Ocean acidification affects iron speciation in seawater

Ocean acidification affects iron speciation in seawater E. Breitbarth, R. J. Bellerby, C. C. Neill, M. V. Ardelan, M. Meyerhöfer, E. Zöllner, P. L. Croot, and U. Riebesell Bjerknes Centre for Climate Research, University of Bergen, Bergen, Allégaten 55, 5007 Bergen, Norway Department of Chemistry, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand Leibniz Institute of Marine Sciences (IFM-GEOMAR), Düsternbrooker Weg 20, 24105 Kiel, Germany Norwegian University of Science and Technology, Department of Chemistry, 7491 Trondheim, Norway Received: 31 May 2009 – Accepted: 15 June 2009 – Published: 9 July 2009 Correspondence to: E. Breitbarth (ebreitbarth@chemistry.otago.ac.nz) Published by Copernicus Publications on behalf of the European Geosciences Union.


Introduction
Paleoclimate data indicate significant effects from the deposition of iron in aeolian dust on ocean biogeochemistry with feedbacks on global climate (Watson et al., 2000).Studies of artificial and natural iron input have demonstrated iron control of phytoplankton productivity and CO 2 drawdown over vast oceanic regions (Boyd et al., 2007;Blain et al., 2007;Pollard et al., 2009) and in coastal upwelling regions (Bruland et al., 2001;Hutchins and Bruland, 1998).Temporal control of iron on phytoplankton productivity was also observed in a Norwegian fjord system ( Özt ürk et al., 2002).The Pelagic ecosystem CO 2 enrichment study (PeECE III) studied natural phytoplankton blooms under atmospheric CO 2 scenarios of 350, 700, and 1050 µatm pCO 2 in a coastal mesocosm experiment (Schulz et al., 2008).We used this unique opportunity to investigate the combined effects of phytoplankton bloom development and ocean acidification on Fe chemistry.
Iron solubility in surface seawater is low and the speciation is largely controlled by organic complexation and photochemical processes (Kuma et al., 1996;Sunda and Huntsman, 2003;Kuma et al., 1992).In addition to organic compounds generally present in coastal seawater, phytoplankton blooms can affect Fe(III)-complexation, Introduction

Conclusions References
Tables Figures

Back Close
Full which affects the dissolved Fe fraction and photoreactivity (Croot et al., 2001;Kuma et al., 1992;Rue and Bruland, 1995).Ligand production is generally facilitated via zooplankton and protist grazing, microbial production, and potentially also by phytoplankton cell degradation (Heldal et al., 1996;Barbeau et al., 1996;Hutchins and Bruland, 1994).In return, iron bioavailability differs among types of organic iron complexation and prokaryotic or eukaryotic phytoplankton (Hutchins et al., 1999).Fe(III)complexation is interlinked with Fe(II) production in marine water, mainly via supplying the substrate for photoreduction in sunlit surface waters (Kuma et al., 1992;Özt ürk et al., 2004;Barbeau et al., 2001;Barbeau et al., 2003).Fe(II) is generally considered bioavailable, but rapid reoxidation to Fe(III) in temperate waters result in limited concentrations.Half-life times range in the order of minutes and are largely dependent on temperature, oxygen and hydrogen peroxide concentrations, and pH (Santana-Casiano et al., 2005;Millero et al., 1987;Millero and Sotolongo, 1989), with presently limited knowledge about the role of organic Fe(II) complexation in natural seawater.However, the contribution of Fe(II) to phytoplankton nutrition may be significant in the open ocean (Roy et al., 2008) as well as in estuarine waters (Breitbarth et al., 2009).Despite our growing knowledge of iron biogeochemistry in seawater, we currently have little information on the effects of ocean acidification thereon.Seawater pH affects phytoplankton physiology (Fu et al., 2008;Hare et al., 2008;Riebesell, 2004) and thus indirect effects via phytoplankton exudates that complex iron may also alter biological influences on iron solubility and cycling.Further, the photoreduction of organic Feligand complexes is the main pathway for Fe(II) production in the euphotic zone (King et al., 1993) and moreover Fe(II) oxidation rates are strongly pH dependent (e.g.Santana-Casiano et al., 2005).For unabated CO 2 emissions, oceanic uptake of anthropogenic CO 2 will lower surface ocean pH from a pre-industrial 8.25 to an estimated 7.85 within this century, and further by up to 0.7 units until 2300 (Caldeira and Wickett, 2003;Jacobson, 2005).This change far exceeds any glacial-interglacial differences (Caldeira and Wickett, 2003)  scale.TA was measured using the classical Gran electrotitration method (Gran, 1952) (precision ±4µmol kg −1 ).DIC was measured by coulometric titration (Johnson et al., 1987) with a precision of 2 µmol kg −1 .Chl-a concentrations were determined using HPLC (Barlow et al., 1997) and particulate organic carbon (POC) was measured on an elemental analyzer (EuroEA 3000, EuroVector) (Ehrhard and Koeve, 1999).Please see Schulz et al. (2008) for more details about the experimental set-up.Total (tFe) and dissolved iron (dFe, 0.2 µm filtered) measurements were conducted using chemiluminescence flow injection analysis (CL-FIA, Waterville Analytical) (Bowie et al., 1998) and focused on the period of strong bloom development and pH shifts (days 7-13) and a past bloom measurement (day 23).Fe(II) was determined based on Croot and Laan (2002) using the same CL-FIA instrument, which was installed on the mesocosm raft for this purpose, during days 20 and 22 of the experiment.Samples Introduction

