The relative importance of phytoplankton aggregates and zooplankton fecal pellets to carbon export: insights from free-drifting sediment trap deployments in naturally iron-fertilised waters near the Kerguelen Plateau

The first KErguelen Ocean and Plateau compared Study (KEOPS1), conducted in the naturally iron-fertilised Kerguelen bloom, demonstrated that fecal material was the main pathway for exporting carbon to the deep ocean during summer (January–February 2005), suggesting a limited role of direct export via phytodetrital aggregates. The KEOPS2 project reinvestigated this issue during the spring bloom initiation (October–November 2011), when zooplankton communities may exert limited grazing pressure, and further explored the link between carbon flux, export efficiency and dominant sinking particles depending upon surface plankton community structure. Sinking particles were collected in polyacrylamide gel-filled and standard free-drifting sediment traps (PPS3/3), deployed at six stations between 100 and 400 m, to examine flux composition, particle origin and their size distributions. Results revealed an important contribution of phytodetrital aggregates (49 ± 10 and 45 ± 22% of the total number and volume of particles respectively, all stations and depths averaged). This high contribution dropped when converted to carbon content (30 ± 16% of total carbon, all stations and depths averaged), with cylindrical fecal pellets then representing the dominant fraction (56 ± 19%).At 100 and 200 m depth, iron- and biomass-enriched sites exhibited the highest carbon fluxes (maxima of 180 and 84 ± 27 mg C m-2 d-1, based on gel and PPS3/3 trap collection respectively), especially where large fecal pellets dominated over phytodetrital aggregates. Below these depths, carbon fluxes decreased (48 ± 21% decrease on average between 200 and 400 m), and mixed aggregates composed of phytodetritus and fecal matter dominated, suggesting an important role played by physical aggregation in deep carbon export.Export efficiencies determined from gels, PPS3/3 traps and 234Th disequilibria (200 m carbon flux/net primary productivity) were negatively correlated to net primary productivity with observed decreases from ~ 0.2 at low-iron sites to ~ 0.02 at high-iron sites. Varying phytoplankton communities and grazing pressure appear to explain this negative relationship. Our work emphasises the need to consider detailed plankton communities to accurately identify the controls on carbon export efficiency, which appear to include small spatio-temporal variations in ecosystem structure

The relative importance of phytoplankton aggregates and zooplankton fecal pellets to carbon export: insights from free-drifting sediment trap deployments in naturally iron-fertilised waters near the Kerguelen Plateau

The first KErguelen Ocean and Plateau compared Study (KEOPS1), conducted in the naturally iron-fertilised Kerguelen bloom, demonstrated that fecal material was the main pathway for exporting carbon to the deep ocean during summer (January–February 2005), suggesting a limited role of direct export via phytodetrital aggregates. The KEOPS2 project reinvestigated this issue during the spring bloom initiation (October–November 2011), when zooplankton communities may exert limited grazing pressure, and further explored the link between carbon flux, export efficiency and dominant sinking particles depending upon surface plankton community structure. Sinking particles were collected in polyacrylamide gel-filled and standard free-drifting sediment traps (PPS3/3), deployed at six stations between 100 and 400 m, to examine flux composition, particle origin and their size distributions. Results revealed an important contribution of phytodetrital aggregates (49+/-10 and 45+/-22% of the total number and volume of particles respectively, all stations and depths averaged). This high contribution dropped when converted to carbon content (30+/-16% of total carbon, all stations and depths averaged), with cylindrical fecal pellets then representing the dominant fraction (56+/-19 %). At 100 and 200m depth, iron- and biomass-enriched sites exhibited the highest carbon fluxes (maxima of 180 and 84+/- 27 mgCm-2 d-1, based on gel and PPS3/3 trap collection respectively), especially where large fecal pellets dominated over phytodetrital aggregates. Below these depths, carbon fluxes decreased (48+/-21%decrease on average between 200 and 400 m), and mixed aggregates composed of phytodetritus and fecal matter dominated, suggesting an important role played by physical aggregation in deep carbon export. Export efficiencies determined from gels, PPS3/3 traps and 234Th disequilibria (200m carbon flux/net primary productivity) were negatively correlated to net primary productivity with observed decreases from ~0.2 at low-iron sites to ~0.02 at high-iron sites. Varying phytoplankton communities and grazing pressure appear to explain this negative relationship. Our work emphasises the need to consider detailed plankton communities to accurately identify the controls on carbon export efficiency, which appear to include small spatio-temporal variations in ecosystem structure

Chemometric perspectives on plankton community responses to natural iron fertilisation over and downstream of the Kerguelen Plateau in the Southern Ocean

