Deep-Sea Research I 73 (2013) Contents lists available at SciVerse ScienceDirect. Deep-Sea Research I

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1 Deep-Sea Research I 73 (2013) 1 16 Contents lists available at SciVerse ScienceDirect Deep-Sea Research I journal homepage: Retrospective satellite ocean color analysis of purposeful and natural ocean iron fertilization Toby K. Westberry a,n, Michael J. Behrenfeld a, Allen J. Milligan a, Scott C. Doney b a Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR , USA b Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, 266 Woods Hole Road, Woods Hole, MA 02543, USA article info Article history: Received 1 May 2012 Received in revised form 15 November 2012 Accepted 23 November 2012 Available online 3 December 2012 Keywords: Phytoplankton physiology Remote sensing Iron enrichment Fluorescence abstract Significant effort has been invested in understanding the role of iron in marine ecosystems over the past few decades. What began as shipboard amendment experiments quickly grew into a succession of in situ, mesoscale ocean iron fertilization (OIF) experiments carried out in all three high nutrient low chlorophyll (HNLC) regions of the world ocean. Dedicated process studies have also looked at regions of the ocean that are seasonally exposed to iron-replete conditions as natural OIF experiments. However, one problem common to many OIF experiments is determination of biological response beyond the duration of the experiment (typicallyo1 month). Satellite-derived products have been used to address this shortcoming with some success, but thus far, have been limited snapshots of a single parameter, chlorophyll. Here, we investigate phytoplankton responses to OIF in both purposeful and naturally iron enriched systems using estimates of chlorophyll (Chl), phytoplankton carbon biomass (C phyto ), their ratio (Chl:C phyto ) and two fluorescence indices, fluorescence per unit chlorophyll (FLH:Chl) and the chlorophyll fluorescence efficiency (f f ). These quantities allow partitioning of the biological response to OIF into that due to changes in biomass and that due to phytoplankton physiology. We find that relative increases in Chl (10 20x) following OIF far exceed increases in C phyto (o4 5x), suggesting that a significant fraction of the observed Chl increase is associated with physiological adjustment to increased growth rates, photoacclimation, and floristic shifts in the phytoplankton community. Further, a consistent pattern of decreased satellite fluorescence efficiency (FLH:Chl or f f ) following OIF is observed that is in agreement with current understanding of phytoplankton physiological responses to relief from iron stress. The current study extends our ability to retrieve phytoplankton physiology from space-based sensors, strengthens the link between satellite fluorescence and iron availability, and shows that satellite ocean color analyses provide a unique tool for monitoring OIF experiments. & 2012 Elsevier Ltd. All rights reserved. 1. Introduction High-nutrient low-chlorophyll (HNLC) conditions are found in approximately one third of the world oceans and owe their existence to limiting levels of the trace element iron. A succession of iron enrichment experiments were conducted over the last two decades to elucidate this connection, first in small volume bottle incubations (Martin and Fitzwater, 1988; Martin et al., 1990; Price et al., 1991), then in mesoscale patches (100 km) of HNLC waters (see Boyd et al., 2007 for a review). In situ oceanironfertilization(oif) experiments have been conducted in all three major HNLC regions of the ocean; the Equatorial Pacific (Coale et al., 1996; Martin et al., 1994), the Southern Ocean (Boyd et al., 2000; Coale et al., 2004; Smetacek, 2001), and the Subarctic North Pacific (Boyd et al., 2004; n Corresponding author. Tel.: þ ; fax: þ address: westbert@science.oregonstate.edu (T.K. Westberry). Tsuda et al., 2003). Each experiment provided new insights to controls on biomass, productivity, and export, and recent syntheses have examined similarities and differences across experiments (Boyd et al., 2007; de Baar et al., 2005). In parallel with the execution of mesoscale OIF, it was recognized that oceanic areas of seasonal or periodic Fe enrichment serve as natural analogs to purposeful OIF (Blain et al., 2001). Regions that meet this description are small island ecosystems embedded in HNLC waters, such as the Kerguelen and Crozet Archipelagos in the Southern Ocean and the Galapagos Islands in the eastern Equatorial Pacific. The seasonal evolution of hydrography and insolation in these locations allows for temporary relief from Fe stress through convective winter mixing, upwelling and re-suspension of particulates associated with the bathymetric features surrounding the islands, and runoff from the islands themselves (Blain et al., 2008). The Kerguelen and Crozet systems have been the sites of dedicated process studies (KEOPS and CROZEX, respectively) designed to characterize the seasonal /$ - see front matter & 2012 Elsevier Ltd. All rights reserved.

2 2 T.K. Westberry et al. / Deep-Sea Research I 73 (2013) 1 16 Fe-induced blooms (Blain et al., 2007; Pollard et al., 2007a). Findings from these studies are similar to purposeful OIF, but the spatial and temporal scales are much broader. Near the Galapagos, the second leg of IronEx I (dubbed PlumEx ) contrasted the regions upstream and downstream (relative to the prevailing westerly flow) of the Galapagos and found a significant island mass effect, which in fact was noted in early Coastal Zone Color Scanner imagery (e.g., Fiedler, 1994). Marked differences in Chl, primary production rate, quantum yield of photochemistry (Lindley and Barber, 1998), and nutrient and carbon drawdown (Sakamoto et al., 1998) were all documented and attributed to Fe inputs from the Galapagos system. Broadly speaking, phytoplankton responses to OIF can be viewed in terms of physiological or biomass-related changes. Both aspects have been described (Boyd, 2002), and understanding controls on each is requisite for interpreting ecosystem behavior following OIF. For example, one well-documented physiological response to relief from Fe stress is increased intracellular pigmentation associated with changes in growth rate (Geider et al., 1993; Greene et al., 1992; Sunda and Huntsman, 1997). In other words, the chlorophyll per unit phytoplankton carbon (Chl:C phyto ) increases as growth rate increases. This phenomenon is the result of upregulation of photosynthetic machinery and light harvesting capacity (Laws and Bannister, 1980) and occurs in approximate proportion to growth rate. In addition, photoacclimation to changes in the underwater light field as a bloom develops can also be important. In many parts of the ocean, photoacclimation