases
(particulate, colloidal, soluble), which may lead to a redef-
inition of the term dissolved iron. This will also lead to a
better structural definition of bioavailable iron. We need to
learn how iron is fractionated into specific size classes, what
the exchange kinetics between these phases are, and what
controls/catalyzes them. Specifically, the origin and nature
of iron binding ligands needs to be further addressed to elu-
cidate the role and characteristics of different ligand classes
(L1, L2). In that, we may need to overcome measurement
artifacts due to pre-concentration procedures that are neces-
sitated due to the detection limits especially in open ocean
applications (see also last two paragraphs of Sect. 6).
6 Linking biological processes to iron chemistry
Most areas of the open ocean have surface trace metal con-
centrations between picomolar and nanomolar levels, which
are about one millionth of the concentration in phytoplank-
ton cells (Morel and Price, 2003). Iron is required for many
important cellular processes such as photosynthesis, respira-
tion, nitrogen fixation and nitrate reduction. A recent labo-
ratory study involving 15neritic and oceanic phytoplankton
species produced an elemental ratio of C124N16P1Fe0.0075
(Ho et al., 2003), similar to previous reviews of Fe:C ratios
which have found a range of 2.3–370µmol:mol (Sarthou et
al., 2005; see also Twining et al., 2004). Research has linked
the oxygenation of the oceans and the subsequent drop in
iron solubility and thus iron availability to the evolution of
more iron efficient phytoplankton (Quigg et al., 2003; Saito
conditions. Phytoplankton species have evolved very effec-
tive acquisition mechanisms with high trace mtal affinities
that involve interactions with organic iron binding ligands.
Uncertainties remain on the nature of such ligands, which
control Fe chemistry and bioavailability in marine systems
(Hunter and Boyd, 2007).
Culture experiments have established that marine phyto-
and bacterioplankton have different iron requirements that
are linked to their biogeographical sources (Sunda and
Huntsman, 1995; Brand et al., 1983). More recent work
has shown that picophytoplankton, which dominate the olig-
otrophic regions of the oceans, are able to grow optimally in
culture at extremely low inorganic iron concentrations of 10–
15pM inorganic Fe, (Timmermans et al., 2005). Our ability
to relate these studies to the real environment is however lim-
ited by our understanding of the chemical speciation of iron
in the ocean (Gledhill and van den Berg, 1994; Rue and Bru-
land, 1995). These studies indicated that dissolved iron is
strongly complexed in the ocean, results which have been
confirmed on many occasions since (as discussed in Hunter
and Boyd, 2007). The composition of this organic fraction
is still not well understood, although it appears likely that it
will consist of autochthonous complexing ligands produced
by marine phyto- and bacterioplankton (Mawji et al., 2008;
Boye et al., 2005; Kondo et al., 2008; Vong et al., 2007)
and complex organics such as humic/fulvic acids (Laglera
and van den Berg, 2009). Calculations of the inorganic iron
concentration based on measurements carried out by compet-
itive equilibration cathodic stripping voltammetry show that
inorganic iron concentrations in the ocean are of the order of
10−14–10−11M (Morel et al., 2008), although these calcula-
tions neglect the contribution of Fe(II), which may also be
present at concentrations of the order of 10−11M in surface
waters (e.g. Hansard et al., 2009; Roy et al., 2008b; Croot et
al., 2001). It is not clear how much of the organically com-
plexed iron is available to marine phyto- and bacterioplank-
ton, and parameters controlling Fe bioavailability to primary
producers are still poorly understood.
Fe bioavailability is influenced by its chemical forms (spe-
ciation, redox state), biological cycling, and the different up-
take strategies of the phyto- and bacterio-plankton commu-
nities (Barbeau et al., 1996; Hutchins et al., 1999a; Strzepek
et al., 2005). Competition for available Fe is strongest when
Fe is in short supply (e.g. Worms et al., 2006). Recent ad-
vances in our understanding and abilities to model iron up-
take by marine phytoplankton (Morel et al., 2008; Shaked
et al., 2005; Salmon et al., 2006) indicate that even at these
low inorganic iron concentrations, open ocean phytoplank-
ton will have sufficient iron to grow. Initially iron uptake
was thought to be proportional to the concentration of in-
organic Fe species (Fe’) (Hudson and Morel, 1990). How-
ever, this model proved to be too simplistic to explain phy-
toplankton growth in natural systems where concentrations
of inorganic iron species were extremely low due to organic
complexation. Thus either the iron-ligand complex (FeL)
is directly taken up, or the inorganic Fe availability is in-
creased, e.g. by reduction to Fe(II). More recently two mod-
els have been published to describe the kinetics of Fe up-
take.The Fe(II) model by Shaked et al. (2005) and the
FeL model by Salmon et al. (2006). There are significant
distinctions between these models which lead to differences
in the predictions of phytoplankton iron limitation in cul-
ture experiments. While the Fe(II) model considers the sur-
face Fe(II) concentration and explicitly includes unchelated
Fe(III) as a source of Fe(II) for phytoplankton uptake, the
FeL model considers the bulk concentration of Fe(II) in the
www.biogeosciences.net/7/1075/2010/Biogeosciences, 7, 1075–1097, 2010
1084 E. Breitbarth et al.: Iron biogeochemistry across marine systems – progress from the past decade
media as the controlling parameter and excludes unchelated
Fe(III) as an irrelevant source (Morel et al., 2008). Morel et
al. (2008) point out that the observed decrease in Fe uptake
rates with increasing EDTA concentrations can only be ex-
plained by the Fe(II) model, which results in the conclusion
for phytoplankton uptake. However, phytoplankton species
behave differently under Fe limitation and it is likely that fu-
ture experiments under more natural conditions without the
presence of EDTA will result in more realistic iterations of
the iron uptake models. The role of other trace metals and or-
ganic material in the partly species specific adaptations of the
iron acquisition system are not completely understood. As
one example, Peers and Price (2006) have shown that copper
is essential for electron transport in T. oceanica regardless
of Fe status implying that selection pressure imposed by Fe
limitation has resulted in the use of a Cu protein for photo-
synthesis in an oceanic diatom.
Adaptations to low iron environments have been found to
include a reduction in cell size (Sarthou et al., 2005), changes
in photosynthetic architecture (Strzepek and Harrison, 2004;
Peers and Price, 2006) and substitution of iron containing
proteins for non-iron containing proteins (Peers and Price,
2006; McKay et al., 1999). Further possible adaptations
include the induction of high affinity uptake mechanisms
specific iron containing compounds such as hemes (Hopkin-
son et al., 2008) or the production of iron storage proteins
(Marchetti et al., 2009).
Microorganisms can exert a feedback effect on Fe chem-
istry, for example by releasing organic matter which is able
to react with Fe (e.g. siderophores, exopolymeric substances
(EPS), cell lysis material or fecal pellets), which can en-
hance iron bioavailability (e.g. Hutchins et al., 1999b). Hel-
dal et al. (1996), for example, visualized and quantified met-
als bound to bacterial extracellular matrixes in applying X-
ray transmission electron microscopy. The role of grazing as
a source of organic, iron binding material via sloppy feeding
and/or as a direct source of iron is often discussed. Several
studies address this topic and a general consensus about the
importance of grazing for iron recycling in surface seawa-
ter exists (Sato et al., 2007; Barbeau et al., 1996; Dalbec
and Twining, 2009; Sarthou et al., 2008; Hutchins and Bru-
land, 1994; Hutchins et al., 1995; Tovar-Sanchez et al., 2007;
ZhangandWang, 2004). However, someresultsareinconsis-
tent and the detailed mechanisms as well as the contribution
of different grazer types such as protozoa, copepods, krill,
and salps and their specific feeding mechanisms are poorly
understood. Therefore, it is difficult today to estimate the
overall function of grazing on the biogeochemical cycles of
iron especially in HNLC regions.
Most marine microorganisms (bacterio- and phyto-
plankton) produce polysaccharides that are either stored
as energy reserves or secreted as exopolymeric substances
(EPS) (Schoemann et al., 2001; Decho, 1990; Hoagland et
al., 1993). It has recently been shown that iron starvation is
coupled to transparent expolymer particles (TEP) production
in Trichodesmium (Berman-Frank et al., 2007). Recent stud-
ies also provide evidence that high concentrations of saccha-
rides or carbon-rich organic matrices can enhance the growth
of phytoplankton (Vasconcelos et al., 2002) and efficiently
retain Fe (II) (¨Ozt¨ urk et al., 2004; Toner et al., 2009), a
highly bioavailable form (Morel et al., 2008). Steigenberger
et al. (2010) show that polysaccharides and cell exudates of
Phaeodactylum sp. can also result in high hydrogen peroxide
production, while the authors still observe a net stabilizing
effect of Fe(II) potentially due to a combination of organic
Fe(II) retention paralleled by superoxide production.
Hassler and Schoemann (2009) explore a Fe-related bio-
geochemical role for polysaccharides, by examining the in-
fluence of various organic ligands (siderophore, porphyrin,
mono- and poly-saccharides) on iron solubility and its
bioavailability to four keystone phytoplankton species of the
Southern Ocean, representing different phytoplankton func-
tional groups and size classes (Phaeocystis sp., Chaetoceros
sp., Fragilariopsis kerguelensis and Thalassiosira antarc-
tica Comber). Results show that saccharides can increase
Fe uptake rates and Fe solubility above the level observed
for inorganic Fe. Similar observations were made on natu-
ral plankton community from the Southern Ocean (Hassler
et al., 2007). Given the ubiquitous presence of saccharides
in the ocean, these compounds might represent an important
factor to control the basal level of soluble and bioavailable
Over the past years, the Fe(II) pool has been recognized
as an important source of bioavailable Fe and intermediate
in Fe cycling. Albeit short-lived due to rapid re-oxidation
to Fe(III), significant concentrations of Fe(II) were detected
in different oceanic and coastal provinces (Breitbarth et al.,
2009; Croot and Laan, 2002; Croot et al., 2008, 2005; Roy
et al., 2008b; Hopkinson and Barbeau, 2007; Ussher et al.,
2007). There has been emerging evidence that Fe(II) is re-
tained in oxygenated water by organic ligands (Croot et al.,
2001), which may be a product of marine biota (Roy et al.,
2008b) or also of other origin and rain introduced (Willey et
al., 2008). See Barbeau (2006) for a comprehensive review
and also Sect. 7. The role of Fe(II) for phytoplankton nutri-
tion and Fe(II) organic complexation provide interesting and
relevant research topics for the near future.
Iron limitation also induces a decoupling in the use of
macronutrients by phytoplankton, likely to influence the cy-
cling of the major biogeochemical cycles (C, N, P, Si, S) over
geological time scales (de Baar and La Roche, 2003). Fur-
ther, light intensity can play an important role (Hoffmann et
al., 2008; Maldonadoetal., 1999; deBaaretal., 2005; Moore
et al., 2007a and b). Moreover, Bucciarelli et al. (2010) ex-
amined the effect of Fe-light co-limitation on cellular sil-
ica, carbon and nitrogen in two marine diatom species, Tha-
lassiosira oceanica and Ditylum brightwellii, observing a
Biogeosciences, 7, 1075–1097, 2010 www.biogeosciences.net/7/1075/2010/
E. Breitbarth et al.: Iron biogeochemistry across marine systems – progress from the past decade1085
1.4-fold increase in C:N ratio with a decrease in growth rate
by 70% in both species and a decrease in biogenic silica
per cell under severe Fe or Fe-light limitation. These results
however are seemingly in contradiction with many previous
lab and field studies showing increased diatom silicification
under Fe limitation (Hutchins and Bruland, 1998; Takeda,
1998; Firme et al., 2003; Franck et al., 2003).
A significant contribution to the increasing knowledge on
the interaction of biological processes with iron chemistry
is made by the improvement of methods in this field. Inter-
calibrations of Fe detection methods were carried out and
measurements of Fe are now possible in near real time in
the field at picomolar level (Bowie et al., 2002, 2005, 2006;
Johnson et al., 2007), including Fe(II) (Croot and Laan,
2002). More sophisticated shipboard incubation systems are
available (Hare et al., 2007a; Hutchins et al., 2003; Pick-
ell et al., 2009; Hare et al., 2005), allowing for more realis-
tic experimental designs to assess Fe phytoplankton interac-
tions. Methods were developed to detect cell surface Fe re-
duction and uptake (Shaked et al., 2004) and to measure cel-
lular Fe (Hassler et al., 2004). New highly sensitive electro-
chemical methods have pushed our understanding of organic
iron complexation in new directions (Croot and Johansson,
2000; Laglera and van den Berg, 2009). Utilization of labo-
ratory based extensive instrumentation such as FlFFF, x-ray
spectroscopy with TEM microscopy, as well as bioreporters,
molecular techniques and genomic information allow for in
depth studies and visualization of Fe limitation and Fe or-
ganic matter interactions (e.g. Heldal et al., 1996; Toner et
al., 2009; Stolpe et al., 2005) and particularly also of iron
bioavailability (Lam et al., 2006; Boyanapalli et al., 2007;
Hassler et al., 2006).
