Importance of refractory ligands and their photodegradation for iron oceanic inventories and cycling
Christel Hassler A E , Damien Cabanes A , Sonia Blanco-Ameijeiras A , Sylvia G. Sander B D and Ronald Benner C
+ Author Affiliations
- Author Affiliations
A University of Geneva, Department F.-A. Forel for Environmental and Aquatic Sciences, 66 Boulevard Carl-Vogt, CH-1205 Geneva, Switzerland.
B University of Otago, Department of Chemistry, NIWA/UO Research Centre for Oceanography, PO Box 56, Dunedin, 9054, New Zealand.
C University of South Carolina, Department of Biological Sciences and School of the Earth, Ocean, and Environment, Columbia,1521 Green Street, SC 29208, USA.
D Present address: Marine Environmental Study Laboratory, IAEA-NAEL, 4 Quai Antoine 1er, Monaco 98000, Principality of Monaco.
E Corresponding author. Present address: Ecole polytechique fédérale de Lausanne (EPFL), Swiss Polar Institute, GR C2 505, Station 2, CH-1015 Lausanne, Switzerland. Email: christel.hassler@epfl.ch
Marine and Freshwater Research 71(3) 311-320 https://doi.org/10.1071/MF19213
Submitted: 12 June 2019 Accepted: 15 August 2019 Published: 2 December 2019
Journal Compilation © CSIRO 2020 Open Access CC BY-NC-ND
Abstract
Iron is an essential micronutrient that limits primary production in up to 40% of the surface ocean and influences carbon dioxide uptake and climate change. Dissolved iron is mostly associated with loosely characterised organic molecules, called ligands, which define key aspects of the iron cycle such as its residence time, distribution and bioavailability to plankton. Models based on in situ ligand distributions and the behaviour of purified compounds include long-lived ligands in the deep ocean, bioreactive ligands in the surface ocean and photochemical processes as important components of the iron cycle. Herein, we further characterise biologically refractory ligands in dissolved organic matter (DOM) from the deep ocean and labile ligands in DOM from the surface ocean, and their photochemical and biological reactivities. Experimental results indicated that photodegradation of upwelled refractory iron-binding ligands can fuel iron remineralisation and its association with labile organic ligands, thus enhancing iron bioavailability in surface waters. These observations better elucidate the roles of biologically refractory and labile molecules and global overturning circulation in the ocean iron cycle, with implications for the initiation and sustainment of biological activity in iron-limited regions and the residence time of iron in the ocean.
Additional keywords: DOC, organic matter, primary productivity.
References
Abualhaija, M. M., and van den Berg, C. M. G. (2014). Chemical speciation of iron in seawater using catalytic cathodic stripping voltammetry with ligand competition against salicylaldoxime. Marine Chemistry 164, 60–74.| Chemical speciation of iron in seawater using catalytic cathodic stripping voltammetry with ligand competition against salicylaldoxime.Crossref | GoogleScholarGoogle Scholar |
Amin, S. A., Greene, D. H., Hart, M. C., Küpper, F. C., Sunda, W. G., and Carrano, C. J. (2009). Photolysis of iron, siderophore chelates promotes bacterial, algal mutualism. Proceedings of the National Academy of Sciences of the United States of America 106, 17071–17076.
| Photolysis of iron, siderophore chelates promotes bacterial, algal mutualism.Crossref | GoogleScholarGoogle Scholar | 19805106PubMed |
Azam, F., and Malfatti, F. (2007). Microbial structuring of marine ecosystems. Nature Reviews. Microbiology 5, 782–791.
| Microbial structuring of marine ecosystems.Crossref | GoogleScholarGoogle Scholar | 17853906PubMed |
Barbeau, K., Rue, E. L., Bruland, K. W., and Butler, A. (2001). Photochemical cycling of iron in the surface ocean mediated by microbial iron(III)-binding ligands. Nature 413, 409–413.
| Photochemical cycling of iron in the surface ocean mediated by microbial iron(III)-binding ligands.Crossref | GoogleScholarGoogle Scholar | 11574885PubMed |
Benner, R., and Amon, R. M. W. (2015). The size-reactivity continuum of major bioelements in the ocean. Annual Review of Marine Science 7, 185–205.
