Phytoplankton community structure and photophysiological strategies in the oligotrophic Indian Ocean spawning ground of Southern Bluefin Tuna

Abstract

The Argo Basin, a persistently oligotrophic seascape downstream of the Indonesian Throughflow (ITF), is the only known spawning ground of Southern Bluefin Tuna (Thunnus maccoyii). Its surface waters are capped by the warm, low saline, nitrate-depleted Pacific Ocean outflow, that leads to intense water-column stratification and chronic nutrient scarcity. During the BLOOFINZ campaign (R/V Roger Revelle, January-March 2022), we combined high-resolution underway surveys with Lagrangian experiments to examine hydrography, nutrient stoichiometry, and phytoplankton photophysiology across the basin. This study was motivated by the need to: 1) identify the phytoplankton communities capable of persisting in this nutrient-impoverished region, and 2) uncover the unique photophysiological traits that underpin their survival and growth, particularly under acute nitrate limitation. Nutrient fields revealed strongly negative N*, positive Si*, and elevated Si:P ratios, indicating a system of acute nitrate scarcity but with residual phosphate and latent silicate availability. Phytoplankton communities were dominated by the cyanobacteria, Prochlorococcus, whose survival strategies included small functional absorption cross section of PSII ({sigma}PSII), enhanced PSII connectivity (p), highly elastic and reversible diel photophysiology that balanced high-light stress and nitrogen scarcity. Longer turnover times especially {tau}2 ({micro}s; PSII-PSI electron transport) seen in the region around 115{degrees} and 120{degrees}E and at 15{degrees}S, and during Cycles 3 and 4 are indicative of populations that were being stressed by Fe limitation as well. Our inference of Prochlorococcus is supported by complimentary measurements of flow cytometry, phytoplankton pigment composition and microscopy all of which confirmed the dominance of Prochlorococcus in these nutrient impoverished waters. Our observations further indicate that mesoscale eddies generated by ITF-SICC (South Indian Counter Current) interactions, can episodically shoal the nutricline, triggering transient pulses of larger eukaryotes. Collectively, these results demonstrate how acute nitrate depletion, compounded by Fe stress, structures a microbial community finely tuned to oligotrophy and capable of sustaining a short food chain involving appendicularians that directly support larval tuna. The Argo Basin therefore exemplifies how circulation-nutrient coupling shapes microbial communities and ecosystem function within a globally significant spawning habitat. Highlights1) Chronic nitrate limitation, with strongly negative N* and persistent N:P imbalance defines the Argo Basin while phosphate and silicate remain in relative excess. 2) Picocyanobacteria especially Prochlorococcus dominate the ecosystem, sustaining productivity under extreme oligotrophy through photophysiological strategies of reduced {sigma}PSII, enhanced PSII connectivity, and diel recovery from light stress. 3) Mesoscale eddies at the ITF-SICC front provide episodic relief, shoaling the nutricline and fueling transient pulses of larger phytoplankton that episodically reshape phytoplankton community structure and biomass 4) This oligotrophic-frontal seascape supports a short, efficient food web, enabling transfer of picophytoplankton to Southern Bluefin Tuna larvae via mainly appendicularians.