Nevertheless, some methods still depend on high ma-
terial/biomass concentrations and future development and
work may lead towards more direct measurement techniques
overcoming pre-concentration artifacts. The majority of phy-
toplankton iron interaction studies have been carried out in-
vitro and with a limited range of species, and mostly did not
include co-effects of other trace metals. Strong iron chela-
tors such as EDTA and DFOB are commonly used to induce
iron limitation in culture experiments and experiments are in
part difficult to compare due to the variety and combination
of factors (e.g. light intensity, temperature) applied. Thus,
it is not clear how predominant the known low iron regime
adaptations are in the oceanic environment. Albeit very chal-
lenging, future experiments should aim towards using more
realistic media chemistries and natural biomass densities of
cultures that were recently isolated. Methods and experi-
ments need to be designed to link Fe chemistry to biologi-
cal processes, including potential biological feedback mech-
anisms on Fe chemistry as also discussed with regard to cli-
mate change in Sect. 7. Further, our increasing ability to
detect and characterize iron in seawater and in organisms
(Mawji et al., 2008; Gledhill, 2007; Laglera and van den
Berg, 2009; Vong et al., 2007) coupled to developments in
techniques such as shotgun genomics (Rusch et al., 2007;
Venter et al., 2004; Yooseph et al., 2007) and the potential
of proteomics (Nunn and Timperman, 2007; Dupont et al.,
2006) should lead to great advances over the coming years
in our understanding of how organisms have adapted to low
iron environments, and the implications of these adaptations
to overall marine productivity and biodiversity. The devel-
opment of in-situ measurement technology as for example
suggested in the approach of Roy at al. (2008a), with the po-
tential for deployment on moored sensor arrays, will greatly
improve the spatial and temporal resolution of Fe measure-
7 Iron and climate change
Global climate change will greatly influence atmospheric
and hydrographic processes in the future. Most prominent
features include changes in thermohaline circulation of the
North Atlantic, warming of the polar regions, changing wind
patterns resulting in reduced upwelling and wind driven mix-
ing, as well as increased sea-surface temperatures and strati-
fication (Boyd and Doney, 2003). Projected changes in rela-
tive humidity and land vegetation cover, affecting soil mois-
ture and local dust availability, together with changed pat-
terns in wind and precipitation, as well as riverine transport,
will ultimately modify the iron supply to the open ocean
(Boyd and Doney, 2003; Jickells et al., 2005). Further, rising
atmospheric CO2acidifies the oceans, leading to changes in
saturation state with respect to calcium carbonate and shifts
and potentially trace metal solubility. The abovementioned
processes, albeit uncertainty over their magnitude and exact
interrelations in the future exists, will affect marine biota,
causing regime shifts, and modifications of biogeochemi-
cal cycling (Boyd and Doney, 2003). While climate change
needs to be understood holistically, there is a need to evaluate
regional and small scale physical, chemical, and biological
processes in order to derive potential biogeochemical feed-
We here focus on direct local effects acting upon iron
chemistry in seawater and primarily discuss the emerging
field of trace metal biogeochemistry research encompassing
two main areas, temperature shifts and changing seawater
pH. Both temperature and pH are master variables for chem-
ical and biological processes and effects on trace metal bio-
geochemistry may be multifaceted and complex. Ten years
ago, this research field did not exist and data are scarce.
Assessing the potential effects of sea-surface warming and
ocean acidification on iron biogeochemistry is crucial and
predictions to date are based on our understanding of the cur-
rent ocean system. Despite the expanding knowledge and in-
creasing awareness for trace metal chemistry in open ocean
research during the past 20 years and the recently defined
www.biogeosciences.net/7/1075/2010/Biogeosciences, 7, 1075–1097, 2010
1086 E. Breitbarth et al.: Iron biogeochemistry across marine systems – progress from the past decade
field and intensifying work on ocean acidification research,
there is yet little communication between these fields.
A decrease of the surface seawater pH from pre-industrial
8.25 to 7.85 within this century, and further by up to 0.7 units
until 2300 is predicted (Caldeira and Wickett, 2003; Jacob-
son, 2005). In general, the H+ion concentration can directly
affect metal uptake by phytoplankton via altered membrane
transport activity or via direct competition of the H+ion with
metal ions for membrane transporters or other metabolically
active sites on the cell surface (Sunda and Huntsman, 1983;
Vigenault and Campbell, 2005). Further main aspects are the
inorganic solubility of iron, changes in organic complexa-
tion, phytoplankton – trace metal feedback mechanisms, and
differences in redox chemistry.
Fe(OH)3solubility and Fe(III) inorganic speciation are ex-
pected to changed with ocean acidification (Liu and Millero,
2002, 1999). When seawater pH falls below 8, changes in
the inorganic speciation result in an increase of the thermo-
dynamic Fe(III) hydroxide solubility. Enhanced solubility
above pH 7 in seawater of the warm or temperate ocean
though is mainly due to organic ligands and suggests any
change in solubility arising from acidification will be mainly
related to the organic complexes (Liu and Millero, 2002).
However, in cold water the solubility of Fe can exceed FeL
concentrations(P.Croot, personalcommunication, 2009, cal-
culated based on Liu and Millero, 2002), bringing inor-
ganic speciation shifts due to pH and temperature back into
the game. Interesting questions arise concerning whether
ocean acidification could potentially also affect metal leach-
ing from atmospheric deposits (see Sects. 2.1 and 2.2) and
how the metastable colloidal Fe phase may be affected (see
Sect. 5). The potential effect of pH acting directly on FeL
complexes depends on the nature of Fe-binding functional
groups. The H+stoichiometry of the Fe(III) binding sites
defines the magnitude of acid dissociation constants (pKa).
Carboxyl groups have a pKa∼5 and thus the conditional sta-
bility constant of the FeL complex (log KFeL) should remain
unchanged above pH 6. In contrast, phenolic groups have
a pKa ∼9 and logKFeLwill increase with pH (Sillen and
Martell, 1971). Both groups can be found in siderophores.
While to date no published experimental data on the pH ef-
fect for FeL can be found, Averyt et al. (2004) show a de-
crease of logKCuLwith lower pH in two lakes. Similar ef-
fects were observed for Cd ligands, but less so for Zn lig-
ands (Sander et al., 2007). Further, iron chelates are more
photolabile at lower pH (Sunda and Huntsman, 2003), which
directly involves effects on Fe photochemistry (see below).
Overall though, while FeL complexes may or may not be
directly pH affected, alterations of organic iron complexa-
tion may still arise from biological ligand production pro-
cesses, should those be affected by pH and/or temperature
(see below). Several models of Fe uptake mechanisms for
phytoplankton exist (Morel et al., 2008; Shaked et al., 2005;
Salmon et al., 2006, see also Sect. 6) and their pH depen-
dence may be largely connected on their reliance on Fe(II) as
the actual species taken up and on the species capability to
regulate pH at the cell surface.
It can be expected that pH driven changes in trace metal
availability will trigger biological feedback mechanisms,
which regulate trace metal availability to marine phytoplank-
ton. These can be in form of exudates, cell lysates, or chloro-
phyll degradation products, and can serve as trace metal lig-
ands to prevent toxic effects or to increase trace metal uptake
rates. The capability of eukaryotic phytoplankton species to
fects or to increase uptake has been addressed (Ahner et al.,
1997; Barbeauetal., 2001; Hutchinsetal., 1999b). However,
information on biological feedback mechanisms in response
to climate change that affect trace metal chemistry is very
limited. It should be noted that in contrast to the open ocean,
estuaries and coastal areas might show a wide range in pH (5
to >9) (e.g. Chen and Durbin, 1994; Sunda and Huntsman,
1998) and obviously in temperature, to which phytoplankton
species are adapted to. However, even considering that phy-
toplankton blooms may cause temporal increases in surface
water pH due to CO2uptake, open ocean species are adapted
to a very narrow range in pH. Further, some coastal areas
such as the Oregon shelf temporarily experience subsurface
input of low pH water and such systems could be valuable
analogs for acidification and temperature effects in natural
Several studies were carried out during the past years
assessing changes in phytoplankton physiology using lab-
oratory batch cultures and mesocosm pCO2perturbations.
Changes in carbon and nitrogen fixation rates, calcification
rates, and carbon export are reflective of pH effects on the
biogeochemistry of the manipulated system (Riebesell et al.,
2007; Orr et al., 2005, see also Biogeosciences Special Issue
“The ocean in the high-CO2world II”), which unequivocally
will also affect trace metal cycling. Further studies also re-
ported combined effects of pCO2and temperature change
(Hare et al., 2007b), and modeling studies also suggest po-
tential interactions with irradiance effects due to changing
stratification in the future ocean on phytoplankton physiol-
ogy and species composition (Boyd and Doney, 2002). Seen
in coherence with biological effects on organic Fe complexa-
tion, and in return again with Fe availability effects on phyto-
plankton, these studies indicate that phytoplankton physiol-
ogy and species composition could exert biological feedback
mechanisms on trace metal cycling as a function of pCO2
and temperature in seawater.
Data from a coastal mesocosm CO2enrichment experi-
ment (Breitbarth et al., 2010) suggest increasing dissolved
iron concentrations with ocean acidification. The authors
invoke a biological feedback mechanism at future seawa-
ter pCO2resulting in increased organic Fe(III) complexa-
tion, which requires further testing. More so, changes in
Fe(II) chemistry were observed.
processes can theoretically be derived based on established
relationships of Fe(II) oxidation rates and inorganic Fe(II)
In part, the underlying
Biogeosciences, 7, 1075–1097, 2010www.biogeosciences.net/7/1075/2010/
E. Breitbarth et al.: Iron biogeochemistry across marine systems – progress from the past decade1087
speciation in presence of different oxidizers over environ-
mentally relevant ranges in pH, temperature, and salinity
(Santana-Casiano et al., 2006; Gonzalez-Davila et al., 2006;
Santana-Casiano et al., 2005; Millero and Sotolongo, 1989;
Millero et al., 1987; Croot and Laan, 2002). For exam-
ple, over a seawater pH decrease of 0.5 units, a 10-fold in-
crease in the half-life of Fe(II) can be expected and the ef-
fects of ocean acidification may thus override the influences
from sea-surface temperature changes (Santana-Casiano et
al., 2005). Fe(II) oxidation kinetics are seemingly affected
by organic complexation (e.g. Croot et al., 2001; Rose, 2003;
Roy et al., 2008b, see also Sect. 6). Fe(II) ligands may be bi-
ologically mediated and potential biological feedback mech-
requiring focused research in this field. Moreover, changing
light regimes are expected to affect photochemical cycling of
Fe in sunlit surface waters (Boyd and Doney, 2002). Both,
light intensity and the light spectrum penetrating the water
Similar to seawater pH, temperature effects have been
rarely studied in coherence with trace metal biogeochemical
measurements in open ocean systems. It has been standard to
date to carry out measurements of organic iron complexation
at room temperature, but temperature has profound effects on
metal speciation and solubility. Further, Rose et al. (2009)
demonstrate synergistic effects of temperature and iron addi-
tions on phytoplankton physiology and community dynam-
ics in Ross Sea waters. Likewise, Fu et al. (2008) demon-
strate that pCO2perturbations alone may not give the sole
answer to potential physiological changes in phytoplankton,
since these can be modified by interactions with Fe limita-
tion. CO2and N2fixation rates in the future ocean may be
Overall, climate change effects on iron speciation and bio-
logical limitation are likely not going to be driven by a single
factor, and Rose et al. (2009) stress the importance of multi-
variate studies in order to understand ecosystem changes. It
also remains to be shown how climate change may alter the
interrelations of iron with other trace metals and macronu-
trients. For example, laboratory experiments showed that
cadmium toxicity can be reduced under high iron availabil-
ity, suggesting that cadmium is a competitive inhibitor of the
iron uptake system or iron dependent cellular processes (Fos-
ter and Morel, 1982; Sunda and Huntsman, 2000). Similar
observation are made for iron limited natural phytoplankton
assemblages from the Southern Ocean by Cullen et al. (2003)
who suggest that Fe limited phytoplankton take up more Cd
resulting in lower Cd:PO4ratios in surface waters. Iron co-
limitations and interactions with other nutrients and trace
metals have been observed (e.g. Schulz et al., 2004; Mills et
al., 2004; Wu et al., 2003; Wells et al., 2005) and apparently
the composition of trace metals and macro nutrients greatly
over, Statham et al. (2008) recently addressed glacier melt-
water input of iron and colloidal matter from the Greenland
Ice Sheet. In the context of the expected changes for Fe bio-
geochemistry discussed here, their study illustrates how at-
mospheric warming can act on various levels, evidentially
affecting iron biogeochemistry in the sea.
We conclude that ocean acidification may result in in-
creased Fe(III) solubility, is likely to decrease stability of
some FeL complexes, and is likely to increase Fe(II) stabil-
ity. It may also change the mechanisms of Fe acquisition by
cells, which though depends on the Fe status of the regime
and the type of phytoplankton species present. Temperature
effects may be smaller in comparison, with most pronounced
changes though to be expected in polar waters. Recommen-
ments of Fe(III) solubility in pH range 7–9 and effects of Fe-
binding ligands along with the study of temperature effects
thereon, and field experiments in upwelling regions with a
focus on low pH regimes. Moreover, the role of organic lig-
ands in enhancing Fe(II) stability needs to be investigated as
well as effects of pH and temperature on the photoreactivity
of Fe(III)L complexes. It is largely unknown what the pH
controls in organisms are, and how they affect Fe acquisi-
tion. More emphasis is needed on measurements and control
of the seawater carbonate system, including pH, in field stud-
ies and laboratory cultures. Protocols carried out to achieve
pH control need to be reported and researchers are urged
to report pH data on the total or seawater pH scale to en-
sure comparability of different studies. The comprehensive
“Guide for Best Practices in Ocean Acidification Research
and Data Reporting” was recently published and should be
adapted for trace metal research (http://www.epoca-project.