| The size-reactivity continuum of major bioelements in the ocean.Crossref | GoogleScholarGoogle Scholar | 25062478PubMed |
Boiteau, R. M., Mende, D. R., Hawco, N. J., McIlvin, M. R., Fitzsimmons, J. N., Saito, M. A., Sedwick, P. N., DeLong, E. F., and Repeta, D. J. (2016). Siderophore-based microbial adaptations to iron scarcity across the eastern Pacific Ocean. Proceedings of the National Academy of Sciences of the United States of America 113, 14237–14242.
| Siderophore-based microbial adaptations to iron scarcity across the eastern Pacific Ocean.Crossref | GoogleScholarGoogle Scholar | 27911777PubMed |
Browning, T. J., Achterberg, E. P., Rapp, I., Engel, A., Bertrand, E. M., Tagliabue, A., and Moore, M. (2017). Nutrient co-limitation at the boundary of an oceanic gyre. Nature 551, 242–246.
| Nutrient co-limitation at the boundary of an oceanic gyre.Crossref | GoogleScholarGoogle Scholar | 29088696PubMed |
Buck, K. N., Sohst, B., and Sedwick, P. N. (2015). The organic complexation of dissolved iron along the US GEOTRACES (GA03) North Atlantic Section. Deep-sea Research – II Topical Studies in Oceanography 116, 152–165.
| The organic complexation of dissolved iron along the US GEOTRACES (GA03) North Atlantic Section.Crossref | GoogleScholarGoogle Scholar |
Cabanes, D. J. E., Norman, L., Santos-Echeandia, J., Iversen, M. H., Trimborn, S., Laglera, L. M., and Hassler, C. S. (2017). First evaluation of the role of salp fecal pellets on iron biogeochemistry. Frontiers in Marine Science 3, 289.
| First evaluation of the role of salp fecal pellets on iron biogeochemistry.Crossref | GoogleScholarGoogle Scholar |
Caprara, S., Buck, K. N., Gerringa, L. J. A., Rijkenberg, M. J. A., and Monticelli, D. A. (2016). Compilation of iron speciation data for open oceanic waters. Frontiers in Marine Science 3, 1–7.
| Compilation of iron speciation data for open oceanic waters.Crossref | GoogleScholarGoogle Scholar |
Coale, K. H., Johnson, K. S., Fitzwater, S. E., Gordon, R. M., Tanner, S., Chavez, F. P., Ferioli, L., Sakamoto, C., Rogers, P., Millero, F., Steinberg, P., Nightingale, P., Cooper, D., Cochlan, W. P., Landry, M. R., Constantinou, J., Rollwagen, G., Trasvina, A., and Kudela, R. (1996). A massive phytoplankton bloom induced by an ecosystem-scale iron fertilization experiment in the equatorial Pacific Ocean. Nature 383, 495–501.
| A massive phytoplankton bloom induced by an ecosystem-scale iron fertilization experiment in the equatorial Pacific Ocean.Crossref | GoogleScholarGoogle Scholar | 18680864PubMed |
Death, R., Wadham, J. L., Monteiro, F. M., Le Brocq, A. M., Tranter, M., Ridgwell, A., Dutkiewicz, S., and Raiswell, R. (2014). Antarctic ice sheet fertilises the Southern Ocean. Biogeosciences 11, 2635–2643.
| Antarctic ice sheet fertilises the Southern Ocean.Crossref | GoogleScholarGoogle Scholar |
England, M. H. (1995). The age of water and ventilation timescales in a global ocean model. Journal of Physical Oceanography 25, 2756–2777.
| The age of water and ventilation timescales in a global ocean model.Crossref | GoogleScholarGoogle Scholar |
Fitzsimmons, J. N., Conway, T. M., Lee, J.-M., Kayser, R., Thyng, K. M., John, S. G., and Boyle, E. A. (2016). Dissolved iron and iron isotopes in the southeastern Pacific Ocean. Global Biogeochemical Cycles 30, 1372–1395.
| Dissolved iron and iron isotopes in the southeastern Pacific Ocean.Crossref | GoogleScholarGoogle Scholar |
Gerringa, L. J. A., Rijkenberg, M. J. A., Schoemann, V., Laan, P., and de Baar, H. J. W. (2015). Organic complexation of iron in the West Atlantic Ocean. Marine Chemistry 177, 434–446.
| Organic complexation of iron in the West Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar |
Gledhill, M., and Buck, K. N. (2012). The organic complexation of iron in the marine environment: a review. Frontiers in Microbiology 3, 1–17.
| The organic complexation of iron in the marine environment: a review.Crossref | GoogleScholarGoogle Scholar |
Hansell, D. A. (2013). Recalcitrant dissolved organic carbon fractions. Annual Review of Marine Science 5, 421–445.
| Recalcitrant dissolved organic carbon fractions.Crossref | GoogleScholarGoogle Scholar | 22881353PubMed |
Hansell, D. A., and Carlson, C. A. (2015). ‘Biogeochemistry of Marine Dissolved Organic Matter’, 2nd edn. (Academic Press: London, UK.)
