The role of iron in the biogeochemistry of the Southern Ocean and equatorial Pacific: a comparison of in situ iron enrichments

Deep-Sea Research II 49 (2002) 1803–1821

The role of iron in the biogeochemistry of the Southern Ocean and equatorial Pacific: a comparison of in situ iron enrichments Philip W. Boyd* National Institute of Water and Atmosphere, Department of Chemistry, Centre for Chemical and Physical Oceanography, University of Otago, Dunedin, New Zealand

Abstract A better understanding of the relationship between iron supply and the biogeochemical functioning of high nitrate low chlorophyll (HNLC) regions may be obtained by comparing and contrasting observations from oceanic provinces. The open polar Southern Ocean and the eastern equatorial Pacific are HNLC regimes, but have different oceanographic properties. Until recently, there have been insufficient datasets on the role of iron (mainly from deckboard iron enrichments) to enable a comprehensive comparison of these regions. However, the recent Southern Ocean Iron RElease Experiment (SOIREE), the first in situ iron enrichment in polar waters, provides a detailed suite of time-series measurements to compare with those from the equatorial Pacific IronEx II study. As expected, a comparison of these polar and tropical studies yielded differences in the timing of iron-mediated responses that are mainly due to the temperature-dependence of biological rates. However, trends from both studies are similar with respect to the magnitude of iron-mediated changes in bulk signals (such as macronutrient uptake), algal physiological responses, and shifts in algal community structure. There are also parallels between these studies in the response of components of the pelagic ecosystem such as heterotrophic bacteria. Such convergence suggests that it is possible to incorporate considerable detail into future generic models investigating the role of the biota in the biogeochemical cycling of iron. There are also significant differences, such as the degree of herbivory, and the fate of the accumulated algal carbon during these two iron-stimulated phytoplankton blooms. Such departures offer a means to understand better important regional differences in the biogeochemical cycling of iron in HNLC waters, and to investigate the possible effects of physical artefactsFcaused by mixing with surrounding HNLC waters at the boundaries of these labelled patchesFduring such mesoscale perturbation experiments. r 2002 Elsevier Science Ltd. All rights reserved. Re´sume´ # compar!e du fer sur la biog!eochimie de deux zones de l’oc!ean mondial, paradoxales par leur pauvret!e en Le role phytoplancton dans des environnements riches en sels nutritifs (zones dites ‘‘HNLC’’), est de! crit a" travers deux exp!eriences de fertilisation artificielle : IronEx II (Pacifique Equatorial) et SOIREE (Ocean Austral). La deux e! cosyst"emes diff"erent par le d!elai de r!eponse a" la fertilisation en fer, la r!eaction des herbivores, et le devenir du carbone algal accumule! . Par contre leur mode de re! ponse est tre" s comparable du point de vue de la consommation de sels nutritifs, des r!eponses physiologiques et des changements dans la composition des communaut!es algales. Bien que l’ensemble des ph!enom"enes observ!es n’ait pas rec-u d’explication compl"ete (ainsi les perturbations e! ventuelles du

*Tel.: +64-3-479-5249; fax: +64-3-479-5249. E-mail address: [email protected] (P.W. Boyd). 0967-0645/02/$ - see front matter r 2002 Elsevier Science Ltd. All rights reserved. PII: S 0 9 6 7 - 0 6 4 5 ( 0 2 ) 0 0 0 1 3 - 9

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P.W. Boyd / Deep-Sea Research II 49 (2002) 1803–1821

syst"eme fertilis!e sous l’effet des e! changes physiques a" m!eso!echelle avec le milieu environnant n’est pas d!ecrit), cette e! tude compare! e donnent des bases inte! ressantes pour mode! liser la bioge! ochimie du fer dans les syste" mes pe! lagiques.

1. Introduction Oceanic regions characterised by perennially high macronutrient levels yet low and constant levels of phytoplankton stocks have been a paradox long recorded by oceanographers (Gran, 1931). As early as the mid 1930s iron supply was invoked as an explanation for these so-called high nitrate low chlorophyll a (HNLC) regions (Hart, 1934). In the last 15 years these provinces, comprising around 25% of the World Ocean (de Baar et al., 1999), have been the focus of a large research effort. Much of this research was based on laboratory culture (Morel et al., 1991a) and/or shipboard iron enrichments (Martin and Fitzwater, 1988), and is summarised in various reviews (please refer to Wells et al., 1995; de Baar and Boyd, 2000). A key advance due to this early research was the development of the Iron Hypothesis (Martin, 1990), which linked changes in iron supply to the ocean with alteration of rates of primary production and the subsequent magnitude of carbon sequestration in HNLC waters during both the present day and the geological past. Subsequently, the formulation of the Ecumenical Iron hypothesis (Morel et al., 1991b; Cullen, 1995) has provided a detailed framework that links iron supply, foodweb structure, and macronutrient supply to explain the persistence of low and constant phytoplankton stocks in these HNLC regions. Although lab cultures and shipboard iron enrichments provided many insights into the key role of iron on phytoplankton processes such as inorganic iron uptake kinetics (Hudson and Morel, 1990), floristic shifts (Martin et al., 1989), and nitrogen uptake (Price et al., 1991), it was thought that conducting large-scale in situ fertilisations would yield further valuable insights into the functioning of these regions (Martin et al., 1991). The first in situ iron fertilisation, IronEx I was conducted in equatorial Pacific waters in October 1993 (Martin et al., 1994). The experiment, which

marked a major advance in biological oceanography, was confounded by the subduction of the fertilised waters to depth early in the experiment (day 4/5); nevertheless, the intrinsic response of the phytoplankton to iron supply provided tantilising evidence of an iron-stressed algal assemblage (Kolber et al., 1994). The results were viewed as equivocal and four hypotheses were put forward by Coale et al. (1996) to explain the lack of a sustained biogeochemical response upon iron addition (rapid loss of iron from the patch; reduced levels of iron photochemistry upon subduction; rapid cropping of biomass by zooplankton; another limiting nutrient (zinc or silicic acid)). In May 1995, a second experiment in these waters (3.51S, 1051W), IronEx II, demonstrated unequivocally the role of iron supply in controlling phytoplankton processes in eastern equatorial Pacific waters. However, it was evident from modelling studies of the biogeochemical effects of persistent iron enrichment of HNLC waters, that the Southern Ocean rather than the equatorial Pacific was the region where any such ironmediated carbon sequestration might have the greatest effect on atmospheric carbon dioxide concentrations (Sarmiento and Orr, 1991). Furthermore, given the growing realisation that the physics (Gargett, 1991), geochemistry (Martin et al., 1989; de Baar et al., 1995), and ecology/ biology (Banse, 1991a; Boyd et al., 1999a, b) of HNLC regions was different, it was not possible to extrapolate the findings of IronEx II to the Southern Ocean. Recently, an in situ iron enrichment experiment was conducted in the Southern Ocean (Boyd et al., 2000). The Southern Ocean Iron RElease Experiment (SOIREE) provides unequivocal evidence of iron limitation of phytoplankton processes in summer in the waters in the polar AustralasianPacific sector of the Southern Ocean. A second in situ iron release experiment, EisenEx, was performed in austral spring 2001 in the Atlantic sector of the Southern Ocean (Smetacek, 2001), and