Acknowledgements. Funding for the workshop was provided by
EUR-OCEANS and the Swedish Research Council (VR). E. B. and
L. J. H. acknowledge current funding by the German Research
Foundation (DFG, BR 3794 and HO 4217). S. D. is funded by the
DFG and the multi-disciplinary research group NOVUM (Nutrients
Originating in Volcanoes and their effect on the eUphotic zone of
the Marine ecosystem) by the Leibniz Institute of Marine Sciences,
IFM-GEOMAR. D. H. acknowledges funding by US NSF ANT
0741411 and OCE 0825319. The authors greatly appreciate the
comments received from P. W. Boyd on the manuscript.
Edited by: U. Riebesell
www.biogeosciences.net/7/1075/2010/Biogeosciences, 7, 1075–1097, 2010
1088 E. Breitbarth et al.: Iron biogeochemistry across marine systems – progress from the past decade
Aguilar-Islas, A. M., Rember, R. D., Mordy, C. W., and Wu, J.:
Sea ice-derived dissolved iron and its potential influence on the
spring algal bloom in the Bering Sea, Geophys. Res. Lett., 35,
L24601, doi:10.1029/2008gl035736, 2008.
Ahner, B. A., Morel, F. M. M., and Moffett, J. W.: Trace metal
control of phytochelatin production in coastal waters, Limnol.
Oceanogr., 42, 601–608, 1997.
Aluwihare, L. I., Repeta, D. J., and Chen, R. F.: A major biopoly-
meric component to dissolved organic carbon in surface sea wa-
ter, Nature, 387, 166–169, 1997.
Andersson, K., Dahlqvist, R., Turner, D., Stolpe, B., Larsson,
T., Ingri, J., and Andersson, P.: Colloidal rare earth elements
in a boreal river: Changing sources and distributions during
the spring flood, Geochim. Cosmochim. Acta, 70, 3261–3274,
Ardelan, M. V., Holm-Hansen, O., Hewes, C. D., Reiss, C. S., Silva,
N. S., Dulaiova, H., Steinnes, E., and Sakshaug, E.: Natural
iron enrichment around the Antarctic Peninsula in the Southern
Ocean, Biogeosciences, 7, 11–25, 2010,
Assemi, S., Newcombe, G., Hepplewhite, C., and Beckett, R.:
Characterization of natural organic matter fractions separated by
ultrafiltration using flow field-flow fractionation, Water Res., 38,
1467–1476, doi:10.1016/j.watres.2003.11.031, 2004.
Aumont, O. and Bopp, L.: Globalizing results from ocean in situ
iron fertilization studies, Global Biogeochem. Cy., 20, GB2017,
Gb2017, doi:10.1029/2005gb002591, 2006.
Averyt, K. B., Kim, J. P., and Hunter, K. A.: Effect of pH on
measurement of strong copper binding ligands in lakes, Limnol.
Oceanogr., 49, 20–27, 2004.
Baker, A. R. and Jickells, T. D.: Mineral particle size as a con-
trol on aerosol iron solubility, Geophys. Res. Lett., 33, L17608
Baker, A. R., Jickells, T. D., Witt, M., and Linge, K. L.: Trends in
the solubility of iron, aluminium, manganese and phosphorus in
aerosol collected over the Atlantic Ocean, Mar. Chem., 98, 43–
58, doi:10.1016/j.marchem.2005.06.004, 2006.
Baker, A. R., and Croot, P. L.: Atmospheric and marine controls on
aerosol iron solubility in seawater, Mar. Chem., in press, 2009.
Barbeau, K., Moffett, J. W., Caron, D. A., Croot, P. L., and Erdner,
D. L.: Role of protozoan grazing in relieving iron limitation of
phytoplankton, Nature, 380, 61–64, 1996.
Barbeau, K. and Moffett, J. W.: Laboratory and field studies of
colloidal iron oxide dissolution as mediated by phagotrophy and
photolysis, Limnol. Oceanogr., 45, 827–835, 2000.
Barbeau, K., Rue, E. L., Bruland, K. W., and Butler, A.: Photo-
chemical cycling of iron in the surface ocean mediated by micro-
bial iron(III)-binding ligands, Nature, 413, 409–413, 2001.
Barbeau, K.: Photochemistry of organic iron(III) complexing lig-
ands in oceanic systems, Photochem. Photobiol., 82, 1505–1516,
Bauer, J. E., Williams, P. M., and Druffel, E. R. M.: C-14 activity of
dissolved organic-carbon fractions in the North-Central Pacific
and Sargasso Sea, Nature, 357, 667–670, 1992.
Benitez-Nelson, C. R., Vink, S. M., Carrillo, J. H., and Huebert,
B. J.: Volcanically influenced iron and aluminum cloud water
deposition to Hawaii, Atmos. Environ., 37, 535–544, 2003.
Bergquist, B. A. and Boyle, E. A.: Iron isotopes in the Amazon
River system: Weathering and transport signatures, Earth Planet.
Sci. Lett., 248, 54–68, doi:10.1016/j.epsl.2006.05.004, 2006.
Bergquist,B. A.,Wu, J., and Boyle,
ity in oceanic dissolved iron is dominated by the col-
loidal fraction, Geochim. Cosmochim. Acta, 71, 2960–2974,
Berman-Frank, I., Rosenberg, G., Levitan, O., Haramaty, L., and
Mari, X.: Coupling between autocatalytic cell death and trans-
parent exopolymeric particle production in the marine cyanobac-
terium Trichodesmium, Environ. Microbiol., 9, 1415–1422,
Blain, S., Queguiner, B., Armand, L., Belviso, S., Bombled, B.,
Bopp, L., Bowie, A., Brunet, C., Brussaard, C., Carlotti, F.,
Christaki, U., Corbiere, A., Durand, I., Ebersbach, F., Fuda, J.-L.,
Garcia, N., Gerringa, L., Griffiths, B., Guigue, C., Guillerm, C.,
Jacquet, S., Jeandel, C., Laan, P., Lefevre, D., Lo Monaco, C.,
Malits, A., Mosseri, J., Obernosterer, I., Park, Y.-H., Picheral,
M., Pondaven, P., Remenyi, T., Sandroni, V., Sarthou, G.,
Savoye, N., Scouarnec, L., Souhaut, M., Thuiller, D., Timmer-
mans, K., Trull, T., Uitz, J., van Beek, P., Veldhuis, M., Vincent,
D., Viollier, E., Vong, L., and Wagener, T.: Effect of natural iron
fertilization on carbon sequestration in the Southern Ocean, Na-
ture, 446, 1070–1074, 2007.
Blain, S., Bonnet, S., and Guieu, C.: Dissolved iron distribution
in the tropical and sub tropical South Eastern Pacific, Biogeo-
sciences, 5, 269–280, 2008,
Boehme, J. and Wells, M.: Fluorescence variability of marine and
terrestrial colloids: Examining size fractions of chromophoric
dissolved organic matter in the Damariscotta River estuary,
Mar. Chem., 101, 95–103, doi:10.1016//j.marchem.2006.02.001,
Bopp, L., Kohfeld, K. E., Le Quere, C., and Aumont, O.: Dust
impact on marine biota and atmospheric CO2during glacial pe-
riods, Paleoceanography, 18, 1046, doi:10.1029/2002pa000810,
Borer, P. M., Sulzberger, B., Reichard, P., and Kraemer, S. M.: Ef-
fect of siderophores on the light-induced dissolution of colloidal
iron(III) (hydr)oxides, Mar. Chem., 93, 179–193, 2005.
Bowie, A. R., Achterberg, E. P., Sedwick, P. N., Ussher, S., and
Worsfold, P. J.: Real-time monitoring of picomolar concentra-
tions of iron(II) in marine waters using automated flow injection-
chemiluminescence instrumentation, Environ. Sci. Technol., 36,
Bowie, A. R., Achterberg, E. P., Ussher, S., and Worsfold, P. J.: De-
sign of an automated flow injection-chemiluminescence instru-
ment incorporating a miniature photomultiplier tube for moni-
toring picomolar concentrations of iron in seawater, Journal of
Automated Methods andManagement in Chemistry, 2005, 37–
43, doi:10.1155/JAMMC.2005.1137, 2005.
Bowie, A.R., Achterberg, E.P., Croot, P.L., deBaar, H.J.W., Laan,
P., Moffett, J. W., Ussher, S., and Worsfold, P. J.: A community-
wide intercomparison exercise for the determination of dissolved
iron in seawater, Mar. Chem., 98, 81–99, 2006.
Boyanapalli, R., Bullerjahn, G. S., Pohl, C., Croot, P. L., Boyd, P.
W., and McKay, R. M. L.: Luminescent whole-cell cyanobac-
terial bioreporter for measuring Fe availability in diverse ma-
rine environments, Appl. Environ. Microbiol., 73, 1019–1024,
E. A.: Variabil-
Biogeosciences, 7, 1075–1097, 2010 www.biogeosciences.net/7/1075/2010/
E. Breitbarth et al.: Iron biogeochemistry across marine systems – progress from the past decade 1089
Boyd, P.: Ironing out algal issues in the southern ocean, Science,
304, 396–397, 2004.
Boyd, P. W., Wong, C. S., Merrill, J., Whitney, F., Snow, J., Harri-
son, P. J., and Gower, J.: Atmospheric iron supply and enhanced
vertical carbon flux in the NE subarctic Pacific: Is there a con-
nection?, Global Biogeochem. Cy., 12, 429–441, 1998.
Boyd, P. W., Watson, A. J., Law, C. S., and Abraham, E. R.: A
mesoscale phytoplankton bloom in the polar Southern Ocean
stimulated by iron fertilization, Nature, 407, 695–702, 2000.
Boyd, P. W., Crossley, A. C., DiTullio, G. R., Griffiths, F. B.,
Hutchins, D. A., Queguiner, B., Sedwick, P. N., and Trull, T. W.:
Control of phytoplankton growth by iron supply and irradiance
in the subantarctic Southern Ocean: Experimental results from
the SAZ Project, J. Geophys. Res.-Oceans, 106, 31573–31583,
Boyd, P. W. and Doney, S. C.: Modeling regional responses by ma-
rine pelagic ecosystems to global climate change, Geophys. Res.
Lett., 29, 5351–5354, 2002.
Boyd, P. W. and Doney, S. C.: The impact of climate change and
feedbackprocessesontheoceancarboncycle, in: OceanBiogeo-
chemistry, Global Change – the IGBP Series, Springer-Verlag
Berlin, Berlin, 157–193, 2003.
Boyd, P. W., Law, C. S., Wong, C. S., Nojiri, Y., Tsuda, A., Lev-
asseur, M., Takeda, S., Rivkin, R., Harrison, P. J., Strzepek, R.,
Gower, J., McKay, R. M., Abraham, E., Arychuk, M., Barwell-
Clarke, 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., and Yoshimura, T.: The decline and
fate of an iron-induced subarctic phytoplankton bloom, Nature,
428, 549–553, 2004.
Boyd, P. W., Law, C. S., Hutchins, D. A., Abraham, E. R., Croot,
P. L., Ellwood, M., Frew, R. D., Hadfield, M., Hall, J., Handy,
S., Hare, C., Higgins, J., Hill, P., Hunter, K. A., LeBlanc,
K., Maldonado, M. T., McKay, R. M., Mioni, C., Oliver, M.,
Pickmere, S., Pinkerton, M., Safi, K., Sander, S., Sanudo-
Wilhelmy, S. A., Smith, M., Strzepek, R., Tovar-Sanchez, A.,
and Wilhelm, S. W.: FeCycle: Attempting an iron biogeochem-
ical budget from a mesoscale SF6 tracer experiment in unper-
turbed low iron waters, Global Biogeochem. Cy., 19, GB4S20,
Boyd, P. W., Jickells, T., Law, C. S., Blain, S., Boyle, E. A.,
Buesseler, K. O., Coale, K. H., Cullen, J. J., de Baar, H. J.
W., Follows, M., Harvey, M., Lancelot, C., Levasseur, M.,
Owens, N. P. J., Pollard, R., Rivkin, R. B., Sarmiento, J., Schoe-
mann, V., Smetacek, V., Takeda, S., Tsuda, A., Turner, S., and
Watson, A. J.: Mesoscale Iron Enrichment Experiments 1993–
2005: Synthesis and Future Directions, Science, 315, 612–617,
Boyd, P. W.: Implications of large-scale iron fertilization of the
oceans – Introduction and synthesis, Mar. Ecol.-Prog. Ser., 364,
Boyd, P. W., Mackie, D. S., and Hunter, K. A.:
iron deposition to the surface ocean – Modes of iron
supply and biological responses,
Boye, M., Nishioka, J., Croot, P. L., Laan, P., Timmermans, K. R.,
anddeBaar, H.J.W.: Majordeviationsofironcomplexationdur-
Mar. Chem.,in press,
ing 22 days of a mesoscale iron enrichment in the open Southern
Ocean, Mar. Chem., 96, 257–271, 2005.
Brand, L. E., Sunda, W. G., and Guillard, R. R. L.: Limitation
of marine-phytoplankton reproductive rates by zinc, manganese,
and iron Limnol. Oceanogr., 28, 1182–1198, 1983.