can account for the entire range of seasonal variability in bulk Chl (Westberry et al., 2008; Winn et al., 1995) and a significant amount of observed global, interannual variability in bulk Chl (Behrenfeld et al., 2008; Siegel et al., in press). An obvious question to ask, then, is to what extent are physiological effects on Chl:C phyto reflected in the satellite Chl record following OIF? For example, Marchetti et al. (2006b) noted significant uncoupling of Chl and C phyto following Fe addition during SERIES in the subarctic Northeast Pacific and documented a lag of a few days between initial increases in Chl and C phyto. Another aspect of phytoplankton physiology that has been universally used to monitor responses to OIF is cellular chlorophyll fluorescence. Typical applications employ active stimulated variable fluorescence (Fv/Fm) where a seawater sample is interrogated with short, frequent pulses of sub-saturating light that probe different aspects of the linear electron transport chain (Kolber et al., 1998; Suggett et al., 2009). In past work, chronically depressed Fv/Fm ( ) has been interpreted as a signature of iron stress, while higher Fv/Fm (0.5) is consistently observed upon release from Fe stress (Behrenfeld et al., 1996; Kolber et al., 1994). Although generally true, recent work has underscored the richness and complexity contained in these simple measurements beyond this simple high/low pattern (Behrenfeld et al., 2006); Behrenfeld and Milligan, in press). These studies have also helped unravel the physiological mechanisms underlying cellular fluorescence properties when phytoplankton are exposed to Fe and provide a basis for linking changes in Fe nutrition to remote sensing measurements of passive solar stimulated chlorophyll fluorescence. One problem common to many OIF experiments is determination of responses beyond the duration of the experiment (typicallyo1 month). Satellite-derived products have been used to address this shortcoming with some success (e.g., Abraham et al., 2000), but thus far have been limited snapshots of a single parameter, chlorophyll. However, advances in interpreting satellite ocean color data have paralleled the progression of OIF experiments over the past years. For example, we are no longer limited to simple estimates of chlorophyll concentration, but rather, can reliably retrieve particle scattering indices (Lee et al., 2002; Maritorena et al., 2002), particulate and dissolved organic absorption, various size and taxonomic indices (Alvain et al., 2008; Bracher et al., 2009; Brewin et al., 2011; Ciotti et al., 2002; Hirata et al., 2008; Kostadinov et al., 2009; Mouw and Yoder, 2010), and chlorophyll fluorescence (Behrenfeld et al., 2009). In turn, many of these new properties can be further related to higher order ecosystem properties (e.g., net community production, calcification rate, trace gas (DMS, CO) production, etc.). The available suite of modern satellite-derived quantities reflects diverse characteristics of phytoplankton abundance, diversity, and physiological status and should provide a more complete picture of phytoplankton (or community) response to OIF. In this work we focus on a subset of newly available ocean color-derived products that provide information on phytoplankton physiology and that show consistent responses to OIF. In particular, we utilize estimates of phytoplankton carbon biomass (C phyto ), its ratio with Chl (Chl:C phyto ), and two fluorescence indices; FLH:Chl and the chlorophyll fluorescence efficiency (f f ). Variability in these properties is examined for both purposeful (e.g., SERIES, SOFeX, SOIREE) and natural OIF (in the Kerguelen, Crozet, and Galapagos systems) with results demonstrating a prominent role of phytoplankton physiological processes on bulk properties such as Chl. 2. Methods 2.1. Data products Satellite ocean color data were obtained from the NASA Ocean Color website ( Standard products from the Sea-viewing Wide Field-of-view Sensor (SeaWiFS) and MODerate resolution Imaging Spectrometer (MODIS) on Aqua and on Terra were used to achieve maximal coverage of purposeful OIF experiments, while only MODIS Aqua was used for natural OIF regions. There are known issues with ocean color data quality from MODIS Terra (Franz et al., 2008), and it was used qualitatively in this work when coverage from other sensors was limited. Primary products from all three sensors included spectral remote sensing reflectance, Rrs(l), and chlorophyll a concentration (Chl, mg m 3 ). The Garver Siegel Maritorena model (GSM, Maritorena et al., 2002) and the quasi-analytical algorithm (QAA, Lee et al., 2002) were applied to Rrs(l) in order to estimate the particulate backscattering coefficient at 443 nm, b bp (443). Phytoplankton carbon concentrations (C phyto, mgm 3 ) were estimated from b bp (443) following Westberry et al. (2008). The mass ratio Chl:C phyto has units of mg Chl (mg C) 1, but this unit notation is omitted for the remainder of the manuscript. Both MODIS sensors provide additional products that allow quantification of solar stimulated chlorophyll fluorescence. MODIS fluorescence line height (FLH, mw cm 2 mm 1 sr 1 ) products can be used together with the incident daily [integrated] broadband irradiance (PAR, Ein m 2 d 1 ) and the instantaneous broadband irradiance at the time of satellite overpass (ipar, m Ein m 2 s 1 ) to calculate the fluorescence quantum yield, j f (Behrenfeld et al., 2009). We also evaluated variability in the related property of fluorescence per unit chlorophyll (FLH:Chl), which has units of mw m 3 cm 2 mm 1 sr 1 mgchl 1 (units hereafter omitted). Median mixed layer growth irradiances, I G (Ein m 2 h 1 ), were calculated as described in Westberry et al. (2008) and require an estimate of surface irradiance (PAR) and mixed layer depth (MLD). Here, PAR was also obtained from the NASA Ocean Color website at the same spatial and temporal resolution as the other MODIS products described above. The simple ocean data assimilation reanalysis dataset was used as a source for monthly climatological MLD (Carton and Giese, 2008). Weekly (8-day), level 3 (L3) data were mapped to 9km(1/121) spatial resolution and used to investigate natural OIF systems. However, L3 data were generally too coarse for examining the

