Iron uptake and physiological response of phytoplankton during a mesoscale Southern Ocean iron enrichment

Iron supply is thought to regulate primary production in high nitrate, low chlorophyll (HNLC) regions of the sea in both the past and the present. A critical aspect of this relationship is acquisition of iron (Fe) by phytoplankton, which occurs through a complex series of extracellular reactions that are influenced by Fe chemistry and speciation. During the first in situ mesoscale Fe-enrichment experiment in the Southern Ocean (Southern Ocean iron release experiment [SOIREE]), we monitored the uptake of Fe by three size classes of plankton and their ensuing physiological response to the Fe enrichment. Rates of Fe uptake from both inorganic Fe (Fe9) and organic Fe complexes (FeL) were initially fast, indicative of Fe-limitation. After Fe enrichment phytoplankton down-regulated Fe uptake and optimized physiological performance, but by day 12 they had greatly increased their capacity to acquire Fe from FeL. The increase in Fe uptake from FeL coincided with a sixfold decrease in Fe9 that followed the production of Fe-binding organic ligands. Phytoplankton were able to use organically bound Fe at rates sufficient to maintain net growth for more than 42 d. Adaptation to such shifts in Fe chemistry may contribute to bloom longevity in these polar HNLC waters. High nitrate, low chlorophyll (HNLC) waters account for 25% of the world surface ocean and have been the focus of recent investigations examining what factor(s) control primary productivity. Culture (Sunda and Huntsman 1997) and shipboard (Martin et al. 1989; Coale et al. 1996a) studies show that low Fe availability limits phytoplankton growth, a result that has been confirmed by in situ Fe enrichments in HNLC regions (Martin et al. 1994; Coale et al. 1996b; Boyd et al. 2000). The chemical complexities of Fe and its potential interactions with microbes in natural waters, however, may obfuscate the relationship between phytoplankton physiology and Fe concentrations (Geider 1999). Physiological adaptations of Fe-limited phytoplankton include variations in inorganic Fe uptake kinetics (Harrison and Morel 1986; Hudson and Morel 1990) and in their abilities to acquire Fe from organic Fe complexes (FeL) (Maldonado and Price 1999, 2001). However, the physiological responses of natural phytoplankton assemblages to shifts in Fe speciation in situ are unknown. Pronounced in situ changes in Fe speciation occurred during IronEx II in the Equatorial Pacific (Rue and Bruland 1997), but no concurrent measurements of algal Fe uptake physiology were made. Because Fe speciation strongly affects the ability of phytoplankton to acquire Fe (Geider 1999; Maldonado and Price 1999, 2001), changes in Fe speciation will undoubtedly determine the algal response to Fe enrichment. Southern Ocean waters are characterized by a large reservoir of macronutrients and are thought to have a disproportionate influence on past and present global climate (Broecker and Henderson 1998; Sarmiento et al. 1998). The SOIREE (Boyd et al. 2000) was conducted in February 1999 to assess whether Fe supply controls phytoplankton production in polar waters (618S 1408E). A 50 km2 area of surface ocean was fertilized with inorganic Fe(II) labeled with SF6 (sulfur hexafluoride) and with three subsequent additions of Fe on days 3, 5, and 7 of the experiment (Fig. 1A) (Boyd et al. 2000). The Fe enrichment resulted in significant changes in Fe speciation and dissolved Fe concentrations. Within 13 d, a pronounced accumulation of phytoplankton stocks, an increase in growth rate and photosynthetic competence of the dominant taxa, and a change in species composition were observed (Boyd et al. 2000). Moreover, SeaWiFS remotesensing images of the Fe-fertilized patch showed that the bloom was still present 42 d after the onset of SOIREE and had spread over a ribbon-shaped area of 1,100 km2 (Abraham et al. 2000). This observation raised fundamental questions regarding the mechanisms for the sustenance and longevity of this bloom. This paper investigates the physiological response of plankton to changes in Fe chemistry and speciation following this in situ Fe enrichment