The role of nutricline depth in regulating ocea1_yz

1 1The role of nutricline depth in regulating ocean’s 2carbon cycle 4Pedro Cermeño1, Stephanie Dutkiewicz2, Roger P Harris3, Mick Follows2, Oscar 5Schofield1 & Paul G Falkowski1,4 71 Environmental Biophysics & Molecular Ecology Program, Institute of Marine & 8Coastal Sciences, Rutgers University, 71 Dudley Rd, New Brunswick, 08901, New 9Jersey, USA 102 Earth, Atmospheric, and Planetary Sciences, 77 Massachusetts Ave., 11Massachusetts Institute of Technology, Cambridge, MA 02139-4307 USA 123 Plymouth Marine Laboratory, Prospect Place, Plymouth PL1 3DH, UK 134 Department of Earth and Planetary Science, Rutgers University, 610 Taylor 14Road, Piscataway, 08854, New Jersey, USA 15 16Carbon uptake by marine phytoplankton, and its export below the 17thermocline, lowers the partial pressure of carbon dioxide (pCO2) in the 18upper ocean, and stimulates the diffusion of CO2 gas from the atmosphere1 19Conversely, precipitation of calcium carbonate by marine planktonic 20calcifiers such as coccolithophorids increases pCO2, and promotes its 21outgassing2,3 Over the past ~50 million years, these carbon exchange fluxes 22between the atmosphere and the ocean have been largely controlled by the 1balance between diatom and coccolithophorid abundance, contributing 2significantly to the regulation of atmospheric pCO2 and Earth’s climate4,5 3Yet, the mechanisms that control this critical balance remain poorly 4understood The ecological distribution of these two phytoplankton 5functional groups has been linked to their distinct abilities to compete for 6nutrients6 Here we analyse phytoplankton community composition across 7latitudinal gradients in the Atlantic Ocean to show that the balance between 8diatoms and coccolithophorids is dependent upon the nutricline depth, a 9proxy of nutrient supply to the upper mixed layer of the ocean Coupled 10atmosphere-ocean general circulation models (GCMs) predict a dramatic 11reduction in the nutrient supply to the euphotic layer as a result of increased 12ocean stratification7-9 Our findings indicate that, by shifting phytoplankton 13community composition, this causal relationship may lead to a decreased role 14of the biological pump in sequestering atmospheric CO2, implying a positive 15feedback in the climate system These results are fundamental to understand 16the connection between upper ocean dynamics, the calcium carbonate-to17organic C production ratio and atmospheric pCO2 variations on time scales 18ranging from seasonal cycles to geological transitions 19 Diatoms and coccolithophorids are derived from a common Rhodophyte 20ancestor, yet the evolutionary trajectories have channelled these two 21phytoplankton functional groups into distinct ecological strategies that have 22significant biogeochemical implications2,3,4,6,10,11 From an evolutionary 23perspective, they constitute an example of the classical ecological divergence of r24and K-strategists6 Diatoms, as opportunists, efficiently exploit resources in 25unstable, rarefied environments6,11,12 Coccolithophorids, possessing high affinity 26for nutrients and low resource requirements, may grow under quiescent conditions 1characteristic of stratified, open ocean waters11,12,13 The ecological distribution of 2these two phytoplankton functional groups has been hypothesised to be linked to 3the mechanisms that supply nutrients into the upper mixed layer of the ocean6,14 4Here, we use data of phytoplankton biomass and species composition along with 5concurrent measurements of hydrographic variables from four Atlantic Meridional 6Transects (AMTs) (Fig 1a, see also Supplementary Table 1) in order to elucidate 7the mechanisms that control the balance between diatoms and coccolithophorids 8in the ocean and their role in the carbon cycle Across latitudinal gradients in the ocean, the availability of inorganic 10nutrients exerts a major control on phytoplankton biomass, primary productivity 11and community structure15 Typically, high latitude, temperate and upwelling 12systems receive substantial amounts of nutrients from deep waters by wind-driven 13vertical mixing and fluid transport along isopycnal layers In contrast, 14phytoplankton communities inhabiting low latitude environments, such as 15stratified, subtropical gyres, largely rely on local recycling and diapycnal nutrient 16fluxes to sustain their standing stocks In general, high nutrient conditions 17enhance diatom productivity Coccolithophorids, instead, are thought to be more 18widely distributed in oligotrophic ocean waters Contrary to conventional 19wisdom, our data analysis showed shows that the biomass (and biovolume) of 20both, diatoms and coccolithophorids, increases consistently from subtropical 21regions to temperate and upwelling systems in response to increased nutrient 22supply (Fig 1b) Though both phytoplankton groups exhibited similar latitudinal 23trends in biomass, our results revealed striking differences in their ranges of 24variation Diatom biomass increased over four orders of magnitude from low 25latitudes to temperate and upwelling systems, whereas coccolithophorid standing 26stocks varied by two orders of magnitude (Fig 1b) These latitudinal variations in 1diatom and coccolithophorid biomass were are