P.W. Boyd / Deep-Sea Research II 49 (2002) 1803–1821

although few results are so far available, Smetacek reported that a massive diatom bloom (chlorophyll >2 mg m
3) resulted. Large-scale manipulation experiments are increasingly being advocated as the most appropriate tools to interpret and better understand the functioning of natural systems (Sarmiento and Wofsy, 1999; SOLAS Science Plan, 2000). Now that such experiments have been conducted in two HNLC regions, a comparison of these two detailed studies (IronEx II and SOIREE) may yield insights into common trends in and/or departures between the functioning of such HNLC regions. Furthermore, such a comparison provides an opportunity to assess how to improve the design of such mesoscale experiments. Such information will be essential if we are to better model the ocean biogeochemistry of iron and how it relates to the carbon cycle (Fung et al., 2000; Archer and Johnson, 2000). These models will be particularly useful tools to help provide a better understanding the biogeochemistry of these watersFone of the goals of the Brest 2000 Southern Ocean Symposium (Tre! guer et al., 2002). In this paper, I provide a brief summary of the main findings of SOIREE, compare the SOIREE and IronEx II datasets, and suggest research topics that should be the focus of future Southern Ocean studies.

2. SOIREEFa summary of the experimental findings SOIREE took place in February 1999, at a site (611S 1401E) south of the Polar Front, and N of the southern branch of the Antarctic Circumpolar Current in the Australasian-Pacific sector of the Southern Ocean (Boyd et al., 2000). Just prior to the enrichment an oceanographic survey, upstream of the proposed site, revealed properties characteristic of HNLC waters (Table 1). The first infusion of dissolved iron (tracked using the conservative tracer sulphur hexafluoride (SF6)) raised iron levels to around 3 nM initially within a 65 m mixed-layer depth. Three additional iron infusions were required (days 3, 5 and 7) during the 13-day experiment, since after each of infusions 1–3, dissolved iron concentrations quickly

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returned towards background levels. However, following infusion 4, there was an initial decline in dissolved iron concentration, after which time levels remained close to 1 nM (mainly as FeII) for the remaining occupation of the SOIREE site (Bowie et al., 2001; Croot et al., 2002). During SOIREE there were iron-mediated 6-fold increases in chlorophyll concentrations, a floristic shift to large cells (diatoms), and a 6-fold increase in rates of primary production (Boyd et al., 2000). These increases resulted in a marked consumption of macronutrients (Frew et al., 2001), drawdown of pCO2 (Watson et al., 2000), and increases in Dimethyl Sulphide (DMS) (Boyd et al., 2000; Turner et al., 2002). There were subsequent changes in the magnitude of stocks and rate processes within the microbial foodweb (Hall and Safi, 2001), but little change in mesozooplankton activity (Zeldis, 2001). Over the course of SOIREE, there was no significant increase in the export flux of biogenic particulates to depth during the brief 13-day occupation of this site (Nodder and Waite, 2001; Trull and Armand, 2001; Charette and Buesseler, 2000). The SOIREE bloom was monitored intermittently from SeaWiFS after our departure; the bloom was still present 55 days after the initial infusion, with chlorophyll levels of up to 3 mg l
1, comprised an area of >1000 km2, containing an estimated algal biomass of up to of 3000 tonnes carbon (Abraham et al., 2000).

3. A comparison of SOIREE and IronEx II In the present paper, I mainly focus on comparing the results of SOIREE with those of IronEx II (Coale et al., 1996), since interpretation of the IronEx I study (Martin et al., 1994) was confounded by a subduction event 4 days after the onset of this experiment (Martin et al., 1994). I first compare trends in the bulk signalsFsuch as chlorophyll concentrationsFbetween the experiments, then assess shifts in algal physiological properties and community structure. Next, I shall compare and contrast the responses of the pelagic foodweb, and the fate of both these iron-mediated algal blooms.

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Table 1 A summary of the initial and bloom conditions during the IronEx II and SOIREE studies Property

IronEx II initial

SOIREE initial

IronEx II bloom

SOIREE bloom

Temperature (C) Mixed layer depth (m) Nitrate (mM) Silicic acid (mM) Dissolved iron (pM) Iron-binding ligands (nM) Chlorophyll (mg m
3) Algal community structure Heterotrophic bacterial abundances (cells l
1) Fv =Fm Mesozooplankton abundance (mg C m
3)

>23 25.0 10.0 5.0 20 0.3c 0.20 Pico-dominated 6  108 e 0.24 3.8

2.0 65.0 25.0 10.0 80 3.5 0.25 Pico-dominated 1.1  109 0.22 19.7

>23 >25.0a 5.0b o1.0b 800–1000b 1.3c,d >2.0 Diatom-dominated 3  108 d,e 0.57 >12f

2.5 65.0 22.0b >6.0b 1000b 8.0d >1.5 Diatom-dominated 3  108 0.65 20.0

Bloom denotes the day when highest chlorophyll concentrations were recordedFday 6/7 for IronEx II, and day 12/13 for SOIREE (Fig. 1). Data for IronEx II and SOIREE are from Coale et al. (1996) and Boyd et al. (2000), respectively, unless otherwise stated. a Denotes that the mixed layer deepened to 50 m over the duration of the study. b Denotes from the centre of the patch and thus the highest recorded levels. c Denotes strong ligands (see Fig. 7 caption). d In some cases the maximum observed value for a property was observed on a different day. e Cochlan (2001). f Rollwagen Bollens and Landry (2000).

4. Phytoplankton biomass and production Each experiment demonstrated that iron supply controlled phytoplankton processes at the respective HNLC site (Coale et al., 1996; Boyd et al., 2000). At the onset of IronEx II, chlorophyll concentrations were similar to those just prior to SOIREE (Table 1, Fig. 1). The magnitude of the observed increases in chlorophyll concentrations were comparable in both the IronEx II (mean 2.4 mg l
1 (Cavender-Bares et al., 1999) maximum close to 4 mg l
1, Coale et al., 1996) and SOIREE (mean 1.8 mg l
1, values up to 3 mg l
1Fsee Gall et al., 2001a). However, during IronEx II these elevated concentrations were attained after 5/6 days of the experiment (Cavender-Bares et al., 1999) whereas they did not peak until days 10/11 during SOIREE (Gall et al., 2001a). In contrast to chlorophyll, the ‘baseline’ rates of community column-integrated primary production at the IronEx II site were more than double those at the SOIREE locale (Fig. 2). Column-integrated primary production increased around 5-fold in both studies (Fig. 2) and attained a rate of

Fig. 1. A comparison of changes in chlorophyll concentrations during the time-course of SOIREE and IronEx II. Chlorophyll was expressed as mean water-column concentrations to take into account increases in mixed-layer depth during IronEx II, and vertical heterogeneity in chlorophyll profiles observed in SOIREE due to thermal transients within the seasonal mixed layer (Boyd et al., 2000). Data are courtesy of R. Barber (unpublished, IronEx II) and from Boyd and Gall (SOIREE, unpublished data). No data on the standard errors of the measurements were available from IronEx II, for SOIREE errors were generally o0.1 mg m
3 (Boyd et al., 2000).

