Deep Sea Research Part I: Oceanographic Research Papers
Vertical distribution of phytoplankton biomass, production and growth in the Atlantic subtropical gyres
Introduction
The deep chlorophyll maximum (DCM) is a consistent oceanographic feature of tropical and subtropical oceans. Several mechanisms have been proposed to explain its formation and maintenance, including higher in-situ growth at the nutricline than in the upper mixed layer, physiological acclimation to low irradiance and high nutrient concentrations, accumulation of sinking phytoplankton at density gradients, behavioural aggregation of phytoplankton groups, and differential grazing on phytoplankton (e.g. Cullen, 1982; Gould, 1987).
In the subtropical gyres, the DCM has been suggested to be the result of a physiological acclimation of phytoplankton to low light levels in the presence of high nutrient concentrations (Cullen,1982) resulting in an increase in cellular chlorophyll a (Chl-a) content and, consequently, in a decrease in the carbon to Chl-a (C:Chl-a) ratio. These areas, considered as the oligotrophic extreme of the “typical tropical structure” (TTS) regions described by Herbland and Voituriez (1979), are characterised by an upper mixed layer, where nutrients are usually undetectable, a light-limited deep layer, and the presence of a Chl-a maximum located in the vicinity of the nutricline. In the subtropical gyres, therefore, the use of Chl-a concentration as an indicator of phytoplankton biomass could very likely result in the false identification of the DCM as a carbon-biomass maximum.
Studies based on Chl-a size fractionation (Herbland et al., 1985; LeBouteiller et al., 1992) show that in areas characterised by the TTS, the contribution of small phytoplankton cells to total Chl-a is higher in surface waters and decreases with depth, reaching 50% at the DCM. However, studies based on flow cytometry show that the slope of the size-abundance spectrum, which is a log–log plot of cell abundance (y-axis) versus cell size (x-axis), becomes more negative from surface to the DCM and then increases with depth. These results reveal a growing importance of small phytoplankton cells at the DCM and a progressive change toward larger cells underneath (Gin et al., 1999), and they suggest that the phytoplankton community structure shows significant vertical variability in oligotrophic environments. Species, pigment analyses and flow-cytometry studies reveal a two-layered structure of the phytoplankton composition in the tropical and subtropical Atlantic and Pacific (Gieskes and Kraay, 1986; Ondrusek et al., 1991; Venrick 1999; Veldhuis and Kraay, 2004). Usually, Prochlorophytes and Cyanophytes dominate the upper mixed layer while pico and nanoeukaryotes constitute a high portion of phytoplankton biomass at the DCM. In terms of abundance, Prochlorococcus dominates the picophytoplankton community throughout the water column in tropical and subtropical oceans (Campbell and Vaulot, 1993; Partensky et al., 1996; Zubkov et al., 1998). However, Prochlorococcus dominance in terms of cell numbers does not always translate into a parallel dominance in terms of biomass (Claustre and Marty, 1995; Barlow et al., 2002; Veldhuis and Kraay, 2004).
Primary production rates measured in the gyres (Letelier et al., 1996; Marañón et al., 2000) are higher in the upper metres of the water column. Moreover, small differences (less than 10%) have been observed in satellite-derived primary production estimates of the North Atlantic and Pacific subtropical gyres, depending on whether parameterized or uniform Chl-a profiles are used (Sathyendranath et al., 1995; Ondrusek et al., 2001). These results suggest a relatively low contribution of the DCM to depth-integrated primary production. Equally, phytoplankton turnover rates are generally higher in the upper mixed layer than in the proximity of the DCM (Malone et al., 1993; Goericke and Welschmeyer, 1998; Quevedo and Anadón, 2001), although a large variability in growth rate, ranging from 0.15 to 1.3 d−1, has been reported in the subtropical gyres (e.g., Marañón, 2005), revealing the existence of a more dynamic environment in the upper mixed layer of the oligotrophic oceans.
Most previous analyses of the vertical variability of phytoplankton biomass, production and size structure in the subtropical ocean have been based on a relatively small number of observations, or have limited spatial or temporal coverage. A recent study (Teira et al., 2005) aimed to characterise the temporal and spatial variability of primary production and Chl-a in the northeastern subtropical Atlantic based on observations collected for 12 years in the region. In the present study, we use part of the Teira et al. data together with data from the South Atlantic subtropical gyre to obtain a large dataset (>90 stations) of total and size-fractionated Chl-a and primary production, together with phytoplankton C biomass measured in the North and South Atlantic subtropical gyres on 10 cruises conducted during different seasons from 1995 to 2001. While Teira et al. (2005) focussed on the temporal and spatial variability, we used this extensive dataset to characterize the patterns of phytoplankton vertical variability in the subtropical gyres. In order to assess the biogeochemical and ecological role that the DCM plays in the oligotrophic ocean, we aim to answer the following specific questions: (1) How does phytoplankton size structure change with depth? (2) Is the DCM a phytoplankton biomass maximum? (3) Is the DCM a productivity maximum? and (4) Do phytoplankton grow faster at the DCM than in surface water?
Section snippets
Methods
Sampling was carried out at 94 oligotrophic stations (surface chlorophyll <0.2 mg m−3, undetectable surface nitrate concentration, sharp thermocline) of the subtropical gyres of the Atlantic Ocean during 10 cruises conducted from 1995 to 2001 (Fig. 1, Table 1). Fifty-five stations were sampled in the eastern North Atlantic subtropical gyre between 20° and 35°N and 39 stations in the South Atlantic gyre between 5° and 30°S. Hereafter, we shall use the terms NASTE and SATL to refer the two areas,
The DCM in the subtropical gyres
Table 2 shows averaged values of selected physical, chemical and biological variables in the subtropical gyres during the present study. Nitracline depth was similar in the NASTE and the SATL (t-test, p>0.05), while the thermocline was significantly deeper in the SATL than in the NASTE (t-test, p<0.001). The depth of the DCM was also significantly higher in the SATL (t-test, p<0.001). Mean temperature difference between the DCM depth and surface was 2.29 °C in the NASTE and 2.70 °C in the SATL.
Vertical distribution of phytoplankton size fractions
The importance of small phytoplankton cells in the oligotrophic regions of the ocean is well established in terms of Chl-a concentrations, cell abundances and primary production rates (e.g., Zubkov et al., 1998; Marañón et al., 2001). However, the vertical pattern of the relative contribution of picoplankton to total phytoplankton biomass remains unclear. In the tropical Atlantic, Herbland et al. (1985) found that the contribution of the small (<1 μm) phytoplankton to total Chl-a was maximum
Conclusions
We have characterized the vertical variability of phytoplankton biomass, size structure, production and growth in the Atlantic subtropical gyres. In answer to the questions posed in the Introduction, we concluded that: (1) picophytoplankton contribution to total Chl-a and primary production increased with depth to the DCM; (2) the deep chlorophyll maximum does not represent a phytoplankton-biomass or primary-productivity maximum but contributes a substantial fraction of the vertically
Acknowledgments
Thanks are given to Derek Harbour for providing data on phytoplankton abundance and biomass. Comments by Alex Poulton and three anonymous reviewers improved an early version of the manuscript. We are indebted to the Captain and crew of the research vessels, as well as to all colleagues on board during the 10 cruises. This study was supported by the UK Natural Environment Research Council through the Atlantic Meridional Transect programme (NER/O/S/2001/00680), the EU Contract CANIGO
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