Conclusions References
Tables Figures

Back Close
Full were obtained from 2.5 m depth via syringe pumping through PTFE tubing, immediately followed by 0.2 µm filtration and injection into CL-FIA system.Additionally, Fe(II) oxidation rates were determined on 0.2 µm filtered samples form day 25 of the experiment, which were stored in the dark for 24 h to oxidize any Fe(II) present.Measurements were performed while having the samples, all reagents, and the sample loop of the flow injection analyzer immerged in a temperature controlled (10 • C) water bath, in order to minimize analytical temperature effects during the measurements.The temperature was chosen as it is representative of the temperature inside the mesocosms during the study.The naperian log transformed chemiluminescent signal over time of 0.5, 0.75, and 1 nmol L −1 Fe(II) standard additions yield a linear signal decrease and the slope represents the Fe(II) oxidation rate constant (k ox s −1 ).Predicted Fe(II) oxidation rates were further calculated based on Millero et al. (1987) after calculating the [OH − ] concentration of the water using the CO 2 SYS program (Lewis and Wallace, 1998), taking seawater carbonate chemistry measurements and oxygen concentrations into account.

Results and discussion
CO 2 perturbation and phytoplankton bloom development result in pH shifts from 7.67-7.97,7.82-8.06,and 8.13-8.26 at 1050, 700, and 350 µatm pCO 2 , respectively during days 3-12 and relatively constant levels thereafter (Figs. 1 and 2).The peak of the bloom is marked by Chl-a concentrations at days 9 (low CO 2 ) and 10 (mid and high CO 2 ) and results in particulate organic carbon (POC) concentrations peaking at days 10 (low CO 2 , 91.9 µmol L −1 ) and 11 (mid and high CO 2 , 98.9 and 97.4 µmol L −1 respectively) (Figs. 1 and 2).Please see Schulz et al. (2008) for more details about the bloom development.
The Chl-a and POC biomasses in the three pCO 2 treatments are not markedly different.Nevertheless, our experiments show significantly higher dissolved iron (<0.2 µm, dFe) concentrations for high CO 2 treatments in comparison to the mid-and low CO 2 scenarios (e.g.4.42 vs. 1.92 and 2.73 nmol L −1 on day 9, Fig. 3).During the bloom dFe Introduction

