Maternal Effects and Trophodynamics Drive Interannual Larval Growth Variability of Atlantic Bluefin Tuna (Thunnus thynnus) from the Gulf of Mexico.

Two cohorts of Atlantic bluefin tuna (Thunnus thynnus) larvae were sampled in 2017 and 2018 during the peak of spawning in the Gulf of Mexico (GOM). We examined environmental variables, daily growth, otolith biometry and stable isotopes and found that the GOM18 cohort grew at faster rates, with larger and wider otoliths. Inter and intra-population analyses (deficient vs. optimal growth groups) were carried out for pre- and post-flexion developmental stages to determine maternal and trophodynamic influences on larval growth variability based on larval isotopic signatures, trophic niche sizes and their overlaps. For the pre-flexion stages in both years, the optimal growth groups had significantly lower δ15N, implying a direct relationship between growth potential and maternal inheritance. Optimal growth groups and stages for both years showed lower C:N ratios, reflecting a greater energy investment in growth. The results of this study illustrate the interannual transgenerational trophic plasticity of a spawning stock and its linkages to growth potential of their offsprings in the GOM.

Anchovy boom and bust linked to trophic shifts in larval diet.

Although massive biomass fluctuations of coastal-pelagic fishes are an iconic example of the impacts of climate variability on marine ecosystems, the mechanisms governing these dynamics are often elusive. We construct a 45-year record of nitrogen stable isotopes measured in larvae of Northern Anchovy (Engraulis mordax) in the California Current Ecosystem to assess patterns in food chain length. Larval trophic efficiency associated with a shortened food chain increased larval survival and produced boom periods of high adult biomass. In contrast, when larval food chain length increased, and energy transfer efficiency decreased, the population crashed. We propose the Trophic Efficiency in Early Life (TEEL) hypothesis, which states that larval fishes must consume prey that confer sufficient energy for survival, to help explain natural boom-bust dynamics of coastal pelagic fishes. Our findings illustrate a potential for trophic indicators to generally inform larval survival and adult population dynamics of coastal-pelagic fishes.

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".

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.

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.

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.

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.

A Cryptic Marine Ciliate Feeds on Progametes of Noctiluca scintillans.

The dinoflagellate Noctiluca scintillans (Noctiluca) has the ability to reproduce sexually, which may help to increase or restore its population size during periods of blooms or environmental stress. Here, we documented for the first time a marine ciliate Strombidium sp. that feeds on Noctiluca's progametes undergoing stages 5 to 9 of nuclear division. This ciliate frequently swam on or around gametogenic and some vegetative Noctiluca cells. The ciliates associated with gametogenic cells had significantly lower swimming speed and changed direction more frequently than those associated with vegetative cells, which overall increased their time spent around the food patches (progametes). This trophic interaction constitutes an upside-down predator-prey link, in which ciliates within the typical size range of Noctiluca prey, become the predators. Based on the phylogenetic tree (maximum-likelihood), there are 14 environmental clones similar to Strombidium sp. found in other coastal waters, where Noctiluca presence or blooms have been reported. This novel predator-prey relationship could therefore be common in other Noctiluca habitats. Additional studies are needed to assess the magnitude of its impacts on Noctiluca population dynamics and plankton bloom succession.

Zooplankton and the Ocean Carbon Cycle.

Marine zooplankton comprise a phylogenetically and functionally diverse assemblage of protistan and metazoan consumers that occupy multiple trophic levels in pelagic food webs. Within this complex network, carbon flows via alternative zooplankton pathways drive temporal and spatial variability in production-grazing coupling, nutrient cycling, export, and transfer efficiency to higher trophic levels. We explore current knowledge of the processing of zooplankton food ingestion by absorption, egestion, respiration, excretion, and growth (production) processes. On a global scale, carbon fluxes are reasonably constrained by the grazing impact of microzooplankton and the respiratory requirements of mesozooplankton but are sensitive to uncertainties in trophic structure. The relative importance, combined magnitude, and efficiency of export mechanisms (mucous feeding webs, fecal pellets, molts, carcasses, and vertical migrations) likewise reflect regional variability in community structure. Climate change is expected to broadly alter carbon cycling by zooplankton and to have direct impacts on key species.

Technical comment on Boersma et al. (2016) Temperature driven changes in the diet preference of omnivorous copepods: no more meat when it's hot? Ecology Letters, 19, 45-53.

A recent study concluded that omnivorous plankton will shift from predatory to herbivorous feeding with climate warming, as consumers require increased carbon:phosphorous in their food. Although this is an appealing hypothesis, we suggest the conclusion is unfounded, based on the data presented, which seem in places questionable and poorly interpreted.