P.W. Boyd / Deep-Sea Research II 49 (2002) 1803–1821

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Fig. 2. Rates of column-integrated primary production during the evolution of SOIREE and IronEx II blooms. Rates were estimated in both cases using the 14C method and 24 h incubations, and computed to the base of the mixed layer (25–50 m range, IronEx II; 65 m, SOIREE). Data are courtesy of R Barber (unpublished, IronEx II) and for SOIREE from Gall et al. (2001b). No data on the standard errors of the measurements are available from IronEx II, for SOIREE errors were generally o50 mg C m
2 d
1 (Gall et al., 2001b).

Fig. 3. Time-series of the rates of chlorophyll-normalised rates of primary production (Pbopt ) during SOIREE and IronEx II. Pbopt was calculated from column-integrated production rates normalised with the column-integrated chlorophyll inventory (mixed-layer depths used were as for Fig. 2). Data are courtesy of R. Barber (unpublished, IronEx II) and for SOIREE from Gall et al. (2001b). No data on the standard errors of the measurements are available from IronEx II, for SOIREE errors were generally o2 mg C (mg chla
1) d
1 (Gall et al., 2001b).

2.5 g C m
2 d
1 in IronEx II, and around half this rate by days 12/13 of SOIREE, but took 1.5 times longer to attain the highest observed rate in SOIREE. In contrast to IronEx II, there was no evidence of a decline in rates of production during SOIREE which is often indicative of the onset of the bloom’s decline. The faster initial production rates, and response times to iron fertilisation observed in IronEx II may be attributed to their temperature dependence. The maximum chlorophyll-specific carbon fixation rates (Pbopt ; see review Behrenfeld and Falkowski, 1997) at the onset of IronEx II were 4fold faster than those initially observed during SOIREE (Fig. 3). A comparison of published models of the temperature versus Pbopt relationship (see Fig. 4 in Behrenfeld and Falkowski, 1997) indicates that initial Pbopt in both SOIREE and IronEx II were less than the Megard (1972) estimated rates for polar (2.0C; 1 mg C (mg Chl
1) h
1, photoperiod 16 h during SOIREE) and tropical (>23C; 4 mg C (mg Chl
1) h
1, photoperiod 12 h during IronEx II). In both experiments, after iron enrichment Pbopt increased

Fig. 4. A comparison of trends in nitrate removal during the time-course of SOIREE and IronEx II. In both experiments the iron-mediated uptake of nitrate and silicic acid were reported to be equimolar so this plot also approximates the magnitude and timing of the removal of silicic acid. For each day of the experiment, nitrate removal was defined as the ambient mixedlayer concentration at time zero minus the concentration on that subsequent day. Data are derived from Coale et al. (1996) (IronEx II) and Boyd et al. (2000) (SOIREE). Note these estimated removal rates are for the centre of each iron-labelled patch and thus represent the highest recorded removal rates (see Coale et al., 1996). No data on the standard errors of the measurements are available from IronEx II, for SOIREE errors were generally o0.3 mM (Boyd et al., 2000).

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P.W. Boyd / Deep-Sea Research II 49 (2002) 1803–1821

around 2-fold (Fig. 3), over 6 days in IronEx II, yet despite polar water temperatures required 3 days to double in SOIREE. The highest value of Pbopt in IronEx II (75) exceeded the estimate of the Megard (1972) model, but was similar to that predicted by other models (see Fig. 4, Behrenfeld and Falkowski, 1997). Pbopt declined after day 8 in IronEx II and had returned to initial values by day 17 (Fig. 3), whereas in the SOIREE study Pbopt peaked on day 3 and slowly declined thereafter (Fig. 3). As for Pbopt ; estimates of algal growth rate in both experiments reflected temperature dependency (Eppley, 1972, re-appraised by Banse, 1991b). Landry et al. (2000a) reported increased growth rates from 0.6 d
1 (prior to the experiment, using the dilution technique, i.e. gross algal growth) to around 1.6 d
1 after 7 days. Net growth rates for diatoms were estimated to be 0.6–0.8 d
1 (based on biomass, 0.6 d
1; pigments, 0.8 d
1; abundances, 0.8 d
1; see Table 2, Landry et al., 2000b; the dilution technique, m-m=0.8 d
1; Landry et al., 2000a, b). In SOIREE, Gall et al. (2001b) recorded an increase in growth rate from an initial value of 0.05 to 0.2 d
1 (using the instantaneous change in chlorophyll or algal carbon, i.e. net algal growth). These net rates are similar to those reported by Abbott et al. (2000) during the development of a bloom in the vicinity of the Polar Front near 170W. The highest algal loss term during SOIREE was due to lateral advection (0.07 d
1) followed by sedimentation and grazing (0.03 d
1, Abraham et al., 2000). Thus, gross algal growth rates during SOIREE may have been around 0.3 d
1. The ironelevated gross rates from Landry et al. are close to the maximal rates at this temperature (mmax ) reported by Banse (1.9 d
1), whereas those from SOIREE are around half of the maximal rate at polar temperatures (0.6 d
1). Such maximal rates have been reported in polar deckboard (Martin et al., 1991; de Baar et al., 1990) and coastal mesocosm (Agusti and Duarte, 2000) experiments. During days 12/13 of SOIREE, cells were photosynthetically competent (i.e. Fv =Fm ¼ 0:65; the theoretical maximum) yet were growing at ommax : Such suboptimal growth rates may be due to the ability of phytoplankton to acquire iron strongly bound to organic ligands at

