Coexisting picoplankton experience different relative grazing pressures across an ocean productivity gradient.

Picophytoplankton populations [Prochlorococcus, Synechococcus (SYN), and picoeukaryotes] are dominant primary producers in the open ocean and projected to become more important with climate change. Their fates can vary, however, with microbial food web complexities. In the California Current Ecosystem, picophytoplankton biomass and abundance peak in waters of intermediate productivity and decrease at higher production. Using experimental data from eight cruises crossing the pronounced CCE trophic gradient, we tested the hypothesis that these declines are driven by intensified grazing on heterotrophic bacteria (HBAC) passed to similarly sized picophytoplankton via shared predators. Results confirm previously observed distributions as well as significant increases in bacterial abundance, cell growth, and grazing mortality with primary production. Mortalities of picophytoplankton, however, diverge from the bacterial mortality trend such that relative grazing rates on SYN compared to HBAC decline by 12-fold between low and high productivity waters. The large shifts in mortality rate ratios for coexisting populations are not explained by size variability but rather suggest high selectivity of grazer assemblages or tightly coupled tradeoffs in microbial growth advantages and grazing vulnerabilities. These findings challenge the long-held view that protistan grazing mainly determines overall biomass of microbial communities while viruses uniquely regulate diversity by "killing the winners".

Carbon sequestration by multiple biological pump pathways in a coastal upwelling biome.

Multiple processes transport carbon into the deep ocean as part of the biological carbon pump, leading to long-term carbon sequestration. However, our ability to predict future changes in these processes is hampered by the absence of studies that have simultaneously quantified all carbon pump pathways. Here, we quantify carbon export and sequestration in the California Current Ecosystem resulting from (1) sinking particles, (2) active transport by diel vertical migration, and (3) the physical pump (subduction + vertical mixing of particles). We find that sinking particles are the most important and export 9.0 mmol C m-2 d-1 across 100-m depth while sequestering 3.9 Pg C. The physical pump exports more carbon from the shallow ocean than active transport (3.8 vs. 2.9 mmol C m-2 d-1), although active transport sequesters more carbon (1.0 vs. 0.8 Pg C) because of deeper remineralization depths. We discuss the implications of these results for understanding biological carbon pump responses to climate change.

Salp blooms drive strong increases in passive carbon export in the Southern Ocean.

The Southern Ocean contributes substantially to the global biological carbon pump (BCP). Salps in the Southern Ocean, in particular Salpa thompsoni, are important grazers that produce large, fast-sinking fecal pellets. Here, we quantify the salp bloom impacts on microbial dynamics and the BCP, by contrasting locations differing in salp bloom presence/absence. Salp blooms coincide with phytoplankton dominated by diatoms or prymnesiophytes, depending on water mass characteristics. Their grazing is comparable to microzooplankton during their early bloom, resulting in a decrease of ~1/3 of primary production, and negative phytoplankton rates of change are associated with all salp locations. Particle export in salp waters is always higher, ranging 2- to 8- fold (average 5-fold), compared to non-salp locations, exporting up to 46% of primary production out of the euphotic zone. BCP efficiency increases from 5 to 28% in salp areas, which is among the highest recorded in the global ocean.

Plankton food webs in the oligotrophic Gulf of Mexico spawning grounds of Atlantic bluefin tuna.

We used linear inverse ecosystem modeling techniques to assimilate data from extensive Lagrangian field experiments into a mass-balance constrained food web for the Gulf of Mexico open-ocean ecosystem. This region is highly oligotrophic, yet Atlantic bluefin tuna (ABT) travel long distances from feeding grounds in the North Atlantic to spawn there. Our results show extensive nutrient regeneration fueling primary productivity (mostly by cyanobacteria and other picophytoplankton) in the upper euphotic zone. The food web is dominated by the microbial loop (>70% of net primary productivity is respired by heterotrophic bacteria and protists that feed on them). By contrast, herbivorous food web pathways from phytoplankton to metazoan zooplankton process <10% of the net primary production in the mixed layer. Nevertheless, ABT larvae feed preferentially on podonid cladocerans and other suspension-feeding zooplankton, which in turn derive much of their nutrition from nano- and micro-phytoplankton (mixotrophic flagellates, and to a lesser extent, diatoms). This allows ABT larvae to maintain a comparatively low trophic level (~4.2 for preflexion and postflexion larvae), which increases trophic transfer from phytoplankton to larval fish.

