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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. 

The eastern Indian Ocean is substantially under sampled with respect to the biological carbon pump – the suite of processes that transport the carbon fixed by phytoplankton into the deeper ocean. Using sediment traps and other ecosystem measurements, we quantified sinking organic matter flux and investigated the characteristics of sinking particles in waters overlying the Argo Abyssal Plain directly downstream of the Indonesian Throughflow off northwest Australia. Carbon export from the euphotic zone averaged 7.0 mmol C m􀀀 2 d􀀀 1, which equated to an average export efficiency (export/net primary production) of 0.19. Sinking particle flux within the euphotic zone (beneath the mixed layer, but above the deep chlorophyll maximum) averaged slightly higher than flux at the base of the euphotic zone, suggesting that the deep euphotic zone was a depth stratum of net particle remineralization. Carbon flux attenuation continued into the twilight zone with a transfer efficiency (export at euphotic depth + 100m/export at euphotic depth) of 0.62 and an average Martin's b-value of 1.1. Within the euphotic zone, fresh phytoplankton (chlorophyll associated with sinking particles, possibly contained within appendicularian houses) were an important component of sinking particles, but beneath the euphotic zone the fecal pellets of herbivorous zooplankton (phaeopigments) were more important. Changes in carbon and nitrogen isotopic composition with depth further reflected remineralization processes occurring as particles sank. We show similarities with biological carbon pump functioning in a similar semi-enclosed oligotrophic marginal sea, the Gulf of Mexico, including net remineralization across the deep chlorophyll maximum. 

Phytoplankton, the foundational organisms in ocean food webs, have been little studied in the Indonesian Throughflow region of the eastern Indian Ocean, the spawning area of Southern Bluefin Tuna. Here, we assess phytoplankton abundance, biomass, size structure, pigment composition, taxonomic diversity and percent functional mixotrophs of that region based on complementary approaches of flow cytometry, microscopy, taxonspecific pigments and rRNA gene sequencing. During summer (January–February) 2022, the region was characterized by warm (up to 30.5 ◦C), stratified, oligotrophic (nitrogen-limited) waters, with integrated euphotic zone (EZ) chlorophyll a (CHLa) of 13 mg m−2. EZ mean CHLa was low in the upper layer (85 ng L−1) and 3.8 times higher (320 ng L−1) at the pronounced deep CHLa maximum. EZ-integrated phytoplankton carbon averaged 1229 mg C m−2. Prochlorococcus dominated throughout the EZ, but eukaryotic carbon biomass was ~4- times greater in the lower than upper EZ, along with a distinct community. In the upper EZ, haptophytes, dinoflagellates and prasinophycean taxa without prasinoxanthin contributed most to monovinyl chlorophyll a (MV-CHLa). In the more diverse lower EZ, haptophytes, dinoflagellates, prasinophycean taxa with prasinoxanthin, pelagophytes, and cryptophytes were the main contributors to MV-CHLa. Diatoms were a minor part of the community. A higher percentage of the upper EZ community showed mixotrophy (35–84%) relative to the lower EZ (30–51%). Nitrogen-fixing organisms (as symbionts of diatoms and free-living cyanobacteria taxa) were ubiquitous, but low in abundance. Overall, community characteristics were similar to those at the Hawaii Ocean Time-series site and the central Gulf of Mexico. 

Plankton sampling was undertaken across the 5000 m deep Argo Abyssal Plain (hereafter Argo Basin), the only known spawning region for Southern Bluefin Tuna (SBT). The Continuous Plankton Recorder was towed from Darwin across the Northern Australian shelf to the Argo Basin and bottle and net samples collected during experimental studies in the southern Argo Basin. Larger diatoms (>15 μm) were the main phytoplankton group that distinguished Coastal shelf from Slope and Argo Basin provinces, with higher diatom and total cell abundances, higher diatom diversity and a higher ratio of diatoms to dinoflagellates in Coastal waters. We confirm the descriptions of the phytoplankton provinces defined from historical data and show that zooplankton distributions follow a similar pattern in terms of abundance but not diversity. The shelf-slope province boundary also occurred further east than in historical records. Whilst this region of the Indian Ocean is characterised by low productivity compared to other Eastern Boundary Current regions, tropical storms during the SBT spawning season are shown to be important for stimulating productivity and increasing abundances of zooplankton prey for tuna larvae. Results of this study solidify prior knowledge from this poorly studied area and highlight the need to better understand the ephemeral dynamics of plankton communities of this region. 