Hassler, C. S., and Schoemann, V. (2009). Bioavailability of organically bound Fe to model phytoplankton of the Southern Ocean. Biogeosciences 6, 1677–1712.
| Bioavailability of organically bound Fe to model phytoplankton of the Southern Ocean.Crossref | GoogleScholarGoogle Scholar |
Hassler, C. S., Schoemann, V., Nichols, C. M., Butler, E. C. V., and Boyd, P. W. (2011). Saccharides enhance iron bioavailability to Southern Ocean phytoplankton. Proceedings of the National Academy of Sciences of the United States of America 108, 1076–1081.
| Saccharides enhance iron bioavailability to Southern Ocean phytoplankton.Crossref | GoogleScholarGoogle Scholar | 21169217PubMed |
Hassler, C. S., Norman, L., Mancuso-Nichols, C. A., Clementson, L. A., Robinson, C., Schoemann, V., Watson, R. J., and Doblin, M. A. (2015). Iron associated with exopolymeric substances is highly bioavailable to oceanic phytoplankton. Marine Chemistry 173, 136–147.
| Iron associated with exopolymeric substances is highly bioavailable to oceanic phytoplankton.Crossref | GoogleScholarGoogle Scholar |
Hassler, C. S., van den Berg, C. M. G., and Boyd, P. W. (2017). Toward a regional classification to provide a more inclusive examination of the ocean biogeochemistry of iron-binding ligands. Frontiers in Marine Science 4, 19.
| Toward a regional classification to provide a more inclusive examination of the ocean biogeochemistry of iron-binding ligands.Crossref | GoogleScholarGoogle Scholar |
Hawkes, J. A., Hansen, C. T., Goldhammer, T., Bach, W., and Dittmar, T. (2016). Molecular alteration of marine dissolved organic matter under experimental hydrothermal conditions. Geochimica et Cosmochimica Acta 175, 68–85.
| Molecular alteration of marine dissolved organic matter under experimental hydrothermal conditions.Crossref | GoogleScholarGoogle Scholar |
Hedges, J. I., Hatcher, P. G., Ertel, J. R., and Meyersschulte, K. J. A. (1992). Comparison of dissolved humic substances from seawater with amazon river counterparts by 13C-NMR spectrometry. Geochimica et Cosmochimica Acta 56, 1753–1757.
| Comparison of dissolved humic substances from seawater with amazon river counterparts by 13C-NMR spectrometry.Crossref | GoogleScholarGoogle Scholar |
Hernes, P. J., and Benner, R. (2006). Terrigenous organic matter sources and reactivity in the North Atlantic Ocean and a comparison to the Arctic and Pacific oceans. Marine Chemistry 100, 66–79.
| Terrigenous organic matter sources and reactivity in the North Atlantic Ocean and a comparison to the Arctic and Pacific oceans.Crossref | GoogleScholarGoogle Scholar |
Hertkorn, N., Benner, R., Frommberger, M., Schmitt-Kopplin, P., Witt, M., Kaiser, K., Kettrup, A., and Hedges, J. I. (2006). Characterization of a major refractory component of marine dissolved organic matter. Geochimica et Cosmochimica Acta 70, 2990–3010.
| Characterization of a major refractory component of marine dissolved organic matter.Crossref | GoogleScholarGoogle Scholar |
Hudson, R. J. M. (1998). Which aqueous species control the rates of trace metal uptake by aquatic biota? Observation and predictions of non-equilibrium effects. The Science of the Total Environment 219, 95–115.
| Which aqueous species control the rates of trace metal uptake by aquatic biota? Observation and predictions of non-equilibrium effects.Crossref | GoogleScholarGoogle Scholar |
Hutchins, D. A., Witter, A. E., Butler, A., and Luther, G. W. (1999). Competition among marine phytoplankton for different chelated iron species. Nature 400, 858–861.
