Photosynthetic Response of Phytoplankton during the Southern Ocean Iron Experiment (SOFEX)

1. Layer dominated by big cells (>20 um) with low Fv/Fm = 0.28 Layer dominated by small cells (< 5 um) with high Fv/Fm Layer dominated by big cells (>20 um) with high Fv/Fm = 0.50 Effect of iron In the iron fertilized patch Fv/Fm increased up to 0.65, the maximum value typical for nutrient replete phytoplankton. This result clearly suggests that iron is the central factor limiting primary production in the Southern Ocean. Water column integrated [Chl-a], as assessed from the vertical profiles of variable fluorescence, increased 6-fold within the fertilized area. Methods and Protocols: Fast Repetition Rate (FRR) fluorometry • The FRRF technique measures a comprehensive suite of fluorescent and photosynthetic parameters (Kolber et all 1998) and provides a rapid and sensitive diagnostics of specific limiting factors such as iron. • Simultaneous measurement of fluorescence and photosynthetic parameters also permits the precision of fluorescence-derived Chl-a concentration to be significantly improved (compared to conventional fluorometers). • Instruments and sampling strategies: • bench-top FRR fluorometers (continuous underway measurements and sample analysis); • Single-Celled FRR fluorometer (cell size fractionated photosynthetic parameters in selected samples). • The Single Celled FRRF records photosynthetic characteristics in individual algal cells within the size range from ~ 1 to 300 mm (Gorbunov et al., 1999). • Parameters retrieved by FRR fluorometry • - yields of chlorophyll fluorescence at Fo and Fm levels; • - functional absorption cross section of PSII (sPSII); • - quantum yield of photochemistry in PSII (Fv/Fm); • - rate of electron transport on the acceptor side of PSII (tQa); • - rate of electron transport between PSII and PSI (tPQ); • - energy transfer between photosynthetic units; • - coefficients of photochemical and non-photochemical quenching; • - parameters of photosynthesis versus irradiance (P-I) curve. Assessment of the total amount of Chl-a produced by iron fertilization in the South Patch Vertical profiles of variable fluorescence 10 km The iron fertilization of the South Patch produced 107,000 kg of Chl-a (on Day 22) Photosynthetic Response of Phytoplankton during the Southern Ocean Iron Experiment (SOFEX) Maxim Y. Gorbunov, Sasha Tozzi, Michal Koblizek, Zbigniew Kolber, Paul G. Falkowski Environmental Biophysics and Molecular Ecology Program, Institute of Marine and Coastal Sciences Rutgers, the State University of New Jersey, 71 Dudley Road, New Brunswick, NJ 08901 ABSTRACT The Southern Ocean Iron Experiment (SOFeX) was conducted in the Pacific sector of the Southern Ocean in the austral summer of 2002 with the goal to test Martin's "iron hypothesis". Two mesoscale patches were fertilized by iron in a low and high silica regions (56°S and 66°S along the 172° W meridian, respectively). The temporal evolution (in 3D) of the iron-fertilized patches was monitored by using Fast Repetition Rate (FRR) fluorometry. Here we report the dynamics of bio-optical and photosynthetic characteristics and the abundance of phytoplankton during the SOFeX. In both patches, iron enrichment resulted in a rapid (~2-3 days) increase in the photochemical efficiency (Fv/Fm) and the rate of electron transport in Photosystem II, with a parallel decrease in chlorophyll-a fluorescence yield. All together, these are the established biophysical signatures of iron limitation. In near-surface phytoplankton Fv/Fm increased from 0.2 to 0.5 in the Northern patch, and from 0.25 to 0.65 in the Southern patch. Chl-a concentration in the euphotic zone increased over the period of three weeks from 0.15 to 2.2 mg/L and 0.3 to 4 mg/L, respectively. The 3-D mapping of phytoplankton distribution in the Southern patch showed that the iron infusion produced 107 tons of Chl-a. The single-celled FRR measurements revealed that big cells were characterized by lowered values of Fv/Fm, suggesting that big cells were more susceptible to iron deficiency than small ones. Following the iron fertilization, Fv/Fm increased in all cell size groups (from ~1 um to >100 um), indicating that iron enrichment stimulated photosynthetic activity in all groups of phytoplankton. However, the relative increase in Fv/Fm was higher in big cells (mainly diatoms), suggesting stronger stimulation of photosynthetic activity by iron. The study provide direct evidence that iron availability is the central factor limiting primary productivity in both high and low silica regions of the Southern Ocean. The Effect of Cell Specific Photosynthetic Characteristics on the Structure of Phytoplankton Community during the Iron-Stimulated Bloom (Inferences from the Single-Celled FRRF) Objectives Development of the North Patch (low silica region) Temporal Evolution of the South Patch (high silica region) • FRR fluorometry served three basic objectives: • to test the iron limitation hypothesis with biophysical data; • to provide real-time measurements of phytoplankton photosynthetic characteristics before, during and following iron enrichments; • to assess the effects of iron