3 T.K. Westberry et al. / Deep-Sea Research I 73 (2013) mesoscale OIF experiments. For these instances, we therefore employ level 2 (L2) data mapped to 1 km and made into daily composites when multiple valid scenes were available. Default masking was applied to all data and, other than the difference in spatial and temporal binning/resolution, the L2 products are identical to those described for L OIF locations Three areas encompassing known natural OIF environments were evaluated for this analysis; the Kerguelen and Crozet island systems in the Southern Ocean and the Galapagos Islands in the eastern Equatorial Pacific Ocean (Table 1, Fig. 1). Within each study region, small (1 21) boxes were selected to be representative of bloom and non-bloom waters (small boxes in Fig. 1b d). The Kerguelen system consists of a 2200 km long plateau extending northwest from Heard Island in the south to the Kerguelen islands in the north and has been fairly well characterized in situ (Blain et al., 2007 and references therein). Water depths on the plateau do not exceed 1000 m, and broad areas of much shallower water are found in particular around the Kerguelen islands on the northern end. The Crozet archipelago was the site of a major process study in and an overview of the findings are reported by Pollard et al. (2007a). The bathymetry around the Crozet Plateau contrasts with the Kerguelen Plateau in that the shallow portion (o1000 m) is rather small, while the larger plateau is generally m deep and Table 1 Locations, study domains, and time periods of interest for natural and purposeful in situ OIF. Analyses of in situ OIF were conducted for days surrounding field experiment duration. Fractional clear sky statistics are calculated using MODIS L3 8-Day composites for fixed box surrounding each OIF site. Average and standard deviations given represent the fraction (%) of a year that these domains are cloud free over 50% and 25% of their area. Standard deviations reflect interannual variability in cloudiness for individual years ( ). S¼SeaWiFS, Ma¼MODIS Aqua, Mt¼MODIS Terra. OIF Nominal location Latitude limits Longitude limits Number of pixels at 9 km mapped (approximately) Experiment duration Sensors Fraction clear sky over 50% Fraction clear sky over 25% Natural Kerguelen S, E S E 9,216 Ma Crozet S, E S E 9,216 Ma Galapagos 0.671S, W 51N 51S W 14,400 Ma Artificial SOIREE 611S, 1401E 9 22 Feb, 1999 S EisenEx 481S, 211E 6 29 Nov 2000 S SEEDS I 48.51N, 1651E 18 Jul 1 Aug S, Mt SOFEX S S, W 24 Jan mid-feb S, Mt SOFEX N S, 1721W 10 Jan mid-feb S, Mt SERIES 501N, 1451W (50 km NE) 10 Jul 5 Aug 2002 S, Ma, Mt EIFEX 501S, 21E 21 Jan 04 Mar 2004 S, Ma, Mt μm Galapagos Crozet Kerguelen IN IN OUT OUT OUT IN Fig. 1. Map of study sites used in this analysis. Colored background is World Ocean Atlas (WOA) 2009 climatological annual surface NO 3 concentration (mm) given at Large white dots are locations of purposeful ocean iron fertilization (OIF) experiments. Black rectangular boxes indicate regions of natural OIF examined, which are enlarged in the callouts (NOTE: scale changes in colored backgrounds). In each case, small black boxes outline areas used to designate IN and OUT of bloom and thin black lines are 200 and 1000 m isobaths. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

4 4 T.K. Westberry et al. / Deep-Sea Research I 73 (2013) 1 16 contains the Crozet Basin and neighboring Del Caño Rise.Abranchof the Antarctic Circumpolar Current vigorously scours this plateau and transports material and dissolved substances to deeper water to the north (Pollard et al., 2007b). Because of this transport, the resulting bloom is not constrained by bathymetry, but occurs primarily in deep water. The Galapagos Islands are located just south of the equator and are surrounded by HNLC conditions, although ambient macronutrient concentrations are much lower than those found in the Southern Ocean (Fig. 1).ThetropicallatitudeoftheGalapagosIslandsmitigates large seasonal variations in many environmental quantities (e.g., SST, incident light). Seven mesoscale OIF experiments occurred during the satellite ocean color era (since Sept. 1997), which in chronological order were SOIREE (Boyd et al., 2000), EisenEx (Smetacek, 2001), SEEDS (Tsuda et al., 2003), SOFeX (Coale et al., 2004), SERIES (Boyd et al., 2004), EiFeX (Hoffmann et al., 2006), and SEEDS II. The SOFeX experiment consisted of two separate enrichment sites, which are referred to as the northern and southern site throughout the manuscript. A few additional field experiments were conducted during the satellite ocean color era that are not explored in this work due to their targeted emphasis on specific ecosystem processes (e.g., iron budgeting in FeCycle, gas exchange during SAGE, and nitrogen fixation during FeeP). Table 1 summarizes the locations, start/stop times, durations, and various satellite coverage statistics for each OIF. In the planning of these experiments, care was taken to choose study sites that were relatively stable in relation to the dynamic physical environment (e.g., Boyd et al., 2000). Thus in all cases, the fertilized patch did not advect beyond the 41 square boxes (250 km 400 km) chosen for the analyses presented here (cf., Coale et al., 2004). 3. Results 3.1. Natural OIF Kerguelen The seasonal evolution of satellite-derived chlorophyll around the Kerguelen plateau has been discussed previously (Mongin et al., 2008). Widespread areas of elevated Chl (41mgm 3 )coverthe plateau and extend to the east from October through January (Fig. 2). Over shallow portions of the plateau, regions of elevated Chl may persist through March. The climatological pattern in the C phyto product shows a very strong signal immediately surrounding the islands at the beginning of the growing season (Aug Oct). However, given the low light levels this early in the austral spring (incident PAR during Aug¼ Ein m 2 d 1 )andthestrong wind-driven mixing in this region, this signal likely reflects resuspended sediment or runoff-derived material and not phytoplankton biomass. As the Kerguelen bloom (C phyto ) begins in November, there is a concurrent increase in the surrounding waters off the shelf, although the magnitude is lower (peak C phyto values during January on and off the plateau are 50 and 30 mg m 3, respectively). The ratio of Chl:C phyto is significantly higher above the plateau than in the surrounding waters (Fig. 2), suggesting that much of the observed Chl is associated with physiology. Annual cycles of Chl, C phyto, and Chl:C phyto averaged within a area above the Kerguelen plateau are shown in Fig. 3a c. For comparison, these same quantities averaged within another box away from the plateau in prevailing HNLC waters are also presented. Both regions show an increase in Chl and C phyto as austral spring arrives, but the Chl increase on the plateau is much Aug-Oct Nov-Jan Feb-Apr May-Jul Chl:C phyto C phyto (mg m -3 ) Fig. 2. Climatological seasonal cycles of Chl, C phyto, Chl:C phyto around Kerguelen islands based on weekly (8-day) MODIS data from 2003 to From left to right, panels are 3 month averages starting in the austral spring (far left) through the austral winter (far right). From top to bottom, panels are Chl (mg m 3 ), C phyto (mg m 3 ), and the ratio Chl:C phyto. Scale bars are given for each quantity and 200 and 1000 m isobaths are shown in each panel.