moderateFrather than maximal rates (Maldonado et al., 2001). During both the IronEx II and SOIREE blooms, the consumption of nitrate was of a similar magnitude (3 mM, and up to 5 mM in SOIREE and IronEx II, respectivelyFsee Fig. 4). In both studies, the iron-mediated uptake of nitrate and silicic acid was reported to be equimolar (i.e. 1:1, Table 1). In the HNLC waters surrounding the SOIREE site (i.e. control treatment) the Si:N uptake stoichiometry was >2 (Watson et al., 2000). Thus, the effect of iron enrichment on Si:N uptake during SOIREE was as reported for lab culture and deckboard studies when iron has been added (Hutchins and Bruland, 1998; Takeda, 1998). Although no published data on the initial Si:N uptake ratio were available for IronEx II, it is probable that it was greater than unity, as observed for polar (Takeda, 1998; Watson et al., 2000), subpolar (Takeda, 1998) and continental shelf HNLC waters (Hutchins and Bruland, 1998). The nitrate:phosphate uptake ratio was around 10 during SOIREE (Frew et al., 2001) and was thus similar to that reported for diatom blooms in the Ross Sea by Arrigo et al. (1999). No data on N:P uptake stoichiometry were available for the HNLC waters surrounding the SOIREE site, nor published from the IronEx II study (see Coale et al., 1996). The drawdown of pCO2 during SOIREE was around 35 matm (Watson et al., 2000; Bakker et al., 2001) whereas during IronEx II a total consumption of 90 matm was reported (Cooper et al., 1996). DMS concentrations in the upper ocean were up to 3-fold higher than ambient at the end of both experiments (Turner et al., 1996; Boyd et al., 2000; Turner et al., 2002). Nitrous oxide, another biologically mediated climate-reactive gas, was reported to increase slightly at depth within the SOIREE fertilised waters (Law and Ling, 2001), but to my knowledge no published data on N2O are available from IronEx II.

5. Algal physiology Phytoplankton physiological shifts accompanied iron-mediated changes in the magnitude of

P.W. Boyd / Deep-Sea Research II 49 (2002) 1803–1821

bulk phytoplankton properties during both experiments. Such physiological data provide insights into the relative timing of photosynthetic and biochemical changes in the cells in response to iron enrichment (McKay et al., 1997). During both IronEx II and SOIREE, the photochemical conversion efficiency of photosystem (PS) II (Fv =Fm ) was the first (measured) phytoplankton property to respond to iron supply (Behrenfeld et al., 1996; Boyd and Abraham, 2001). Kolber et al. (1994) also noted this trend during the IronEx I study. Behrenfeld et al. reported an exponential increase in Fv =Fm Fdoubling after 24 hFin IronEx II, whereas in contrast the increase in Fv =Fm was slower during SOIREE (Fig. 5). Boyd and Abraham (2001) speculate that this slower response

Fig. 5. Temporal trends in Fv =Fm in iron-fertilised waters and from the surrounding HNLC waters for: (A) IronEx II (data from Behrenfeld et al., 1996, underway data (5 m depth)) and (B) SOIREE (from Boyd and Abraham, 2001, 30 m depth). In both cases data were obtained using Fast Repetition Rate Fluorometry (Kolber and Falkowski, 1993). Standard errors were o0.02 in both experiments.

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time to iron enrichment during SOIREE was due to the colder water temperatures and in part to the deeper mixed-layer depths: similarly, slow response times of Fv =Fm have been reported during recent deckboard iron enrichments in polar Southern Ocean waters (Olson et al., 2000). In contrast, Boyd et al. (1998) observed a relatively fast ironmediated increase in Fv =Fm (48 h) during a deckboard iron fertilisation in HNLC subarctic Pacific waters in summer conditions (water temperature 121C). Behrenfeld et al. (1996) reported a relatively rapid iron-induced increase in sigmaFthe crosssectional area of PSII, whereas during IronEx I there was an equally fast but pronounced decrease in sigma (Kolber et al., 1994), while in SOIREE there was a small decrease over time in sigma (Boyd and Abraham, 2001). The reasons for these different trends in sigma upon iron fertilisation in these three experiments are not currently understood (Boyd and Abraham, 2001). The response times of other physiological properties to iron fertilisation were slower during both SOIREE and IronEx II. For example, decreases in flavodoxin levels in diatoms (a proxy for the alleviation of iron stressFLaRoche et al. 1996) during SOIREE were not observed until day 5, 4 days after initial iron-mediated increases in Fv =Fm : These data support the contention of Erdner and Anderson (1999)Fbased on their IronEx II resultsFthat components of the photosystem such as light-harvesting pigments do not have equivalent substitutes, and hence any switch from the synthesis of flavodoxin to ferredoxin upon iron limitation will be delayed until other processes with obligate iron requirements have been met. Erdner and Anderson (1999), using an HPLC technique, found no evidence of ferredoxin in diatoms during the IronEx II bloom. During SOIREE, there was no observed response to antibodies for ferredoxin (R.M. McKay, pers. comm.), and thus the results could not be related to IronEx II or those observed in deckboard iron enrichments such as in the subantarctic Pacific (Boyd et al., 1999b). During SOIREE, data were obtained on a number of other proxies for the alleviation of algal iron stressFsuch as diatom sinking rates (see Muggli et al., 1996, Waite and Nodder, 2001) and

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the uptake of organically bound iron (see Maldonado and Price, 1999). These proxies exhibited similar temporal trends to that of flavodoxin levels in diatoms during SOIREE (Boyd et al., 2000), and are presented in detail in Maldonado et al. (2001). Other physiological properties of the autotrophic community exhibited similar responses to iron enrichment during both SOIREE and IronEx II. Iron-replete conditions during IronEx II (Cavender-Bares et al., 1999) resulted in increased cell size (1.5-fold) for pico-prokaryotes and picoeukaryotes, the cell size of nanoplankton approximately doubled, while that for the dominant

pennate diatoms increased to a lesser extent. Similarly, during SOIREE mean cell size increased upon iron enrichment for nanoplankton (mainly haptophytes) and the chain length of Fragilariopsis kerguelensis doubled (Gall et al., 2001a). During both experiments there were increases in cellular chlorophyll levels (Cavender-Bares et al., 1999; Gall et al., 2001a) and decreases in algal carbon:chlorophyll ratios (Fig. 6A) in response to ironmediated growth, with the largest decreases in this ratio being recorded for the large diatoms (Fig. 6B). Such trends also have been reported in lab culture experiments (Greene et al., 1991; Sunda and Huntsman, 1997). Thus, during both mesoscale iron enrichments the observed increases in chlorophyll were due to both increases in cell abundances and in cellular concentrations.

6. Floristic shifts and the ecumenical iron hypothesis

Fig. 6. Changes in the ratio of algal carbon:chlorophyll for (A) all algal cells and (B) for diatoms in the IronEx II (Landry et al., 2000b) and SOIREE (Gall et al., 2001a) blooms. In both studies, diatom carbon data were obtained from microscopy and taxon-specific biovolume/carbon algorithms. In the former study, diatom pigments were obtained from HPLC analysis, whereas in the latter they were derived from size-fractionated chlorophyll in conjunction with data on diatom size/abundance from microscopy.

