Ian Salter

Southern Ocean deep-water carbon export enhanced by natural iron fertilization

The addition of iron to high-nutrient, low-chlorophyll regions induces phytoplankton blooms that take up carbon. Carbon export from the surface layer and, in particular, the ability of the ocean and sediments to sequester carbon for many years remains, however, poorly quantified. Here we report data from the CROZEX experiment in the Southern Ocean, which was conducted to test the hypothesis that the observed north–south gradient in phytoplankton concentrations in the vicinity of the Crozet Islands is induced by natural iron fertilization that results in enhanced organic carbon flux to the deep ocean. We report annual particulate carbon fluxes out of the surface layer, at three kilometres below the ocean surface and to the ocean floor. We find that carbon fluxes from a highly productive, naturally iron-fertilized region of the sub-Antarctic Southern Ocean are two to three times larger than the carbon fluxes from an adjacent high-nutrient, low-chlorophyll area not fertilized by iron. Our findings support the hypothesis that increased iron supply to the glacial sub-Antarctic may have directly enhanced carbon export to the deep ocean. The CROZEX sequestration efficiency (the amount of carbon sequestered below the depth of winter mixing for a given iron supply) of 8,600 mol mol-1 was 18 times greater than that of a phytoplankton bloom induced artificially by adding iron, but 77 times smaller than that of another bloom initiated, like CROZEX, by a natural supply of iron. Large losses of purposefully added iron can explain the lower efficiency of the induced bloom6. The discrepancy between the blooms naturally supplied with iron may result in part from an underestimate of horizontal iron supply.

Structure of the rare archaeal biosphere and seasonal dynamics of active ecotypes in surface coastal waters

Marine Archaea are important players among microbial plankton and significantly contribute to biogeochemical cycles, but details regarding their community structure and long-term seasonal activity and dynamics remain largely unexplored. In this study, we monitored the interannual archaeal community composition of abundant and rare biospheres in northwestern Mediterranean Sea surface waters by pyrosequencing 16S rDNA and rRNA. A detailed analysis of the rare biosphere structure showed that the rare archaeal community was composed of three distinct fractions. One contained the rare Archaea that became abundant at different times within the same ecosystem; these cells were typically not dormant, and we hypothesize that they represent a local seed bank that is specific and essential for ecosystem functioning through cycling seasonal environmental conditions. The second fraction contained cells that were uncommon in public databases and not active, consisting of aliens to the studied ecosystem and representing a nonlocal seed bank of potential colonizers. The third fraction contained Archaea that were always rare but actively growing; their affiliation and seasonal dynamics were similar to the abundant microbes and could not be considered a seed bank. We also showed that the major archaeal groups, Thaumarchaeota marine group I and Euryarchaeota group II.B in winter and Euryarchaeota group II.A in summer, contained different ecotypes with varying activities. Our findings suggest that archaeal diversity could be associated with distinct metabolisms or life strategies, and that the rare archaeal biosphere is composed of a complex assortment of organisms with distinct histories that affect their potential for growth.

Production of giant marine diatoms and their export at oceanic frontal zones: Implications for Si and C flux from stratified oceans

From a synthesis of recent oceanic observations and paleo-data it is evident that certain species of giant diatoms including Rhizosolenia spp. Thalassiothrix spp. and Ethmodiscus rex may become concentrated at oceanic frontal zones and subsequently form episodes of mass flux to the sediment. Within the nutrient bearing waters advecting towards frontal boundaries, these species are generally not dominant, but they appear selectively segregated at fronts, and thus may dominate the export flux. Ancient Thalassiothrix diatom mat deposits in the eastern equatorial Pacific and beneath the Polar Front in the Southern Ocean record the highest open ocean sedimentation rates ever documented and represent vast sinks of silica and carbon. Several of the species involved are adapted to a stratified water column and may thrive in Deep Chlorophyll Maxima. Thus in oceanic regions and/or at times prone to enhanced surface water stratification (e.g., during meltwater pulses) they provide a mechanism for generating substantial biomass at depth and its subsequent export with concomitant implications for Si export and C drawdown. This ecology has important implications for ocean biogeochemical models suggesting that more than one diatom “functional type” should be used. In spite of the importance of these giant diatoms for biogeochemical cycling, their large size coupled with the constraints of conventional oceanographic survey schemes and techniques means that they are undersampled. An improved insight into these key species will be an important prerequisite for enhancing our understanding of marine biogeochemical cycling and for assessing the impacts of climate change on ocean export production.