We investigated ontogenetic variability in feeding and prey selection by Southern Bluefin Tuna larvae (SBT; Thunnus maccoyii) in their only global spawning region, located in the eastern Indian Ocean between northwestern Australia and Indonesia. Zooplankton prey and SBT larvae were sampled during four multi-day Lagrangian experiments conducted in the southern Argo Basin during the peak midsummer spawning season in January–February 2022. The zooplankton were identified, enumerated, sizes measured, and their developmental stages ascertained both in situ and from the stomach contents of the larvae. Larval stomach contents revealed high feeding incidence of 95 % with at least one prey item ingested with an average of 3.9 zooplankton prey per larva. Diet and prey selection transitioned during larval ontogeny from copepod nauplii to calanoid and corycaeid copepodites, and ultimately to cladocerans, as well as fish larvae when these were available. However, for all developmental stages and experiments, appendicularians stood out as the most significant prey taxon, constituting an average of 57 % of prey carbon biomass consumed and up to 79 % for postflexion stages. We observed some indication of increasing selection for appendicularians and fish larvae where they were most abundant, even when other suitable prey items were more readily available. Our study documents unprecedented high feeding incidence and positive selection for appendicularians compared to previous investigations of bluefin species, highlighting a pathway that enhances food web transfer efficiency. Appendicularians are uniquely able to thrive in oligotrophic environments and could be an optimal food source supporting SBT larvae in the future ocean. 

Maternal effects play a fundamental role in shaping early larval growth and survival in marine fishes. This study explores the relationship between maternal trophic ecology and larval growth in bluefin tunas, with a focus on Southern Bluefin Tuna (SBT) and an expanded dataset from multiple Atlantic Bluefin Tuna (ABT) populations incorporated into the General Bluefin Model (GBM). Daily growth and stable isotopes (δ15N and δ13C) were obtained from 80 pre-flexion SBT larvae and 355 pre-flexion larvae from the GBM dataset. Results revealed a significant negative linear trend between larval age and δ15N values, consistent with the gradual attenuation of maternally inherited isotopic signatures during development. Faster growing larvae showed significantly lower δ15N and δ13C values, indicating that maternal trophic behaviour and prey sources critically influence larval growth potential. Maternal isotopic niche breadth, inferred from larval isotope data, was markedly narrower in groups with optimal larval growth, suggesting that specialized (stenophagous) maternal feeding strategies promote enhanced offspring performance. These patterns were observed consistently in two bluefin species across seven different populations, despite geographic and temporal variability, highlighting a robust ecological link between maternal foraging behaviour and larval development. From these findings, we introduce the hypothesis of an Optimal Maternal Feeding Isotopic Niche, representing a constrained isotopic range associated with increased larval growth and survival. This framework advances our understanding of the influence of maternal trophic ecology on offspring fitness and offers valuable insights for the conservation and management of highly migratory pelagic species with complex reproductive strategies. 

The Argo Basin, located in the eastern Indian Ocean off northwestern Australia, is the primary spawning ground for Southern Bluefin Tuna (Thunnus maccoyii). Understanding the environmental drivers of larval distribution in this region is essential to anticipate potential climate impacts. Using data from the BLOOFINZ cruise, we applied spatially explicit Bayesian models with Tweedie likelihoods to evaluate the influence of sea surface temperature, sea level anomaly, sea surface salinity, chlorophyll-a concentration, bathymetry, and seabed aspect on larval density (density standardized by filtered volume). The best-supported model revealed strong nonlinear responses to temperature, mesoscale activity, and depth. Larval density increased with warmer surface waters, peaked at intermediate depths, and was highest under moderate sea level anomalies, suggesting that retention and feeding conditions are maximized under these circumstances. Seabed aspect had a negative effect, consistent with topography-flow interactions that can reduce retention. The spatial component of the model identified a hotspot of larval density in the southern–southwestern basin and lower density toward the north, with lowest uncertainty in well-sampled central areas. Projections for 2050 under a mid-range climate scenario indicated a heterogeneous redistribution of suitable larval habitat, with declines in central and southeastern spawning areas and increases toward the northeast. These findings highlight the sensitivity of Southern Bluefin Tuna larvae to oceanographic conditions and climate change, and they emphasize the need for adaptive, climate-informed management of spawning habitats. 

