Southern Ocean Phytoplankton Research Articles

History and evolution of primary productivity studies of the Southern Ocean

The main objective of the article is to give an overview of the history and evolution of phytoplankton research in the Southern Ocean during the past century and a half. It traces the evolution of phytoplankton investigations as it went through several phases commencing with intensive collecting and cataloging and leading to the Discovery investigations with its extensive and detailed studies of Southern Ocean phytoplankton. Following, in the footsteps of the Discovery was the USNS Eltanin with its specialized cruises that centered around the study of the ecology of the primary producers and the dynamics of the lower trophic levels of the food chain. Spurred by the findings of the Eltanin cruises and with the growing concern over the impending exploitation of the Antarctic marine living resources, in particular krill, the BIOMASS program was initiated. The program was the first international collaborative effort to study the dynamic functioning of the Antarctic marine ecosystem. The success of the program has rekindled great international interest in the Southern Ocean which resulted in an explosion of programs such as SO-JGOFS, SO-GLOBEC, EPOS, and several others. In recent years, there has been a major shift in phytoplankton research in the Southern Ocean. This was in response to worldwide concern over the effects of global warming and stratospheric ozone depletion on species diversity, primary production and ecosystem function. This has led to process-oriented programs to study phenomena and processes of global significance in which Antarctica and its surrounding seas play key roles.

Bottom-up versus top-down control in phytoplankton of the Southern Ocean

Oceanic phytoplankton communities are a mixture of various algal functional groups, all of which are of different sizes, have variable physiologies, and interact differently with disparate herbivores. We suggest that polar plankton communities, and specifically the larger phytoplankton of Southern Ocean HNLC (high nutrient, low chlorophyll) systems, are controlled primarily by bottom-up processes, but that smaller (pico- and nanoplankton) reach an equilibrium that is set simultaneously by light, iron and grazing by microzooplankton. Thus Southern Ocean phytoplankton conforms to the “ecumenical iron hypothesis”, albeit with the further addition of light as an environmental control. Examples of bottom-up controls include iron availability, irradiance regulation (either by the incident surface irradiance as controlled by season and sea ice cover, or by the effects of vertical turbulence and mixed layer depths), and macronutrient availability (silicic acid and nitrate). While the contribution of various phytoplankton taxa varies spatially and temporally within the Antarctic, we suggest that this is largely due to the specific responses of the important functional groups to the patterns of physical forcing and micronutrient inputs, rather than to changes in controls by small and large grazers. Examples of abiotic and biotic controls are examined from representative regions of the Antarctic, including continental shelf regions and open ocean HNLC systems. Results from models further support our contention that bottom-up control of large forms is paramount in the Southern Ocean, but top-down controls play an important part in regulating the equilibrium standing stocks of smaller taxa. If bottom-up control is indeed universal in the Antarctic, then it has profound implications for the understanding of interannual variability, food web structure, and population dynamics of higher trophic levels in both the present and past Southern Ocean.

Optical studies in the Southern Ocean

During the Austral summer of 1997-1998, measurements of absorption, attenuation, downwelling and upwelling irradiance were made in the Southern Ocean along a S-N transect at 6degreesE. Measurements were made to quantify the penetration of ultraviolet B radiation (UVBR) in the water column and daily doses of UVBR at different water depths, to study the attenuation of photosynthetically active radiation (PAR), and to judge if in the investigated areas of the Southern Ocean phytoplankton are light limited. The results show that the UVBR affects a substantial portion of the upper mixed layer. The diffuse attenuation coefficients (K-PAR) for PAR were found to vary between 0.03 and 0.09 m(-1). Using the values for KPAR and the definition of the Sverdrup critical depth, the studied Southern Ocean plankton systems were found not to be light limited. (C) 2004 Elsevier Ltd. All rights reserved. (Less)

Enhanced carbohydrate production by Southern Ocean phytoplankton in response to in situ iron fertilization