Conclusions References
Tables Figures

Back Close
Full decreases and reflects iron uptake in all treatments.Remineralization during bloom decline increases dFe levels again and dFe was maintained at significantly higher levels in the future scenario compared to the mid and low CO 2 treatments.Distinctions in dFe towards the end of the bloom (day 23, 2.8-4.2 nmol L −1 at low and mid CO 2 , 6.0-8.2 nmol L −1 under high CO 2 , Fig. 3) suggest differences in Fe remineralization in the treatments.Fe concentrations in the mesocosms were higher than in nearby fjord water (6.2 nmol L −1 total Fe (tFe) and 3.0 nmol L −1 dFe on day 13).Total Fe ranged from 23.7 to 96.1 nmol L −1 and varied between enclosures and over time.However, dissolved Fe values do not correlate with tFe and thus tFe concentrations are not responsible for the systematically increased dFe values in the high CO 2 treatments (Fig. 4).The total Fe data suggest an input of relatively unreactive particulate Fe during the filling process of the enclosures.Clearly, the mesocosms were Fe-replete and while we lack iron measurements from the start of the experiment, applying an Fe:C ratio of 65 µmol:mol (Sarthou et al., 2005) yields an iron demand of 2-6 nmol L −1 during the bloom, which approximates the iron detected in fjord water.
Any Fe(III)-hydroxide solubility change over the observed pH ranges during the iron measurements (7.77-8.21 up to 7.94-8.26,Fig. 2) is significantly lower than the observed differences in dFe suggesting biological iron-ligand production and colloid formation to be responsible for maintaining elevated dFe in the high CO 2 mesocosms (Kuma et al., 1996;Millero, 1998).Croot et al. (2001) show a ∼2-fold Fe-ligand concentration increase resulting in rising dFe concentrations after 12-13 days iron induced phytoplankton bloom development.This was paralleled by a ∼5-fold increase in chlorophyll-a biomass, similar to our study.Likewise, Croot et al. (2004) suggest a biological source of iron ligands in association with chlorophyll maxima in the water column.Further supporting the inclination that the increased dFe concentrations during the high CO 2 treatments are biologically controlled are associations of colloidal and organically complexed Fe fractions with phytoplankton blooms in Norwegian coastal waters ( Özt ürk et al., 2002, 2003), which may further be controlled by bacterial production of extracellular matrixes (Heldal et al., 1996).Introduction