Patterns of microbial community biomass, composition and HPLC diagnostic pigments in the Costa Rica upwelling dome.

We investigated biomass, size-structure, composition, depth distributions and spatial variability of the phytoplankton community in the Costa Rica Dome (CRD) in June-July 2010. Euphotic zone profiles were sampled daily during Lagrangian experiments in and out of the dome region, and the community was analyzed using a combination of digital epifluorescence microscopy, flow cytometry and HPLC pigments. The mean depth-integrated biomass of phytoplankton ranged 2-fold, from 1089 to 1858 mg C m-2 (mean ± SE = 1378 ± 112 mg C m-2), among 4 water parcels tracked for 4 days. Corresponding mean (±SE) integrated values for total chlorophyll a (Chl a) and the ratio of autotrophic carbon to Chl a were 24.1 ± 1.5 mg Chl a m-2 and 57.5 ± 3.4, respectively. Absolute and relative contributions of picophytoplankton (∼60%), Synechococcus (>33%) and Prochlorococcus (17%) to phytoplankton community biomass were highest in the central dome region, while >20 µm phytoplankton accounted for ≤10%, and diatoms <2%, of biomass in all areas. Nonetheless, autotrophic flagellates, dominated by dinoflagellates, exceeded biomass contributions of Synechococcus at all locations. Order-of-magnitude discrepancies in the relative contributions of diatoms (overestimated) and dinoflagellates (underestimated) based on diagnostic pigments relative to microscopy highlight potential significant biases associated with making community inferences from pigments.

Plankton dynamics and biogeochemical fluxes in the Costa Rica Dome: introduction to the CRD Flux and Zinc Experiments.

The Costa Rica Dome (CRD) is an open-ocean upwelling system in the Eastern Tropical Pacific that overlies the ocean's largest oxygen minimum zone (OMZ). The region has unique characteristics, biomass dominance by picophytoplankton, suppressed diatoms, high biomass of higher consumers and presumptive trace metal limitation, but is poorly understood in terms of pelagic stock and process relationships, including productivity and production controls. Here, we describe the goals, project design, physical context and major findings of the Flux and Zinc Experiments cruise conducted in June-July 2010 to assess trophic flux relationships and elemental controls on phytoplankton in the CRD. Despite sampling during a year of suppressed summertime surface chlorophyll, cruise results show high productivity (∼1 g C m-2 day-1), high new production relative to export, balanced production and grazing, disproportionate biomass-specific productivity of large phytoplankton and high zooplankton stocks. Zinc concentrations are low in surface waters relative to phosphorous and silicate in other regions, providing conditions conducive to picophytoplankton, like Synechococcus, with low Zn requirements. Experiments nonetheless highlight phytoplankton limitation or co-limitation by silicic acid, driven by a strong silica pump that is linked to low dissolution of biogenic silica in the cold shallow thermocline of the lower euphotic zone.

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.

Biomass and composition of protistan grazers and heterotrophic bacteria in the Costa Rica Dome during summer 2010.

We investigated biomass and composition of heterotrophic microbes in the Costa Rica Dome during June-July 2010 as part of a broader study of plankton trophic dynamics. Because picophytoplankton (<2 µm) are known to dominate in this unique upwelling region, we hypothesized tight biomass relationships between size-determined predator-prey pairs (i.e. picoplankton-nano-grazers, nanoplankton-micro-grazers) within the microbial community. Integrated biomass of heterotrophic bacteria ranged from 180 to 487 mg C m-2 and was significantly correlated with total autotrophic carbon. Heterotrophic protist (H-protist) biomass ranged more narrowly from 488 to 545 mg C m-2, and was comprised of 60% dinoflagellates, 30% other flagellates and 11% ciliates. Nano-sized (<20 µm) protists accounted for the majority (57%) of grazer biomass and were positively correlated with picoplankton, partially supporting our hypothesis, but nanoplankton and micro-grazers (>20 µm) were not significantly correlated. The relative constancy of H-protist biomass among locations despite clear changes in integrated autotrophic biomass, Chl a, and primary production suggests that mesozooplankton may exert a tight top-down control on micro-grazers. Biomass-specific consumption rates of phytoplankton by protistan grazers suggest an instantaneous growth rate of 0.52 day-1 for H-protists, similar to the growth rate of phytoplankton and consistent with a trophically balanced ecosystem dominated by pico-nanoplankton interactions.

Preferential depletion of zinc within Costa Rica upwelling dome creates conditions for zinc co-limitation of primary production.