Storage carbohydrates (e.g., water-extractable β-1,3- d-glucan in diatoms) are of key importance for phytoplankton growth in a variable light climate, because they facilitate continued growth of the cells in darkness by providing energy and carbon skeletons for protein synthesis. Here, we tested the hypothesis that synthesis of storage carbohydrates by phytoplankton in the Southern Ocean is reduced by low iron and light availability. During the EisenEx/CARbon dioxide Uptake by the Southern Ocean (CARUSO) in situ iron enrichment experiment in the Atlantic sector of the Southern Ocean in November 2000, we studied the dynamics of water-extractable carbohydrates in the particulate fraction over the period of 3 weeks following the iron release. The areal amount (integral between 0- and 100-m depth) of carbohydrates increased from 1400 to 2300 mg m −2 inside the iron-enriched patch, while remaining roughly constant in the surrounding waters. Most of the increase inside the patch was associated with the fraction of large (>10 μm) phytoplankton cells, consistent with the shift in the community structure towards larger diatoms. Deck incubations at 60% of the ambient irradiance revealed that the diurnal chlorophyll a (Chl a)-specific production rates of water-extractable polysaccharides were significantly higher for “in-patch” than for “out-patch” samples (0.5 vs. 0.3 μg C [μg Chl a] −1 h −1, respectively). Together with the higher photochemical efficiency of photosystem II ( F v/ F m), this indicates enhanced photosynthetic performance in response to iron fertilization. In addition, the nocturnal polysaccharide consumption rates were also enhanced by iron release, causing a striking increase in the diel dynamics of polysaccharide concentration. An iron-stimulated increase in diel dynamics was also observed in the fluorescence and size of pico- and nanophytoplankton cells (measured by flow cytometry) and is indicative of enhanced phytoplankton growth. Diurnal polysaccharide production by phytoplankton inside the patch was light-limited when they were incubated at intensities below ca. 200 μmol m −2 s −1 (daytime average). These irradiance levels correspond to those at 20- to 30-m depth in situ, whereas the upper mixed layer was frequently several-fold deeper due to storms. Therefore, these first measurements of phytoplankton carbohydrates during an in situ iron release experiment have revealed that both light and iron availability are the key factors controlling the synthesis of storage carbohydrates in phytoplankton and, hence, the development of diatom blooms in the Southern Ocean.

Increased exposure of Southern Ocean phytoplankton to ultraviolet radiation

[1] Satellite remote sensing of both surface solar ultraviolet radiation (UVR) and chlorophyll over two decades shows that biologically significant ultraviolet radiation increases began to occur over the Southern Ocean three years before the ozone “hole” was discovered. Beginning in October 1983, the most frequent occurrences of enhanced UVR over phytoplankton-rich waters occurred in the Weddell Sea and Indian Ocean sectors of the Southern Ocean, impacting 60% of the surface biomass by the late 1990s. These results suggest two reasons why more serious impacts to the base of the marine food web may not have been detected by field experiments: (1) the onset of UVR increases several years before dedicated field work began may have impacted the most sensitive organisms long before such damage could be detected, and (2) most biological field work has so far not taken place in Antarctic waters most extensively subjected to enhanced UVR.

Light rather than iron controls photosynthate production and allocation in Southern Ocean phytoplankton populations during austral autumn