5 T.K. Westberry et al. / Deep-Sea Research I 73 (2013) IN OUT I g FLH: Chl Chl: C phyto C phyto (mg m -3 ) MLD (m) Fig. 3. Annual cycles in 8-day ocean-color derived biomass and physiological quantities around the Kerguelen plateau (average between 2003 and 2010). In each panel, mean 71s variability on the plateau (IN) are shown as black, solid line and gray envelope, while mean 71s variability off the plateau (OUT) are shown by blue, solid line and error bars. (A) Chl (mg m 3 ), (B) C phyto (mg m 3 ), (C) Chl:C phyto, (D) FLH:Chl, and (E) mixed layer growth irradiance, I g (m Ein m 2 h 1 ) on plateau (black line, left axis) and mixed layer depth, MLD (m) on plateau (red dashed line, right axis). Note that log-scale is used for the y-axis of Chl and FLH:Chl panels. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.) greater than off the plateau (410x and o2x, respectively, Fig. 3a). Chl peaks at 2 mgm 3 in December and persists until February. In contrast to the large differences in the annual trajectories of Chl on and off the plateau, patterns in C phyto are relatively similar to one another. Both regions show an initial 3 month period of stable and low biomass (o10 mg m 3 ) after emerging from winter darkness. Beginning in October, C phyto on the plateau steadily increases to peak values near 50 mg m 3 in January, then slowly declines throughout the remainder of the year (Fig. 3b). In the surrounding HNLC waters, the rate of biomass increase is slower (possibly the result of slower growth rates), and the peak occurs in mid-february. The associated annual cycle of Chl:C phyto reflect the divergent trajectory of Chl and C phyto, as seen previously in the climatological maps. On the Kerguelen plateau, Chl:C phyto is elevated 2 5x above that seen in the surrounding waters throughout the year (Fig. 3c). The annual cycles of fluorescence normalized to Chl on and off the plateau begin the growing season statistically indistinguishable from one another (p¼0.02, two tailed t-test July midnovember), but slowly diverge throughout the year (p¼0.009, November June). FLH:Chl is 2x lower on the plateau than off the plateau during this latter portion of the year (November June, Fig. 3d) Crozet The largest extent of elevated Chl (Z0.4 mg m 3 ) around the Crozet Plateau is seen shortly after the growing season begins in October (Fig. 4). The region of high Chl is primarily off the shelf beyond the 1000 m isobaths and overlays large-scale latitudinal gradients in physics and biology that are related to the prevailing currents such as the Antarctic Circumpolar Current (Pollard et al., 2007a, 2007b). As the year progresses, the region of highest Chl recedes and by February April, it is directly above the plateau. The maximum concentration (50 g m 3 ) and extent of C phyto are observed at the peak of austral summer (November January) and are much later than Chl (Fig. 4). In the surrounding HNLC waters the relative increase of C phyto (4x, from 8 to 30 mg m 3 ) is also much larger than in Chl. The corresponding Chl:C phyto patterns exhibit maxima early in the year (August October) and decrease afterward both in the bloom and surrounding waters. A compact region of very high Chl:C phyto exists toward the end of the growing season (February April) and is tightly constrained to the plateau. This feature likely reflects Fe-enriched growth via turbulent resupply from below the mixed layer or resuspension of Fe-rich sediments in this shallow region. Fig. 5 shows the annual trajectories of Chl, C phyto, and Chl:C phyto averaged over a box in and out of the bloom, as indicated in Fig. 1b. On the plateau, a large increase in Chl (410x) from0.1 to 2mgm 3 is seen after the austral winter (July), peaking in late November. A second increase is observed around March April, but the magnitude and extent of this feature are much less than earlier in the year. In fact, the seasonal climatological maps of Chl (Fig. 4)shows that this secondary bloom is strongly confined by bathymetry and does not extend past 200 m water depth (see note above). Off the plateau, a modest, unimodal bloom is observed that peaks in November and persists until January, with Chl increasing by only 2x. In contrast, maxima found in the annual trajectory of C phyto on and off the plateau differ by only a factor o2x. In the surrounding HNLC waters, C phyto exhibits a single broad peak between the months of November and March, while on the plateau the pattern is more complex (Fig. 5b). C phyto values increase from o10 mg m 3 to mg m 3 and mg m 3 on and off the plateau, respectively. The Chl:C phyto ratio shows the two peaks seen in the Chl record, which is also accentuated by the steep decline in Chl during

6 6 T.K. Westberry et al. / Deep-Sea Research I 73 (2013) 1 16 Aug-Oct Nov-Jan Feb-Apr May-Jul Chl:C phyto C phyto (mg m -3 ) Fig. 4. Climatological seasonal cycles of Chl, C phyto, Chl:C phyto around Crozet islands based on MODIS data from 2003 to From left to right, panels are 3 month averages starting in the austral spring (far left) through the austral winter (far right). From top to bottom, panels are Chl (mg m 3 ), C phyto (mg m 3 ), and the ratio Chl:C phyto. Scale bars are given for each quantity and 200 m and 1000 m isobaths are shown in each panel. IN OUT I g FLH: Chl Chl: C phyto C phyto (mg m -3 ) MLD (m) Fig. 5. Annual cycles in 8-day ocean color derived biomass and physiological quantities around the Crozet plateau (average between 2003 and 2010). In each panel, mean 71s variability on the plateau (IN) are shown as black, solid line and gray envelope, while mean 71s variability off the plateau (OUT) are shown by blue, solid line and errorbars. (A) Chl (mg m 3 ), (B) C phyto (mg m 3 ), (C) Chl:C phyto, (D) FLH:Chl, and (E) mixed layer growth irradiance, I g (m Ein m 2 h 1 ) on plateau (black line, left axis) and mixed layer depth, MLD (m) on plateau (red dashed line, right axis). Note that log-scale is used for the y-axis of Chl and FLH:Chl panels. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

