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.

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.

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.

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.

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.

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.

Factors affecting Fe and Zn contents of mesozooplankton from the Costa Rica Dome.

Mineral limitation of mesozooplankton production is possible in waters with low trace metal availability. As a step toward estimating mesozooplankton Fe and Zn requirements under such conditions, we measured tissue concentrations of major and trace nutrient elements within size-fractioned zooplankton samples collected in and around the Costa Rica Upwelling Dome, a region where phytoplankton growth may be co-limited by Zn and Fe. The geometric mean C, N, P contents were 27, 5.6 and 0.21 mmol gdw-1, respectively. The values for Fe and Zn were 1230 and 498 nmol gdw-1, respectively, which are low compared with previous measurements. Migrant zooplankton caused C and P contents of the 2-5 mm fraction to increase at night relative to the day while the Fe and Zn contents decreased. Fe content increased with size while Zn content decreased with size. Fe content was strongly correlated to concentrations of two lithogenic tracers, Al and Ti. We estimate minimum Fe:C ratios in large migrant and resident mixed layer zooplankton to be 15 and 60 µmol mol-1, respectively. The ratio of Zn:C ranged from 11 µmol mol-1 for the 0.2-0.5 mm size fraction to 33 µmol mol-1 for the 2-5 mm size fraction.

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.