Breitbarth, E., Gelting, J., Walve, J., Hoffmann, L. J., Turner, D. R.,
Hassell¨ ov, M., and Ingri, J.: Dissolved iron (II) in the Baltic Sea
surface water and implications for cyanobacterial bloom devel-
opment, Biogeosciences, 6, 2397–2420, 2009,
Breitbarth, E., Bellerby, R. J., Neill, C. C., Ardelan, M. V., Mey-
erh¨ ofer, M., Z¨ ollner, E., Croot, P. L., and Riebesell, U.: Ocean
acidification affects iron speciation during a coastal seawater
mesocosm experiment, Biogeosciences, 7, 1065–1073, 2010,
Bruland, K. W., Rue, E. L., and Smith, G. J.: Iron and macronu-
trients in California coastal upwelling regimes: Implications for
diatom blooms, Limnol. Oceanogr., 46, 1661–1674, 2001.
Bucciarelli, E., Pondaven, P., and Sarthou, G.: Effects of an iron-
light co-limitation on the elemental composition (Si, C, N) of the
Biogeosciences, 7, 657–669, 2010,
Buck, K. N., Lohan, M. C., Berger, C. J. M., and Bruland, K. W.:
Dissolved iron speciation in two distinct river plumes and an es-
tuary: Implications for riverine iron supply, Limnol. Oceanogr.,
52, 843–855, 2007.
Buesseler, K. O., Bauer, J. E., Chen, R. F., Eglinton, T. I., Gustafs-
son, O., Landing, W., Mopper, K., Moran, S. B., Santschi, P.
H., VernonClark, R., and Wells, M. L.: An intercomparison of
cross-flow filtration techniques used for sampling marine col-
loids: Overview and organic carbon results, Mar. Chem., 55, 1–
Buesseler, K. O., Andrews, J. E., Pike, S. M., and Charette, M. A.:
The Effects of Iron Fertilization on Carbon Sequestration in the
Southern Ocean, Science, 304, 414–417, 2004.
Buesseler, K. O., Doney, S. C., Karl, D. M., Boyd, P. W., Caldeira,
K., Chai, F., Coale, K. H., de Baar, H. J. W., Falkowski, P. G.,
Johnson, K. S., Lampitt, R. S., Michaels, A. F., Naqvi, S. W.
A., Smetacek, V., Takeda, S., and Watson, A. J.: Ocean Iron
Fertilization – Moving Forward in a Sea of Uncertainty, Science,
319, 162, doi:10.1126/science.1154305, 2008.
Caldeira, K. and Wickett, M. E.: Anthropogenic carbon and ocean
pH, Nature, 425, 365–365, 2003.
Chase, Z., Johnson, K. S., Elrod, V. A., Plant, J. N., Fitzwa-
ter, S. E., Pickell,L., and Sakamoto,
ganese and iron distributions off central California influenced
by upwelling and shelf width, Mar. Chem., 95, 235–254,
Chen, C.Y., andDurbin, E.G.: EffectsonpHonthegrowthandcar-
bon uptake of marine phytoplankton, Marine Ecology Progress
Series, 109, 83-94, 1994.
Chen, M.andWang, W.X.: Bioavailabilityofnaturalcolloid-bound
iron to marine plankton: Influences of colloidal size and aging,
Limnol. Oceanogr., 46, 1956–1967, 2001.
Chever, F., Sarthou, G., Bucciarelli, E., Blain, S., and Bowie, A. R.:
An iron budget during the natural iron fertilisation experiment
KEOPS (Kerguelen Islands, Southern Ocean), Biogeosciences,
7, 455–468, 2010,
www.biogeosciences.net/7/1075/2010/Biogeosciences, 7, 1075–1097, 2010
1090 E. Breitbarth et al.: Iron biogeochemistry across marine systems – progress from the past decade
Chin, W.-C., Orellana, M. V., and Verdugo, P.: Spontaneous assem-
bly of marine dissolved organic matter into polymer gels, Nature,
391, 568–572, 1998.
Chisholm, S. W., Falkowski, P. G., and Cullen, J. J.: Oceans – Dis-
crediting ocean fertilization, Science, 294, 309–310, 2001.
Coale, K., Johnson, K., Fitzwater, S., Gordon, R., Tanner, S.,
Chavez, F., Ferioli, L., Sakamoto, C., Rogers, P., Millero,
F., Steinberg, P., Nightingale, P., Cooper, D., Cochlan, W.,
Landry, M., Constantinou, J., Rollwagen, G., Trasvina, A., and
Kudela, R.: A massive phytoplankton bloom induced by an
ecosystem-scale iron fertilization experiment in the equatorial
Pacific Ocean, Nature, 383, 495–501, 1996.
Coale, K. H., Johnson, K. S., Chavez, F. P., Buesseler, K. O., Bar-
ber, 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., 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, J. L., Tozzi, S., Koblizek, M., Roberts, A. E., Herndon,
J., Brewster, J., Ladizinsky, N., Smith, G., Cooper, D., Timo-
thy, D., Brown, S. L., Selph, K. E., Sheridan, C. C., Twining,
B. S., and Johnson, Z. I.: Southern Ocean Iron Enrichment Ex-
periment: Carbon Cycling in High- and Low-Si Waters, Science,
304, 408–414, 2004.
Croot, P. L., and Johansson, M.: Determination of iron speciation
by cathodic stripping voltammetry in seawater using the com-
peting ligand 2-(2-thiazolylazo)-p-cresol (TAC), Electroanalysis,
12, 565–576, 2000.
Croot, P. L., Bowie, A. R., Frew, R. D., Maldonado, M. T., Hall,
J. A., Safi, K. A., La Roche, J., Boyd, P. W., and Law, C. S.:
Retention of dissolved iron and Fe-II in an iron induced South-
ern Ocean phytoplankton bloom, Geophys. Res. Lett., 28, 3425–
Croot, P. L. and Laan, P.: Continuous shipboard determination of
Fe(II) in polar waters using flow injection analysis with chemi-
luminescence detection, Analytica Chimica Acta, 466, 261–273,
Croot, P. L., Andersson, K.,¨Ozt¨ urk, M., and Turner, D. R.: The dis-
tribution and speciation of iron along 6◦E in the Southern Ocean,
Deep Sea Res., 51, 2857–2879, 2004.
Croot, P. L., Laan, P., Nishioka, J., Strass, V., Cisewski, B., Boye,
M., Timmermans, K. R., Bellerby, R. G., Goldson, L., Nightin-
gale, P., and de Baar, H. J. W.: Spatial and temporal distribution
of Fe(II) and H2O2during EisenEx, an open ocean mescoscale
iron enrichment, Mar. Chem., 95, 65–88, 2005.
Croot, P. L., Bluhm, K., Schlosser, C., Streu, P., Breit-
barth, E., Frew, R. D., and Ardelan, M. V.:
Fe(II) in Southern Ocean Iron Mesoscale Enrichment Experi-
ments: EIFEX and SOFEX, Geophys. Res. Lett., 35, L19606.
Cullen, J. J. and Boyd, P. W.:
intended and unintended consequences of large-scale ocean
iron fertilization, Mar. Ecol. Progress Ser., 364, 295–301,
Cullen, J. T., Chase, Z., Coale, K. H., Fitzwater, S. E., and Sherrell,
R. M.: Effect of iron limitation on the cadmium to phosphorus
Predicting and verifying the
ratio of natural phytoplankton assemblages from the Southern
Ocean, Limnol. Oceanogr., 48, 1079–1087, 2003.
Dalbec, A. A. and Twining, B. S.: Remineralization of bioavailable
iron by a heterotrophic dinoflagellate, Aquatic Microbial Ecol.,
54, 279–290, doi:10.3354/ame01270, 2009.
de Baar, H. J. W., Buma, A. G. J., Nolting, R. F., Cad´ ee, G. C.,
Jacques, G., and Tr´ eguer, P. J.: On iron limitation of the South-
ern Ocean: experimental observations in the Weddell and Scotia
Seas, Mar. Ecol. Progr. Series, 65, 105–122, 1990.
de Baar, H. J. W., Dejong, J. T. M., Bakker, D. C. E., Loscher,
B. M., Veth, C., Bathmann, U., and Smetacek, V.: Importance
of iron for plankton blooms and carbondioxide drawdown in the
Southern Ocean, Nature, 373, 412–415, 1995.
de Baar, H. J. W., and La Roche, J.: Trace Metals in the Oceans:
Evolution, Biology and Global Change, in: Marine Science
Frontiers for Europe, edited by: Wefer, G., Lamy, F., and Man-
toura, F., Springer Verlag, Berlin, 79–105, 2003.
de Baar, H. J. W., Boyd, P. W., Coale, K. H., Landry, M. R.,
Tsuda, A., Assmy, P., Bakker, D. C. E., Bozec, Y., Barber, R.
T., Brzezinski, M. A., Buesseler, K. O., Boye, M., Croot, P.
L., Gervais, F., Gorbunov, M. Y., Harrison, P. J., Hiscock, W.
T., Laan, P., Lancelot, C., Law, C. S., Levasseur, M., Marchetti,
A., Millero, F. J., Nishioka, J., Nojiri, Y., van Oijen, T., Riebe-
sell, U., Rijkenberg, M. J. A., Saito, H., Takeda, S., Timmer-
mans, K. R., Veldhuis, M. J. W., Waite, A. M., and Wong, C. S.:
Synthesis of iron fertilization experiments: From the Iron Age
in the Age of Enlightenment, J. Geophys. Res., 110, C09S16,
de Baar, H. J. W., Gerringa, L. J. A., Laan, P., and Timmer-
mans, K. R.: Efficiency of carbon removal per added iron in
ocean iron fertilization, Mar. Ecol. Progr. Series, 364, 269–282,
de Jong, J., Schoemann, V., Tison, J. L., Becquevort, S., Mas-
son, F., Lannuzel, D., Petit, J., Chou, L., Weis, D., and Mat-
tielli, N.: Precise measurement of Fe isotopes in marine sam-
ples by multi-collector inductively coupled plasma mass spec-
trometry (MC-ICP-MS), Analytica Chimica Acta, 589, 105–119,
Decho, A. W.: Microbial exopolymer secretions in ocean envi-
ronments – their role(s) in food webs and marine processes,
Oceanogr. Mar. Biol., 28, 73–153, 1990.
Duce, R. A., Liss, P. S., Merrill, J. T., Atlas, E. L., Buat-Menard,
P., Hicks, B. B., Miller, J. M., Prospero, J. M., Arimoto, R.,
Church, T. M., Ellis, W., Galloway, J. N., Hansen, L., Jickells,
T. D., Knap, A. H., Reinhardt, K. H., Schneider, B., Soudine,
A., Tokos, J. J., Tsunogai, S., Wollast, R., and Zhou, M.: The
atmospheric input of trace species to the world ocean, Global
Biogeochem. Cy., 5, 193–259, 1991.
Duce, R. A., LaRoche, J., Altieri, K., Arrigo, K. R., Baker, A.
R., Capone, D. G., Cornell, S., Dentener, F., Galloway, J.,
Ganeshram, R. S., Geider, R. J., Jickells, T., Kuypers, M. M.,
Langlois, R., Liss, P. S., Liu, S. M., Middelburg, J. J., Moore,
C. M., Nickovic, S., Oschlies, A., Pedersen, T., Prospero, J.,
Schlitzer, R., Seitzinger, S., Sorensen, L. L., Uematsu, M., Ul-
loa, O., Voss, M., Ward, B., and Zamora, L.: Impacts of atmo-
spheric anthropogenic nitrogen on the open ocean, Science, 320,
893–897, doi:10.1126/science.1150369, 2008.
Duggen, S., Croot, P., Schacht, U., and Hoffmann, L.: Subduc-
tion zone volcanic ash can fertilize the surface ocean and stim-
Biogeosciences, 7, 1075–1097, 2010www.biogeosciences.net/7/1075/2010/
E. Breitbarth et al.: Iron biogeochemistry across marine systems – progress from the past decade 1091
ulate phytoplankton growth: Evidence from biogeochemical ex-
periments and satellite data, Geophys. Res. Lett., 34, L01612,
Duggen, S., Olgun, N., Croot, P., Hoffmann, L., Dietze, H.,
Delmelle, P., and Teschner, C.: The role of airborne volcanic
ash for the surface ocean biogeochemical iron-cycle: a review,
Biogeosciences, 7, 827–844, 2010,
Dupont, C.L., Yang, S., Palenik, B., andBourne, P.E.: Modernpro-
teomes contain putative imprints of ancient shifts in trace metal
geochemistry, Proc. Natl. Acad. Sci. USA, 103, 17822–17827,
Dutkiewicz,S., Follows,M. J.,
actions of the iron and phosphorus cycles:
dimensional model study, Global Biogeochem. Cy., 19, GB1021,
Editorial: The Law of the Sea, Nature Geosci., 2, 153–153,
Edwards, R. and Sedwick, P.: Iron in East Antarctic snow: Impli-
cations for atmospheric iron deposition and algal production in
Antarctic waters, Geophys. Res. Lett., 28, 3907–3910, 2001.
Elrod, V. A., Berelson, W. M., Coale, K. H., and Johnson, K. S.:
The flux of iron from continental shelf sediments: A missing
source for global budgets, Geophys. Res. Lett., 31(4), L12307,
Engel, A., Thoms, S., Riebesell, U., Rochelle-Newall, E., and Zon-
dervan, I.: Polysaccharide aggregation as a potential sink of ma-
rine dissolved organic carbon, Nature, 428, 929–932, 2004.
Fan, S.-M.: Photochemical and biochemical controls on reactive
oxygen and iron speciation in the pelagic surface ocean, Mar.
Chem., 109, 152–164, 2008.
