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Deep Maxima of Phytoplankton Biomass, Primary Production and Bacterial Production in the Mediterranean Sea

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Deep Maxima of Phytoplankton Biomass, Primary Production and Bacterial Production in the Mediterranean Sea Biogeosciences, 18, 1749–1767, 2021 https://doi.org/10.5194/bg-18-1749-2021 © Author(s) 2021. This work is distributed under the Creative Commons Attribution 4.0 License. Deep maxima of phytoplankton biomass, primary production and bacterial production in the Mediterranean Sea Emilio Marañón1, France Van Wambeke2, Julia Uitz3, Emmanuel S. Boss4, Céline Dimier3, Julie Dinasquet5, Anja Engel6, Nils Haëntjens4, María Pérez-Lorenzo1, Vincent Taillandier3, and Birthe Zäncker6,7 1Department of Ecology and Animal Biology, Universidade de Vigo, 36310 Vigo, Spain 2Mediterranean Institute of Oceanography, Aix-Marseille Université, CNRS, Université de Toulon, CNRS, IRD, MIO UM 110, 13288 Marseille, France 3Laboratoire d’Océanographie de Villefranche, Sorbonne Université, CNRS, 06230 Villefranche-sur-Mer, France 4School of Marine Sciences, University of Maine, Orono, Maine, USA 5Scripps Institution of Oceanography, University of California, San Diego, San Diego, California, USA 6GEOMAR, Helmholtz Centre for Ocean Research Kiel, 24105 Kiel, Germany 7The Marine Biological Association of the United Kingdom, Plymouth, PL1 2PB, United Kingdom Correspondence: Emilio Marañón ([email protected]) Received: 7 July 2020 – Discussion started: 20 July 2020 Revised: 5 December 2020 – Accepted: 8 February 2021 – Published: 15 March 2021 Abstract. The deep chlorophyll maximum (DCM) is a ubiq- 10–15 mgCm−3 at the DCM. As a result of photoacclima- uitous feature of phytoplankton vertical distribution in strati- tion, there was an uncoupling between chlorophyll a-specific fied waters that is relevant to our understanding of the mech- and carbon-specific productivity across the euphotic layer. anisms that underpin the variability in photoautotroph eco- The ratio of fucoxanthin to total chlorophyll a increased physiology across environmental gradients and has impli- markedly with depth, suggesting an increased contribution cations for remote sensing of aquatic productivity. During of diatoms at the DCM. The increased biomass and carbon the PEACETIME (Process studies at the air-sea interface af- fixation at the base of the euphotic zone was associated with ter dust deposition in the Mediterranean Sea) cruise, carried enhanced rates of heterotrophic prokaryotic activity, which out from 10 May to 11 June 2017, we obtained 23 concur- also showed a surface peak linked with warmer temperatures. rent vertical profiles of phytoplankton chlorophyll a, carbon Considering the phytoplankton biomass and turnover rates biomass and primary production, as well as heterotrophic measured at the DCM, nutrient diffusive fluxes across the nu- prokaryotic production, in the western and central Mediter- tricline were able to supply only a minor fraction of the pho- ranean basins. Our main aims were to quantify the relative toautotroph nitrogen and phosphorus requirements. Thus the role of photoacclimation and enhanced growth as underly- deep maxima in biomass and primary production were not ing mechanisms of the DCM and to assess the trophic cou- fuelled by new nutrients but likely resulted from cell sink- pling between phytoplankton and heterotrophic prokaryotic ing from the upper layers in combination with the high pho- production. We found that the DCM coincided with a max- tosynthetic efficiency of a diatom-rich, low-light acclimated imum in both the biomass and primary production but not community largely sustained by regenerated nutrients. Fur- in the growth rate of phytoplankton, which averaged 0.3 d−1 ther studies with increased temporal and spatial resolution and was relatively constant across the euphotic layer. Pho- will be required to ascertain if the peaks of deep primary pro- toacclimation explained most of the increased chlorophyll a duction associated with the DCM persist across the western at the DCM, as the ratio of carbon to chlorophyll a (C V Chl a) and central Mediterranean Sea throughout the stratification decreased from ca. 90–100 (g V g) at the surface to 20–30 season. at the base of the euphotic layer, while phytoplankton car- bon biomass increased from ca. 6 mgCm−3 at the surface to Published by Copernicus Publications on behalf of the European Geosciences Union. 