Trade-offs between risks of predation and starvation in larvae make the shelf break an optimal spawning location for Atlantic bluefin tuna.

Atlantic bluefin tuna (ABT) (Thunnus thynnus) travel long distances to spawn in oligotrophic regions of the Gulf of Mexico (GoM) which suggests these regions offer some unique benefit to offspring survival. To better understand how larval survival varies within the GoM a spatially explicit, Lagrangian, individual-based model was developed that simulates dispersal and mortality of ABT early life stages within realistic predator and prey fields during the spawning periods from 1993 to 2012. The model estimates that starvation is the largest cumulative source of mortality associated with an early critical period. However, elevated predation on older larvae is identified as the main factor limiting survival to late postflexion. As a result, first-feeding larvae have higher survival on the shelf where food is abundant, whereas older larvae have higher survival in the open ocean with fewer predators, making the shelf break an optimal spawning area. The modeling framework developed in this study explicitly simulates both physical and biological factors that impact larval survival and hence could be used to support ecosystem based management efforts for ABT under current and future climate conditions.

Relating sinking and suspended microbial communities in the California Current Ecosystem: digestion resistance and the contributions of phytoplankton taxa to export.

We used 16S, 18S, plastid and internal transcribed spacer (for Synechococcus strains) sequencing to quantify relative microbial abundances in water-column samples and on sediment-trap-collected particles across an environmental gradient in the California Current Ecosystem (CCE) spanning a > 60-fold range of surface chlorophyll. Most mixed-layer dominant eukaryotes and prokaryotes were consistently underrepresented on sinking particles. Diatoms were the only phototrophic taxa consistently overrepresented. Even within this class, however, one genus (Thalassiosira) was a particle-enriched dominant, while a similarly abundant species was poorly represented. Synechococcus was significantly enriched on sinking particles at only one of four sites, but clade I was disproportionately abundant on sinking particles throughout the region compared with clade IV, the euphotic-zone co-dominant. The most abundant microbes on particles across the CCE were organisms with distributional maxima close to the sediment-trap depth (rhizarians), microbes associated with metazoans or sinking particles as a nutritional habitat (certain alveolates, Gammaproteobacteria) and organisms that resist digestive degradation of their DNA (Thalassiosira, Synechococcus). For assessing taxon contributions of phytoplankton to carbon export, our results highlight the need for sequence-based quantitative approaches that can be used to integrate euphotic-zone abundances, compute rates and account for taxon differences in preservation of sequence markers through trophic processing.

Lateral advection supports nitrogen export in the oligotrophic open-ocean Gulf of Mexico.

In contrast to its productive coastal margins, the open-ocean Gulf of Mexico (GoM) is notable for highly stratified surface waters with extremely low nutrient and chlorophyll concentrations. Field campaigns in 2017 and 2018 identified low rates of turbulent mixing, which combined with oligotrophic nutrient conditions, give very low estimates for diffusive flux of nitrate into the euphotic zone (< 1 µmol N m-2 d-1). Estimates of local N2-fixation are similarly low. In comparison, measured export rates of sinking particulate organic nitrogen (PON) from the euphotic zone are 2 - 3 orders of magnitude higher (i.e. 462 - 1144 µmol N m-2 d-1). We reconcile these disparate findings with regional scale dynamics inferred independently from remote-sensing products and a regional biogeochemical model and find that laterally-sourced organic matter is sufficient to support >90% of open-ocean nitrogen export in the GoM. Results show that lateral transport needs to be closely considered in studies of biogeochemical balances, particularly for basins enclosed by productive coasts.

Towards integrated modeling of the long-term impacts of oil spills.