International audienceWe examined phytoplankton community responses to natural iron fertilisation at 32 sites over and downstream from the Kerguelen Plateau in the Southern Ocean during the austral spring bloom in October–November 2011. The community structure was estimated from chemical and isotopic measurements (particulate organic carbon – POC; 13C-POC; particulate nitrogen – PN; 15N-PN; and biogenic silica – BSi) on size-fractionated samples from surface waters (300, 210, 50, 20, 5, and 1 μm fractions). Higher values of 13C-POC (vs. co-located 13C values for dissolved inorganic carbon – DIC) were taken as indicative of faster growth rates and higher values of 15N-PN (vs. co-located 15N-NO3 source values) as indicative of greater nitrate use (rather than ammonium use, i.e. higher f ratios).Community responses varied in relation to both regional circulation and the advance of the bloom. Iron-fertilised waters over the plateau developed dominance by very large diatoms (50–210 μm) with high BSi / POC ratios, high growth rates, and significant ammonium recycling (lower f ratios) as biomass built up. In contrast, downstream polar frontal waters with a similar or higher iron supply were dominated by smaller diatoms (20–50 μm) and exhibited greater ammonium recycling. Stations in a deep-water bathymetrically trapped recirculation south of the polar front with lower iron levels showed the large-cell dominance observed on the plateau but much less biomass. Comparison of these communities to surface water nitrate (and silicate) depletions as a proxy for export shows that the low-biomass recirculation feature had exported similar amounts of nitrogen to the high-biomass blooms over the plateau and north of the polar front. This suggests that early spring trophodynamic and export responses differed between regions with persistent low levels vs. intermittent high levels of iron fertilisation

Decoding drivers of carbon flux attenuation in the oceanic biological pump

The biological pump supplies carbon to the oceans’ interior, driving long-term carbon sequestration and providing energy for deep-sea ecosystems1,2. Its efficiency is set by transformations of newly formed particles in the euphotic zone, followed by vertical flux attenuation via mesopelagic processes3. Depth attenuation of the particulate organic carbon (POC) flux is modulated by multiple processes involving zooplankton and/or microbes4,5. Nevertheless, it continues to be mainly parameterized using an empirically derived relationship, the ‘Martin curve’6. The derived power-law exponent is the standard metric used to compare flux attenuation patterns across oceanic provinces7,8. Here we present in situ experimental findings from C-RESPIRE9, a dual particle interceptor and incubator deployed at multiple mesopelagic depths, measuring microbially mediated POC flux attenuation. We find that across six contrasting oceanic regimes, representing a 30-fold range in POC flux, degradation by particle-attached microbes comprised 7–29 per cent of flux attenuation, implying a more influential role for zooplankton in flux attenuation. Microbial remineralization, normalized to POC flux, ranged by 20-fold across sites and depths, with the lowest rates at high POC fluxes. Vertical trends, of up to threefold changes, were linked to strong temperature gradients at low-latitude sites. In contrast, temperature played a lesser role at mid- and high-latitude sites, where vertical trends may be set jointly by particle biochemistry, fragmentation and microbial ecophysiology. This deconstruction of the Martin curve reveals the underpinning mechanisms that drive microbially mediated POC flux attenuation across oceanic provinces

What causes the inverse relationship between primary production and export efficiency in the Southern Ocean?

The ocean contributes to regulating atmospheric CO2 levels, partly via variability in the fraction of primary production (PP) which is exported out of the surface layer (i.e. the e-ratio). Southern Ocean studies have found that, contrary to global scale analyses, an inverse relationship exists between e-ratio and PP. This relationship remains unexplained, with potential hypotheses being i) large export of dissolved organic carbon (DOC) in high PP areas, ii) strong surface microbial recycling in high PP regions and/ or iii) grazing mediated export varies inversely with PP. We find that the export of DOC has a limited influence in setting the negative e-ratio/PP relationship. However, we observed that at sites with low PP and high e-ratios, zooplankton mediated export is large and surface microbial abundance low suggesting that both are important drivers of the magnitude of the e-ratio in the Southern Ocean

Resupply of mesopelagic dissolved iron controlled by particulate iron composition

The dissolved iron supply controls half of the oceans’ primary productivity. Resupply by the remineralization of sinking particles, and subsequent vertical mixing, largely sustains this productivity. However, our understanding of the drivers of dissolved iron resupply, and their influence on its vertical distribution across the oceans, is still limited due to sparse observations. There is a lack of empirical evidence as to what controls the subsurface iron remineralization due to difficulties in studying mesopelagic biogeochemistry. Here we present estimates of particulate transformations to dissolved iron, concurrent oxygen consumption and iron-binding ligand replenishment based on in situ mesopelagic experiments. Dissolved iron regeneration efficiencies (that is, replenishment over oxygen consumption) were 10- to 100-fold higher in low-dust subantarctic waters relative to higher-dust Mediterranean sites. Regeneration efficiencies are heavily influenced by particle composition. Their make-up dictates ligand release, controls scavenging, modulates ballasting and may lead to the differential remineralization of biogenic versus lithogenic iron. At high-dust sites, these processes together increase the iron remineralization length scale. Modelling reveals that in oceanic regions near deserts, enhanced lithogenic fluxes deepen the ferricline, which alter the vertical patterns of dissolved iron replenishment, and set its redistribution at the global scale. Such wide-ranging regeneration efficiencies drive different vertical patterns in dissolved iron replenishment across oceanic provinces

