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Abstract The current conventional paradigm of ocean food web structure inserts one full level or more of microzooplankton heterotrophic consumption, a substantial energy drop, between phytoplankton and mesozooplankton. Using a dataset with contemporaneous measurements of primary production (PP), size-fractioned mesozooplankton biomass, and micro- and mesozooplankton grazing rates from 10 tropical to temperate ocean ecosystems, we examined whether the structural inefficiencies in this paradigm allow sufficient energy transfer to support active metabolism and growth of observed zooplankton standing stocks. Zooplankton carbon requirements (ZCR) were determined from allometric equations that account for ecosystem differences in temperature and size structure. ZCRs were relatively low (∼30% of PP or less) for both oligotrophic systems and bloom biomass accumulation in eutrophic coastal waters. Higher relative ZCRs (>30% PP) were associated with elevated mesozooplankton grazing scenarios (bloom declines, abundant salps), advective subsidies, and open-ocean upwelling systems. Microzooplankton generally dominated as grazers of PP but were equal or secondary to direct herbivory as nutritional support for mesozooplankton in five of eight regional studies. All systems were able to satisfy ZCR within the conventional food-web interpretation, but balanced open-ocean upwelling systems required the most efficient alignments of contributions from microzooplankton grazing, direct herbivory, and carnivory to do so. 

Abstract Western Atlantic bluefin tuna (ABT) undertake long-distance migrations from rich feeding grounds in the North Atlantic to spawn in oligotrophic waters of the Gulf of Mexico (GoM). Stock recruitment is strongly affected by interannual variability in the physical features associated with ABT larvae, but the nutrient sources and food-web structure of preferred habitat, the edges of anticyclonic loop eddies, are unknown. Here, we describe the goals, physical context, design and major findings of an end-to-end process study conducted during peak ABT spawning in May 2017 and 2018. Mesoscale features in the oceanic GoM were surveyed for larvae, and five multi-day Lagrangian experiments measured hydrography and nutrients; plankton biomass and composition from bacteria to zooplankton and fish larvae; phytoplankton nutrient uptake, productivity and taxon-specific growth rates; micro- and mesozooplankton grazing; particle export; and ABT larval feeding and growth rates. We provide a general introduction to the BLOOFINZ-GoM project (Bluefin tuna Larvae in Oligotrophic Ocean Foodwebs, Investigation of Nitrogen to Zooplankton) and highlight the finding, based on backtracking of experimental waters to their positions weeks earlier, that lateral transport from the continental slope region may be more of a key determinant of available habitat utilized by larvae than eddy edges per se. 

Abstract 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⁻²d⁻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⁻²d⁻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. 

Abstract Bluefin tuna spawn in restricted areas of subtropical oligotrophic seas. Here, we investigate the zooplankton prey and feeding selectivity of early larval stages of Atlantic bluefin tuna (ABT, Thunnus thynnus) in larval rearing habitat of the Gulf of Mexico. Larvae and zooplankton were collected during two multi-day Lagrangian experiments during peak spawning in May 2017 and 2018. Larvae were categorized by flexion stage and standard length. We identified, enumerated and sized zooplankton from larval gut contents and in the ambient community. Ciliates were quantitatively important (up to 9%) in carbon-based diets of early larvae. As larvae grew, diet composition and prey selection shifted from small copepod nauplii and calanoid copepodites to larger podonid cladocerans, which accounted for up to 70% of ingested carbon. Even when cladoceran abundances were <0.2 m−3, they comprised 23% of postflexion stage diet. Feeding behaviors of larvae at different development stages were more specialized, and prey selection narrowed to appendicularians and primarily cladocerans when these taxa were more abundant. Our findings suggest that ABT larvae have the capacity to switch from passive selection, regulated by physical factors, to active selection of presumably energetically optimal prey. 

Whereas recruitment success for many fisheries depends on coincident timing of larvae with abundance peaks of their prey, less can be more in the tropical/subtropical spawning areas of bluefin tunas if lower but steady food resources are offset by reduced larval vulnerability to pelagic predators. To understand larval habitat characteristics for Southern Bluefin Tuna (SBT), we quantified microbial community carbon flows based on growth and grazing rates from depth profiles of dilution incubations and carbon biomass assessments from microscopy and flow cytometry (FCM) during their peak spawning off NW Australia (Indian Ocean) in February 2022. Two Chla-based estimates of phytoplankton production gave differing offsets due to cycling or mixotrophy, exceeding 14C net community production on average (677 ± 98 versus 447 ± 43 mg C m−2 d−1). Productivity was higher than in the Gulf of Mexico spawning area for Atlantic Bluefin Tuna but less than similar studies of oceanic upwelling regions. Microzooplankton grazing averaged 482 ± 63 mg C m−2 d−1 (71 ± 13 % of production). Two measurement variables for Prochlorococcus gave average production and grazing rates of 282 ± 36 and 248 ± 32 mg C m−2 d−1 (86 ± 6 % grazed). Prochlorococcus comprised almost half of production and grazing fluxes in the upper (0–25 m) euphotic zone where SBT larvae reside. Prochlorococcus declined and eukaryotic phytoplankton and heterotrophic bacteria increased in relative importance in the lower euphotic zone. These results describe relatively classic open-ocean oligotrophic conditions as the food web base for nutritional flows to SBT larvae. 

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. 

Abstract Larval abundances of Atlantic bluefin tuna (ABT) in the Gulf of Mexico are currently utilized to inform future recruitment by providing a proxy for the spawning potential of western ABT stock. Inclusion of interannual variations in larval growth is a key advance needed to translate larval abundance to recruitment success. However, little is known about the drivers of growth variations during the first weeks of life. We sampled patches of western ABT larvae in 3–4 day Lagrangian experiments in May 2017 and 2018, and assessed age and growth rates from sagittal otoliths relative to size categories of zooplankton biomass and larval feeding behaviors from stomach contents. Growth rates were similar, on average, between patches (0.37 versus 0.39 mm d−1) but differed significantly through ontogeny and were correlated with a food limitation index, highlighting the importance of prey availability. Otolith increment widths were larger for postflexion stages in 2018, coincident with high feeding on preferred prey (mainly cladocerans) and presumably higher biomass of more favorable prey type. Faster growth reflected in the otolith microstructures may improve survival during the highly vulnerable larval stages of ABT, with direct implications for recruitment processes.