7 T.K. Westberry et al. / Deep-Sea Research I 73 (2013) Aug-Oct Nov-Jan Feb-Apr May-Jul Chl: C phyto C phyto (mg m -3 ) Fig. 6. Climatological seasonal cycles of Chl, C phyto, Chl:C phyto around the Galapagos islands based on MODIS data from 2003 to From left to right, panels are 3 month averages starting in the austral spring (far left) through the austral winter (far right). From top to bottom, panels are Chl (mg m 3 ), C phyto (mg m 3 ), and the ratio Chl:C phyto. Scale bars are given for each quantity and 200 and 1000 m isobaths are shown in each panel. December January. The areal extent of this decrease is impressive, and regions with Chl41mgm 3 drop from 458,000 km 2 to 240 km 2 between October and December (Fig. 4). As in the Kerguelen example, FLH:Chl is less distinguishable than Chl itself in and out of the bloom, but is nevertheless statistically different for much of the year (p¼0.017, t-test November to May). From November onward to the austral winter (June), FLH:Chl is 42x higher outside the bloom than within the bloom (Fig. 5d) Galapagos Seasonal climatologies of Chl, C phyto and Chl:C phyto around the Galapagos do not exhibit the marked seasonality seen in the Kerguelen and Crozet systems (Fig. 6). Rather, the region is characterized by strong meridional gradients in all three properties associated with the unique east-west currents in the Equatorial Pacific. Also, a significant amount of variability occurs at submonthly timescales (not shown) that is dampened in the seasonal climatological view. Nevertheless, a region of elevated Chl (40.3 mg m 3 ) is observed along the Galapagos belt that extends much further to the west than the region of elevated C phyto. Furthermore, the extent of C phyto enhancement is relatively low (o20 mg m 3 ), except in the immediate wake of the islands. Chl:C phyto is clearly elevated in this same region, but there are also broad areas upstream of the Galapagos that display relatively higher Chl:C phyto. Fig. 7a shows that chlorophyll is persistently elevated throughout the year (p510 3 ) in the wake of the Galapagos compared to the HNLC waters east of the islands. Average Chl in the wake ranges from 0.6 to 1 mg m 3, but a large degree of variability exists which encompasses the mean HNLC value (see gray shaded area in Fig. 7a). Chl values 42mgm 3 are observed in nearly all months. Outside the influence of the islands, Chl is always o0.5 mg m 3 and the spatial variability is also much smaller (blue error bars in Fig. 7a). Phytoplankton biomass in the bloom region west of the Galapagos shows a similar pattern as Chl, with mean values of mg m 3 and a significant amount of variance around these values (full range from 5 to 60 mg m 3 ). In contrast, the surrounding HNLC region exhibits C phyto from 10 to 20 mg m 3, with a much smaller range of variation. Patterns in Chl:C phyto for these two regions show no significant variability at any point during the year, but Chl:C phyto is always 50% higher in the downstream location compared to east of the islands (p{10 3 ). Average FLH:Chl in the bloom region is also very stable throughout the year ( ). In the prevailing HNLC waters to the east, FLH:Chl is also uniform for much of the year, but does undergo some significant deviations both greater than and less than that found in the bloom waters Mesoscale OIFs The primary limitation for satellite-based analyses of OIF is lack of coverage due to clouds. Most of the purposeful OIF experiments are of relatively short duration (15 30 days) and take place at high latitudes, which can experience persistent cloudiness. Table 1 shows the percent of the year that cloud free conditions exist over 25% or 50% of the area of a fixed box surrounding each purposeful OIF site. When averaged over the seven OIF sites, only 28% and 12% of each year is cloud free at the 25% and 50% level,

8 8 T.K. Westberry et al. / Deep-Sea Research I 73 (2013) 1 16 IN OUT FLH: Chl Chl: C phyto Cphyto (mg m -3 ) Fig. 7. Annual cycles in 8-day ocean color derived biomass and physiological quantities around the Galapagos (average between 2003 and 2010). In each panel, mean 71s variability on the plateau (IN) are shown as black, solid line and gray envelope, while mean 71s variability off the plateau (OUT) are shown by blue, solid line and errorbars. (A) Chl (mg m 3 ), (B) C phyto (mg m 3 ), (C) Chl:C phyto, and (D) FLH:Chl. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.). C phyto (mg m -3 ) Chl: C phyto Fig. 8. SeaWiFS L2 composite for year days (46 days after initial fertilization) during SOIREE (Feb 1999). (A) Horseshoe shaped feature in Chl has been documented previously (e.g., Abraham et al., 2000). (B) Bloom not as clearly defined in terms of C phyto and many other high biomass features are seen. (C) However, only the Fe-enriched bloom exhibits elevated Chl:C phyto over nearly the entire feature. Spatial resolution is 1km 0.5 km and bloom outline (visually determined) is indicated by thin black line. Filled black diamond indicates initial fertilization site. respectively. Therefore, in the best case scenario, these sites generally have satellite ocean color coverage less than 30% of the time, which equates to partially clear days per year. As a result, some OIF experiments yielded no usable coverage (e.g., SEEDS I, SEEDS II, EisenEx) and are thus, not investigated further in this work SOIREE The few images available during SOIREE have been previously used as a basis to demonstrate the longevity of this iron induced bloom and also to characterize the effects of horizontal mixing or stirring on patch evolution (Abraham et al., 2000). Fig. 8 shows composites of Chl (similar to that seen in Abraham et al., 2000), C phyto, and Chl:C phyto from 21 to 23 March (Fig. 8a c, respectively). These scenes correspond to 30 days after the station had been vacated and 440 days after the initial Fe amendment. Chl in the patch is mg m 3, while typical concentrations in the surrounding waters are mg m 3 (Table 2). These values are significantly lower than peak values (2.0 mg m 3 ) measured in situ 10 days after Fe addition (Boyd et al., 2000). In contrast, C phyto is only 2x higher in the patch than outside (36711 and 1677mgm 3, respectively) (Fig. 8b). Interestingly, the satellite-

9 T.K. Westberry et al. / Deep-Sea Research I 73 (2013) Table 2 Satellite estimates of Chl, C phyto, and Chl:C phyto from purposeful OIF in (IN) patch versus out (OUT). Patch boundaries determined visually as shown in each corresponding figure (black outlines). OUT statistics calculated from quasi-randomly selected box with roughly the same number of pixels as IN patch, but well away from the patch (411). Values reported are mean 71s and value of 95th percentile is also shown in parentheses. Year day Exp. day Chl (mg m 3 ) C phyto (mg C m 3 ) Chl:C phyto N pixels Area (km 2 ) IN OUT IN OUT IN OUT IN OUT SOIREE (0.74) (47) 1677(26) (0.1) (0.02) (0.007) SERIES (2.7) (0.45) (159) 3679 (54) (0.02) (0.008) SOFEX-S (0.64) 0.177(0.2) N/A 197 (24) N/A (0.01) SOFEX-N (1.47) (0.24) 1579 (35) 1978 (38) (0.05) (0.02) SOFEX-N central (1.88) N/A (48) N/A (0.05) N/A 369 N/A 216 derived C phyto out of the patch is roughly equivalent to microscopybased estimates made prior to SOIREE both in and out of the patch, suggesting that biomass in the surrounding waters was relatively constant over the intervening period. Satellite-derived Chl:C phyto is elevated to within the patch, compared to outside the patch. Gall et