Although great progress has been made to advance the scientific understanding of oil spills, tools for integrated assessment modeling of the long-term impacts on ecosystems, socioeconomics and human health are lacking. The objective of this study was to develop a conceptual framework that could be used to answer stakeholder questions about oil spill impacts and to identify knowledge gaps and future integration priorities. The framework was initially separated into four knowledge domains (ocean environment, biological ecosystems, socioeconomics, and human health) whose interactions were explored by gathering stakeholder questions through public engagement, assimilating expert input about existing models, and consolidating information through a system dynamics approach. This synthesis resulted in a causal loop diagram from which the interconnectivity of the system could be visualized. Results of this analysis indicate that the system naturally separates into two tiers, ocean environment and biological ecosystems versus socioeconomics and human health. As a result, ocean environment and ecosystem models could be used to provide input to explore human health and socioeconomic variables in hypothetical scenarios. At decadal-plus time scales, the analysis emphasized that human domains influence the natural domains through changes in oil-spill related laws and regulations. Although data gaps were identified in all four model domains, the socioeconomics and human health domains are the least established. Considerable future work is needed to address research gaps and to create fully coupled quantitative integrative assessment models that can be used in strategic decision-making that will optimize recoveries from future large oil spills.

High contribution of Rhizaria (Radiolaria) to vertical export in the California Current Ecosystem revealed by DNA metabarcoding.

Passive sinking of particulate organic matter (POM) is the main mechanism through which the biological pump transports surface primary production to the ocean interior. However, the contribution and variability of different biological sources to vertical export is not fully understood. Here, we use DNA metabarcoding of the 18S rRNA gene and particle interceptor traps (PITs) to characterize the taxonomic composition of particles sinking out of the photic layer in the California Current Ecosystem (CCE), a productive system with high export potential. The PITs included formalin-fixed and 'live' traps to investigate eukaryotic communities involved in the export and remineralization of sinking particles. Sequences affiliated with Radiolaria dominated the eukaryotic assemblage in fixed traps (90%), with Dinophyta and Metazoa making minor contributions. The prominence of Radiolaria decreased drastically in live traps, possibly due to selective consumption by copepods, heterotrophic nanoflagellates, and phaeodarians that were heavily enriched in these traps. These patterns were consistent across the water masses surveyed extending from the coast to offshore, despite major differences in productivity and trophic structure of the epipelagic plankton community. Our findings identify Radiolaria as major actors in export fluxes in the CCE.

A new approach for incorporating 15N isotopic data into linear inverse ecosystem models with Markov Chain Monte Carlo sampling.

Oceanographic field programs often use δ15N biogeochemical measurements and in situ rate measurements to investigate nitrogen cycling and planktonic ecosystem structure. However, integrative modeling approaches capable of synthesizing these distinct measurement types are lacking. We develop a novel approach for incorporating δ15N isotopic data into existing Markov Chain Monte Carlo (MCMC) random walk methods for solving linear inverse ecosystem models. We test the ability of this approach to recover food web indices (nitrate uptake, nitrogen fixation, zooplankton trophic level, and secondary production) derived from forward models simulating the planktonic ecosystems of the California Current and Amazon River Plume. We show that the MCMC with δ15N approach typically does a better job of recovering ecosystem structure than the standard MCMC or L2 minimum norm (L2MN) approaches, and also outperforms an L2MN with δ15N approach. Furthermore, we find that the MCMC with δ15N approach is robust to the removal of input equations and hence is well suited to typical pelagic ecosystem studies for which the system is usually vastly under-constrained. Our approach is easily extendable for use with δ13C isotopic measurements or variable carbon:nitrogen stoichiometry.

Spring-summer net community production, new production, particle export and related water column biogeochemical processes in the marginal sea ice zone of the Western Antarctic Peninsula 2012-2014.