| Competition among marine phytoplankton for different chelated iron species.Crossref | GoogleScholarGoogle Scholar |
Jiao, N., Herndl, G. J., Hansell, D. A., Benner, R., Kattner, G., Wilhelm, S. W., Kirchman, D. L., Weinbauer, M. G., Tingwei, L., Chen, F., and Azam, F. (2010). Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nature Reviews. Microbiology 8, 593–599.
| Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean.Crossref | GoogleScholarGoogle Scholar | 20601964PubMed |
Laglera, L. M., and van den Berg, C. M. G. (2009). Evidence for geochemical control of iron by humic substances in seawater. Limnology and Oceanography 54, 610–619.
| Evidence for geochemical control of iron by humic substances in seawater.Crossref | GoogleScholarGoogle Scholar |
Laglera, L. M., Battaglia, G., and van den Berg, C. M. G. (2007). Determination of humic substances in natural waters by cathodic stripping voltammetry of their complexes with iron. Analytica Chimica Acta 599, 58–66.
| Determination of humic substances in natural waters by cathodic stripping voltammetry of their complexes with iron.Crossref | GoogleScholarGoogle Scholar | 17765064PubMed |
Lam, B., Baer, A., Alaee, M., Lefedvre, B., Moser, A., Williams, A., and Simpson, A. J. (2007). Major structural components in freshwater dissolved organic matter. Environmental Science & Technology 41, 8240–8247.
| Major structural components in freshwater dissolved organic matter.Crossref | GoogleScholarGoogle Scholar |
Lang, S. Q., Butterfield, D. A., Lilley, M. D., Paul Johnson, H., and Hedges, J. I. (2006). Dissolved organic carbon in ridge-axis and ridge-flank hydrothermal systems. Geochimica et Cosmochimica Acta 70, 3830–3842.
| Dissolved organic carbon in ridge-axis and ridge-flank hydrothermal systems.Crossref | GoogleScholarGoogle Scholar |
Lannuzel, D., Vancoppenolle, M., van der Merwe, P., de Jong, J., Meiners, K. M., Nishioka, J., and Schoemann, V. (2016). Iron in sea ice: review and new insights. Elementa 4, 000130.
| Iron in sea ice: review and new insights.Crossref | GoogleScholarGoogle Scholar |
Lechtenfeld, O. J., Kattner, G., Flerus, R., McCallister, S. L., Schmitt-Kopplin, P., and Koch, B. P. (2014). Molecular transformation and degradation of refractory dissolved organic matter in the Atlantic and Southern Ocean. Geochimica et Cosmochimica Acta 126, 321–337.
| Molecular transformation and degradation of refractory dissolved organic matter in the Atlantic and Southern Ocean.Crossref | GoogleScholarGoogle Scholar |
Legendre, L., Rivkin, R. B., Weinbauer, M. G., Guidi, L., and Uitz, J. (2015). The microbial carbon pump concept: potential biogeochemical significance in the globally changing ocean. Progress in Oceanography 134, 432–450.
| The microbial carbon pump concept: potential biogeochemical significance in the globally changing ocean.Crossref | GoogleScholarGoogle Scholar |
Lis, H., Shaked, Y., Kranzler, C., Keren, N., and Morel, F. M. M. (2015). Iron bioavailability to phytoplankton: an empirical approach. The ISME Journal 9, 1003–1013.
| Iron bioavailability to phytoplankton: an empirical approach.Crossref | GoogleScholarGoogle Scholar | 25350155PubMed |
Liu, X., and Millero, F. J. (2002). The solubility of iron in seawater. Marine Chemistry 77, 43–54.
| The solubility of iron in seawater.Crossref | GoogleScholarGoogle Scholar |
Maldonado, M. T., Strzepek, R. F., Sander, S. G., and Boyd, P. W. (2005). Acquisition of iron bound to strong organic complexes – with different Fe binding groups and photochemical reactivities by plankton communities in Fe-limited subantarctic waters. Global Biogeochemical Cycles 19, GB4S20.