al. (2001a) observed that the in situ pre-fertilization community Chl:C phyto was and reached a maximum on experiment day 13 of Abraham et al. (2000) provided estimates of the spatiallyintegrated algal carbon inventory within the fertilized patch based on similar ocean color imagery. They assumed a 65 m mixed layer and extrapolated SeaWiFS Chl and in situ Chl:C phyto (from microscopy and flow cytometry biovolume conversions) to yield t of carbon (¼ kg C). This contrasted with the surrounding waters which contained kgc in the same volume of water, suggesting that the bloom accumulated kg C ( t). Using our satellite C phyto directly, assuming the same 65 m mixed layer and extrapolating over the patch area outlined in Fig. 8b, we estimate total algal carboninthebloomtobe kg C. Substituting typical C phyto out of the patch (Table 2) and integrating over the same area and mixing depth, we estimate that there would have been kg C present without fertilization, again suggesting that the bloom accumulated kg C or 880 t. Thus, this satellite-based analysis yields values consistent with the low end of the distribution reported by Abraham et al. (2000), but our integration area is also 20% smaller than in that study Series Day 19 of the SERIES experiment (year day 210, 29 July 2002) provided the first clear images from both the SeaWiFS and MODIS Terra sensors. A large patch approximately 1000 km 2 is seen with elevated Chl 1.5 mg m 3 and a maximum of 3mgm 3 (Fig. 9a, d). By comparison, typical background Chl for the region was 0.4 mg m 3 (Table 2). The corresponding image of C phyto also shows significantly elevated values approaching 100 mg C m 3 for the enrichment patch (Fig. 9b). Boyd et al. (2005) also estimated C phyto for SERIES by transforming SeaWiFS Chl data using an in situ measured POC:Chl value of 50 yielding values of mg m 3. However, this approach likely overestimates C phyto due to the assumption that all POC was phytoplankton. This condition is likely not valid during the bloom decline phase when this image was collected. Our estimated increase in satellite C phyto supports an 3x higher value than outside the fertilized patch. Marchetti et al. (2006b) reported an 3.5x increase in total particulate carbon in the 45 mm size fraction. Nevertheless, when compared to the 4 8x increase in Chl above background values (Table 2), it is clear that the additional Chl increase must be due to physiological changes in the phytoplankton community. Indeed, a distinct Chl:C phyto feature is evident in the imagery with Chl:C phyto values approximately a factor of two to four higher than surrounding HNLC waters (Fig. 9c). This is similar to the factor of 4 5 difference in POC:Chl reported by Marchetti et al. (2006b) over the duration of the SERIES deployment. MODIS Terra showed a similar Chl response to that from SeaWiFS, both in pattern and magnitude (Fig. 9d), which is reassuring given concerns about its ocean color data quality (Franz et al., 2008). MODIS FLH generally mimics the pattern in Chl to first order (Fig. 9e). However, when normalized to Chl, this feature is expressed as a large decrease in FLH/Chl and represents a reduction in the fluorescence yield (Fig. 9f). FLH data can be further transformed to estimate the quantum yield of fluorescence (j f ) following Behrenfeld et al. (2009). Estimates of j f still register the bloom signature, but its difference with background values is dampened from that seen with the ratio of FLH:Chl (not shown). Since the ratio FLH:Chl is used in calculating j f, this implies that some other aspect of the calculation, such as estimation of phytoplankton absorption from Chl (i.e., pigment packaging) or correction for non-photochemical quenching, is mitigating the Fe-based signal. Partial coverage of the SERIES bloom was also available on year days 215 and 234, demonstrating the continued decline of the bloom (not shown). Five days after the images shown in Fig. 9a f, the areal extent of high Chl (41mgm 3 ) and C phyto (4100 mg m 3 ) had shrunk from 4600 km 2 to o100 km 2, and the Chl:C phyto and FLH:Chl signatures were faint. Two weeks later (year day 234, equivalent to 43 days after fertilization), the signal in all properties was not distinguishable from the surrounding water (not shown) SOFeX Satellite coverage for both SOFeX campaigns (northern and southern) was limited. However, clear images are available that correspond to times when the fertilized patches were still occupied; year days (12 13 Feb 2002) in the southern patch and year day 36 (5 Feb 2002) in the northern patch. The northern patch was initiated in a physically dynamic environment that resulted in significant stretching and advection of the bloom from its starting position (Coale et al., 2004). Fig. 10 shows a single daily composite of Chl, C phyto, and Chl:C phyto from SeaWiFS and FLH:Chl from MODIS Terra. The bloom is clearly identifiable in each panel as a filamentous ribbon extending 200 km from the southwest to the northeast and occupying an area 990 km 2 (Table 2).Atthecoreofthebloom(541S, 1691W) Chl is mg m 3, with peak values 42.5 mg m 3.Outside

10 10 T.K. Westberry et al. / Deep-Sea Research I 73 (2013) 1 16 C phyto (mg m -3 ) Chl: C phyto FLH FLH: Chl Fig. 9. SeaWiFS and MODIS Terra L2 daily composite for year day 210 (¼experiment day 19) around SERIES site (July 2002). Top panels show SeaWiFS data for (A) Chl, mg m 3, (B) C phyto,mgm 3, and (C) Chl:C phyto. Bottom panels show MODIS Terra data for (D) Chl mg m 3,(E)FLH,mWcm 2 mm 1 sr 1, and (F) FLH:Chl. Station Papa is at lower left corner of each panel (501N, 1451W) and fertilization site is indicated by black diamond. Bloom outline shown on all panels was visually derived from SeaWiFS Chl image. the patch in the prevailing HNLC waters Chl is mg m 3. Similarly, phytoplankton biomass and Chl:C phyto are also elevated in the bloom (35710 mg C m 3 and , respectively, Table 2). Chl measured in the field was reported at mg m 3 during this period of the bloom, and total particulate organic carbon was measured at 9 10 mm ( mg m 3 ) (Coale et al., 2004). These values agree well with the satellite derived values and suggest that phytoplankton biomass comprised 30% of total POC. In addition, a portion of the bloom with the highest Chl and C phyto also exhibited much lower FLH:Chl than the surrounding waters (Fig. 10d). As in other examples, these observations are all evidence of an iron-mediated bloom, but there are also many additional features that occur along the Polar Front that have similar magnitudes of Chl (Moore and Doney, 2006). These other biological features are characterized by elevated Chl and C phyto, but not necessarily Chl:C phyto, nor decreased FLH:Chl (not shown). The southern SOFEX patch developed in high