The role of iron and light in controlling photosynthate production and allocation in phytoplankton populations of the Atlantic sector of the Southern Ocean was investigated in April–May 1999. The 14C incorporation into five biochemical pools (glucan, amino acids, proteins, lipids and polysaccharides) was measured during iron/light perturbation experiments. The diurnal Chl a-specific rates of carbon incorporation into these pools did not change in response to iron addition, yet were decreased at 20 μmol photons m−2 s−1, an irradiance comparable with the one at 20–45 m in situ depth. This suggests that the low phytoplankton biomass encountered (0.1–0.6 μg Chl a L−1) was mainly caused by light limitation in the deep wind mixed layer (>40 m). Regional differences in Chl a-specific carbon incorporation rates were not found in spite of differences in phytoplankton species composition: at the Antarctic Polar Front, biomass was dominated by a diatom population of Fragilariopsis kerguelensis, whereas smaller cells, including chrysophytes, were relatively more abundant in the Antarctic Circumpolar Current beyond the influence of frontal systems. Because mixing was often in excess of 100 m in the latter region, diatom cells may have been unable to fulfil their characteristically high Fe demand at low average light conditions, and thus became co-limited by both resources. Using a model that describes the 14C incorporation, the consistency was shown between the dynamics in the glucan pool in the field experiments and in laboratory experiments with an Antarctic diatom, Chaetoceros brevis. The glucan respiration rate was almost twice as high during the dark phase as during the light phase, which is consistent with the role of glucan as a reserve supplying energy and carbon skeletons for continued protein synthesis during the night.

Bicarbonate uptake by Southern Ocean phytoplankton

Marine phytoplankton have the potential to significantly buffer future increases in atmospheric carbon dioxide levels. However, in order for CO2 fertilization to have an effect on carbon sequestration to the deep ocean, the increase in dissolved CO2 must stimulate primary productivity; that is, marine phototrophs must be CO2 limited [Riebesell et al., 1993]. Estimation of the extent of bicarbonate (HCO3−) uptake in the oceans is therefore required to determine whether the anthropogenic carbon sources will enhance carbon flux to the deep ocean. Using short‐term 14CO2‐disequilibrium experiments during the Southern Ocean Iron Experiment (SOFeX), we show that HCO3− uptake by Southern Ocean phytoplankton is significant. Since the majority of dissolved inorganic carbon (DIC) in the ocean is in the form of bicarbonate, the biological pump may therefore be insensitive to anthropogenic CO2. Approximately half of the DIC uptake observed was attributable to direct HCO3− uptake, the other half being direct CO2 uptake mediated either by passive diffusion or active uptake mechanisms. The increase in growth rates and decrease in CO2 concentration associated with the iron fertilization did not trigger any noticeable changes in the mode of DIC acquisition, indicating that under most environmental conditions the carbon concentrating mechanism (CCM) is constitutive. A low‐CO2 treatment induced an increase in uptake of CO2, which we attributed to increased extracellular carbonic anhydrase activity, at the expense of direct HCO3− transport across the plasmalemma. Isotopic disequilibrium experimental results are consistent with Southern Ocean carbon stable isotope fractionation data from this and other studies. Although iron fertilization has been shown to significantly enhance phytoplankton growth and may potentially increase carbon flux to the deep ocean, an important source of the inorganic carbon taken up by phytoplankton in this study was HCO3−, whose concentration is negligibly affected by the anthropogenic rise in CO2. We conclude that biological productivity in this region of the world's ocean is unlikely to be directly regulated by natural or anthropogenic variations in atmospheric CO2 concentrations because of the presence of a constitutive CCM.

Retention of dissolved iron and FeII in an iron induced Southern Ocean phytoplankton bloom

During the 13 day Southern Ocean Iron RE‐lease Experiment (SOIREE), dissolved iron concentrations decreased rapidly following each of three iron‐enrichments, but remained high (>1 nM, up to 80% as FeII) after the fourth and final enrichment on day 8. The former trend was mainly due to dilution (spreading of iron‐fertilized waters) and particle scavenging. The latter may only be explained by a joint production‐maintenance mechanism; photoreduction is the only candidate process able to produce sufficiently high FeII, but as such levels persisted overnight (8 hr dark period) —ten times the half—life for this species—a maintenance mechanism (complexation of FeII) is required, and is supported by evidence of increased ligand concentrations on day 12. The source of these ligands and their affinity for FeII is not known. This retention of iron probably permitted the longevity of this bloom raising fundamental questions about iron cycling in HNLC (High Nitrate Low Chlorophyll) Polar waters.