| Acquisition of iron bound to strong organic complexes – with different Fe binding groups and photochemical reactivities by plankton communities in Fe-limited subantarctic waters.Crossref | GoogleScholarGoogle Scholar |
Mawji, E., Schlitzer, R., Masferrer Dodas, E., Abadie, C., Abouchami, W., Anderson, R. F., Baars, O., Bakker, K., Baskaran, M., Bates, N. R., Bluhm, K., Bowie, A., Bown, J., Boye, M., Boyle, E. A., Branellec, P., Bruland, K. W., Brzezinski, M. A., Bucciarelli, E., Buesseler, K., Butler, E., Cai, P., Cardinal, D., Casciotti, K., Chaves, J., Cheng, H., Chever, F., Church, T. M., Colman, A. S., Conway, T. M., Croot, P. L., Cutter, G. A., de Baar, H. J. W., de Souza, G. F., Dehairs, F., Deng, F., Thi Dieu, H., Dulaquais, G., Echegoyen-Sanz, Y., Edwards, R. L., Fahrbach, E., Fitzsimmons, J., Fleisher, M., Frank, M., Friedrich, J., Fripiat, F., Galer, S. J. G., Gamo, T., Garcia Solsona, E., Gerringa, L. G. A., Marcus Godoy, J., Gonzalez, S., Grossteffan, E., Hatta, M., Hayes, C. T., Iris Heller, M., Henderson, G., Huang, K.-F., Jeandel, C., Jenkins, W. J., John, S., Kenna, T. C., Klunder, M., Kretschmer, S., Kumamoto, Y., Laan, P., Labatut, M., Lacan, F., Lam, P. J., Lannuzel, D., le Moigne, F., Lechtenfeld, O. J., Lohan, M. C., Lu, Y., Masqué, P., McClain, C. R., Measures, C., Middag, R., Moffett, J., Navidad, A., Nishioka, J., Noble, A., Obata, H., Ohnemus, D. C., Owens, S., Planchon, F., Pradoux, C., Puigcorbé, V., Quay, P., Radic, A., Rehkämper, M., Remenyi, T., Rijkenberg, M. J. A., Rintoul, S., Robinson, L. F., Roeske, T., Rosenberg, M., van der Loeff, M. R., Ryabenko, E., Saito, M. A., Roshan, S., Salt, L., Sarthou, G., Schauer, U., Scott, P., Sedwick, P. N., Sha, L., Shiller, A. M., Sigman, D. M., Smethie, W., Smith, G. J., Sohrin, Y., Speich, S., Stichel, T., Stutsman, J., Swift, J. H., Tagliabue, A., Thomas, A., Tsunogai, U., Twining, B. S., van Aken, H. M., van Heuven, S., van Ooijen, J., van Weerlee, E., Venchiarutti, C., Voelker, A. H. L., Wake, B., and Warner, M. J. (2015). The GEOTRACES intermediate data product 2014. Marine Chemistry 177, 1–8.
| The GEOTRACES intermediate data product 2014.Crossref | GoogleScholarGoogle Scholar |
Myklestad, S. M., Skanoy, E., Hestmann, S., Skånøy, E., and Hestmann, S. A. (1997). Sensitive and rapid method for analysis of dissolved mono- and polysaccharides in seawater. Marine Chemistry 56, 279–286.
| Sensitive and rapid method for analysis of dissolved mono- and polysaccharides in seawater.Crossref | GoogleScholarGoogle Scholar |
Norman, L., Worms, I. A. M., Angles, E., Bowie, A. R., Mancuso Nichols, C., Pham, A. N., Slaveykova, V. I., Townsend, A. T., Waite, D., and Hassler, C. S. (2015). The role of bacterial and algal exopolymeric substances in iron chemistry. Marine Chemistry 173, 148–161.
| The role of bacterial and algal exopolymeric substances in iron chemistry.Crossref | GoogleScholarGoogle Scholar |
Omanović, D., Garnier, C., and Pižeta, I. (2015). ProMCC: an all-in-one tool for trace metal complexation studies. Marine Chemistry 173, 25–39.
| ProMCC: an all-in-one tool for trace metal complexation studies.Crossref | GoogleScholarGoogle Scholar |
Rafter, P. A., Sigman, D. M., and Mackey, K. R. M. (2017). Recycled iron fuels new production in the eastern equatorial Pacific Ocean. Nature Communications 8, 1100.
| Recycled iron fuels new production in the eastern equatorial Pacific Ocean.Crossref | GoogleScholarGoogle Scholar | 29062103PubMed |
Sander, S. G., and Koschinsky, A. (2011). Metal flux from hydrothermal vents increased by organic complexation. Nature Geoscience 4, 145–150.
| Metal flux from hydrothermal vents increased by organic complexation.Crossref | GoogleScholarGoogle Scholar |
Shaked, Y., Kustka, A. B., and Morel, F. M. M. (2005). A general kinetic model for iron acquisition by eukaryotic phytoplankton. Limnology and Oceanography 50, 872–882.