consistent with their patterns of 2diversity (Fig 1c) Again, their ranges of variation were remarkably different, 3with the number of diatom species varying two-fold more than coccolithophorids 4(Fig 1c) We found a striking correspondence between the coccolithophorid-to- 6diatom (C/D) ratio and the nutricline depth (Fig 2) Specifically, our analysis 7indicates that, across the entire latitudinal gradient considered, coccolithophorids 8rapidly rise to dominance relative to diatoms as the water column stratifies and 9the nutricline deepens in the ocean 10 When physical mixing increases, the upper mixed layer penetrates the 11nutricline, thereby providing nutrients to the euphotic zone, and either the 12nutricline shoals or nutrients become elevated throughout the water column (i.e., 13zero-depth nutricline in this study) Conversely, when stratification increases, the 14upper mixed layer is deprived of nutrients, which leads to a progressive deepening 15of the nutricline The depth of the nutricline may thus be used as a proxy of 16nutrient supply into the upper mixed layer of the ocean In fact, the primary 17productivity of phytoplankton is negatively correlated with the depth of the 18nutricline (Supplementary Fig 1) This inverse relationship suggests a strong 19coupling between the position of the nutricline in the water column, the rate of 20nutrient supply into the euphotic layer, and the photosynthetic performance of 21phytoplankton 22 Different factors, such as the availability of silicic acid16, the mineral used 23by diatoms to construct their cell walls, or the saturation state of seawater with 24respect to calcium carbonate, a key controller of calcification17, have been put 1forward to explain the distribution of diatoms and coccolithophorids in different 2marine environments For instance, the low silicate-to-nitrate input ratios 3characteristic of the equatorial Pacific Ocean are thought to limit diatom 4productivity and C drawdown in this high nutrient-low biomass ocean region16 5Though these factors play a role, our study, covering temperate, upwelling, 6tropical, subtropical, and equatorial ecosystems, lends weight to the view6 that 7upper ocean turbulence and nutrient supply dynamics exert a dominant control 8upon the ecological selection and evolutionary success of these two 9phytoplankton functional groups in the ocean In this lineIn line with this, a suite 10of competition experiments in chemostats have shown that the population 11dynamics of diatoms and coccolithophorids can be controlled by simply varying 12the rate of nitrate supply with the C/D-ratio going up and down in response to 13steady-state and nutrient pulsing conditions, respectively (unpublished results) 14Remarkably, the strong linkage between the nutricline depth and phytoplankton 15community composition reported here arises despite that, in nature, ecological 16systems are influenced by manifold and ever changing environmental templates 17and complex biotic interactions 18 Our field observations illustrate very well how the balance between diatoms 19and coccolithophorids is primarily driven by variations in diatom biomass and 20diversity, with coccolithophorids exhibiting comparatively minor response to 21environmental variability (Fig 1b,c) But why these phytoplankton groups 22exhibit such different ranges of variability? 23 Microbial plankton are ubiquitous in the world oceans Their global 24biogeography is determined by local environmental factors that select for a 25particular species based on its optimal growth potential According to this 1‘universal distribution, local selection rule,’ the patterns depicted here for diatoms 2and coccolithophorids reflect their divergent life histories and survival 3strategies6,11,12,13 Diatoms, afforded by their high maximum growth rates, luxury 4nutrient uptake, and ability to store inorganic nutrients in vacuoles, exploit 5unstable environments where resources are supplied in excess relative to 6biological demand6,12,14, and diatoms bloom But adaptation to unstable 7environments imposes severe nutritional constraints under stable conditions 8Prolonged stability, such as increased ocean stratification, drives plankton 9ecosystems to operate near their carrying capacity (i.e., resource demand-to10supply ratio close to unity) and, under these conditions, ecological selection 11depends primarily on the ability of each individual species to compete for limited 12resources18 With the exception of species that migrate vertically and take up 13inorganic nutrients in the vicinity of the nutricline, or in symbiotic association 14with nitrogen fixers, diatoms are at a disadvantage under strong resource 15limitation due to their high nutritional requirements and high half saturation 16constants12 Consequently, across contrasting marine environments, the 17distribution of diatoms is inextricably tied to ample variations in biomass and 18diversity (Fig 1b,c) In contrast, coccolithophorids have lower maximum nutrient 19uptake and growth rates12,19 Instead, they possess low half saturation constants for 20nutrient uptake and small intracellular nutrient quotas (i.e., low nutritional 21requirements)12 These ecophysiological features allow coccolithophorids to 22inhabit a broad array of open oceanic