The region off northwestern Australia in the eastern Indian Ocean is an oligotrophic open-ocean ecosystem characterized by low nutrients and high stratification, and is the only known spawning ground for Southern Bluefin Tuna (SBT). We conducted four multi-day Lagrangian experiments (cycles) and transect sampling to investigate plankton trophic flows during the peak SBT spawning season (Jan–Feb 2022). These cycles were carried out after recent storm mixing and subsequent warming and stratification of the water column. We quantified mesozooplankton size-fractionated biomass and grazing, targeting processes that coincide with SBT larval habitat (upper 30 m) and the full euphotic zone (150 m). Higher grazing occurred in the upper 30 m at the start of our study, coinciding with the deeper mixed layer. Euphotic-zone integrated grazing peaked later, coinciding with higher stratification and increased abundance of diatoms at depth. Mesozooplankton grazing impact averaged 0.11 ± 0.01 d-1 for the region, equivalent to 21.2 % of phytoplankton growth. Combined with microzooplankton grazing removals, phytoplankton growth and total zooplankton grazing losses were approximately in balance for the euphotic zone. While direct consumption of phytoplankton only supported respiratory needs of a portion of the assemblage in two of the four experimental cycles, respiratory and production needs were largely met by including the consumption of microzooplankton production. Thus, the production of mesozooplankton prey required to sustain SBT larvae in this nutrient-poor environment was obtained by both high grazing and efficient trophic coupling. This study highlights the role of metazoan zooplankton in warm oligotrophic waters of the eastern tropical Indian Ocean, and indicates that efficient ecosystem transfer can be achieved even under conditions assumed to severely limit production and biomass accumulation. 

Oligotrophic ocean regions are characterized by strong nutrient limitation, low standing phytoplankton biomass, and highly efficient nutrient recycling. During the BLOOFINZ-IO expedition (February 2022), we quantified nutrient inventories, primary productivity and N2 fixation in the Argo Basin of the eastern Indian Ocean, the sole known spawning ground for Southern Bluefin Tuna. Low concentrations of surface nitrate (<0.02 μmol L−1) and persistent residual phosphate indicated N as the limiting macronutrient, with photophysiological indices consistent with iron colimitation. Depth-integrated net primary production (NPP), from 14C-based in-situ incubations during 4 Lagrangian experiments, averaged ~460 mg C m−2d−1, generally agreeing with mean satellite-based NPP estimates (459 mg C m−2d−1) but with spatial discrepancies. Nitrogen fixation provided a consistent new nitrogen source, contributing ~16 % to local NPP in the upper euphotic zone. Gross primary production (GPP), from fast-repetition-rate-fluorometry-based estimates of electron transport, revealed significant autotrophic respiration losses, with mean GPP:NPP ratios of ~1.8 consistent with metabolic costs under nutrient limitation. Net community production (NCP) from O2/Ar ratios averaged ~20 % of NPP in the upper 30 m. This result, in combination with N2 fixation measurement, indicates that N2 fixation supports most of the export production in the region. Together, the multimethod approach revealed a recycling-dominated ecosystem affected by episodic mixing events, where primary productivity is maintained primarily through efficient nitrogen recycling and physiological photoacclimation. These results provide a comprehensive baseline of bottom-up support of ecosystem productivity for the Argo Basin for assessing future climate-driven changes in stratification, nutrient cycling, and food-web dynamics. 

This study analyzed the growth patterns and survival of Southern bluefin tuna (SBT, Thunnus maccoyii) larvae collected during January–February 2022 in their only known spawning area in the eastern Indian Ocean (IO). Otolith microstructure was examined to characterize both population-level and intra-population growth (OPToptimal and DEF-deficient group), with special emphasis on the flexion process, as well as to provide insights into larval survival. SBT larvae began flexion at sizes and ages comparable to those reported in other bluefin tuna species. At the intra-population level, OPT larvae reached flexion earlier in a better physical condition, with greater length, weight, and body depth, likely increasing their chances of survival at later stages. The observed larval growth rates (0.38 mm d−1) exceeded that from a historical study in 1987 (0.33 mm d−1), likely due to a ~2 ◦C increase in sea surface temperature and shifts in prey availability. Larval survival appears to depend on a selective process based on growth, in which only a small proportion of individuals (<2 %) exhibited width increment in otoliths similar to those of surviving larvae, allowing for faster development and earlier access to larger prey. These findings highlight the need for expanded research on the early life stages of SBT, particularly in the context of ongoing ocean warming and climate change.