silicate waters, and the increase in biomass was comprised primarily of diatoms (Coale et al., 2004). Average SeaWiFS Chl in the patch was mg m 3 ( mg m 3 from MODIS Terra) (Fig. 11). By comparison, field measurements indicated much greater inpatch Chl of mg m 3 (Coale et al., 2004). Coale et al. (2004) subsequently used a carbon to chlorophyll ratio of 78 to equate total integrated Chl produced by the Fe infusions (107 t or kg Chl) to 8300 t of carbon (or kg C). Close inspection of Fig. 11 shows that the bloom signature in the C phyto field (that is, in the underlying b bp retrievals) is suspiciously absent. Given that this image is from experiment day 19 when the bloom was still being monitored at sea, we know that total particulate carbon was still 4100 mg m 3 and the bloom was still well underway (Coale et al., 2004). Further, the bloom feature shows up distinctly in all other satellite ocean color quantities (as in Fig. 11), including estimates of Chl and component absorption derived from the same inversions (not shown), which fail to show asignalinb bp and thus, C phyto.last,thec phyto response is not observed when an alternative reflectance inversion model is used

11 T.K. Westberry et al. / Deep-Sea Research I 73 (2013) C phyto (mg m -3 ) Chl: C phyto FLH: Chl Fig. 10. SeaWiFS and MODIS Terra L2 daily composite for year day 36 (¼experiment day 26) in the vicinity of the SOFEX northern site (Feb 2002). Bloom patch has been significantly stretched in northeast-southwest direction. (A) SeaWiFS Chl (mg m 3 ), (B) C phyto (mg m 3 ) from GSM model, (C) Chl:C phyto, and (D) FLH:Chl from MODIS Terra. (QAA, Lee et al., 2002) or when either SeaWiFS or MODIS Terra reflectance are used (not shown). This behavior is not seen in any of the other OIF investigated and suggests that there is some unique bio-optical aspect of this particular bloom. One possible explanation is that the predominance of diatoms (70%, see Coale et al., 2004 Supplementary material) both in and out of the patch resulted in a unique optical signal, which confounds the inversion models. If this were the case, however, it is difficult to imagine why the inversion based Chl estimates still agree well with operational band ratio Chl algorithms. 4. Discussion Since the landmark publication of Martin and Fitzwater (1988), an extensive body of research has accumulated documenting the importance and wide-spread occurrence of iron stress in marine ecosystems. Iron is an essential nutrient for phytoplankton and, when occurring at limiting levels, impacts both their standing stock and physiological status. Over the course of field iron limitation studies, satellite observations have been employed to evaluate the spatial and temporal extent of iron enrichment responses, but these studies have focused exclusively on chlorophyll variability alone. Accordingly, such analyses are incapable of distinguishing physiological and standing stock responses. Here, we have employed new satellite products that, when viewed in conjunction with chlorophyll data, allow a deeper evaluation of iron stress expressions. Two central physiological properties were investigated; variability in phytoplankton Chl:C phyto ratio and solar-stimulated chlorophyll fluorescence. We find that a consistent story emerges from these data for both purposeful OIF experiments and natural OIF systems. Specifically, iron enrichment leads to (1) significant pigment and biomass increases and (2) strong physiological responses within the phytoplankton community. While physiological impacts of iron stress have been thoroughly studied in the laboratory and field enrichment experiments have documented both physiological and biomass responses to iron perturbations, the current study represents a novel investigation of these signatures using remote sensing

12 12 T.K. Westberry et al. / Deep-Sea Research I 73 (2013) 1 16 C phyto (mg m -3 ) Chl: C phyto FLH: Chl ϕ f Fig. 11. SeaWiFS and MODIS Terra L2 daily composite for year day 43 (¼experiment day 19) in the vicinity of the SOFEX southern site (Feb 2002). Top panels show SeaWiFS (A) Chl, mg m 3, (B), C phyto,mgm 3, (C) Chl:C phyto. Bottom panels show MODIS Terra (D) Chl mg m 3, (E) FLH/Chl, and (F), j f. Black diamond indicates initial site of iron fertilization. data. The consistency observed in iron responses across enrichment sites suggests that our satellite phytoplankton indices are indeed registering prominent physiological attributes. Observed patterns in Chl, Chl:C phyto, and FLH:Chl are further interpreted in the following sections in the context of their underlying physiology Reconciling Chl:C A common observation across the OIF sites investigated here is that relative changes in Chl ( 10 20x) are greater than those of phytoplankton carbon biomass (o4 5x). After accounting for increases in standing stock of phytoplankton, the excess Chl represents changes in intracellular pigmentation and is quantified by the chlorophyll per unit carbon (Chl:C phyto ). Variations in Chl:C phyto arise from several processes, notably changes in growth rate (Laws and Bannister, 1980), photoacclimation (Falkowski and Laroche, 1991; Geider et al., 1996), species composition (Geider, 1987) and the form of nutrient limitation (e.g., iron or macronutrients). These forms of Chl variability can be uncoupled from changes in biomass. Over the course of an Fe-induced bloom, each of the above processes likely plays an important role in determining the bulk chlorophyll concentration. For example, the initial physiological response by phytoplankton to the addition of iron (assuming light is not limiting) is to increase growth rate (m), which requires proportional increases in Chl:C phyto (Sunda and Huntsman, 1997). In addition to growth rate related changes in Chl:C phyto, phytoplankton must photoacclimate as a bloom develops. Increasing biomass and pigment stocks within the water column lead to increased light attenuation. Notable decreases in euphotic zone depth were documented in the iron-induced blooms of SOFEX (Coale et al., 2004), SERIES (Marchetti et al., 2006b), SOIREE (Gall et al., 2001b) and EisenEx (Gervais et al., 2002). The ensuing result is that phytoplankton photoacclimate themselves to lower light levels by further increasing Chl:C phyto. As a bloom continues to develop, shifts in community species composition also take place as the result of competitive advantage in the uptake of nutrients, selective grazing, and other ecosystem structuring properties (e.g., physics). Therefore, an instructive exercise is to identify the extent to which biomass and each physiological process described above (growth rate, photoacclimation, and species composition) influence the bulk chlorophyll concentration following Fe enrichment.