Fan, S. M., Moxim, W. J., and Levy, H.:
bioavailable iron to the ocean, Geophys. Res. Lett., 33, L07602,
Feely, R. A., Sabine, C. L., Lee, K., Berelson, W., Kleypas, J.,
Fabry, V. J., and Millero, F. J.: Impact of Anthropogenic CO2
on the CaCO3System in the Oceans, Science, 305, 362–366,
Firme, G. F., Rue, E. L., Weeks, D. A., Bruland, K. W., and
Hutchins, D. A.: Spatial and temporal variability in phytoplank-
ton iron limitation along the California coast and consequences
for Si, N, and C biogeochemistry, Global Biogeochem. Cy.,
17(13), 1016, doi:10.1029/2001gb001824, 2003.
Floge, S. A. and Wells, M. L.: Variation in colloidal chromophoric
dissolved organic matter in the Damariscotta Estuary, Maine,
Limnol. Oceanogr., 52, 32–45, 2007.
Foster, P. L. and Morel, F. M. M.: Reversal of cadmium toxicity
in a diatom: An interaction between cadmium activity and iron,
Limnol. Oceanogr., 27, 745–752, 1982.
Franck, V. M., Bruland, K. W., Hutchins, D. A., and Brzezinski,
M. A.: Iron and zinc effects on silicic acid and nitrate uptake
kinetics in three high-nutrient, low-chlorophyll (HNLC) regions,
Mar. Ecol.-Prog. Ser., 252, 15–33, 2003.
Frew, R. D., Hutchins, D. A., Nodder, S., Sanudo-Wilhelmy, S.,
Tovar-Sanchez, A., Leblanc, K., Hare, C. E., and Boyd, P. W.:
Particulate iron dynamics during FeCycle in subantarctic waters
southeast of New Zealand, Global Biogeochemical Cycles, 20,
GB1S93, doi:10.1029/2005GB002558, 2006.
Frogner, P., Gislason, S. R., and Oskarsson, N.: Fertilizing potential
and Parekh,P.: Inter-
Aeolian input of
of volcanic ash in ocean surface water, Geology, 29, 487–490,
Fu, F.-X., Mulholland, M. R., Garcia, N. S., Beck, A., Bernhardt, P.
W., Warner, M.E., Sa˜ nudo-Wilhelmy, S.A., andHutchins, D.A.:
Interactions between changing pCO2, N2fixation, and Fe limi-
tation in the marine unicellular cyanobacterium Crocosphaera,
Limnol. Oceanogr., 53, 2472–2484, 2008.
Furman, J. A. and Capone, D. G.: Possible biogeochemical con-
sequences of ocean fertilization, Limnol. Oceanogr., 36, 1951–
Gelting, J., Breitbarth, E., Stolpe, B., Hassell¨ ov, M., and Ingri, J.:
Fractionation of iron species and iron isotopes in the Baltic Sea
euphotic zone, Biogeosciences Discuss., 6, 6491–6537, 2009,
Gerringa, L. J. A., Rijkenberg, M. J. A., Wolterbeek, H. T., Verburg,
T. G., Boye, M., and de Baar, H. J. W.: Kinetic study reveals
weak Fe-binding ligand, which affects the solubility of Fe in the
Scheldt estuary, Mar. Chem., 103, 30–45, 2007.
Gervais, F., Riebesell, U., andGorbunov, M.Y.: Changesinprimary
productivity and chlorophyll a in response to iron fertilization in
the Southern Polar Frontal Zone, Limnol. Oceanogr., 47, 1324–
Ginoux, P., Prospero, J. M., Torres, O., and Chin, M.: Long-
term simulation of global dust distribution with the GOCART
model: correlation with North Atlantic Oscillation, Environ-
mental Modelling & Software, 19, 113–128, doi:10.1016/s1364-
Gledhill, M. and van den Berg, C. M. G.: Determination of com-
peaxtion of Fe(III) with natural organic complexing ligands in
seawater using cathodic stripping voltammetry, Mar. Chem., 47,
Gledhill,M.: The determination of heme b in marine
phyto- and bacterioplankton, Mar. Chem., 103, 393–403,
Gnanadesikan, A., Sarmiento, J. L., and Slater, R. D.: Effects of
patchy ocean fertilization on atmospheric carbon dioxide and
biological production, Global Biogeochem.l Cy., 17(17), 1050,
Gonzalez-Davila, M., Santana-Casiano, J. M., and Millero, F. J.:
Competition between O-2 and H2O2in the oxidation of Fe(II) in
natural waters, J. Solut. Chem., 35, 95–111, 2006.
Guieu, C., Bonnet, S., Wagener, T., and Loye-Pilot, M. D.: Biomass
burning as a source of dissolved iron to the open ocean?, Geo-
phys. Res. Lett., 32, L19608, doi:10.11029/12005GL022962,
Gustafsson, O., Widerlund, A., Andersson, P. S., Ingri, J., Roos, P.,
and Ledin, A.: Colloid dynamics and transport of major elements
through a boreal river – brackish bay mixing zone, Mar. Chem.,
71, 1–21, 2000.
Han, Q., Moore, J. K., Zender, C., Measures, C., and Hy-
des, D.: Constraining oceanic dust deposition using surface
ocean dissolved Al, Global Biogeochem. Cy., 22, GB2003,
Hansard, S. P., Landing, W. M., Measures, C. I., and Voelkar, B. M.:
Dissolved iron(II) in the Pacific Ocean: Measurements from PO2
and P16N Clivar/CO2repeat hydrography expeditions, Deep Sea
Res. I, 56(7), 1117–1129, 2009.
Hare, C. E., DiTullio, G. R., Trick, C. G., Wilhelm, S. W., Bruland,
K. W., Rue, E. L., and Hutchins, D. A.: Phytoplankton commu-
www.biogeosciences.net/7/1075/2010/ Biogeosciences, 7, 1075–1097, 2010
1092 E. Breitbarth et al.: Iron biogeochemistry across marine systems – progress from the past decade
nity structure changes following simulated upwelled iron inputs
in the Peru upwelling region, Aquatic Microbial Ecology, 38,
Hare, C. E., DiTullio, G. R., Riseman, S. F., Crossley, A. C., Popels,
L. C., Sedwick, P. N., and Hutchins, D. A.: Effects of changing
continuous iron input rates on a Southern Ocean algal assem-
blage, Deep-Sea Research Part I-Oceanographic Research Pa-
pers, 54, 732–746, doi:10.1016/j.dsr.2007.02.001, 2007a.
Hare, C. E., Leblanc, K., DiTullio, G. R., Kudela, R. M., Zhang,
Y., Lee, P. A., Riseman, S., and Hutchins, D. A.: Consequences
of increased temperature and CO2for phytoplankton community
structureintheBeringSea, MarineEcologyProgressSeries, 352,
9–16, doi:10.3354/meps07182, 2007b.
Hassell¨ ov, M. and von der Kammer, F.: Iron Oxides as Geochemi-
cal Nanovectors for Metal Transport in Soil-River Systems, Ele-
ments, 4, 401–406, doi:10.2113/gselements.4.6.401, 2008.
Hassler, C. S., Slaveykova, V. I., and Wilkinson, K. J.: Discrim-
inating between intra- and extracellular metals using chemical
extractions, Limnol. Oceanogr. Methods, 2, 237–247, 2004.
Hassler, C. S., Twiss, M. R., McKay, R. M. L., and Bullerjahn, G.
S.: Optimization of iron-dependent cyanobacterial (Synechococ-
cus, cyanophyceae) bioreporters to measure iron bioavailability,
J. Phycol., 42, 324–335, 2006.
Hassler, C. S., Chafin, R. D., Klinger, M. B., and Twiss, M. R.:
Application of the biotic ligand model to explain potassium in-
teraction with thallium uptake and toxicity to plankton, Environ.
Toxicol. Chem., 26, 1139–1145, 2007.
Hassler, C. S. and Schoemann, V.: Bioavailability of organically
bound Fe to model phytoplankton of the Southern Ocean, Bio-
geosciences, 6, 2281–2296, 2009,
Heldal, M., Fagerbakke, K. M., Tuomi, P., and Bratbak, G.: Abun-
dant populations of iron and manganese sequestering bacteria in
coastal water, Aquatic Microbial Ecology, 11, 127–133, 1996.
Ho, T. Y., Quigg, A., Finkel, Z. V., Milligan, A. J., Wyman, K.,
Falkowski, P. G., and Morel, F. M. M.: The elemental composi-
tion of some marine phytoplankton, J. Phycol., 39, 1145–1159,
Hoagland, K. D., Rosowski, J. R., Gretz, M. R., and Roemer, S.
C.: Diatom extracellular polymetric substances – function, fine-
structure, chemistry, and physiology, J. Phycol., 29, 537–566,
Hoffmann, L. J., Peeken, I., and Lochte, K.: Iron, silicate, and
light co-limitation of three Southern Ocean diatom species, Polar
Biol., 31, 1067–1080, doi:10.1007/s00300-008-0448-6, 2008.
Holm-Hansen, O., Mitchell, B. G., Hewes, C. D., and Karl, D. M.:
Phytoplankton blooms in the vicinity of Palmer Station, Antarc-
tica, Polar Biology, 10, 49–57, 1989.
Hopkinson, B. M. and Barbeau, K. A.: Organic and redox speci-
ation of iron in the eastern tropical North Pacific suboxic zone,
Mar. Chem., 106, 2–17, 2007.
Hopkinson, B. M., Roe, K. L., and Barbeau, K. A.: Heme uptake by
Microscilla marina and evidence for heme uptake systems in the
genomes of diverse marine bacteria, Appl. Environ. Microbiol.,
74, 6263–6270, doi:10.1128/aem.00964-08, 2008.
Howell, K. A., Achterberg, E. P., Tappin, A. D., and Worsfold, P.
J.: Colloidal metals in the tamar estuary and their influence on
metal fractionation by membrane filtration, Environ. Chem., 3,
199–207, doi:10.1071/en06004, 2006.
Hudson, R. J. M. and Morel, F. M. M.: Iron transport in marine
phytoplankton – kinetics of cellular and medium coordination
reactions, Limnol. Oceanogr., 35, 1002–1020, 1990.
Hunter, K. A., and Boyd, P. W.: Iron-binding ligands and their role
in the ocean biogeochemistry of iron, Environ. Chem., 4, 221–
232, doi:10.1071/en07012, 2007.
Hurst, M. P. and Bruland, K. W.: An investigation into the exchange
of iron and zinc between soluble, colloidal, and particulate size-
fractions in shelf waters using low-abundance isotopes as tracers
in shipboard incubation experiments, Mar. Chem., 103, 211–226,
Hutchins, D. A. and Bruland, K. W.: Grazer-mediated regeneration
and assimilation of Fe, Zn and Mn from planktonic prey, Mar.
Ecol. Progr. Series, 110, 259–269, 1994.
Hutchins, D. A., Wang, W. X., and Fisher, N. S.: Copepod grazing
and the biogeochemical fate of diatom iron, Limnol. Oceanogr.,
40, 989–994, 1995.
Hutchins, D. A. and Bruland, K. W.: Iron-limited diatom growth
and Si:N uptake ratios in a coastal upwelling regime, Nature,
393, 561–564, 1998.
Hutchins, D. A., Franck, V. M., Brzezinski, M. A., and Bruland,
K. W.: Inducing phytoplankton iron limitation in iron-replete
coastal waters with a strong chelating ligand, Limnol. Oceanogr.,
44, 1009–1018, 1999a.
Hutchins, D. A., Witter, A. E., Butler, A., and Luther III, G. W.:
Competition among marine phytoplankton for different chelated
iron species, Nature, 400, 858–861, 1999b.
Hutchins, D. A., Pustizzi, F., Hare, C. E., and DiTullio, G. R.:
A shipboard natural community continuous culture system for
ecologically relevant low-level nutrient enrichment experiments,
Limnol. Oceanogr.-Methods, 1, 82–91, 2003.
Ingri, J., Malinovsky, D., Rodushkin, I., Baxter, D. C., Widerlund,
A., Andersson, P., Gustafsson, O., Forsling, W., and Ohlander,
B.: Iron isotope fractionation in river colloidal matter, Earth
Planet. Sci. Lett., 245, 792–798, 2006.
Jacobson, M. Z.: Studying ocean acidification with conservative,
stable numerical schemes for nonequilibrium air-ocean exchange
and ocean equilibrium chemistry, J. Geophys. Res.-Atmos., 110,
D07302, doi:10.01029/02004JD005220 2005.
Jickells, T. and Spokes, L. J.: Atmospheric iron inputs into the
oceans, in: The Biogeochemistry of Iron in Seawater, edited by:
Turner, D. R., and Hunter, K. A., John Wiley and Sons Ltd., West
Sussex, England, 85–121, 2001.
Jickells, T. D., Dorling, S., Deuser, W. G., Church, T. M., Arimoto,
R., and Prospero, J. M.: Air-borne dust fluxes to a deep water
sediment trap in the Sargasso Sea, Global Biogeochem. Cy., 12,
Jickells, T. D., An, Z. S., Andersen, K. K., Baker, A. R., Bergametti,
G., Brooks, N., Cao, J. J., Boyd, P. W., Duce, R. A., Hunter,
K. A., Kawahata, H., Kubilay, N., laRoche, J., Liss, P. S., Ma-
howald, N., Prospero, J. M., Ridgwell, A. J., Tegen, I., and Tor-
res, R.: Global Iron Connections Between Desert Dust, Ocean
Biogeochemistry, and Climate, Science, 308, 67–71, 2005.