A numerical analysis of carbon dynamics of the Southern Ocean phytoplankton community: the roles of light and grazing in effecting both sequestration of atmospheric CO 2 and food availability to larval krill

Reduced ice extent within coastal regions of the Southern Ocean may lead to deeper surface mixed layers (SML), as prevail in offshore areas. A future decline of ice melt-induced stability of the water column may be associated with a shift in dominant food webs, from larger, sun-adapted diatoms grazed by euphausiids to smaller, shade-adapted flagellates consumed by salps. A basically one-dimensional numerical model of three dominant groups of the Antarctic phytoplankton community (diatoms, cryptophytes, and colonial prymnesiophytes) and four types of herbivore (protozoans, salps, copepods, and euphausiids) is used to explore the seasonal importance of both light limitation and grazing pressure on the amount of annual carbon sequestration and larval krill survival within contrasting oceanic and neritic waters, where respective validation data have been gathered during austral spring by the European JGOFS and RACER programs. With imposition of moderate and large grazing stresses, thought to be typical of offshore waters, we were able to replicate the European JGOFS 1992 observations of light penetration, phytoplankton biomass, primary production, pCO 2, bacterial biomass, labile DOC, ammonium, and total particle effluxes at 100 m within the deep SML of our model. The fidelity of such a large set of simulated state variables suggests that multiple limiting factors are indeed operating on different components of the oceanic phytoplankton community — selective grazing losses on the flagellates, but light limitation of diatoms. Release of protozoan grazing pressure in our model instead leads to unobserved spring blooms of cryptophytes, found only in laboratory enclosures. On an annual basis, weak sequestration of atmospheric CO 2 is simulated in a habitat typical of the Polar Front, while evasion of carbon dioxide occurs under biophysical conditions of the Antarctic Circumpolar Current. Stratification in shallow SML and the same absolute grazing demands by krill and copepods allows sun-adapted diatoms of our model to bloom at the expense of shade-adapted cryptophytes and prymnesiophytes, eaten by salps and protozoans. We were also able to replicate RACER-I observations of the same suite of variables in 1986–1987, as well as the observed 10-fold range of detrital fluxes caught by other sediment trap deployments during 1980 and 1983 along the Antarctic Peninsula. In western Bransfield Strait, coastal waters are a strong sink for atmospheric CO 2 within parcels of Bellingshausen Sea origin, but not perhaps in those from the Weddell Sea, which resemble the oceanic regime of deep SML. We conclude that even in shallow neritic SML, some protozoan rivals of larval krill must still crop flagellates to ensure sufficient abundance of diatom food for both euphausiid survival and possible clogging of the mucous nets of other salp rivals.

Controls on the carbon isotopic composition of southern ocean phytoplankton

Carbon isotopic compositions of suspended organic matter and biomarker compounds were determined for 59 samples filtered from Southern Ocean surface waters in January 1994 along two north‐south transects (WOCE SR3 from Tasmania to Antarctica, and across the Princess Elizabeth Trough (PET) east of Prydz Bay, Antarctica). Along the SR3 line, bulk organic matter show generally decreasing 13C contents southward, which are well correlated with increasing dissolved molecular carbon dioxide concentrations, CO2(aq). This relationship does not hold along the PET transect. Using concentrations and isotopic compositions of molecular compounds, we evaluate the relative roles of several factors affecting the δ13C of Southern Ocean suspended particulate organic matter. Along the WOCE SR3 transect, the concentration of CO2(aq) plays an important role. It is well described by a supply versus demand model for the extent of cellular CO2 utilization and its associated linear dependence of isotopic fractionation (EP) on the reciprocal of CO2(aq). An equally important factor appears to be changes in algal assemblages along the SR3 transect, with their contribution to isotopic fractionation also well described by the supply and demand model, when formulated to include the cell surface/volume control of supply. Changes in microalgal growth rates appear to have a minor effect on EP. Along the PET transect, algal assemblage changes and possibly changes in microalgal growth rates appear to strongly affect the carbon isotopic variations of suspended organic matter. These results can be used to improve the formulation of modern carbon cycle models that include phytoplankton carbon isotopic fractionation.