1750 E. Marañón et al.: Deep maxima of phytoplankton biomass and production 1 Introduction maximum that manifests as a peak in beam attenuation or backscattering (Mignot et al., 2014). Both ends of this trophic One of the most remarkable features of phytoplankton distri- gradient can be found in the Mediterranean Sea along its bution in lakes and oceans is the presence of a deep chloro- well-known longitudinal trend in nutrient availability, phy- phyll maximum (DCM), typically located at the base of the toplankton biomass and productivity (Antoine et al., 1995; euphotic layer and coinciding with the top of the nutricline, D’Ortenzio and Ribera d’Alcalà, 2009; Lavigne et al., 2015). which occurs in permanently and seasonally stratified wa- Using data from Biogeochemical-Argo (BGC-Argo) profil- ter columns (Herbland and Voituriez, 1979; Cullen, 2015). ing floats deployed throughout the Mediterranean, Barbieux Multiple mechanisms that are not mutually exclusive may et al. (2019) established general patterns in the distribution contribute to the development of a DCM, including pho- and seasonal dynamics of biomass (estimated from the par- toacclimation (the increase in cellular chlorophyll content ticulate backscattering coefficient) and chlorophyll subsur- as a response to low-light conditions) (Geider, 1987), en- face maxima. They found that in the western Mediterranean hanced growth conditions at the layer where elevated nu- Sea, during late spring and summer, a subsurface biomass trient diffusion from below coexists with still sufficient ir- maximum develops that coincides with a chlorophyll max- radiance (Beckmann and Hense, 2007), a decrease in sink- imum and is located roughly at the same depth as the nu- ing rates near the pycnocline (Lande and Wood, 1987), and tricline and above the 0.3 molquantam−2 d−1 isolume. In changes in buoyancy regulation or swimming behaviour of contrast, in the Ionian and Levantine seas the DCM, which cells (Durham and Stocker, 2012). Photoacclimation is a has a smaller magnitude, arises solely from photoacclima- rapid process that takes place in a matter of hours (Fisher tion and is located well above the nutricline at a depth that et al., 1996), and therefore part of the increased chloro- corresponds closely with the 0.3 molquantam−2 d−1 isol- phyll concentration at the DCM is always the result of a de- ume (Barbieux et al., 2019). The presence of a subsurface crease in the ratio of phytoplankton carbon to chlorophyll a or deep biomass maximum may suggest that a particularly (C V Chl a), which results mainly from decreased irradiance favourable combination of light and nutrients occurs at that but is also favoured by enhanced nutrient supply (Geider et depth, leading to enhanced phytoplankton growth and new al., 1996). Although the role of photoacclimation, particu- production. It remains unknown, however, whether phyto- larly in strongly oligotrophic environments, has long been plankton growth and biomass turnover rates are actually acknowledged (Steele, 1964), the fact that Chl a is used rou- higher at the depth of the biomass maximum. An additional tinely as a surrogate for photoautotrophic biomass has helped source of uncertainty is that both the particulate attenuation to fuel the assumption, often found in the scientific litera- and backscattering coefficients relate not only to phytoplank- ture and in textbooks, that the DCM is always a maximum ton abundance but to the entire pool of particles, including in the biomass and, by extension, the growth rate of phy- non-algal and detrital particles, which are known to con- toplankton. The assessment of total phytoplankton biomass tribute significantly to total suspended matter in oligotrophic along vertical gradients has been traditionally hindered by regions (Claustre et al., 1999). Combining direct and specific the time-consuming nature of microscopy techniques, but the measurements of phytoplankton production (with the 14C up- increasing use of optical properties such as the particulate take technique) and biovolume (with flow cytometry) offers beam attenuation and backscattering coefficients to estimate a way to determine photoautotrophic biomass turnover rates the concentration of suspended particles in the water col- (Kirchman, 2002; Marañón et al., 2014) and thus gain further umn (Martinez-Vicente et al., 2013; Behrenfeld et al., 2016) insight into the dynamics and underlying mechanisms of the has allowed for the characterization of biogeographic and DCM. By investigating concurrently the vertical variability seasonal patterns in the vertical variability of phytoplankton in heterotrophic prokaryotic production in relation to phyto- chlorophyll and biomass in stratified environments (Fennel plankton standing stocks and productivity, it is also possible and Boss, 2003; Mignot et al., 2014; Cullen, 2015). to ascertain potential implications of the DCM for trophic It is now established that the nature of the DCM changes coupling within the microbial-plankton community. fundamentally along a gradient of thermal stability and nu- The PEACETIME (Process studies at the air-sea interface trient availability (Cullen, 2015). In the oligotrophic ex- after dust deposition in the Mediterranean Sea) cruise, which treme, represented by permanently stratified regions such as investigated atmospheric deposition fluxes and their impact the subtropical
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