Johnson, K. S.: Iron supply and demand in the upper ocean: Is ex-
traterrestrial dust a significant source of bioavailable iron?, Glob.
Biogeochem. Cy., 15, 61–63, 2001.
Johnson, K. S., Boyle, E., Bruland, K. W., Coale, K., Measures, C.,
Moffett, J., Aguilar-Islas, A., Barbeau, K., Bergquist, B., Bowie,
A., Buck, K., Cai, Y., Chase, Z., Cullen, J., Doi, T., Elrod, V.,
Biogeosciences, 7, 1075–1097, 2010www.biogeosciences.net/7/1075/2010/
E. Breitbarth et al.: Iron biogeochemistry across marine systems – progress from the past decade 1093
Fitzwater, S., Gordon, M., King, A., Laan, P., Laglera-Baquer,
L., Landing, W., Lohan, M., Mendez, J., Milne, A., Obata, H.,
Ossiander, L., Plant, J., Sarthou, G., Sedwick, P., Smith, G. J.,
Sohst, B., Tanner, S., van den Berg, S., and Wu, J.: The SAFe
Iron Intercomparison Cruise: An International Collaboration to
Develop Dissolved Iron in Seawater Standards, EOS, Transac-
tions of the American Geophysical Union, 88, 131–132, 2007.
Johnson, W. K., Miller, L. A., Sutherland, N. E., and Wong, C. S.:
Iron transport by mesoscale Haida eddies in the Gulf of Alaska,
Deep-Sea Res., 52, 933–953, doi:10.1016/j.dsr2.2004.08.017,
Jones, M. T. and Gislason, S. R.: Rapid releases of metal salts
and nutrients following the deposition of volcanic ash into aque-
ous environments, Geochim. Cosmochim. Acta, 72, 3661–3680,
Journet, E., Desboeufs, K. V., Caquineau, S., and Colin, J. L.: Min-
eralogy as a critical factor of dust iron solubility, Geophys. Res.
Lett., 35, L07805, doi:10.1029/2007gl031589, 2008.
Kintisch, E.: Carbon sequestration: Should oceanographers pump
iron?, Science, 318, 1368–1370, 2007.
Kondo, Y., Takeda, S., Nishioka, J., Obata, H., Furuya, K., John-
son, W. K., and Wong, C. S.:
ing ligands during an iron enrichment experiment in the west-
ern subarctic North Pacific, Geophys. Res. Lett., 35, L12601,
Krachler, R., Jirsa, F., and Ayromlou, S.: Factors influencing the
dissolved iron input by river water to the open ocean, Biogeo-
sciences, 2, 311–315, 2005,
Lacan, F., Radic, A., Jeandel, C., Poitrasson, F., Sarthou, G.,
Pradoux, C., and Freydier, R.: Measurement of the isotopic com-
position of dissolved iron in the open ocean, Geophys. Res. Lett.,
35, L24610, doi:10.1029/2008gl035841, 2008.
La¨ es, A., Blain, S., Laan, P., Achterberg, E. P., Sarthou, G., and de
Baar, H. J. W.: Deep dissolved iron profiles in the eastern North
Atlantic in relation to water masses, Geophys. Res. Lett., 30(4),
1902, doi:10.1029/2003gl017902, 2003.
La¨ es, A., Blain, S., Laan, P., Ussher, S. J., Achterberg, E. P., Trguer,
P., and de Baar, H. J. W.: Sources and transport of dissolved
iron and manganese along the continental margin of the Bay of
Biscay, Biogeosciences, 4, 181–194, 2007,
Laglera, L. M. and van den Berg, C. M. G.: Evidence for geochem-
ical control of iron by humic substances in seawater, Limnol.
Oceanogr., 54, 610–619, 2009.
Lam, C. K. S. C. C., Jickells, T. D., Richardson, D. J., and Russell,
D. A.: Fluorescence-Based Siderophore Biosensor for the Deter-
mination of Bioavailable Iron in Oceanic Waters, Anal. Chem.,
78, 5040–5045, doi:10.1021/ac060223t, 2006.
Lam, P. J. and Bishop, J. K. B.: The continental margin is a key
source of iron to the HNLC North Pacific Ocean, Geophys. Res.
Lett., 35(5), L07608, doi:10.1029/2008gl033294, 2008.
Lancelot, C., de Montety, A., Goosse, H., Becquevort, S., Schoe-
mann, V., Pasquer, B., and Vancoppenolle, M.: Spatial distribu-
tion of the iron supply to phytoplankton in the Southern Ocean:
a model study, Biogeosciences, 6, 2861–2878, 2009,
Lannuzel, D., Schoemann, V., de Jong, J., Tison, J. L., and
Chou, L.: Distribution and biogeochemical behaviour of iron
Organic iron(III) complex-
in the East Antarctic sea ice, Mar. Chem., 106, 18–32,
Lannuzel, D., Schoemann, V., de Jong, J., Chou, L., Delille, B.,
Becquevort, S., and Tison, J.-L.: Iron study during a time series
in the western Weddell pack ice, Mar. Chem., 108, 85–95, 2008.
Liss, P., Chuck, A., Bakker, D., and Turner, S.: Ocean fertilization
with iron: effects on climate and air quality, Tellus Ser. B-Chem.
Phys. Meteorol., 57, 269–271, 2005.
Liu, X. W. and Millero, F. J.: The solubility of iron hydroxide
in sodium chloride solutions, Geochim. Cosmochim. Acta, 63,
Liu, X. W. and Millero, F. J.: The solubility of iron in seawater,
Mar. Chem., 77, 43–54, 2002.
Lohan, M. C. and Bruland, K. W.: Importance of vertical mixing
for additional sources of nitrate and iron to surface waters of the
Columbia River plume: Implications for biology, Mar. Chem.,
98, 260–273, doi:10.1016/j.marchem.2005.10.003, 2006.
Loscher, B. M., DeBaar, H. J. W., DeJong, J. T. M., Veth, C., and
Dehairs, F.: The distribution of Fe in the Antarctic Circumpolar
Current, Deep-Sea Res., 44, 143–187, 1997.
Luo, C., Mahowald, N., Bond, T., Chuang, P. Y., Artaxo, P.,
Siefert, R., Chen, Y., and Schauer, J.: Combustion iron distribu-
tion and deposition, Global Biogeochem. Cy., 22(17), GB1012,
Lyv´ en, B., Hassellov, M., Turner, D. R., Haraldsson, C., and An-
dersson, K.: Competition between iron- and carbon-based col-
loidal carriers for trace metals in a freshwater assessed using
flow field-flow fractionation coupled to ICPMS, Geochim. Cos-
mochim. Acta, 67, 3791–3802, 2003.
Mackey, D. J., O’Sullivan, J. E., and Watson, R. J.: Iron in the
western Pacific: a riverine or hydrothermal source for iron in the
Equatorial Undercurrent?, Deep-Sea Res., 49, 877–893, 2002.
Mahowald, N., Jickells, T. D., Baker, A. R., Artaxo, P., Benitez-
Nelson, C. R., Bergametti, G., Bond, T. C., Chen, Y., Cohen,
D. D., Herut, B., Kubilay, N., Losno, R., Luo, C., Maenhaut,
W., McGee, K. A., Okin, G. S., Siefert, R. L., and Tsukuda, S.:
Global distribution of atmospheric phosphorus sources, concen-
trations and deposition rates, and anthropogenic impacts, Global
Biogeochem. Cy., 22, GB4026, doi:10.1029/2008gb003240,
Mahowald, N. M., Baker, A. R., Bergametti, G., Brooks, N.,
Duce, R. A., Jickells, T. D., Kubilay, N., Prospero, J. M.,
and Tegen, I.: Atmospheric global dust cycle and iron in-
puts to the ocean, Global Biogeochem. Cy., 19, GB4025,
Maldonado, M. T., Boyd, P. W., Harrison, P. J., and Price, N. M.:
Co-limitation of phytoplankton growth by light and Fe during
winter in the NE subarctic Pacific Ocean, Deep-Sea Res., 46,
Maldonado, M. T., Strzepek, R. F., Sander, S., and Boyd, P. W.: Ac-
quisition of iron bound to strong organic complexes, with differ-
ent Fe binding groups and photochemical reactivities, by plank-
ton communities in Fe-limited subantarctic waters, Global Bio-
geochem., 19, GB4S23, doi:10.1029/2005GB002481, 2005.
Marchetti, A., Parker, M. S., Moccia, L. P., Lin, E. O., Ar-
rieta, A. L., Ribalet, F., Murphy, M. E. P., Maldonado, M.
T., and Armbrust, E. V.: Ferritin is used for iron storage in
bloom-forming marine pennate diatoms, Nature, 457, 467–470,
www.biogeosciences.net/7/1075/2010/ Biogeosciences, 7, 1075–1097, 2010
1094E. Breitbarth et al.: Iron biogeochemistry across marine systems – progress from the past decade
Martin, J. H.: Glacial-interglacial CO2change: the iron hypothesis,
Paleoceanography, 5, 1–13, 1990.
Mawji, E., Gledhill, M., Milton, J. A., Tarran, G. A., Ussher, S.,
Thompson, A., Wolff, G. A., Worsfold, P. J., and Achterberg,
E. P.: Hydroxamate Siderophores: Occurrence and Importance
in the Atlantic Ocean, Environ. Sci. Technol., 42, 8675–8680,
McKay, R., Michael, L, la Roche, J., Yakunin, A., F, Durnford, D.
G., and Geider, R. J.: Accumulation of Ferredoxin and Flavo-
doxin in a Marine Diatom in response to Fe, J. Phycology, 35,
Millero, F. J., Sotolongo, S., and Izaguirre, M.: The oxidation kinet-
ics of Fe(II) in seawater, Geochim. Cosmochim. Acta, 51, 793–
Millero, F. J. and Sotolongo, S.: The oxidation of Fe(II) with H2O2
in seawater, Geochim. Cosmochim. Acta, 53, 1867–1873, 1989.
Mills, M. M., Ridame, C., Davey, M., La Roche, J., and Geider, R.
J.: Iron and phosphorus co-limits nitrogen fixation in the eastern
tropical North Atlantic, Nature, 429, 292–294, 2004.
Moore, C. M., Mills, M. M., Milne, A., Langlois, R., Achter-
berg, E. P., Lochte, K., Geider, R. J., and La Roche, J.: Iron
limits primary productivity during spring bloom development in
the central North Atlantic, Global Change Biol., 12, 626–634
Moore, C. M., Hickman, A. E., Poulton, A. J., Seeyave, S., and Lu-
cas, M. I.: Iron-light interactions during the CROZet natural iron
bloom and EXport experiment (CROZEX): II – Taxonomic re-
sponses and elemental stoichiometry, Deep-Sea Res., 54, 2066–
2084, doi:10.1016/j.dsr2.2007.06.015, 2007a.
Moore, C. M., Seeyave, S., Hickman, A. E., Allen, J. T., Lu-
cas, M. I., Planquette, H., Pollard, R. T., and Poulton, A.
J.: Iron-light interactions during the CROZet natural iron
bloom and EXport experiment (CROZEX) I: Phytoplankton
growth and photophysiology, Deep-Sea Res., 54, 2045–2065,
Moran, S.B., Yeats, P.A., andBalls, P.W.: Ontheroleofcolloidsin
A comparison of model results and field data, Cont. Shelf Res.,
16, 397–408, 1996.
Morel, F. M. M. and Price, N. M.: The biogeochemical cycles of
trace metals in the oceans, Science, 300, 944–947, 2003.
Morel, F. M. M., Kustka, A. B., and Shaked, Y.: The role of
unchelated Fe in the iron nutrition of phytoplankton, Limnol.
Oceanogr., 53, 400–404, 2008.
Mosley, L. M., Hunter, K. A., and Ducker, W. A.: Forces between
colloid particles in natural waters, Environ. Sci. Technol., 37,
3303–3308, doi:10.1021/es026216d, 2003.
Mylon, S. E., Chen, K. L., and Elimelech, M.: Influence of
natural organic matter and ionic composition on the kinet-
ics and structure of hematite colloid aggregation:
tions to iron depletion in estuaries, Langmuir, 20, 9000–9006,
Nowostawska, U., Kim, J. P., and Hunter, K. A.: Aggregation of
riverine colloidal iron in estuaries: A new kinetic study using
stopped-flow mixing, Mar. Chem., 110, 205–210, 2008.
Nunn, B. L. and Timperman, A. T.: Marine Proteomics, Mar. Ecol.
Progr. Series, 332, 281–289, 2007.
Orr, J. C., Fabry, V. J., Aumont, O., Bopp, L., Doney, S. C., Feely,
R. A., Gnanadesikan, A., Gruber, N., Ishida, A., Joos, F., Key,
R. M., Lindsay, K., Maier-Reimer, E., Matear, R., Monfray, P.,
Mouchet, A., Najjar, R. G., Plattner, G. K., Rodgers, K. B.,
Sabine, C. L., Sarmiento, J. L., Schlitzer, R., Slater, R. D., Tot-
terdell, I. J., Weirig, M. F., Yamanaka, Y., and Yool, A.: Anthro-
pogenic ocean acidification over the twenty-first century and its
impact on calcifying organisms, Nature, 437, 681–686, 2005.
¨Ozt¨ urk, M., Steinnes, E., and Sakshaug, E.: Iron Speciation in
the Trondheim Fjord from the Perspective of Iron Limitation
for Phytoplankton, Estuarine, Coastal Shelf Sci.e, 55, 197–212,
¨Ozt¨ urk, M. and Bizsel, N.: Iron speciation and biogeochemistry
in different nearshore waters, Mar. Chem., 83, 145–156, 2003.