Diatom resting spore ecology drives enhanced carbon export from a naturally iron‐fertilized bloom in the Southern Ocean

Southern Ocean Island systems sustain phytoplankton blooms induced by natural iron fertilization that are important for the uptake of atmospheric carbon dioxide and serve as analogues for past and future climate change. We present data on diatom flux assemblages and the biogeochemical properties of sinking particles to explain the enhanced particulate organic carbon (POC) export fluxes observed in response to natural iron supply in the Crozet Islands region (CROZeX). Moored deep-ocean sediment traps (>2000 m) were located beneath a naturally fertilized island bloom and beneath an adjacent High Nutrient Low Chlorophyll (HNLC) control site. Deep-ocean carbon flux from the naturally-fertilized bloom area was tightly correlated (R = 0.83, n = 12, P < 0.0006) with the resting spore flux of a single island-associated diatom species, Eucampia antarctica var. antarctica. The unusually well preserved state of the Eucampia-associated carbon flux, determined by amino acid studies of organic matter degradation, was likely influenced by their ecology, since diatom resting spores are adapted to settle rapidly out of the surface ocean preserving viable cells. The naturally fertilized bloom enhanced carbon flux and the resulting Si/C and Si/N ratios were 2.0–3.4-fold and 2.2–3.5-fold lower than those measured in the adjacent HNLC control area. The enhanced carbon export and distinctive stoichiometry observed in naturally fertilized systems is therefore largely not attributable to iron relief of open ocean diatoms, but rather to the advection and growth of diatom species characteristic of island systems and the subsequent flux of resting spores. Carbon export estimates from current natural iron fertilization studies therefore represent a highly specific response of the island systems chosen as natural laboratories and may not be appropriate analogues for the larger Southern Ocean response. The broader implications of our results emphasize the role of phytoplankton diversity and ecology and highlight the need for a species-centered approach in order to understand the regulation of biogeochemical fluxes.

Seasonal dynamics of active SAR11 ecotypes in the oligotrophic Northwest Mediterranean Sea

A seven-year oceanographic time series in NW Mediterranean surface waters was combined with pyrosequencing of ribosomal RNA (16S rRNA) and ribosomal RNA gene copies (16S rDNA) to examine the environmental controls on SAR11 ecotype dynamics and potential activity. SAR11 diversity exhibited pronounced seasonal cycles remarkably similar to total bacterial diversity. The timing of diversity maxima was similar across narrow and broad phylogenetic clades and strongly associated with deep winter mixing. Diversity minima were associated with periods of stratification that were low in nutrients and phytoplankton biomass and characterised by intense phosphate limitation (turnover time<5 h). We propose a conceptual framework in which physical mixing of the water column periodically resets SAR11 communities to a high diversity state and the seasonal evolution of phosphate limitation competitively excludes deeper-dwelling ecotypes to promote low diversity states dominated (>80%) by SAR11 Ia. A partial least squares (PLS) regression model was developed that could reliably predict sequence abundances of SAR11 ecotypes (Q2=0.70) from measured environmental variables, of which mixed layer depth was quantitatively the most important. Comparison of clade-level SAR11 rRNA:rDNA signals with leucine incorporation enabled us to partially validate the use of these ratios as an in-situ activity measure. However, temporal trends in the activity of SAR11 ecotypes and their relationship to environmental variables were unclear. The strong and predictable temporal patterns observed in SAR11 sequence abundance was not linked to metabolic activity of different ecotypes at the phylogenetic and temporal resolution of our study.

Radiolaria: Major exporters of organic carbon to the deep ocean

Very large pulses of particulate organic matter intermittently sink to the deep waters of the open ocean in the Northeast Atlantic. These pulses, measured by moored sediment traps since 1989, can contribute up to 60% of the organic flux to 3000 m in a particular year and are thus a major cause of the variability in carbon sequestration from the atmosphere in the region. Pulses occur in the late summer and are characterized by material that is very rich in organic carbon but with low concentrations of the biominerals opal and calcite. A number of independent lines of evidence have been examined to determine the causes of these pulses: (1) Data from the Continuous Plankton Recorder (CPR) survey show that in this region, radiolarian protozoans intermittently reach high abundances in the late summer just preceding organic pulses to depth. (2) CPR data also show that the interannual variability in radiolarian abundance since 1997 mirrors very closely the variability of deep ocean organic deposition. (3) The settling material collected in the traps displays a strong correlation between fecal pellets produced by radiolaria and the measured organic carbon flux. These all suggest that the pulses are mediated by radiolarians, a group of protozoans found throughout the worlds oceans and which are widely used by paleontologists to determine past climate conditions. Changes in the upper ocean community structure (between years and on longer timescales) may have profound effects on the ability of the oceans to sequester carbon dioxide from the atmosphere.