This hypothesis put forward by Morel et al. (1991b) offers an explanation for the widespread existence of HNLC waters based jointly on low iron supply constraining the growth rates of large phytoplankton, and grazer control keeping small phytoplankton cropped to low biomass levels. During IronEx I, Kolber et al. (1994) presented evidenceFobtained from active fluorometry on a range of algal size classesFthat all phytoplankton groups responded to iron supply. Furthermore, during IronEx II Cavender-Bares et al. (1999) reported that although all five algal groups exhibited increased cellular fluorescence, they displayed differences in net growth (due to the concomitant influence of micrograzer activity). Boyd and Abraham (2001) also provided evidence that all algal size fractions at the SOIREE site (o2, o5, o20 and >20 mm) displayed increased Fv =Fm upon iron enrichment, indicative of the alleviation of iron stress. However, in both IronEx II and SOIREE, although all algal classes responded to iron enrichment, there was a floristic shift from a small to a large phytoplanktondominated community (Coale et al., 1996; Boyd et al., 2000), suggesting that only the larger cells able to escape predation accumulated. During

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both studies, ultimate control by iron supply (Cavender-Bares et al., 1999; Boyd and Abraham, 2001) and proximal control by micrograzers (Landry et al., 2000a, b; Hall and Safi, 2001) determined the resulting algal species composition and size structure. Although these observations confirm the ecumenical iron hypothesis, the effect of iron enrichment on all algal cellsFincluding small cells hypothesised to be under grazer controlFrepresents a further refinement of this framework to describe the functioning of HNLC waters. This combination of iron supply and grazing pressure led to the dominance of the IronEx II bloom by pennate diatoms (B 20 mm, non-chainforming, see Landry et al., 2000b) which increased in abundance by 15-fold compared, with small increases in the abundances of Synechococcus and nanophytoplankton (Cavender-Bares et al., 1999). In SOIREE, there were no significant sustained increases in pico-eukaryote abundances, whereas the bloom was dominated by large pennate chainforming diatom Fragilariopsis kerguelensis (each cell >35 mm in length, with up to 14 cells per chain) and to a lesser extent by nanoflagellates (mainly haptophytesFsee later). Again, in both experiments trends in the order in which these floristic shifts took place were similar: the initial biomass increase in IronEx II was mainly due to pico-prokaryotes (Synechococcus and Prochlorococcus), and pico-plankton stocks were the first to increase during SOIREE. In both experiments, nanoplankton stocks increased prior to the onset of elevated diatom biomass. One important distinction between these dominant large diatoms is that Fragilariopsis kerguelensis is highly silicified and thought to be morphologically adapted to minimise grazing (Verity and Smetacek, 1996), whereas the Nitzschia spp. in the IronEx II bloom were reported to be grazed by large microzooplankton towards the end of the experiment (Cavender-Bares et al., 1999; Landry et al., 2000a). Thus, during SOIREE iron enrichment resulted in a bloom dominated by a species with very low loss rates, i.e. virtually no herbivory (Hall and Safi, 2001; Zeldis, 2001) and low sinking rates (Waite and Nodder, 2001).

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7. Foodweb response The heterotrophic microbial and metazoan components of the pelagic foodweb also underwent changes in both experiments that were broadly comparable. Heterotrophic bacterial abundances increased slightly from 6–8  108 to 1.1  109 cells l
1 by day 14 of IronEx II (Cochlan, 2001). There was likely a close coupling between bacteria and bacterivores, since bacterial production and growth increased 3-fold between days 2 and 6, and peaked by day 7 (Cochlan, 2001). As for IronEx II, there was little change in bacterial abundances during SOIREE but bacterial production tripled, again indicative of high rates of bacterivory (Hall and Safi, 2001). Increases in bacterial production were not observed until after day 6/7, suggesting that the cells may have initially been limited by the supply of organic substrates such as DOC/DON rather than iron: Hall and Safi (2001) report a robust linear relationship between rates of bacterial and primary production during SOIREE. It is puzzling that upon iron supply at the IronEx II site there was a rapid response by autotrophic bacteria (Synechococcus cell size had increased within 2 days; Cavender-Bares et al., 1999) and concurrent increases in community primary production (Fig. 2), yet there was no significant increase in heterotrophic bacterial production, growth rates or abundances until after day 2 (Cochlan, 2001). This trend also may be indicative of limitation of heterotrophic bacterial growth by factors other that iron, as reported in several deckboard studies in both the HNLC waters of the Southern Ocean (Church et al., 2000) and coastal California (Kirchman et al., 2000). During IronEx I, Banse (1995) reported that the micrograzer community had responded (stocks increased from 4.7 to 7.3 mg l
1) to iron-mediated initial increases in the stocks of small autotrophs in spite of heavy grazing losses. Similarly, during both IronEx II and SOIREE there were increases in both microzooplankton stocks and in rates of herbivory. The microzooplankton community at the IronEx II site was initially dominated by nanoflagellates (>3 mg C m
3), followed by dinoflagellates (>2 mg C m
3), ciliates (>1 mg C m
3)

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and choanoflagellates (>0.03 mg C m
3; Landry et al., 2000b). During the experiment there was a doubling of stocks that was mainly due to ciliates and flagellates (Coale et al., 1996). Moreover, Landry et al. (2000a) recorded a 5-fold increase in grazing rates by the microzooplankton community, with an even greater response, relative to the initial grazing rate, by the larger microzooplankton (>20 mm) such as ciliates. During SOIREE, Hall and Safi (2001) reported a 1.5-fold increase in microzooplankton stocks. However, unlike at the IronEx II site, this polar assemblage was dominated by o20 mm flagellates and the larger grazers (ciliates) made up a relatively small proportion of the community. Hall and Safi suggest that the dominance of this population by relatively small grazers may have permitted the autotrophic nanoflagellates (mainly haptophytes, Gall et al., 2001a) to escape grazer control for 6–7 days, prior to being grazed down by the larger heterotrophic ciliates, which quadrupled in abundance towards the end of the 13-day experiment. The timing of the increase in the haptophyte population and their demise closely follows the initial increase in DMSP levels (days 3–8) followed by increases in DMS levels from day 8–13, respectively. The latter lagged increases in heterotrophic ciliate abundances by 1 day (Turner et al., 2002; Hall and Safi, 2001). Due to the complex trophodynamics during SOIREE (Zeldis, 2001; Hall and Safi, 2001), it is not possible to directly compare the increase in microzooplankton stocks reported during SOIREE (Hall and Safi, 2001) with previous lab culture experiments that reported evidence of iron deficiency in heterotrophic flagellates (Chase and Price, 1997). The metazoan community, which was mainly dominated by calanoid and cyclopoid copepods, exhibited relatively small increases in biomass during IronEx II (Coale et al., 1996; Rollwagen Bollens and Landry, 2000). The latter study suggests that given the rapid generation time of mesozooplankton in tropical waters (7 days from Huntley and Lopez, 1992) a larger increase in stocks might have been expected but did not occur, indicative of significant predation on the copepod community. During SOIREE, copepods also dominated the mesozooplankton assemblage, and

were present at higher biomass than during IronEx II (Table 1), with few salps or krill observed in net hauls (Zeldis, 2001). There was no significant change in metazoan stocks (Table 1) or any evidence of arrested vertical migration during SOIREE. Thus, it appears unlikely that there was any direct influence of iron supply on either the magnitude of microbial or metazoan stocks or rate processes during either study.