¨Ozt¨ urk, M., Croot, P. L., Bertilsson, S., Abrahamsson, K., Karlson,
B., David, R., Fransson, A., and Sakshaug, E.: Iron enrichment
and photoreduction of iron under UV and PAR in the presence of
hydroxycarboxylic acid: implications for phytoplankton growth
in the Southern Ocean, Deep Sea Res., 51, 2841–2856, 2004.
Paytan, A., Mackey, K. R. M., Chen, Y., Lima, I. D., Doney, S.
C., Mahowald, N., Labiosa, R., and Postf, A. F.: Toxicity of
Sci. USA, 106, 4601–4605, di:10.1073/pnas.0811486106, 2009.
Peers, G. and Price, N. M.: Copper-containing plastocyanin used
for electron transport by an oceanic diatom, Nature, 441, 341–
Pickell, L. D., Wells, M. L., Trick, C. G., and Cochlan, W. P.:
A sea-going continuous culture system for investigating phyto-
plankton community response to macro- and micro-nutrient ma-
nipulations, Limnol. Oceanogr.-Methods, 7, 21–32, 2009.
Planquette, H., Statham, P. J., Fones, G. R., Charette, M. A., Moore,
C. M., Salter, I., Nedelec, F. H., Taylor, S. L., French, M., Baker,
A. R., Mahowald, N., and Jickells, T. D.: Dissolved iron in the
vicinity of the Crozet Islands, Southern Ocean, Deep-Sea Res.,
54, 1999–2019, doi:10.1016/j.dsr2.2007.06.019, 2007.
Pollard, R. T., Salter, I., Sanders, R. J., Lucas, M. I., Moore, C. M.,
Mills, R. A., Statham, P. J., Allen, J. T., Baker, A. R., Bakker,
D. C. E., Charette, M. A., Fielding, S., Fones, G. R., French,
M., Hickman, A. E., Holland, R. J., Hughes, J. A., Jickells, T.
D., Lampitt, R. S., Morris, P. J., Nedelec, F. H., Nielsdottir, M.,
Planquette, H., Popova, E.E., Poulton, A.J., Read, J.F., Seeyave,
S., Smith, T., Stinchcombe, M., Taylor, S., Thomalla, S., Ven-
ables, H. J., Williamson, R., and Zubkov, M. V.: Southern Ocean
deep-water carbon export enhanced by natural iron fertilization,
Nature, 457, 577–580, 2009.
Powell, R. T. and Wilson-Finelli, A.: Importance of organic Fe
complexing ligands in the Mississippi River plume, Estuarine,
Coastal Shelf Sci., 58, 757–763, 2003.
Prospero, J. M., Ginoux, P., Torres, O., Nicholson, S. E., and Gill,
T. E.: Environmental characterization of global sources of at-
mospheric soil dust identified with the Nimbus 7 Total Ozone
Mapping Spectrometer (TOMS) absorbing aerosol product, Rev.
Geophys., 40, 1002, doi:1010.1029/2000RG000095, 2002.
Pulido-Villena, E., Wagener, T., and Guieu, C.: Bacterial response
to dust pulses in the western Mediterranean: Implications for car-
bon cycling in the oligotrophic ocean, Global Biogeochem. Cy.,
22(12), GB1020, doi:10.1029/2007GB003091, 2008.
Quigg, A., Finkel, Z. V., Irwin, A. J., Rosenthal, Y., Ho, T. Y., Re-
infelder, J. R., Schofield, O., Morel, F. M. M., and Falkowski, P.
G.: The evolutionary inheritance of elemental stoichiometry in
marine phytoplankton, Nature, 425, 291–294, 2003.
Biogeosciences, 7, 1075–1097, 2010 www.biogeosciences.net/7/1075/2010/
E. Breitbarth et al.: Iron biogeochemistry across marine systems – progress from the past decade 1095
Raiswell, R., Tranter, M., Benning, L. G., Siegert, M., De’ath, R.,
Huybrechts, P., and Payne, T.: Contributions from glacially de-
rived sediment to the global iron (oxyhydr)oxide cycle: Impli-
cations for iron delivery to the oceans, Geochim. Cosmochim.
Acta, 70, 2765–2780, doi:10.1016/j.gca.2005.12.027, 2006.
Raiswell, R., Benning, L. G., Tranter, M., and Tulaczyk, S.:
Bioavailable iron in the Southern Ocean: the significance of the
iceberg conveyor belt, Geochem. Trans., 9(7), doi:10.1186/1467-
Riebesell, U., Schulz, K. G., Bellerby, R. G. J., Botros, M.,
Fritsche, P., Meyerhofer, M., Neill, C., Nondal, G., Oschlies,
A., Wohlers, J., and Zollner, E.: Enhanced biological car-
bon consumption in a high CO2ocean, Nature, 450, 545–510,
Rose, A. L.: Effect of Dissolved Natural Organic Matter on the
Kinetics of Ferrous Iron Oxygenation in Seawater, Environ. Sci.
Technol., 37, 4877–4886, doi:10.1021/es034152g, 2003.
Rose, J. M., Feng, Y., DiTullio, G. R., Dunbar, R. B., Hare, C. E.,
Lee, P. A., Lohan, M., Long, M., W. O. Smith Jr., Sohst, B.,
Tozzi, S., Zhang, Y., and Hutchins, D. A.: Synergistic effects of
iron and temperature on Antarctic phytoplankton and microzoo-
plankton assemblages, Biogeosciences, 6, 3131–3147, 2009,
Roy, E. G., Jiang, C. H., Wells, M. L., and Tripp, C.: Determin-
ing subnanomolar iron concentrations in oceanic seawater using
a siderophore-modified film analyzed by infrared spectroscopy,
Anal. Chem., 80, 4689–4695, doi:10.1021/ac800356p, 2008a.
Roy, E. G., Wells, M. L., and King, D. W.:
iron(II) in surface waters of the western subarctic Pacific, Lim-
nol. Oceanogr., 53, 89–98, 2008b.
Rue, E. L. and Bruland, K. W.: Complexation of iron(III) by natu-
ral organic ligands in the Central North Pacific as determined by
a new competitive ligand equilibration/adsorptive cathodic strip-
ping voltammetric method, Mar. Chem., 50, 117–138, 1995.
Rue, E. L. and Bruland, K. W.: The role of organic complexation
on ambient iron chemistry in the equatorial Pacific Ocean and
the response of a mesoscale iron addition experiment, Limnol.
Oceanogr., 42, 901–910, 1997.
Rusch, D. B., Halpern, A. L., Sutton, G., Heidelberg, K. B.,
Williamson, S., Yooseph, S., Wu, D., Eisen, J. A., Hoffman, J.
M., Remington, K., Beeson, K., Tran, B., Smith, H., Baden-
Tillson, H., Stewart, C., Thorpe, J., Freeman, J., Andrews-
Pfannkoch, C., Venter, J. E., Li, K., Kravitz, S., Heidelberg, J.
F., Utterback, T., Rogers, Y. H., Falc´ on, L. I., Souza, V., Bonilla-
Rosso, G., Eguiarte, L. E., Karl, D. M., Sathyendranath, S., Platt,
T., Bermingham, E., Gallardo, V., Tamayo-Castillo, G., Ferrari,
M. R., Strausberg, R. L., Nealson, K., Friedman, R., Frazier, M.,
and Venter, J. C.: The Sorcerer II Global Ocean Sampling expe-
dition: northwest Atlantic through eastern tropical Pacific, PLoS
biology, 5(e77), 398–431, 2007.
Saito, M. A., Sigman, D. M., and Morel, F. M. M.: The bioinor-
ganic chemistry of the ancient ocean: the co- evolution of
cyanobacterial metal requirements and biogeochemical cycles
at the Archean-Proterozoic boundary?, Inorganic Chimica Acta,
356, 308–318, 2003.
Salmon, T. P., Rose, A. L., Neilan, B. A., and Waite, T. D.: The FeL
model of iron acquisition: Nondissociative reduction of ferric
complexes in the marine environment, Limnol. Oceanogr., 51,
Sander, S., Mosley, L. M., and Hunter, K. A.: Investigation of in-
terparticle forces in natural waters: Effects of adsorbed humic
acids on iron oxide and alumina surface properties, Environ. Sci.
Technol., 38, 4791–4796, doi:10.1021/es049602z, 2004.
Sander, S., Ginon, L., Anderson, B., and Hunter, K. A.: Compar-
ative study of organic Cd and Zn complexation in lake waters –
seasonality, depth and pH dependence, Environ. Chem., 4, 410–
Santana-Casiano, J. M., Gonzalez-Davila, M., and Millero, F. J.:
Oxidation of Nanomolar Levels of Fe(II) with Oxygen in Natural
Waters, Environ. Sci. Technol., 39, 2073–2079, 2005.
Santana-Casiano, J. M., Gonzalez-Davila, M., and Millero, F. J.:
The role of Fe(II) species on the oxidation of Fe(II) in natural
waters in the presence of O2and H2O2, Mar. Chem., 99, 70–82,
Santschi, P. H., Balnois, E., Wilkinson, K. J., Zhang, J. W., Buffle,
J., and Guo, L. D.: Fibrillar polysaccharides in marine macro-
molecular organic matter as imaged by atomic force microscopy
and transmission electron microscopy, Limnol. Oceanogr., 43,
Sarmiento, J. L. and Orr, J. C.: 3-dimensional simulations of the im-
pact of Southern-Ocean nutrient depletion on atmospheric CO2
and ocean chemistry, Symp on What Controls Phytoplankton
Production in Nutrient-Rich Areas of the Open Sea, San Marcos,
Ca, 1991, ISI:A1991HR98100032, 1928–1950,
Sarthou, G., Timmermans, K. R., Blain, S., and Treguer, P.: Growth
physiology and fate of diatoms in the ocean: a review, J. Sea
Res., 53, 25–42, 2005.
Sarthou, G., Vincent, D., Christaki, U., Obernosterer, I., Timmer-
mans, K. R., and Brussaard, C. P. D.: The fate of biogenic
iron during a phytoplankton bloom induced by natural fertilisa-
tion: Impact of copepod grazing, Deep-Sea Res., 55, 734–751,
Sato, M., Takeda, S., and Furuya, K.: Iron regeneration and organic
iron(III)-binding ligand production during in situ zooplankton
grazing experiment, Mar. Chem., 106, 471–488, 2007.
Schmincke, H.-U.: Volcanism, Springer-Verlag, Berlin Heidelberg
New York, 324 pp., 2004.
Schoemann, V., Wollast, R., Chou, L., and Lancelot, C.: Effects of
photosynthesis on the accumulation of Mn and Fe by Phaeocystis
colonies, Limnol. Oceanogr., 46, 1065–1076, 2001.
Schoemann, V., De Jong, J. T. M., Lannuzel, D., Tison, J. L.,
Dellile, B., Chou, L., Lancelot, C., and Becquevort, S.: Micro-
biological control on the cycling Fe and its isotopes in Antarctic
sea ice, 8th Annual V M Goldschmidt Conference, Vancouver,
CANADA, ISI:000257301602198, A837–A837, 2008.
Schroth, A. W., Crusius, J., Sholkovitz, E. R., and Bostick, B. C.:
Iron solubility driven by speciation in dust sources to the ocean,
Nature Geosci., 2, 337–340, 2009.
Schulz, K. G., Zondervan, I., Gerringa, L. J. A., Timmermans, K.
R., Veldhuis, M. J. W., and Riebesell, U.: Effect of trace metal
availability on coccolithophorid calcification, Nature, 430, 673–
Sedwick, P. N., Sholkovitz, E. R., and Church, T. M.: Impact of
anthropogenic combustion emissions on the fractional solubil-
ity of aerosol iron: Evidence from the Sargasso Sea, Geochem.
Geophys. Geosyst., 8, 21, Q10q06, doi:10.1029/2007gc001586,
Shaked, Y., Kustka, A. B., Morel, F. M. M., and Erel, Y.: Simulta-
www.biogeosciences.net/7/1075/2010/Biogeosciences, 7, 1075–1097, 2010
1096E. Breitbarth et al.: Iron biogeochemistry across marine systems – progress from the past decade
neous determination of iron reduction and uptake by phytoplank-
ton, Limnol. Oceanogr.-Methods, 2, 137–145, 2004.
Shaked, Y., Kustka, A. B., and Morel, F. M. M.: A general kinetic
model for iron acquisition by eukaryotic phytoplankton, Limnol.
Oceanogr., 50, 872–882, 2005.
Sholkovitz, E. R.: Flocculation of dissolved Fe, Mn, Al, Cu, Ni,Co,
and Cd during estuarine mixing, Earth Planet. Sci. Lett., 41, 77–
Sholkovitz, E. R., Boyle, E. A., and Price, N. B.: Removal of
dissolved humic acids and iron during estuarine mixing, Earth
Planet. Sci. Lett., 40, 130–136, 1978.
Sigman, D. M. and Boyle, E. A.: Glacial/interglacial variations in
atmospheric carbon dioxide, Nature, 407, 859–869, 2000.
Sillen, L. G. and Martell, A. E.: Stability Constants, Chemical So-
ciety, London, 1971.