New production (New P, the rate of net primary production (NPP) supported by exogenously supplied limiting nutrients) and net community production (NCP, gross primary production not consumed by community respiration) are closely related but mechanistically distinct processes. They set the carbon balance in the upper ocean and define an upper limit for export from the system. The relationships, relative magnitudes and variability of New P (from 15NO3- uptake), O2 : argon-based NCP and sinking particle export (based on the 238U : 234Th disequilibrium) are increasingly well documented but still not clearly understood. This is especially true in remote regions such as polar marginal ice zones. Here we present a 3-year dataset of simultaneous measurements made at approximately 50 stations along the Western Antarctic Peninsula (WAP) continental shelf in midsummer (January) 2012-2014. Net seasonal-scale changes in water column inventories (0-150 m) of nitrate and iodide were also estimated at the same stations. The average daily rates based on inventory changes exceeded the shorter-term rate measurements. A major uncertainty in the relative magnitude of the inventory estimates is specifying the start of the growing season following sea-ice retreat. New P and NCP(O2) did not differ significantly. New P and NCP(O2) were significantly greater than sinking particle export from thorium-234. We suggest this is a persistent and systematic imbalance and that other processes such as vertical mixing and advection of suspended particles are important export pathways.This article is part of the theme issue 'The marine system of the west Antarctic Peninsula: status and strategy for progress in a region of rapid change'.

Mesoscale ocean fronts enhance carbon export due to gravitational sinking and subduction.

Enhanced vertical carbon transport (gravitational sinking and subduction) at mesoscale ocean fronts may explain the demonstrated imbalance of new production and sinking particle export in coastal upwelling ecosystems. Based on flux assessments from 238U:234Th disequilibrium and sediment traps, we found 2 to 3 times higher rates of gravitational particle export near a deep-water front (305 mg C⋅m-2⋅d-1) compared with adjacent water or to mean (nonfrontal) regional conditions. Elevated particle flux at the front was mechanistically linked to Fe-stressed diatoms and high mesozooplankton fecal pellet production. Using a data assimilative regional ocean model fit to measured conditions, we estimate that an additional ∼225 mg C⋅m-2⋅d-1 was exported as subduction of particle-rich water at the front, highlighting a transport mechanism that is not captured by sediment traps and is poorly quantified by most models and in situ measurements. Mesoscale fronts may be responsible for over a quarter of total organic carbon sequestration in the California Current and other coastal upwelling ecosystems.

Phytoplankton production and taxon-specific growth rates in the Costa Rica Dome.

During summer 2010, we investigated phytoplankton production and growth rates at 19 stations in the eastern tropical Pacific, where winds and strong opposing currents generate the Costa Rica Dome (CRD), an open-ocean upwelling feature. Primary production (14C-incorporation) and group-specific growth and net growth rates (two-treatment seawater dilution method) were estimated from samples incubated in situ at eight depths. Our cruise coincided with a mild El Niño event, and only weak upwelling was observed in the CRD. Nevertheless, the highest phytoplankton abundances were found near the dome center. However, mixed-layer growth rates were lowest in the dome center (∼0.5-0.9 day-1), but higher on the edge of the dome (∼0.9-1.0 day-1) and in adjacent coastal waters (0.9-1.3 day-1). We found good agreement between independent methods to estimate growth rates. Mixed-layer growth rates of Prochlorococcus and Synechococcus were largely balanced by mortality, whereas eukaryotic phytoplankton showed positive net growth (∼0.5-0.6 day-1), that is, growth available to support larger (mesozooplankton) consumer biomass. These are the first group-specific phytoplankton rate estimates in this region, and they demonstrate that integrated primary production is high, exceeding 1 g C m-2 day-1 on average, even during a period of reduced upwelling.

Net biogenic silica production and the contribution of diatoms to new production and organic matter export in the Costa Rica Dome ecosystem.

We determined the net rate of biogenic silica (bSiO2) production and estimated the diatom contribution to new production and organic matter export in the Costa Rica Dome during summer 2010. The shallow thermocline significantly reduces bSiO2 dissolution rates below the mixed layer, leading to significant enhancement of bSiO2 relative to organic matter (silicate-pump condition). This may explain why deep export of bSiO2 in this region is elevated by an order of magnitude relative to comparable systems. Diatom carbon, relative to autotrophic carbon, was low (<3%); however, the contribution of diatoms to new production averaged 3 and 13% using independent approaches. The 4-old discrepancy between methods may be explained by a low average C:Si ratio (∼1.4) for the net produced diatom C relative to the net produced bSiO2. We speculate that this low production ratio is not the result of reduced C, but may arise from a significant contribution of non-diatom silicifying organisms to bSiO2 production. The contribution of diatoms to organic matter export was minor (5.7%). These results, and those of the broader project, suggest substantial food-web transformation of diatom organic matter in the euphotic zone, which creates enriched bSiO2 relative to organic matter within the exported material.