8. The fate of the blooms Despite many of the observed similarities between the magnitude of biogeochemical signals, and trends in physiological and foodweb processes between the two studies, the fate of the accumulated algal stocks differed between the SOIREE and IronEx II blooms. During the former, iron enrichment resulted in the dominance of diatom species with relatively small loss terms, i.e. low rates of herbivory (Hall and Safi, 2001; Zeldis, 2001) and sedimentation (Waite and Nodder, 2001; Nodder and Waite, 2001; Trull and Armand, 2001; Charette and Buesseler, 2000). Lateral advection of phytoplankton, rather than grazing or export, was the largest loss term during SOIREE (Abraham et al., 2000) and represented up to 25% (0.07 d
1) of gross algal growth (0.3 d
1). Thus, around 66% of the fixed algal carbon (computed from the cumulative rate of primary production during the bloom) remained in the mixed layer on day 13 of the SOIREE bloom (Boyd et al., 2000). Indeed, the 13-day monitoring period during SOIREE was insufficient to determine the fate of the bloom: 30 days after departing the site SeaWIFS images of chlorophyll displayed a prominent 1100 km2 ribbon shape feature high in chlorophyll (up to 2–3 mg m
3), which was demonstrated to be the SOIREE bloom (Abraham et al., 2000). In contrast, the IronEx II bloom was transient, attaining chlorophyll concentrations of 2.4 mg m
3 within 5 days, which were subsequently subject to loss processes, such that by day 14 chlorophyll concentrations were close to those outside the fertilised waters (Cavender-Bares et al., 1999). The Nitzschia spp. that dominated the

P.W. Boyd / Deep-Sea Research II 49 (2002) 1803–1821

Fig. 7. Temporal trends in the concentration of iron-binding ligands during (A) IronEx II (Rue and Bruland, 1997) and (B) SOIREE (Croot et al., 2001). L1 and L2 for IronEx II denote strong and weakly binding ligands, respectively. The conditional stability constant of the ligands detected during SOIREE was similar to that for the L1 strong ligand class (Croot et al., 2002). The average standard error for both the concentration of the L1 and L2 class of ligands was 0.1 nM (Rue and Bruland, 1997).

bloom were reported to be heavily grazed after day 6/7 of IronEx II (see Figs. 6 and 7 in Landry et al., 2000a). Bidigare et al. (1999) estimated that the downward Particulate Organic Carbon (POC) flux to depth increased 7-fold from initial rates (5 mmol m
2 d
1) between days 7 and 13. Thus, the decline in chlorophyll concentrations (Fig. 1) and in rates of primary production (Fig. 2) were mainly due to both herbivory and sedimentation; however, it is unknown exactly what role the altered environmental conditions (such as nutrient supply) during the bloom played in determining the onset of the bloom decline. The details of the environmental conditions and physiological status of the phytoplankton

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assemblage during the decline of the bloom are unclear as the site of the main IronEx II bloom was vacated after day 7/8 for several days to occupy other fertilised sites (Coale et al., 1996). Prior to this period, there had been decreases in Fv =Fm ; Fig. 3 in Behrenfeld et al. (1996) indicates that Fv =Fm peaked (0.55) on day 4 (after the second iron addition) and subsequently declined to 0.45 by day 6.5 (i.e. prior to the third iron addition), exhibited little change after iron addition 3 and rapidly decreased from 0.45 to 0.3 around day 8. Kolber et al. (1988), based on a lab culture study, reported that marked decreases in Fv =Fm occur only whenever the algal growth rate falls to o0.5 of mmax : By day 6/7, mixed-layer silicic acid levels were 1 mM or less (indicative of nutrient limitation of diatoms, Dugdale and Wilkerson, 1998), and Kudela and Chavez (1996) report that self-shading by the bloom significantly reduced water-column light levels. Based on this evidence it would appear that resource limitation resulted in a marked decline in the physiological status of the phytoplankton assemblage. Such a decline may have triggered the onset of increased sedimentation (7-fold, Bidigare et al., 1999), as this is often driven by nutrient limitation (see Muggli et al., 1996). Landry et al. (2000a) acknowledge the potential role of resource limitation, but also point to a significant numerical response by large protisan grazers to elevated abundances of blooming Nitzschia spp., which resulted in high rates of diatom herbivory. Thus, in IronEx II there are insufficient observations to identify clearly the cause(s) of the fate of the bloom, or to assess the extent to which bottom-up and top-down control determined the timing of the bloom decline and the resulting pathways for phytoplankton carbon. There are several important distinctions between the dynamics of these two blooms that may have influenced the fate of the iron-elevated algal carbon: firstly, macronutrients such as silicic acid were higher (i.e. non-limiting) throughout SOIREE (>6 mM on day 13). Secondly, high levels of dissolved iron (mainly as FeII but organically bound resulting in low [Fe’] Croot et al., 2002) were present on day 13 of SOIREE (Boyd et al., 2000) whereas during IronEx II iron levels decreased markedly to o0.2 nM after day 8 (Coale

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et al., 1996). Thirdly, the influence of the exchange of waters between the iron-labelled patch and surrounding HNLC ocean was more pronounced during SOIREE than in IronEx II and may have acted as a ‘chemostat’ during SOIREE (see later). Fourthly, rates of diatom herbivory were insignificant during SOIREE but were pronounced during IronEx II. Thus, the SOIREE bloomFwhich was not under significant topdown control by grazersFmay not have become nutrient- or iron-limited, and hence the physiological status of the phytoplankton may have remained healthy. Furthermore, as nutrient-replete diatoms sink relatively slowly (Muggli et al., 1996), losses due to settling may have remained low during the SOIREE bloom and played a role in its longevity.

9. Physical behaviour of iron-labelled watersFinteractions with surrounding waters In IronEx I, II and SOIREE the areal extent of the iron-enriched SF6-labelled waters increased during each experiment. In IronEx I, prior to the subduction of the patch the 8  8 km2 patch had increased to a 8  12 km2 rectangle in 4 days (Coale et al., 1998; Stanton et al., 1998), while in IronEx II Coale et al. (1996) reported a lesser increase in the areal extent of the patch from 72 to 120 km2 by day 17, and a deepening of the mixed layer due to a series of small mixing events from 25 to 50 m by day 11. This exchange between the patch and the surrounding waters was most pronounced for SOIREE, where the areal extent of the labelled waters increased 4-fold to 200 km2 during the 13-day experiment. In each case increases in the areal and/or vertical extent of the labelled waters resulted in interactions with the surrounding HNLC waters, resulting in increased nutrient supply due to vertical (Coale et al., 1996) or lateral (Abraham et al., 2000) mixing. Moreover, this exchange between high-iron and HNLC waters also caused cells and iron to be lost from the patch, such that in SOIREE lateral exchange was the highest algal loss term (Abraham et al., 2000). Indeed, it has been suggested that the spreading of the iron-fertilised waters of the

SOIREE bloom over 50 days (from 50 to 1100 km2) may have acted as a ‘chemostat’, entraining the surrounding HNLC waters (characterised by higher silicic acid concentrations) and diluting the relatively high abundances of diatoms in the patch via horizontal dispersion of fertilised waters (Boyd et al., 2000; Boyd and Law, 2001; Boyd et al., 2002). Thus, there may be artefacts associated with such mesoscale perturbation experiments due to the effects of ocean physics that must be taken into consideration when comparing experimental results between studies (see below).