Smith, K. L., Robison, B. H., Helly, J. J., Kaufmann, R. S.,
Ruhl, H. A., Shaw, T. J., Twining, B. S., and Vernet, M.:
Free-drifting icebergs: Hot spots of chemical and biologi-
cal enrichment in the Weddell Sea, Science, 317, 478–482,
Smith, W. O. and Nelson, D. M.: Phytoplankton bloom produced
by a receeding ice edge in the Ross Sea – spacial coherence with
the density field, Science, 227, 163–166, 1985.
Spokes, L. and Jickells, T. D.: Speciation of metals in the atmo-
sphere, in: Chemical Speciation in the Environment, edited by:
Ure, A. and Davidson, C., Blackwell, Malden, 159–187, 2002.
Statham, P. J., Skidmore, M., and Tranter, M.: Inputs of glacially
derived dissolved and colloidal iron to the coastal ocean and im-
plications for primary productivity, Global Biogeochem. Cy., 22,
GB3013, doi:10.1029/2007gb003106, 2008.
Steigenberger, S., Statham, P. J., V¨ olker, C., and Passow, U.: The
role of polysaccharides and diatom exudates in the redox cycling
of Fe and the photoproduction of hydrogen peroxide in coastal
seawaters, Biogeosciences, 7, 109–119, 2010,
Stolpe, B., Hassell¨ ov, M., Andersson, K., and Turner, D. R.: High
resolution ICPMS as an on-line detector for flow field-flow frac-
tionation; multi-element determination of colloidal size distribu-
tions in a natural water sample, Analytica Chimica Acta, 535,
Stolpe, B. and Hassell¨ ov, M.: Changes in size distribution of fresh
ing with seawater, Geochim. Cosmochim. Acta, 71, 3292–3301,
Stolpe, B., and Hassell¨ ov, M.: Colloidal biopolymers binding iron,
copper, silver, lanthanum and lead in coastal seawater – signifi-
cance for the seasonal and spatial variations in element size dis-
tributions, Limnol. Oceanogr., 55(1), 187–202, 2010.
Straub, S. M. and Schmincke, H. U.: Evaluating the tephra input
into Pacific Ocean sediments: distribution in space and time, Ge-
ologische Rundschau, 87, 461–476, 1998.
Strzepek, R. F. and Harrison, P. J.: Photosynthetic architecture dif-
fers in coastal and oceanic diatoms, Nature, 431, 689–692, 2004.
Strzepek, R. F., Maldonado, M. T., Higgins, J. L., Hall, J., Safi,
K., Wilhelm, S. W., and Boyd, P. W.: Spinning the ”Ferrous
Wheel”: The importance of the microbial community in an iron
budget during the FeCycle experiment, Global Biogeochem. Cy.,
19, GB4S26, doi:10.1029/2005GB002490, 2005.
Sunda, W. and Huntsman, S.: Effect of pH, light, and tempera-
ture on Fe-EDTA chelation and Fe hydrolysis in seawater, Mar.
Chem., 84, 35–47, 2003.
Sunda, W. G. and Huntsman, S. A.: Effect of competitive interac-
tions between manganese and copper on cellular manganese and
growth in estuarine and oceanic species of the diatom Thalas-
siosira, Limnol. Oceanogr., 28, 924–934, 1983.
Sunda, W. G. and Huntsman, S. A.: Iron uptake and growth lim-
itation in oceanic and coastal phytoplankton, Mar. Chem., 50,
Sunda, W. G. and Huntsman, S. A.: Processes regulating cellular
metal accumulation and physiological effects: Phytoplankton as
a model system, The Sciences of the Total Environment, 219,
Sunda, W. G. and Huntsman, S. A.: Effect of Zn, Mn, and Fe on
Cd accumulation in phytoplankton: Implications for oceanic Cd
cycling, Limnol. Oceanogr., 45, 1501–1516, 2000.
Takeda, S.: Influence of iron availability on nutrient consumption
ratio of diatoms in oceanic waters, Nature, 393, 774–777, 1998.
Timmermans, K. R., van der Wagt, B., Veldhuis, M. J. W., Maat-
man, A., and de Baar, H. J. W.: Physiological responses of three
species of marine pico-phytoplankton to ammonium, phosphate,
iron and light limitation, J. Sea Res., 53, 109–120, 2005.
Toner, B. M., Fakra, S. C., Manganini, S. J., Santelli, C. M.,
Marcus, M. A., Moffett, J., Rouxel, O., German, C. R., and
Edwards, K. J.: Preservation of iron(II) by carbon-rich ma-
trices in a hydrothermal plume, Nature Geosci., 2, 197–201,
Tovar-Sanchez, A., Sanudo-Wilhelmy, S. A., Kustka, A. B., Agusti,
S., Dachs, J., Hutchins, D. A., Capone, D. G., and Duarte, C.
M.: Effects of dust deposition and river discharges on trace metal
composition of Trichodesmium spp. in the tropical and subtrop-
ical North Atlantic Ocean, Limnol. Oceanogr., 51, 1755–1761,
Tovar-Sanchez, A., Duarte, C. M., Hern´ andez-Le´ on, S., and
Sa˜ nudo-Wilhelmy, S. A.: Krill as a central node for iron cy-
cling in the Southern Ocean, Geophys. Res. Lett., 34, L11601,
doi:10.1029/12006GL029096, 022007, 2007.
Trapp, J. M., Millero, F. J., and Prospero, J. M.: Trends in the
solubility of iron in dust-dominated aerosols in the Equatorial
Atlantic Trade Winds: The importance of iron speciation and
sources, Geochem. Geophys. Geosyst., 11(1), in press, 2010.
Tsuda, A., Takeda, S., Saito, H., Nishioka, J., Nojiri, Y., Kudo,
I., Kiyosawa, H., Shiomoto, A., Imai, K., Ono, T., Shimamoto,
A., Tsumune, D., Yoshimura, T., Aono, T., Hinuma, A., Kinu-
gasa, M., Suzuki, K., Sohrin, Y., Noiri, Y., Tani, H., Deguchi, Y.,
Tsurushima, N., Ogawa, H., Fukami, K., Kuma, K., and Saino,
T.: A mesoscale iron enrichment in the western Subarctic Pacific
induces a large centric diatom bloom, Science, 300, 958–961,
Turner, D. R. and Hunter, K. A.: The Biogeochemistry of Iron in
Seawater, IUPACSeries onAnalytical andPhysicalChemistryof
Environmental Systems, John Wiley and Sons Ltd., West Sussex,
England, 396 pp., 2001.
Twining, B. S., Baines, S. B., Fisher, N. S., and Landry, M.
R.: Cellular iron contents of plankton during the Southern
Ocean Iron Experiment (SOFeX), Deep-Sea Res., 51, 1827–
1850, doi:10.1016/j.dsr.2004.08.007, 2004.
Ussher, S. J., Worsfold, P. J., Achterberg, E. P., Laes, A., Blain, S.,
Laan, P., and de Baar, H. J. W.: Distribution and redox speciation
Biogeosciences, 7, 1075–1097, 2010www.biogeosciences.net/7/1075/2010/
E. Breitbarth et al.: Iron biogeochemistry across marine systems – progress from the past decade 1097 Download full-text
of dissolved iron on the European continental margin, Limnol.
Oceanogr., 52, 2530–2539, 2007.
Vasconcelos, M., Leal, M. F. C., and van den Berg, C. M. G.: In-
fluence of the nature of the exudates released by different marine
algae on the growth, trace metal uptake, and exudation of Emilia-
nia huxleyi in natural seawater, Mar. Chem., 77, 187–210, 2002.
Venter, J. C., Remington, K., Heidelberg, J. F., Halpern, A. L.,
Rusch, D., Eisen, J. A., Wu, D. Y., Paulsen, I., Nelson, K. E.,
Nelson, W., Fouts, D. E., Levy, S., Knap, A. H., Lomas, M. W.,
Nealson, K., White, O., Peterson, J., Hoffman, J., Parsons, R.,
Baden-Tillson, H., Pfannkoch, C., Rogers, Y. H., and Smith, H.
O.: Environmental genome shotgun sequencing of the Sargasso
Sea, Science, 304, 66–74, doi:10.1126/science.1093857, 2004.
Verdugo, P., Alldredge, A. L., Azam, F., Kirchman, D. L., Passow,
U., and Santschi, P. H.: The oceanic gel phase: a bridge in the
DOM-POM continuum, Mar. Chem., 92, 67–85, 2004.
Vigenault, B. and Campbell, P. G. C.: Uptake of cadmium by fresh-
water green algae: Effects of pH and aquatic humic substances,
J. Phycol., 41, 55–61, 2005.
Vong, L., La¨ es, A., and Blain, S.: Determination of iron-porphyrin-
like complexes at nanomolar levels in seawater, Analytica Chim-
icaActa, 588, 237–244, doi:10.1016/j.aca.2007.1002.10072007.
Vraspir, J. and Butler, A.: Chemistry of marine ligands and
siderophores, Ann. Rev. Mar. Sci., 1, 43–63, 2009.
Wagener, T., Guieu, C., Losno, R., Bonnet, S., and Mahowald, N.:
Revisiting atmospheric dust export to the Southern Hemisphere
ocean: Biogeochemical implications, Global Biogeochem. Cy.,
22, GB2006, doi:10.1029/2007gb002984, 2008.
Wang, W. X. and Dei, R. C. H.: Bioavailability of iron complexed
with organic colloids to the cyanobacteria Synechococcus and
Trichodesmium, Aquatic Microbial Ecology, 33, 247–259, 2003.
Watson, A. J.: Iron limitation in the oceans, in: The biogeochem-
istry of iron in seawater, edited by: Turner, D. R., and Hunter, K.
A., John Wiley & Sons Ltd., Chicester, 9–33, 2001.
Weber, L., V¨ olker, C., Oschlies, A., and Burchard, H.: Iron pro-
files and speciation of the upper water column at the Bermuda
Atlantic Time-series Study site: a model based sensitivity study,
Biogeosciences, 4, 689–706, 2007,
Wells, M. L.: A neglected dimension, Nature, 391, 530–531, 1998.
Wells, M. L., Trick, C. G., Cochlan, W. P., Hughes, M. P., and
Trainer, V. L.: Domoic acid: The synergy of iron, copper, and the
toxicity of diatoms, Limnol. Oceanogr., 50, 1908–1917, 2005.
Willey, J. D., Kieber, R. J., Seaton, P. J., and Miller, C.: Rainwa-
ter as a source of Fe(II)-stabilizing ligands to seawater, Limnol.
Oceanogr., 53, 1678–1684, 2008.
Wolff, E. W., Fischer, H., Fundel, F., Ruth, U., Twarloh, B., Littot,
G. C., Mulvaney, R., Rothlisberger, R., de Angelis, M., Boutron,
C. F., Hansson, M., Jonsell, U., Hutterli, M. A., Lambert, F.,
Kaufmann, P., Stauffer, B., Stocker, T.F., Steffensen, J.P., Bigler,
M., Siggaard-Andersen, M. L., Udisti, R., Becagli, S., Castel-
lano, E., Severi, M., Wagenbach, D., Barbante, C., Gabrielli, P.,
and Gaspari, V.: Southern Ocean sea-ice extent, productivity and
iron flux over the past eight glacial cycles, Nature, 440, 491–496,
Worms, I., Simon, D. F., Hassler, C. S., and Wilkinson,
K. J.: Bioavailability of trace metals to aquatic microor-
ganisms: importance of chemical,
ical processes on biouptake, Biochimie, 88, 1721–1731,
Wu, J. F., Boyle, E., Sunda, W., and Wen, L. S.: Soluble and col-
loidal iron in the olgotrophic North Atlantic and North Pacific,
Science, 293, 847–849, 2001.
Wu, J.F., Chung, S.W., Wen, L.S., Liu, K.K., Chen, Y.L.L., Chen,
H. Y., and Karl, D. M.: Dissolved inorganic phosphorus, dis-
solved iron, and Trichodesmium in the oligotrophic South China
Sea, Global Biogeochem. Cy., 17, doi:10.1029/2002GB001924,
Ye, Y., V¨ olker, C., and Wolf-Gladrow, D. A.: A model of Fe spe-
ciation and biogeochemistry at the Tropical Eastern North At-
lantic Time-Series Observatory site, Biogeosciences, 6, 2041–
Yooseph, S., Sutton, G., Rusch, D. B., Halpern, A. L., Williamson,
S. J., Remington, K., Eisen, J. A., Heidelberg, K. B., Manning,
G., Li, W. Z., Jaroszewski, L., Cieplak, P., Miller, C. S., Li, H. Y.,
Mashiyama, S. T., Joachimiak, M. P., van Belle, C., Chandonia,
J. M., Soergel, D. A., Zhai, Y. F., Natarajan, K., Lee, S., Raphael,
B. J., Bafna, V., Friedman, R., Brenner, S. E., Godzik, A., Eisen-
berg, D., Dixon, J. E., Taylor, S. S., Strausberg, R. L., Frazier,
M., and Venter, J. C.: The Sorcerer II Global Ocean Sampling
expedition: Expanding the universe of protein families, PLoS.
Biol., 5, 432–466, doi:10.1371/journal.pbio.0050016, 2007.
Yoshida, T., Hayashi, K., and Ohmoto, H.: Dissolution of iron hy-
droxides by marine bacterial siderophore, Chem. Geol., 184, 1–
Zhang, W. and Wang, W.-X.: Colloidal organic carbon and trace
metal(Cd, Fe, andZn)releasesbydiatomexudationandcopepod
grazing, Journal of Experimental Marine Biology and Ecology,
307, 17–34, 2004.
biological and phys-
www.biogeosciences.net/7/1075/2010/Biogeosciences, 7, 1075–1097, 2010