Conclusions References
Tables Figures

Back Close
Full Screen / Esc Printer-friendly Version

Interactive Discussion
The pH decrease may affect iron-ligand complex stabilities, resulting in altered photolability of Fe(III)-ligand complexes (Lewis et al., 1995;Sunda and Huntsman, 2003).The future ocean scenarios showed higher Fe(II) values compared to the lower CO 2 treatments.Values between 52 and 411 pmol L −1 were detected, depending on treatment and time of day (Fig. 5).Due to fast moving cloud cover though, a clear diel cycle could not be determined.The solubility of Fe(II) is significantly greater than for Fe(III) and though while at these pH levels the oxidation of Fe(II) is still rapid (Santana-Casiano et al., 2006) it points towards an increase in the photolability of the iron organic complexes at lower pH (Sunda and Huntsman, 2003).Predictions of the Fe(II) half-life's over the course of the experiment reflect the expected pH dependence of Fe(II) oxidation rates (Fig. 6).The Fe(II) speciation shifts towards the Fe 2+ ion below pH 8, while the oxidation rate is still largely controlled by Fe(OH) 2 (Santana-Casiano et al., 2006;Millero et al., 1995).Bloom dynamics cause pH shifts in the treatments that result in a much broader range of predicted Fe(II) half-life's in the high CO 2 treatments (3.4-20.6 min and 2.2-9.8min, high and mid CO 2 respectively) vs. the low CO 2 treatment (1.1-2.6 min, Fig. 6).Especially during the early phase of the bloom, the relatively slow Fe(II) oxidation rates at low pH may aid in the bioavailability of iron via allowing for a larger standing stock of Fe(II).Dropping oxygen concentrations with bloom decline and organic matter remineralization after day 12 (by ∼10% saturation overall) do not fully counteract acceleration effects on Fe(II) oxidation of the increasing temperature by ∼0.5 • C each on days 15 and 17 (Fig. 7).The product of both effects is visible in the parallel shift of the oxidation rate and resulting half-life times towards the lower end of the pH range of each treatment (Fig. 6).It should be noted that the contribution of hydrogen peroxide is not considered here, but may have implications when concentrations exceed 200 nmol L half life in the same samples ranges from 1.5-5.1 min (Table 1).Similarly, predicted oxidation rates during the measurements in the mesocosms were faster than actual measured values (Fig. 5, Table 2).While the pH effect on inorganic Fe(II) speciation and thus on Fe(II) oxidation rates is clearly evident, the additional influence of phytoplankton bloom derivates on the actual half-life times are obvious.Hydrocarboxylic acids, such as glucaric acid, affect photoreduction of Fe(III) and may be released from phytoplankton (Kuma et al., 1992;Özt ürk et al., 2004) while their direct effect on Fe(II) oxidation remains to be shown.The data suggest two possible mechanisms tying into Fe(II) cycling at different pH.Differences in oxidation rates and their deviation from the predicted rates indicate organic Fe(II)-complexation, which additionally may affect the Fe(II) half life in the low pH treatments stronger than in the high pH mesocosms.More so, biologically mediated Fe(III)-chelates supply the major pool of iron for photoreduction and this main Fe(II) production pathway (Boyd et al., 2000;Kuma et al., 1992) appears to operate more effectively at high CO 2 allowing for the elevated Fe(II) concentrations detected in the future ocean treatments.Effects thereof on biological production and remineralization may be profound.
Our study indicates that ocean acidification may lead to enhanced Fe-bioavailability due to an increased fraction of dFe and elevated Fe(II) concentrations in coastal systems due to pH induced changes in organic complexation and Fe(II) oxidation rates.Overall this will result in increased residence times for Fe in surface seawater leading ultimately to an enhancement of iron bioavailability since equilibrium partitioning eventually restores the biolabile Fe pools that have been depleted by biological uptake.These processes may further fuel increased phytoplankton carbon acquisition and export at future atmospheric CO 2 levels (Riebesell et al., 2007).Provided that the observed CO 2 sensitivity of iron chemistry represents a general phenomenon operating also in phytoplankton blooms of oceanic areas, it could have a profound effect on productivity in the future ocean (Blain et al., 2007;Boyd et al., 2007).Our results support the notion that changes in iron speciation and the resulting potential negative feedback mechanism of phytoplankton productivity on atmospheric CO 2 need to be Introduction

Conclusions References
Tables Figures

Back Close
Full

BGD Introduction Conclusions References
Tables Figures

Conclusions References
Tables Figures

Back Close
Full Screen / EscPrinter-friendly Version Interactive Discussion −1 , which is possible in coastal waters(Santana-Casiano et al., 2005).Temperature controlled Fe(II) oxidation rate measurements conducted at the end of the study reveal a decrease in oxidation rate from −0.81 to −1.02 min −1 (log K ox ) and result in an increase of Fe(II) half lives from 4.4-7.3min in the pH range from 8.21-7.95respectively.In comparison, estimates of the sole effect of pH on the Fe(II) the ecological effects of ocean acidification.

Fig. 7 .
Fig. 7 and thus may have profound effects on the biogeochemistry of iron in seawater.The PeECE III experiment offered a unique opportunity to study iron Introduction

Table 1 .
Millero et al. (1987)d half lifes at 10 • C for oxygen saturated seawater after incubation the mesocosms for 25 days compared with FE oxidation rates estimated based onMillero et al. (1987).

Table 2 .
Millero et al. (1987)s and half lifes in the mesocosms during mid-day in synchronization with carbonate system measurements on day 11 and day 13 compared with Fe(II) oxidation rates estimated based onMillero et al. (1987).See also Fig.5for the respective Fe(II) concentrations measured.