enrichments on specific (cell size and taxonomic) components of the phytoplankton assemblage. Biophysical Signatures of Iron Limitation North Patch, 10 days after iron fertilization In the North patch Fv/Fm was initially low (ca. 0.25) and increased rapidly up to 0.55 following iron release. This striking response clearly suggests that phytoplankton photosynthesis is primarily and severely limited by iron even in this silica deficient area of the Southern Ocean. Fv/Fm increased with depth, in parallel with an increase in sPSII and a decrease in fluorescence per unit Chl-a. This pattern suggests that the iron limitation in the upper portion of the water column switches to light limitation at depth (at deep chlorophyll max and below). Iron fertilization of the North patch stimulated the photosynthetic activity and growth of large cells, thus resulting in a striking change in the phytoplankton community structure towards large cells being dominant. The North patch, created in a highly dynamic region, became strikingly heterogeneous and was partially subducted 5 weeks after the first iron release. Three distinct water masses have been revealed at that time. These include a sub-patch fertilized only during the first week, a sub-patch fertilized both in the beginning and a month later, and a freshly fertilized region (see Figure above). The community structure and photosynthetic characteristics were all remarkably different in these distinct areas. • Large cells are more susceptible to iron limitation than small ones. • The extent of iron limitation in large diatoms is moderate at depth (DCM), but becomes severe near the surface. • Iron enrichment stimulates photosynthetic activity in all size groups of phytoplankton. However, the relative increase in Fv/Fm is strikingly higher in large diatoms, suggesting stronger stimulation of photosynthetic activity. • Such patterns would not have been observed, if “top-down” grazing pressure by herbivores would be a factor preventing phytoplankton (or their specific size groups) from fully utilizing available nutrients in HNLC regions. • The results are the first evidence that cell specific photosynthetic characteristics are an important factor controlling the structure of phytoplankton community during iron-stimulated bloom. • The discovered size specific response in photosynthetic performance provides a direct clue to the generally observed dominance of large diatoms in iron-stimulated blooms and suggests the importance of “bottom-up” control of the structure of primary producers. Surface manifestation of the South Patch Iron enrichment resulted in: 1. Increase in Fv/Fm, the quantum yield of photochemistry in PSII; 2. Decrease in fluorescence per unit chlorophyll; 3. Increase in the rate of Qa re-oxidation (i.e., the rate at which light-induced electrons can be used in photosynthetic reaction), 4. Decrease in the functional absorption cross section of PSII, sPSII. All together, these are the established biophysical signatures of iron limitation. The initial decrease in sPSII was the same (~20%) in the two patches, but the long-term (2-3 weeks) trends were strikingly different. In the Southern patch, sPSII continued to decrease throughout the experiment. In contrast, the cross section drastically increased in the North patch. The analysis revealed that the slow changes in sPSII were due to specific floristic shifts in the phytoplankton community structure. The bloom in the North Patch was characterized by accumulation of large cells with large sPSII, indicating their high photosynthetic capacity in the low light environment typical for the deep mixed layer. This pattern is similar to that recorded during EISENEX, the previous iron enrichment experiment in the Southern Ocean (Gorbunov et al. 2001; Gervais et al. 2002). References • Gervais, F., Riebesell U., and Gorbunov M.Y. (2002) Changes in primary productivity and chlorophyll a in response to iron fertilization in the Southern Polar Frontal Zone. - Limnol. Oceanogr., 47: 1324-1335. • Gorbunov M.Y., Falkowski P.G. and Kolber Z. S. (2001) Primary productivity and photosynthetic response of phytoplankton to iron enrichment in the Southern Ocean – The Reports on Polar and Marine Research, 400: 199-209. • Gorbunov M.Y., Kolber Z., and Falkowski P.G. (1999) Measuring photosynthetic parameters in individual algal cells by Fast Repetition Rate fluorometry. - Photosynthesis Research, 62(2-3): 141-153. • Kolber Z, O. Prasil, and P. G. Falkowski. (1998). Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. Biochem. Biophys. Acta 1367: 88-106. The spatial distributions of phytoplankton photosynthetic efficiency (Fv/Fm) and Chl-a have been reconstructed from underway FRRF measurements. The ship track is shown as a black line. The data are for Day 22 after iron release. These distributions perfectly match the area of enhanced drawdown in pCO2 (W. Hiscock et al.) and the SeaWIFS ocean color image of the Patch (F.Chavez et al). Acknowledgments: We thank the Captains and the crews of RVs “Melville” and “Revelle” and the SOFEX Team for their invaluable support during the cruise. This work was supported by National Science Foundation.