10. Are there common trends to both these iron enrichments? A comparison of IronEx II and SOIREE has yielded a remarkable convergence with respect to the trends in bulk biological signals, floristic shifts, changes in algal physiological properties, and indirect effects on the microbial food web between experiments conducted in polar and equatorial waters. However, there are several significant departures between bloom trends that may point to important regional differences in the control of algal blooms and the biogeochemical cycling of iron. While this high degree of convergence will be welcomed by modelers investigating the role of the biota in mediating the biogeochemistry of iron, these departures are perhaps the more significant finding in that they indicate important directions for future research. These include the source of, and conditions for, the production of iron-binding ligands, whether these ligands bind FeIII and/or FeII, and the joint impact of photochemistry and ligand production in maintaining iron in polar waters. Furthermore, we need to ascertain the factors determining the magnitude of the delay between bloom evolution and decline in HNLC waters.

11. Iron-binding ligands The temporal trends in ligand concentrations over time in both experiments were different (see

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Fig. 7). The source of these ligands is important, as are the conditions/mechanisms that induce their production (Reid and Butler, 1991; Reid et al., 1993). Croot et al. (2001) point out that relative to tropical waters (IronEx II, >23C) polar water temperatures will increase the half-life of FeII (the main iron species on day 13, produced photochemically) considerably. Furthermore, as both a photochemical mechanism and a coupled complexation mechanism are required to sustain the observed high FeII levels over several day/night cycles (Boyd et al., 2000) the source and timing of the production of iron-binding ligands is also important. Rue and Bruland (1997) speculate that the early increase in the activity of Synechococcus during IronEx II (Behrenfeld et al., 1996; Cavender-Bares et al., 1999) may have been responsible for the production of such ligands. During SOIREE, prokaryotic pico-phytoplankton were not present, which may explain the lack of any early increase in ligands. However, the pico-eukaryotes were the first algal group to exhibit a response to iron enrichment (Gall et al., 2001a), but although picoprokaryotes are reported to produce ligands (Wilhelm and Trick, 1994), nothing is known about whether pico-eukaryotes produce ligands. In contrast to IronEx II, the pronounced increase in ligand concentrations around day 11 of SOIREE may have resulted from heterotrophic bacteria. It is suggested that from what little is known about the production of ligands by microbes (Geider, 1999), that in the absence of autotrophic pico-prokaryotes, heterotrophic bacteria are the other main group known to produce them. Hall and Safi (2001) indicate that the initial increase in bacterial production was several days after iron infusions 1–3, and 3 days after an initial increase in pico-eukaryotic stocks (of similar size to heterotrophic bacteria) in ironfertilised waters. This would point to some other factor limiting bacterial rate processes in these waters. I speculate that upon the alleviation of DOC/DON substrate limitation (after day 7/8) heterotrophic bacteria may have become ironlimited and responded by producing siderophores. This speculation requires further rigorous testing by experiment.

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12. The delay between bloom decline and decay In both SOIREE and IronEx II, mean phytoplankton stocks were at comparable levels (1.8–2.4 mg Chl m
3) yet based on remote-sensing (Abraham et al., 2000) the SOIREE bloom persisted for at least 50 days (February 12–April 6 1999), whereas during IronEx II the bloom was no longer evident in surface waters after 17 days. Due to the temperature dependence of algal growth and zooplankton generation times, a bloom of longer duration was anticipated in polar waters; however, it is puzzling that the onset of elevated rates of sedimentationFseen after 7 days in IronEx IIFwas not observed/inferred (see later) during the 50 days of the SOIREE bloom. Our present understanding of the fate of algal blooms has been informed by detailed observations during the development of coastal blooms (Riebesell, 1991) and specific laboratory mesocosm experiments (e.g. SIGMA, see Alldredge and Jackson, 1995). The current paradigm is that of a rapid increase in export fluxes resulting in a subsequent massive export event, that is initiated jointly by the onset of an environmental stress such as nutrient-deplete conditions, and the accumulation of high abundances of phytoplankton. Such conditions result in increased algal sinking rates (Muggli et al., 1996), the production of transparent exopolymers (Passow and Alldredge, 1995), and increased algal cell stickiness (Kiorboe et al., 1990). These changes in tandem with the accumulation of algal stocks in phytoplankton blooms often result in them attaining levels that exceed Cr Fthe critical threshold for coagulation of phytoplankton (Jackson, 1990). Cr is determined by several factors including algal growth rate, mixed-layer depth, shear and algal stickiness (Jackson, 1990). During IronEx II there was evidence of nutrient stress by day 8 (Behrenfeld et al., 1996) either by iron and/or silicic-acid limitation. Furthermore, the observed pronounced increase in export by day 7–13 (Bidigare et al., 1999) is consistent with the trends observed during the decline of other phytoplankton blooms, and indicates that cell abundancesFeven despite high grazing pressureFwere probably sufficient to initiate

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coagulation (Boyd et al., 2002). In contrast, during SOIREE there was no evidence of nutrient stress after 13 days (Fv =Fm was maximal at this time, Boyd and Abraham, 2001). This in conjunction with low levels of herbivory on heavily silicified diatoms (Hall and Safi, 2001; Zeldis, 2001) may have permitted the bloom to persist for a longer time, but this lack of herbivory should have resulted in cells eventually attaining Cr (see Jackson, 1990), leading to the onset of coagulation and a massive export event. Buesseler (1998) observed that there are considerable variations, between oceanic provinces, in the delay between the end of an algal bloom and the onset of a mass algal sedimentation/high biogenic particulate flux events. Furthermore, recent data from Buesseler et al. (2001), which compare the timing of bloom events in the vicinity of the Polar Front zone along 170W as part of the US-JGOFS AESOPS study, suggest that the delay between the development of blooms and subsequent marked export of biogenic particulates may be of the order of 4–8 weeks. Based on data from a bio-optical mooring array, Abbott et al. (2000) report that a diatom bloom (>1 mg chl m
3) developed in the vicinity of the Polar Front within 15 days, but phytoplankton stocks had rapidly declined to o0.5 mg chl m
3 after a further 15 days. They report that two processes may have terminated the bloom developmentFlimitation of growth by silicic acid and/or grazing pressure. The SOIREE bloom was present for >50 daysFat the upper bound reported by Buesseler et al. (2001) and considerably longer than that reported by Abbott et al. (2000); yet the SOIREE bloom showed no indication of a massive export event during this period. The evidence for this is indirect and is based on a comparison of estimates of the iron-elevated algal carbon in the bloom after 13 days (400–800 tonnes, see Boyd et al., 2000) and after 40 days (600–3000 tonnes, see Abraham et al., 2000), which are indicative of an actively growing bloom. Furthermore, the areal extent of the fertilised waters increased (50–1100 km2) over this period, resulting in the daily loss of around 25% of the carbon fixed due to lateral mixing with the surrounding HNLC waters. Clearly, it was not possible to reconcile such