Exploring the ecology of the mesopelagic biological pump

The oceans’ biological pump (BP) exports large amounts of particulate organic carbon (POC) to the mesopelagic zone (base of the euphotic zone – 1000 m depth). The efficiency at which POC is transferred through the mesopelagic zone determines the size of the deep ocean carbon store. Few observational BP studies focus on the mesopelagic, often leading to the need to oversimplify the representation of processes within this depth horizon in numerical models. In this review, we identify and describe three interlinked biological processes that act to regulate and control the transfer efficiency of POC through the mesopelagic zone; (1) direct sinking of phytoplankton cells and aggregates, (2) zooplankton community structure and (3) the microbial loop and associated carbon pump. We reveal previously unidentified relationships between planktonic community structure and POC transfer efficiency for specific regions. We also compare mesopelagic POC remineralisation depth (a proxy for POC transfer efficiency) with the permanent thermocline in different regions. Our analysis shows that even when mesopelagic POC transfer efficiency is low, such a transfer efficiency does not necessarily mean low carbon sequestration if the permanent thermocline is shallow, and we define a carbon sequestration ratio (Cseq, the remineralisation depth divided by the permanent thermocline) to highlight this. Low latitude regions typically have a higher Cseq than temperate and polar regions, and thus could be more important in transferring carbon on long timescales than previously thought. POC transfer efficiency should be regularly discussed in the context of the physical water properties such as the permanent thermocline, to truly assess an oceanic region’s ability to sequester carbon. Improved understanding of mesopelagic ecological processes and links to surface processes will better constrain ecosystem models and improve projections of the future global carbon cycle

Phytoplankton morphology controls on marine snow sinking velocity

During the second KErguelen Ocean and Plateau compared Study (KEOPS2) in October-November 2011, marine snow was formed in roller tanks by physical aggregation of phytoplankton assemblages sampled at 6 stations over and downstream of the Kerguelen Plateau. Sinking velocities, morphology, bulk composition (transparent exopolymer particles, biogenic silica, particulate organic carbon), and phytoplankton contents were measured individually on 66 aggregates to identify controls on sinking velocities. Equivalent spherical diameters (ESD) ranged from 1 to 12 mm, and the particle aspect ratios, Corey shape factors, and fractal dimensions (D-F1 = 1.5, D-F2 = 1.8) were close to those of smaller natural aggregates (0.2 to 1.5 mm) collected in polyacrylamide gel-filled sediment traps (D-F1 = 1.2, D-F2 = 1.9). Sinking velocities ranged between 13 and 260 m d(-1), and were correlated with aggregate size only when considering individually the experiments conducted at each station, suggesting that a site-dependent control prevailed over the general influence of size. Variation in dominant diatom morphologies among the sites (classified as small spine-forming or chain without spines) appeared to be a determinant parameter influencing the sinking velocity (SV [m d(-1)] = 168 -1.48 x (% small spine-forming cells), r(2) = 0.98), possibly via a control on species-specific coagulation efficiency affecting particle structure and excess density. Our results emphasize the importance of ecological considerations over that of simple compositional perspectives in the control of particle formation, and in accurate parameterizations of marine snow sinking velocities that are essential to predictions of biological carbon sequestration

Concepts Toward a Global Mechanistic Mapping of Ocean Carbon Export

Abstract The gravitational sinking of organic debris from ocean ecosystems is a dominant mechanism of the biological carbon pump (BCP) that regulates the global climate. The fraction of primary production exported downward, the e‐ratio, is an important but poorly constrained BCP metric. In mid‐ and high‐latitude oceans, seasonal and local variations of sinking particle fluxes strongly modulate the e‐ratio. These locally specific e‐ratio variations and their ecological foundations are here encapsulated in the term “export systems” (ES). ES have been partly characterized for a few ocean locations but remain largely ignored over most of the ocean surface. Here, in a fully conceptual approach and with the primary aim to understand rather than to estimate ocean carbon export, we combine biogeochemical (BGC) modeling with satellite observations to map ES at fine spatio‐temporal scales. We identify four plausible ES with distinct e‐ratio seasonalities across mid‐ and high‐latitude oceans. The ES map confirms the outlines of traditional BGC provinces and unveils new boundaries indicating where (and how) the annual relationship between carbon export and production changes markedly. At six sites where ES features can be partially inferred from in situ data, we test our approach and propose key ecological processes driving carbon export. In the light of our findings, a re‐examination of 1,841 field‐based e‐ratios could challenge the conventional wisdom that e‐ratios change strongly with latitude, suggesting a possible seasonal artifact caused by the timing of observations. By deciphering carbon export mechanistically, our conceptual ES map provides timely directions to emergent ocean robotic explorations of the BCP