Inhibition of marine photosynthesis by ultraviolet radiation: Variable sensitivity of phytoplankton in the Weddell‐Scotia Confluence during the austral spring

To assess the potential impacts of ozone depletion on photosynthesis in the Southern Ocean, we need to know more about effects of ultraviolet radiation (UV) on phytoplankton in Antarctic waters, where, in addition to variable stratospheric ozone, temporal and regional differences in vertical mixing might influence photosynthesis and photoacclimation of phytoplankton assemblages. Toward this end, we quantified the responses to UV of Antarctic phytoplankton in the Weddell‐Scotia Confluence during the austral spring of 1993. Experimental results on spectral sensitivity of photosynthesis were fit statistically to a model that incorporated uninhibited photosynthesis as a function of photosynthetically available radiation (PAR), wavelength‐dependence of inhibition, and the kinetics of photosynthesis during exposure to UV. In contrast to previous results on UV‐induced photoinhibition in a diatom culture at 20°C natural phytoplankton from open waters of the Antarctic showed no ability to counter UV‐induced inhibition of photosynthesis during exposures of 0.5–4 h: the rate of photosynthesis declined exponentially as a function of cumulative exposure, and inhibition was not reversed during incubations for up to 3.5 h under benign conditions. The results suggest that nonlinear exposure‐response relationships are necessary for modeling UV dependent photosynthesis in the surface mixed layer of the springtime Weddell‐Scotia Confluence. Consequently, we modified our laboratory‐based model of photosynthesis and photoinhibition to describe photoinhibition as a nonlinear function of biologically weighted cumulative exposure to damaging irradiance. The model described ˜90% of the spectrally dependent experimental variation in photosynthetic rate, and yielded six biological weighting functions (BWFs) for phytoplankton in the Weddell‐Scotia Confluence. Assemblages from different stations showed substantial variability in sensitivity to UV. Tolerance of UV was generally highest in assemblages from shallower mixed layers, which presumably had experienced higher irradiance, including UV, prior to sampling. The BWFs of assemblages that seemed acclimated to low irradiance showed the highest sensitivity to UV yet seen for Southern Ocean phytoplankton. The pattern of UV sensitivity was consistent with acclimation, but also with selection against less tolerant species.

Responses of Southern Ocean phytoplankton to the addition of trace metals

Trace metal enrichment experiments were performed under ultraclean conditions with natural oceanic plankton populations in the Southern Ocean along 6°W in October–November 1992. Five Fe-enrichment experiments were conducted, as well as a further eight experiments with single or combined addition of Fe, Mn, Co and Zn. Water was incubated from the Polar Frontal region at the beginning and again later in the middle of a bloom, from the Antarctic Circumpolar Current south of the Front, from the sea-ice edge area and from the ice-covered northern Weddell Sea. Growth responses of phytoplankton to the addition of Mn (2.5 nM), Co (0.4 nM) or Zn (2 nM) were not very clear (slight enhancement), which may partly have been due to low initial biomass. Growth enhancements by Fe (2 nM) were more pronounced, albeit only where initial biomass was relatively high and where distinct growth in the controls was observed simultaneously. Overall, rates of chlorophyll a increased and final yields increased, relative to the controls, by about 10% to more than 50%. Additions of 5 and 10 nM Fe yielded about 10% higher specific growth rates than additions of 2 nM. Combining Fe with one or more of the other trace metals did not result in significantly higher yields or growth rates as with Fe alone, even at high initial biomass. Moreover, the accumulation of cellular 55Fe over time was neither enhanced nor suppressed by Mn, Co, and Zn, further suggesting that co-limitation by the other metals did not occur. Fe is evidently the most important trace metal controlling phytoplankton development. Microzooplankton grazing was determined (dilution method) at the end of one 9 day experiment where a very clear response by phytoplankton was observed following addition of 2 nM Fe. Gross production and grazing rates (as chlorophyll) were 0.71 and 0.34 day −1, respectively, in the control and 0.89 and 0. 30 day −1 in the Fe enrichment. Apparently only algal production was stimulated by Fe enrichment. We conclude that in the Southern Ocean biomass build-up by phytoplankton is limited by decreasing availability of trace metals, notably Fe, under conditions of sufficient light and low grazing pressure.