increases in stocks with the occurrence of a massive carbon export event. One explanation for the longevity of the SOIREE bloom is based on reports of artefacts during the bloom due to the exchange of waters with the surrounding HNLC oceanFresulting in the bloom acting as a chemostat, i.e. receiving silicic acid from the surrounding waters and losing iron and large diatoms due to ‘washout’ via horizontal dispersion of fertilised waters (Boyd et al., 2000; Boyd and Law, 2001). Despite the loss of iron, there was estimated to be a sufficient inventory within the fertilised waters to sustain algal growth for at least 50 days (Abraham et al., 2000; Maldonado et al., 2001). The lateral loss of phytoplankton cells was speculated to have reduced phytoplankton self-shading and prevented cells attaining Cr (Boyd et al., 2000). Further analysis and modelling studies (Boyd et al., 2002) suggest that the effect of these pronounced losses (0.07 d
1) may have prevented phytoplankton aggregation and the shoaling of the euphotic zone depth (0.1% of incident irradiance) to o40 m within a 65 m mixed layer. If such physically mediated artefacts do occur, then one important consequence of such lateral mixing between ‘waters’ is that the effects will be greatest in the Southern Ocean where algal growth rates are relatively low (Boyd et al., 2002). During SOIREE the ratio of net algal growth: lateral loss rates was 2, whereas during IronEx II this ratio exceeded 6, suggesting that polar mesoscale studies are more prone to the confounding effects of physical artefacts (Boyd et al., 2002). In order to extrapolate the findings of these experiments onto larger temporal and spatial scales, they must be related to existing observational datasets and modelling simulations (Sarmiento and Wofsy, 1999). IronEx II was conducted at the end of the US-JGOFS equatorial Pacific study. The results of this experiment have helped elucidate the role of iron on the biota of the eastern equatorial Pacific, and have informed the production of a synthesis for these waters (see Landry et al., 1997). The JGOFS field programmes in the Southern Ocean have focussed on the Atlantic (Germany, Holland), Indian (France) and Pacific (USA, UK, Australia, New Zealand)

P.W. Boyd / Deep-Sea Research II 49 (2002) 1803–1821

sectors. During the planning of SOIREE we attempted to select a site that would be representative of a broad region of the Australasian-Pacific sector of the polar Southern Ocean (Boyd et al., 2000). Results from SOIREE suggest that the site was occupied was representative of a large body of polar waters. Moreover, the successful application of the SWAMCO model (Lancelot et al., 2000) to the SOIREE bloom (Hannon et al., 2001) has resulted in a subsequent sensitivity analysis regarding how the oceanographic properties of the initial site will influence the bloom dynamics. Both the magnitude and timing of the SOIREE bloom are similar to other observations of blooms in the Southern Ocean from remote sensing (Moore et al., 1999). Although the detailed datasets from SOIREE will provide a useful model of the development of a polar diatom bloom, we must now focus on the factors determining bloom longevity (such as the source and role of iron-binding ligands) and bloom decline (in particular the relationship between increasing algal stocks, self-shading and the onset of coagulation of phytoplankton cells). Such information will be required if we are to fully understand the role of iron in determining the degree of carbon sequestration in the Southern Ocean.

13. Conclusions and lessons learnt (i) There is an encouraging degree of agreement between the trends observed in both these experiments with respect to the effect of iron enrichment on phytoplankton physiology. Furthermore, data on iron uptake and growth kinetics obtained during SOIREE (Maldonado et al., 2001) exhibit a remarkable convergence with respect to those from deckboard studies in other HNLC waters, and lab culture studies using oceanic and coastal species. (ii) Most of the differences in the timing and magnitude of phytoplankton rate processes between these two studies can be accounted for by the temperature dependence of algal phytosynthesis and growth. (iii) The main differences between these studies were the timing of the production of iron-binding

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ligands, the degree of herbivory (low in SOIREE, high in IronEx II), and the fate of the bloom. In IronEx II there was a rapid increase in ligands (o24 h), which was thought to be mediated by autotrophic bacteria, whereas during SOIREE increases in ligands occurred after 9/10 days and may have been due to heterotrophic bacteria. Differences in grazing pressure were due to the dominance of the SOIREE bloom by a large highly silicified (i.e. grazer-resistant) diatom, and in part to the presence of different grazer communities at the two sites. In IronEx II the decline of the bloom was due to the onset of nutrient limitation (silicic acid and/or iron), elevated export/grazing pressure, and potentially influenced to a lesser extent by physical artefacts (exchange with surrounding HNLC waters, Boyd et al., 2002). These research areas, and in particular iron chemistry, require further study in future mesoscale experiments. (iv) Mesoscale perturbation experiments in polar waters may be more prone to the influence of physical artefacts due to the mixing of labelled and the surrounding HNLC waters. The relative magnitude of loss processes due to lateral exchanges in polar waters is higher than in tropical waters due to the low algal growth rates recorded in polar waters (Boyd et al., 2002). Such artefacts may confound the interpretation of experimental results, in particular the assessment of the fate of the iron-elevated algal stocks. Future mesoscale perturbation experiments in the Southern Ocean must be designed carefully to minimise the influence of such physical effects.

Acknowledgements I thank the organisers of the 2000 Brest Symposium for inviting to participate in this excellent meeting, and for encouraging me to contribute to this volume. I am grateful to many participants from the IronEx II study (Richard Barber (Duke University, USA), Mike Landry (University of Hawaii, USA), and Bill Cochlan (UCLA, USA)) for providing me with submitted manuscripts or unpublished datasets. I am grateful to Mike McKay (University of Ohio, USA) for the

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personal communication on the ferredoxin assay, and to George Jackson (Texas A&M University, USA) for useful discussions regarding modelling algal coagulation. I acknowledge the provision of submitted or in press manuscripts by participants in SOIREE, and I wish to thank the SOIREE science team for such an enjoyable and thoughtprovoking experiment. I thank three reviewers and the guest editors of this volume for their valuable insights and comments which helped improve this manuscript.

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