Mesozooplankton biomass and grazing in the Costa Rica Dome: amplifying variability through the plankton food web.

We investigated standing stocks and grazing rates of mesozooplankton assemblages in the Costa Rica Dome (CRD), an open-ocean upwelling ecosystem in the eastern tropical Pacific. While phytoplankton biomass in the CRD is dominated by picophytoplankton (<2-µm cells) with especially high concentrations of Synechococcus spp., we found high mesozooplankton biomass (∼5 g dry weight m-2) and grazing impact (12-50% integrated water column chlorophyll a), indicative of efficient food web transfer from primary producers to higher levels. In contrast to the relative uniformity in water-column chlorophyll a and mesozooplankton biomass, variability in herbivory was substantial, with lower rates in the central dome region and higher rates in areas offset from the dome center. While grazing rates were unrelated to total phytoplankton, correlations with cyanobacteria (negative) and biogenic SiO2 production (positive) suggest that partitioning of primary production among phytoplankton sizes contributes to the variability observed in mesozooplankton metrics. We propose that advection of upwelled waters away from the dome center is accompanied by changes in mesozooplankton composition and grazing rates, reflecting small changes within the primary producers. Small changes within the phytoplankton community resulting in large changes in the mesozooplankton suggest that the variability in lower trophic level dynamics was effectively amplified through the food web.

The biological pump in the Costa Rica Dome: an open-ocean upwelling system with high new production and low export.

The Costa Rica Dome is a picophytoplankton-dominated, open-ocean upwelling system in the Eastern Tropical Pacific that overlies the ocean's largest oxygen minimum zone. To investigate the efficiency of the biological pump in this unique area, we used shallow (90-150 m) drifting sediment traps and 234Th:238U deficiency measurements to determine export fluxes of carbon, nitrogen and phosphorus in sinking particles. Simultaneous measurements of nitrate uptake and shallow water nitrification allowed us to assess the equilibrium balance of new and export production over a monthly timescale. While f-ratios (new:total production) were reasonably high (0.36 ± 0.12, mean ± standard deviation), export efficiencies were considerably lower. Sediment traps suggested e-ratios (export/14C-primary production) at 90-100 m ranging from 0.053 to 0.067. ThE-ratios (234Th disequilibrium-derived export) ranged from 0.038 to 0.088. C:N and N:P stoichiometries of sinking material were both greater than canonical (Redfield) ratios or measured C:N of suspended particulates, and they increased with depth, suggesting that both nitrogen and phosphorus were preferentially remineralized from sinking particles. Our results are consistent with an ecosystem in which mesozooplankton play a major role in energy transfer to higher trophic levels but are relatively inefficient in mediating vertical carbon flux to depth, leading to an imbalance between new production and sinking flux.

Phytoplankton production and grazing balances in the Costa Rica Dome.

We investigated phytoplankton production rates and grazing fates in the Costa Rica Dome (CRD) during summer 2010 based on dilution depth profiles analyzed by flow cytometry and pigments and mesozooplankton grazing assessed by gut fluorescence. Three community production estimates, from 14C uptake (1025 ± 113 mg C m-2 day-1) and from dilution experiments analyzed for total Chla (990 ± 106 mg C m-2 day-1) and flow cytometry populations (862 ± 71 mg C m-2 day-1), exceeded regional ship-based values by 2-3-fold. Picophytoplankton accounted for 56% of community biomass and 39% of production. Production profiles extended deeper for Prochlorococcus (PRO) and picoeukaryotes than for Synechococcus (SYN) and larger eukaryotes, but 93% of total production occurred above 40 m. Microzooplankton consumed all PRO and SYN growth and two-third of total production. Positive net growth of larger eukaryotes in the upper 40 m was balanced by independently measured consumption by mesozooplankton. Among larger eukaryotes, diatoms contributed ∼3% to production. On the basis of this analysis, the CRD region is characterized by high production and grazing turnover, comparable with or higher than estimates for the eastern equatorial Pacific. The region nonetheless displays characteristics atypical of high productivity, such as picophytoplankton dominance and suppressed diatom roles.