The Costa Rica Dome (CRD) is a wind-driven feature characterized by high primary production and an unusual cyanobacterial bloom in surface waters. It is not clear whether this bloom arises from top-down or bottom-up processes. Several studies have argued that trace metal geochemistry within the CRD contributes to the composition of the phytoplankton assemblages, since cyanobacteria and eukaryotic phytoplankton have different transition metal requirements. Here, we report that total dissolved zinc (Zn) is significantly depleted relative to phosphate (P) and silicate (Si) within the upper water column of the CRD compared with other oceanic systems, and this may create conditions favorable for cyanobacteria, which have lower Zn requirements than their eukaryotic competitors. Shipboard grow-out experiments revealed that while Si was a limiting factor under our experimental conditions, additions of Si and either iron (Fe) or Zn led to higher biomass than Si additions alone. The addition of Fe and Zn alone did not lead to significant enhancements. Our results suggest that the depletion of Zn relative to P in upwelled waters may create conditions in the near-surface waters that favor phytoplankton with low Zn requirements, including cyanobacteria.

Microplankton trace element contents: implications for mineral limitation of mesozooplankton in an HNLC area.

Mesozooplankton production in high-nutrient low-chlorophyll regions of the ocean may be reduced if the trace element concentrations in their food are insufficient to meet growth and metabolic demands. We used elemental microanalysis (SXRF) of single-celled plankton to determine their trace metal contents during a series of semi-Lagrangian drift studies in an HNLC upwelling region, the Costa Rica Dome (CRD). Cells from the surface mixed layer had lower Fe:S but higher Zn:S and Ni:S than those from the subsurface chlorophyll maximum at 22-30 m. Diatom Fe:S values were typically 3-fold higher than those in flagellated cells. The ratios of Zn:C in flagellates and diatoms were generally similar to each other, and to co-occurring mesozooplankton. Estimated Fe:C ratios in flagellates were lower than those in co-occurring mesozooplankton, sometimes by more than 3-fold. In contrast, Fe:C in diatoms was typically similar to that in zooplankton. RNA:DNA ratios in the CRD were low compared with other regions, and were related to total autotrophic biomass and weakly to the discrepancy between Zn:C in flagellated cells and mesozooplankton tissues. Mesozooplankton may have been affected by the trace element content of their food, even though trace metal limitation of phytoplankton was modest at best.

Phytoplankton growth and microzooplankton grazing dynamics across vertical environmental gradients determined by transplant in situ dilution experiments.

The Costa Rica Dome (CRD) represents a classic case of the bloom-forming capacity of small phytoplankton. Unlike other upwelling systems, autotrophic biomass in the CRD is dominated by picocyanobacteria and small eukaryotes that outcompete larger diatoms and reach extremely high biomass levels. We investigated responses of the subsurface phytoplankton community of the CRD to changes associated with vertical displacement of water masses, coupling in situ transplanted dilution experiments with flow cytometry and epifluorescence microscopy to assess group-specific dynamics. Growth rates of Synechococcus (SYN) and photosynthetic picoeukaryotes (PEUK) were positively correlated with light (Rpearson_SYN = 0.602 and Rpearson_PEUK = 0.588, P < 0.001). Growth rates of Prochlorococcus (PRO), likely affected by photoinhibition, were not light correlated (Rpearson_PRO = 0.101, P = 0.601). Overall, grazing and growth rates were closely coupled in all picophytoplankton groups (Rspearman_PRO = 0.572, Rspearman_SYN = 0.588, Rspearman_PEUK = 0.624), and net growth rates remained close to zero. Conversely, the abundance and biomass of larger phytoplankton, mainly diatoms, increased more than 10-fold in shallower transplant incubations indicating that, in addition to trace-metal chemistry, light also plays a significant role in controlling microphytoplankton populations in the CRD.

Biological response of Costa Rica Dome phytoplankton to Light, Silicic acid and Trace metals.

The Costa Rica Dome (CRD) is a unique open-ocean upwelling system, with picophytoplankton dominance of phytoplankton biomass and suppressed diatoms, yet paradoxically high export of biogenic silica. As a part of Flux and Zinc Experiments cruise in summer (June-July 2010), we conducted shipboard incubation experiments in the CRD to examine the potential roles of Si, Zn, Fe and light as regulating factors of phytoplankton biomass and community structure. Estimates of photosynthetic quantum yields revealed an extremely stressed phytoplankton population that responded positively to additions of silicic acid, iron and zinc and higher light conditions. Size-fractioned Chl a yielded the surprising result that picophytoplankton, as well as larger phytoplankton, responded most to treatments with added silicic acid incubated at high incident light (HL + Si). The combination of Si and HL also led to increases in cell sizes of picoplankton, notably in Synechococcus. Such a response, coupled with the recent discovery of significant intracellular accumulation of Si in some picophytoplankton, suggests that small phytoplankton could play a potentially important role in Si cycling in the CRD, which may help to explain its peculiar export characteristics.