Glacial‐interglacial CO2 change: The Iron Hypothesis

Several explanations for the 200 to 280 ppm glacial/interglacial change in atmospheric CO2 concentrations deal with variations in southern ocean phytoplankton productivity and the related use or nonuse of major plant nutrients. An hypothesis is presented herein in which arguments are made that new productivity in today's southern ocean (7.4 × 1013g yr−1) is limited by iron deficiency, and hence the phytoplankton are unable to take advantage of the excess surface nitrate/phosphate that, if used, could result in total southern ocean new production of 2−3 × 1015 g C yr−1. As a consequence of Fe‐limited new productivity, Holocene interglacial CO2 levels (preindustrial) are as high as they were during the last interglacial (≈ 280 ppm). In contrast, atmospheric dust Fe supplies were 50 times higher during the last glacial maximum (LGM). Because of this Fe enrichment, phytoplankton growth may have been greatly enhanced, larger amounts of upwelled nutrients may have been used, and the resulting stimulation of new productivity may have contributed to the LGM drawdown of atmospheric CO2 to levels of less than 200 ppm. Background information and arguments in support of this hypothesis are presented.

POTENTIAL EFFECTS OF UV‐B RADIATION ON MARINE ORGANISMS OF THE SOUTHERN OCEAN: DISTRIBUTIONS OF PHYTOPLANKTON AND KRILL DURING AUSTRAL SPRING

AbstractIncreases in UV‐B radiation resulting from ozone depletion during austral spring could potentially alter the balance of the Southern Ocean marine ecosystem. A quantitative assessment ol the effects of UV‐B enhancement requires knowledge of (1) the wavelength‐dependent fluxes of UV‐B in the upper ocean, (2) action spectra for UV‐B damage to Antarctic phytoplankton and zooplankton, and (3) depth‐dependent distributions and residence times of Southern Ocean phytoplankton and zooplankton during austral spring. Unfortunately, only limited data arc currently available to address this impact directly. To provide some of the information required for such an assessment, available data regarding plankton distributions and their photophysiological characteristics have been summarized. A preliminary assessment of the available literature suggests that Antarctic phytoplankton and krill receive very low doses of UV‐B during austral spring. The high spectral attenuation coefficients associated with the environments in which most plankton arc found during springtime precludes the possibility of UV damage. Future research directions are described which should provide a better understanding of the ecological consequences of the “ozone hole” which resides over the Antarctic continent during austral spring.

Nutrient depletion indicates high primary productivity in the Weddell Sea

The Southern Ocean, and in particular the Weddell Sea, have long been considered areas of high biological productivity1, but recent isotopic measurements of primary productivity have not confirmed this view2,3. Because the large Zooplankton and marine mammal populations of the Southern Ocean depend ultimately on phytoplankton as the base of the food web, accurate knowledge of primary productivity is essential to our understanding of the Antarctic ecosystem. Oceanographie data collected aboard the Soviet icebreaker Mikhail Somov have allowed us to derive a new productivity estimate, based on the seasonal depletion of nitrate, phosphate and silicic acid in the surface layer. From these depletions and data on the elemental composition of Southern Ocean phytoplankton, we estimate average primary productivity in the Weddell Sea in the springtime to be 220–420 mg C m−2 day−1. Our most conservative estimate is 1.5–4 times higher than recently reported measurements of productivity in the open ocean areas of the Southern Ocean2–5. Our estimates are inherently averages over time and space, including the effects of brief, intense spring blooms of phytoplankton which may occur near the receding ice edge6–8. Studies of primary productivity based on isotope uptake experiments, particularly in the austral summer, may fail to account for the significance of such blooms.