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Distribution of Phytoplankton Groups Within the Deep Chlorophyll Maximum

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Distribution of Phytoplankton Groups Within the Deep Chlorophyll Maximum LIMNOLOGY and Limnol. Oceanogr. 62, 2017, 665–685 VC 2016 The Authors Limnology and Oceanography published by Wiley Periodicals, Inc. OCEANOGRAPHY on behalf of Association for the Sciences of Limnology and Oceanography doi: 10.1002/lno.10452 Distribution of phytoplankton groups within the deep chlorophyll maximum Mikel Latasa, 1* Ana Mar ıa Cabello, 2 Xos e Anxelu G. Mor an, 3 Ramon Massana, 2 Renate Scharek 1 1Centro Oceanogr afico de Gij on/Xix on, Instituto Espa nol~ de Oceanograf ıa (IEO), Gij on/Xix on, Asturias, Spain 2Institut de Cie`ncies del Mar (CSIC), Barcelona, Catalonia, Spain 3Division of Biological and Environmental Sciences and Engineering, Red Sea Research Center, King Abdullah University of Science and Technology (KAU ST), Thuwal, Saudi Arabia Abstract The fine vertical distribution of phytoplankton groups within the deep chlorophyll maximum (DCM) was studied in the NE Atlantic during summer stratific ation. A simple but unconventional sampling strategy allowed examining the vertical structure with ca. 2 m resolution. The distribution of Prochlorococcus , Synecho- coccus , chlorophytes, pelagophytes, small prymnesiophytes, coccolithophores, diatoms, and dinoflagellates was investigated with a combination of pigment-markers, flow cytometry and optical and FISH microscopy. All groups presented minimum abundances at the surface and a maximum in the DCM layer. The cell distri- bution was not vertically symmetrical around the DCM peak and cells tended to accumulate in the upper part of the DCM layer. The more symmetrical distribution of chlorophyll than cells around the DCM peak was due to the increase of pigment per cell with depth. We found a vertical alignment of phytoplankton groups within the DCM layer indicating preferences for different ecological niches in a layer with strong gra- dients of light and nutrients. Prochlorococcus occupied the shallowest and diatoms the deepest layers. Dinofla- gellates, Synechococcus and small prymnesiophytes preferred shallow DCM layers, and coccolithophores, chlorophytes and pelagophytes showed a preference for deep layers. Cell size within groups changed with depth in a pattern related to their mean size: the cell volume of the smallest group increased the most with depth while the cell volume of the largest group decreased the most. The vertical alignment of phytoplank- ton groups confirms that the DCM is not a homogeneous entity and indicates groups’ preferences for differ- ent ecological niches within this layer. The deep chlorophyll maximum (DCM) is a subsurface lay- becomes negative (Sverdrup 1953; Taylor and Ferrari 2011) er enriched in chlorophyll (Chl) typical of stratified marine producing the spring bloom in temperate areas (although this and freshwater bodies. It might be the result of diverse pro- classical approach has been challenged by Behrenfeld 2010). cesses and may present different characteristics (Cullen 1982, At this moment, the abundant phytoplankton accumulates 2015). In temperate areas, the DCM disappears in winter very close to the surface, limiting the irradiance immediately when mixing takes place and reappears after the spring bloom, below and inducing the synthesis of pigments by the deeper when stratification is established. The dynamics of this kind of phytoplankton and the formation of a shallow DCM that DCM have been described in the literature (Estrada et al. 1993; might not correspond to a biomass maximum. However, this Mignot et al. 2014). Briefly, winter surface waters replete with is a very dynamic situation because phytoplankton quickly nutrients start stratifying after the air-water heat balance (days-weeks) consume the nutrients from the well illuminated layers becoming less abundant at surface and concentrating at depth. This process originates a deeper DCM, coinciding with *Correspondence: [email protected] the nutricline and usually corresponding to a phytoplankton Additional Supporting Information may be found in the online version biomass maximum. Unless other vertical processes take place of this article. (Vaillancourt et al. 2003; Liccardo et al. 2013), phytoplankton This is an open access article under the terms of the Creative Commons keeps depleting the nutrients in the euphotic zone and thus Attribution-NonCommercial-NoDerivs License, which permits use and deepen the DCM. In conclusion, during a relatively long distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are period of the year, the DCM corresponds to a deep biomass made. maximum (DBM) in temperate areas. 