| A general kinetic model for iron acquisition by eukaryotic phytoplankton.Crossref | GoogleScholarGoogle Scholar |
Shen, Y., and Benner, R. (2018). Mixing it up in the ocean carbon cycle and the removal of refractory dissolved organic carbon. Nature Scientific Reports 8, 2542.
| Mixing it up in the ocean carbon cycle and the removal of refractory dissolved organic carbon.Crossref | GoogleScholarGoogle Scholar |
Shen, Y., Fichot, C. G., Liang, S. K., and Benner, R. (2016). Biological hot spots and the accumulation of marine dissolved organic matter in a highly productive ocean margin. Limnology and Oceanography 61, 1287–1300.
| Biological hot spots and the accumulation of marine dissolved organic matter in a highly productive ocean margin.Crossref | GoogleScholarGoogle Scholar |
Tagliabue, A., Bopp, L., Dutay, J.-C., Bowie, A. R., Chever, F., Jean-Baptiste, P., Bucciarelli, E., Lannuzel, D., Remenyi, T., Sarthou, G., Aumont, O., Gehlen, M., and Jeandel, C. (2010). Hydrothermal contribution to the oceanic dissolved iron inventory. Nature Geoscience 3, 252–256.
| Hydrothermal contribution to the oceanic dissolved iron inventory.Crossref | GoogleScholarGoogle Scholar |
Tagliabue, A., Sallée, J.-B., Bowie, A. R., Lévy, M., Swart, S., and Boyd, P. W. (2014). Surface-water iron supplies in the Southern Ocean sustained by deep winter mixing. Nature Geoscience 7, 314–320.
| Surface-water iron supplies in the Southern Ocean sustained by deep winter mixing.Crossref | GoogleScholarGoogle Scholar |
Tagliabue, A., Bowie, A. R., Boyd, P. W., Buck, K. N., Johnson, K. S., and Saito, M. A. (2017). The integral role of iron in ocean biogeochemistry. Nature 543, 51–59.
| The integral role of iron in ocean biogeochemistry.Crossref | GoogleScholarGoogle Scholar | 28252066PubMed |
Tang, D., and Morel, F. M. M. (2006). Distinguishing between cellular and Fe-oxide-associated trace elements in phytoplankton. Marine Chemistry 98, 18–30.
| Distinguishing between cellular and Fe-oxide-associated trace elements in phytoplankton.Crossref | GoogleScholarGoogle Scholar |
Thomas, D. N., and Lara, R. J. (1995). Photodegradation of algal derived dissolved organic carbon. Marine Ecology Progress Series 116, 309–310.
| Photodegradation of algal derived dissolved organic carbon.Crossref | GoogleScholarGoogle Scholar |
Van Wambeke, F., Bonnet, S., Moutin, T., Raimbault, P., Alarcon, G., and Guieu, C. (2008). Factors limiting heterotrophic bacterial production in the southern Pacific Ocean. Biogeosciences 5, 833–845.
| Factors limiting heterotrophic bacterial production in the southern Pacific Ocean.Crossref | GoogleScholarGoogle Scholar |
Vance, D., Little, S. H., de Souza, G. F., Khatiwala, S., Lohan, M. C., and Middag, R. (2017). Silicon and zinc biogeochemical cycles coupled through the Southern Ocean. Nature Geoscience 10, 202–206.
| Silicon and zinc biogeochemical cycles coupled through the Southern Ocean.Crossref | GoogleScholarGoogle Scholar |
Völker, C., and Tagliabue, A. (2015). Modeling organic iron-binding ligands in a three-dimensional biogeochemical ocean model. Marine Chemistry 173, 67–77.
| Modeling organic iron-binding ligands in a three-dimensional biogeochemical ocean model.Crossref | GoogleScholarGoogle Scholar |
Woodward, F. I., and Sheehey, J. E. (1983). ‘Principles and Measurements in Environmental Biology.’ (Butterworth: London, UK.)
Zhang, J., Kattner, G., and Koch, B. P. (2019). Interactions of trace elements and organic ligands in seawater and implications for quantifying biogeochemical dynamics: a review. Earth-Science Reviews 192, 631–649.
| Interactions of trace elements and organic ligands in seawater and implications for quantifying biogeochemical dynamics: a review.Crossref | GoogleScholarGoogle Scholar |