The Effects of Natural Iron Fertilisation on Deep-Sea Ecology: The Crozet Plateau, Southern Indian Ocean

The addition of iron to high-nutrient low-chlorophyll (HNLC) oceanic waters stimulates phytoplankton, leading to greater primary production. Large-scale artificial ocean iron fertilization (OIF) has been proposed as a means of mitigating anthropogenic atmospheric CO2, but its impacts on ocean ecosystems below the photic zone are unknown. Natural OIF, through the addition of iron leached from volcanic islands, has been shown to enhance primary productivity and carbon export and so can be used to study the effects of OIF on life in the ocean. We compared two closely-located deep-sea sites (∼400 km apart and both at ∼4200 m water depth) to the East (naturally iron fertilized; +Fe) and South (HNLC) of the Crozet Islands in the southern Indian Ocean. Our results suggest that long-term geo-engineering of surface oceanic waters via artificial OIF would lead to significant changes in deep-sea ecosystems. We found that the +Fe area had greater supplies of organic matter inputs to the seafloor, including polyunsaturated fatty acid and carotenoid nutrients. The +Fe site also had greater densities and biomasses of large deep-sea animals with lower levels of evenness in community structuring. The species composition was also very different, with the +Fe site showing similarities to eutrophic sites in other ocean basins. Moreover, major differences occurred in the taxa at the +Fe and HNLC sites revealing the crucial role that surface oceanic conditions play in changing and structuring deep-sea benthic communities.

Quantifying export production in the Southern Ocean: Implications for the Baxs proxy

The water column and sedimentary Baxs distribution around the Crozet Plateau is used to decipher the controls and timing of barite formation and to evaluate how export production signals are recorded in sediments underlying a region of natural Fe fertilization within the Fe limited Southern Ocean. Export production estimated from preserved, vertical sedimentary Baxs accumulation rates are compared with published export fluxes assessed from an integrated study of the biological carbon pump to determine the validity of Baxs as a quantitative proxy under different Fe supply conditions typical of the Southern Ocean. Detailed assessment of the geochemical partitioning of Ba in sediments and the lithogenic end-member allows appropriate correction of the bulk Ba content and determination of the Baxs content of sediments and suspended particles. The upper water column distribution of Baxs is extremely heterogeneous spatially and temporally. Organic carbon/Baxs ratios in deep traps from the Fe fertilized region are similar to other oceanic settings allowing quantification of the inferred carbon export based on established algorithms. There appears to be some decoupling of POC and Ba export in the Fe limited region south of the Plateau. The export production across the Crozet Plateau inferred from the Baxs sedimentary proxy indicates that the Fe fertilized area to the north of the Plateau experiences enhanced export relative to equivalent Southern Ocean settings throughout the Holocene and that this influence may also have impacted the site to the south for significant periods. This interpretation is corroborated by alternative productivity proxies (opal accumulation, 231Paxs/230Thxs). Baxs can be used to quantify export production in complex settings such as naturally Fe-fertilized (volcanoclastic) areas, providing appropriate lithogenic correction is undertaken, and sediment focusing is corrected for along with evaluation of barite preservation.

Ecosystem productivity is associated with bacterial phylogenetic distance in surface marine waters

Understanding the link between community diversity and ecosystem function is a fundamental aspect of ecology. Systematic losses in biodiversity are widely acknowledged but the impact this may exert on ecosystem functioning remains ambiguous. There is growing evidence of a positive relationship between species richness and ecosystem productivity for terrestrial macro-organisms, but similar links for marine micro-organisms, which help drive global climate, are unclear. Community manipulation experiments show both positive and negative relationships for microbes. These previous studies rely, however, on artificial communities and any links between the full diversity of active bacterial communities in the environment, their phylogenetic relatedness and ecosystem function remain hitherto unexplored. Here, we test the hypothesis that productivity is associated with diversity in the metabolically active fraction of microbial communities. We show in natural assemblages of active bacteria that communities containing more distantly related members were associated with higher bacterial production. The positive phylogenetic diversity-productivity relationship was independent of community diversity calculated as the Shannon index. From our long-term (7-year) survey of surface marine bacterial communities, we also found that similarly, productive communities had greater phylogenetic similarity to each other, further suggesting that the traits of active bacteria are an important predictor of ecosystem productivity. Our findings demonstrate that the evolutionary history of the active fraction of a microbial community is critical for understanding their role in ecosystem functioning.

The subpolar gyre regulates silicate concentrations in the North Atlantic

The North Atlantic is characterized by diatom-dominated spring blooms that results in significant transfer of carbon to higher trophic levels and the deep ocean. These blooms are terminated by limiting silicate concentrations in summer. Numerous regional studies have demonstrated phytoplankton community shifts to lightly-silicified diatoms and non-silicifying plankton at the onset of silicate limitation. However, to understand basin-scale patterns in ecosystem and climate dynamics, nutrient inventories must be examined over sufficient temporal and spatial scales. Here we show, from a new comprehensive compilation of data from the subpolar Atlantic Ocean, clear evidence of a marked pre-bloom silicate decline of 1.5–2 µM throughout the winter mixed layer during the last 25 years. This silicate decrease is primarily attributed to natural multi-decadal variability through decreased winter convection depths since the mid-1990s, a weakening and retraction of the subpolar gyre and an associated increased influence of nutrient-poor water of subtropical origin. Reduced Arctic silicate import and the projected hemispheric-scale climate change-induced weakening of vertical mixing may have acted to amplify the recent decline. These marked fluctuations in pre-bloom silicate inventories will likely have important consequences for the spatial and temporal extent of diatom blooms, thus impacting ecosystem productivity and ocean-atmosphere climate dynamics.