13 T.K. Westberry et al. / Deep-Sea Research I 73 (2013) In the Kerguelen example (Fig. 3), average Chl increases are 10-fold, C phyto increases are 6-fold, and Chl:C phyto ranges from 2 to5x higher in the bloom region than the surrounding HNLC waters (individual pixel to pixel changes can be significantly higher in all properties). Specifically, between August and mid- October Chl:C phyto is constant and 2x higher in the Fe-enriched bloom waters than outside (0.026 versus 0.013, respectively). During this period, changes in biomass and bulk Chl are negligible in both locations, C phyto is nearly the same in and out of the bloom region, and bulk Chl almost exactly reflects the factor of two difference in intracellular Chl content in the two regions (0.2 and 0.1 mg m 3, respectively). From November through mid-december, both pigment and biomass increase rapidly to their maximal values. Chl:C phyto nearly doubles over this same period, likely reflecting increases in growth rate, though it is not immediately clear what triggers this increase. Mixing depths are still relatively deep during this time (100 m), although they have begun to shoal (Fig. 3e). More important than the absolute value of the MLD however, is the combined effect of MLD together with incident light and attenuation from which we can calculate the average light levels experienced by phytoplankton (e.g., Westberry et al., 2008). The mixed layer growth irradiances (I G ) during this period (November through mid-december) are still extremely small and suggests that the increase is not light-driven (Fig. 3e). We must assume therefore, that the increase is nutrient (Fe) related, but again, it is unclear why this increase was not seen earlier in the year. After December, the steady decline of Chl:C phyto that follows is initially due to decreases in growth rate as Fe sources are exhausted, but the decrease pushes values well below those seen at the beginning of the year (by another 2x). The additional decrease in Chl:C phyto can be partially accounted for by photoacclimation effects as the mixed layer continues to shoal and incident irradiances hover at their mid-summer maxima. Calculation of typical I G between the bloom peak (early December) and the Chl:C phyto minimum (o0.01) in early February would cause a factor of two decrease in Chl:C phyto due solely to changes in the underwater light field. This photoacclimation effect is further supported by the subsequent factor of two increase (o0.01 to 0.02) in Chl:C phyto between Feb and April, the combined result of erosion of the mixed layer and decreases in incident light. So, while biomass (C phyto ) decreases significantly over this time period (from 35 to 10 mg C m 3 ), corresponding decreases in bulk Chl are only 30% and are offset by increases in Chl:C phyto. A similar pattern unfolds during the Crozet bloom (Fig. 5), but with a few nuances to the annual cycle that further highlight the role of physiology in explaining the observed patterns. After the peak in concentration of Chl and C phyto (mid-november), there is a brief period of steep decrease in both stocks (Chl and C phyto ) and physiology (Chl:C phyto ) lasting for 3 weeks. This is followed by a period of uncoupling between biomass and physiology as C phyto stabilizes and even increases significantly (from 25 to 40 mg m 3 ), while Chl:C phyto continues to decrease until mid-january. The majority of this decrease can be accounted for by photoacclimation-driven responses to increased mixed layer irradiances (greater I G, Fig. 5e), and this decrease offsets any evidence of biomass-driven increases in bulk Chl. This secondary maxima in phytoplankton biomass peaks in early January and gradually declines throughout the remainder of the year. During this period of biomass decrease (mid-january April), photoacclimation again causes Chl:C phyto to increase more than 2x as mixing and incident light both act to decrease I G. The result is that bulk Chl remains steady or even slightly increases during these few months. The role of physiology in determining bulk properties (i.e., Chl) can also be identified in the purposeful mesoscale OIF. For example, the available imagery of the SOIREE bloom is long after the infusions of iron (42 days) and well beyond the duration of in situ monitoring. Fig. 8 (and Table 2) shows that while Chl in the fertilized patch is still significantly elevated above background concentrations ( mg m 3 compared with mg m 3 ), C phyto is only double that out of the patch, suggesting that much of the remaining Chl signal is largely physiological. This observation is not totally surprising as it is likely that the grazing (or other loss) rates would catch up with phytoplankton growth over this time scale. Rather, efficient recycling of Fe and turbulent resupply of silicic acid may still be allowing the algal community to have elevated growth rates, but they are likely matched by increases in total losses (e.g., grazing). This scenario would nevertheless allow the Fe-enriched community that is present to have elevated Chl:C phyto, as is indicated in our satellite data. Additionally, lower mixed layer growth irradiances, due to increased light attenuation within the bloom, would also lead to enhanced Chl:C phyto. Assuming incident light and mixing depth were the same inside the patch and just outside, typical growth irradiances should be 3 4x lower within the bloom even at this advanced stage. During the peak of the bloom (Chl 2.0 mg m 3 ), mixed layer growth irradiances were likely 30 40x lower within the patch (assuming 60 m mixed layer, and 40 Ein m 2 d 1 surface irradiance). Depending upon the exact light-dependent expression for photoacclimation used (e.g., Behrenfeld et al., 2002), these differences could elicit a factor of two change in Chl:C phyto. Similar calculations during the SERIES program suggest a six-fold decrease in mixed layer growth irradiance due to the bloom itself, and a resulting 2x increase in Chl:C phyto (assuming a 20 m mixed layer and 25 Ein m -2 d -1 surface PAR, Marchetti et al., 2006a) Fluorescence Fluorescence measurements have long been used to investigate iron effects on phytoplankton. A recurring pattern of low (high) variable fluorescence in Fe-stressed (Fe-replete) waters has been demonstrated in transects across gradients in Fe stress (e.g., the eastern Equatorial Pacific, Behrenfeld et al., 2006; Greene et al., 1994) and in the temporal response to Fe addition in bottle experiments and in situ Fe enrichment experiments (Behrenfeld et al., 1996; Boyd and Abraham, 2001). Historically, low variable fluorescence (Fv/Fm) observed in iron limited HNLC waters has been interpreted as inefficient energy transfer due to Fe limitation. Conversely, high Fv/Fm away from HNLC waters or following addition of iron has been viewed as a characteristic of healthy or Fe-replete phytoplankton. However, the underlying physiological mechanisms that cause this pattern have long been misunderstood and viewed as changes in photochemical efficiency (or functional reaction centers). Incorporation of more recent findings is required to properly understand physiology underlying Fe stress and why an iron-mediated signal is expected in the satellite fluorescence record as well. A brief description is given here, but see Behrenfeld and Milligan (in press) for a comprehensive review. Under typical macronutrient limitation (nitrate, phosphate) in steady-state grown phytoplankton, intracellular chlorophyll (Chl:C phyto ) scales linearly with growth rate (Laws and Bannister, 1980), reflecting a well-tuned balance between light harvesting capacity and metabolic demand. As such, we should not expect changes in fluorescence properties across growth rates for macronutrient limitation. For example, it has been shown that variable fluorescence (Fv/Fm) is insensitive to macronutrient limitation in steady-state laboratory cultures (Parkhill et al., 2001; Schrader et al., 2011) and that maximal Fv/Fm are observed in the macronutrient impoverished open ocean (Behrenfeld et al., 2006). However, several studies have noted an apparent decoupling of growth rate and cellular chlorophyll content in the presence of iron stress. When