665 Latasa et al. Distribution of phytoplankton groups in the DCM It has been recognized that phytoplankton (Venrick 1988, DCM (deep chlorophyll maximum) the Niskin bottl es were 1999; Estrada et al. 2016) and heterotrophic bacterioplankton closed every 8–12 s during the upcast at a constant ascent (Sunagawa et al. 2015) communities at the DCM and in the rate of 0.25 m s 21, i.e., every 2–3 m. The first sample below overlying mixed layer can be different, reflecting the different the DCM was chosen on the basis of the downcast fluores- environmental characteristics of these two major layers and cence profile. An additional surface water sample was collect- indicating that tens of meters in the vertical scale may make ed. In the GB also an intermediate sample was collected in a stronger difference than tens of km in the horizontal scale. the middle of the mixed layer. Because sampling was always The DCM has routinely been considered a single entity and performed at night, irradiance measurements were not avail- most research does not increase the sampling effort at the able. To reconstruct the irradiance profiles we assumed that DCM. Under this view, the starting hypothesis would say the depth of the DCM peak ( ZDCM ) was located at the 1% that the DCM is a homogeneous layer where all phytoplank- surface irradiance (Navarro and Ruiz 2013; Mignot et al. ton groups are equally distributed. However, because the 2014). An attenuation coefficient ( KPAR ) for each profile was DCM layer is located in strong and opposite gradients of obtained as KPAR 5 2/ ZDCM and the vertical irradiance profile 2K z nutrients and irradiance, the main resources for phytoplank- (as percentage of surface) estimated from Ez 5 E0 310 ð PAR Þ, ton growth, it could be expected that different groups are where ZDCM is the depth of the DCM, E0 and Ez are the per- better adapted to the distinctive environmental conditions cent irradiances at surface (100%) and at depth z, within the DCM layer if the conditions persist. Few works respectively. deal with the fine-scale structure of the DCM probably Variables analyzed because of the difficulties to obtain samples with high verti- For nutrient analysis, 8 mL of unfiltered sample were fro- cal resolution. Special procedures have been designed to sam- zen and kept at 220 8C immediately after sampling. Inorgan- ple small-scale vertical structures of thin layers (Lunven et al. ic nutrients were analyzed by standard nutrient techniques 2005) but they have not been yet extended and adapted to with a SKALAR San Plus Autoanalyzer. Detection limits for study the fine structure of the open ocean DCM. the different molecules were, in mmol m 23: 0.02 (NO ), 0.01 Here, we used a simple CTD procedure to obtain samples 3 (NO ), 0.013 (PO ), and 0.018 (SiO ). every 2–3 m and tested the null hypothesis that the DCM is 2 4 4 For flow cytometry analysis, 1.8 mL of sample were fixed a single, homogeneous ecological entity in which phyto- with 1% paraformaldehyde plus 0.05% glutaraldehyde, flash plankton groups are equally distributed. To that aim, we frozen in liquid nitrogen and kept at 280 8C. The analysis studied the vertical distribution of phytoplankton taxa with- was performed with a FACSCalibur flow cytometer (BD Bio- in the DCM layer in offshore waters of the north and north- sciences) equipped with a laser emitting at 488 nm. The flow western Iberian peninsula, belonging to the biogeographic rate was calibrated da ily by weight to estimate cell concen- North Atlantic Drift Province (Longhurst 1998). In this area, trations. A solution of 1 lm fluorescent latex beads (ref. winter mixing reaches ca. 200 m (Somavilla et al. 2011), well F-13081, Molecular Probes) was added as an internal stan- below the nutricline, and the posterior re-stratification dard so that all cellular variables were related to fluorescent beginning around March produces a marked spring bloom. beads values. Prochlorococcus and Synechococcus flow cytome- Summer is characterized by a progressive strengthening of try cell counts were converted to carbon (C) after estimating stratification, following the typical temporal pattern of the their cell volume from the relative side scatter signal as North Atlantic (Lindemann and St. John 2014). Our study described in Calvo-D ıaz and Mor an (2006), and using the was performed during the summer period of pronounced average value of 237 fg C lm3 (Worden et al. 2004). thermal stratification characterized by the presence of a For CARD-FISH analysis of target groups of photosynthet- marked DCM located between 22 m and 65 m depth at the ic picoeukaryotes, 45 mL of sample were prefiltered by 20 different profiles. lm, fixed with 37% formaldehyde (4% final concentration), filtered on 0.6 lm pore size Nucleopore filters (25 mm diam- Material and methods eter) and kept frozen. Group-specific oligonucleotide probes Samples were obtained during the two legs of the cruise were applied to target chlorophytes (CHLO02), small prym- Indemares0710 at Avil es Canyon (AC) and Galicia Bank (GB), nesiophytes (PRYM02) and pelagophytes (PELA01 and in the north and northwestern waters of the Iberian Peninsu- PELA1035). Concentrations were estimated from cell counts la, respectively, in summer 2010 on board the R/V Thalassa under an epifluorescence microscope (Olympus BX61) at (Fig. 1). Cast location, sample parameters and characteristics 1000X under UV (DAPI signal), blue light (Alexa 488 signal), of the DCM layer are described in Table 1.
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