environments without succumbing to 23dramatic variations in standing stocks (Fig 1b,c) 24 The impact of nutrient limitation on the competitive success of diatoms and 25coccolithophorids has profound implications Changes in the C/D-ratio may alter 26the efficiency of the biological pump by controlling the balance between two key 1processes, i) export of carbon into the ocean interior, and ii) release of CO2 due to 2coccolithophorid calcification (i.e., ‘alkalinity pump’, each mole CaCO3 3precipitated results in ~0.7 mole CO2 released, assuming present CO2 4concentrations, temperature T = 12 C and salinity S = 35) (ref 3) Consequently, 5for a given rate of organic productivity, an increase in the C/D-ratio will lead to a 6decreased role of the biological pump in sequestering atmospheric CO2 (refs 3, 720) Our analysis shows that major changes in the C/D-ratio are linked to the 8stabilisation-destabilisation of the water column (Fig 2) Low latitude, stratified 9ecosystems are dominated by coccolithophorids (C/D-ratio >> 1), and therefore 10increased stratification bears little effect on the CaCO3-to-organic C production 11ratio However, in unstable environments, characterised by a significant 12contribution of diatoms, the onset of water column stratification (and subsequent 13nutrient depletion) causes a rapid floristic shift, increases the CaCO3-to-organic C 14mass ratio, and reduces to a far greater extent the efficiency of the biological 15pump (Fig 2) 16 Current evidence and modelling work suggest that climate warming will 17increase ocean stratification, and hence reduce nutrient exchange between the 18ocean interior and the euphotic layer7-9 Recent reports highlight that, indeed, 19these climate driven trends in upper ocean stratification and primary productivity 20across the central, oligotrophic gyres are already detectable and may be occurring 21faster than model expectations21 Yet, predicting the impact that these changes 22may exert on the ecological functioning of marine plankton ecosystems remains 23elusive22 In order to investigate possible shifts in the distribution of diatoms and 24coccolithophorids caused by climate warming, we projected our empirical model 25between the coccolithophorid-to-diatom (C/D) ratio and the nutricline depth onto 26a coupled atmosphere-ocean general circulation model (GCM) (see 1Supplementary information for details) This three dimensional GCM was forced 2by the Intergovernmental Panel on Climate Change (IPCC) IS92a ‘continually 3increasing’ CO2 scenario (880 p.p.m.v in the year 2100) By the end of this 4century, in this model configuration and CO2 scenario, the increased upper ocean 5stratification reduces the supply of macronutrients to the euphotic layer, deepens 6the nutricline and leads to a reduction by 14 % in global oceanic primary 7productivity (Supplementary Figs X) The projection of our empirical model 8shows dramatic increase in the C/D-ratio across vast areas in the North Atlantic, 9but particularly pronounced in temperate ecosystems (Fig 3) By the year 2100, 10the C/D-ratio in the North Atlantic temperate region increases by >80 % relative 11to year 2000 In both hemispheres, the expansion of subtropical systems into 12temperate, equatorial and upwelling regions causes striking shifts in ecosystems 13characterized in the present day by a significant contribution of diatoms (Fig 3) 14 Our prognostic analysis indicates that, in a climate warming scenario, the 15progressive stratification of oceanic systems will increase the C/D-ratio, reducing 16the potential of marine plankton ecosystems to drawdown atmospheric CO2 (ref 1720) The model finds that oceanic regions subjected to the influence of the 18expansive subtropical gyres, such as the North Atlantic drift province or tropical 19upwelling systems, could be particularly susceptible to this biogeochemical 20control (Fig 3) Aside from shifting the C/D-ratio, increased ocean stratification 21and nutrient limitation may decrease primary productivity and export fluxes 7, 22especially those associated with diatoms23 The efficiency of the biological pump 23could further change if, as expected, the invasion of anthropogenic CO2 into the 24ocean alters the rates of coccolithophorid calcification and/or phytoplankton C25consumption (hence deviating the C/N stoichiometry from a static Redfield 26ratio)24,25 A sensitivity analysis indicates that the biogeochemical control 1described in this study (positive feedback on climate) could be of magnitude 2comparable, but inverse, to experimentally-observed reductions in 3coccolithophorid calcification (negative feedback) (Supplementary Fig X) If, on 4the contrary, coccolithophorid calcification increases, as recent reports suggest 26, 5the storage capacity of the surface ocean for CO2 would decrease, which, united to 6the smaller ability of marine plankton ecosystems to drawdown atmospheric CO2, 7would cause a larger reduction of the biological pump’s efficiency Margalef’s thesis that external energy input determines phytoplankton 9community structure6 is empirically demonstrated here Over the past ~50 million 10years, diatoms and coccolithophorids have responded incessantly to upper ocean 11turbulence and nutrient exchange dynamics, contributing significantly to the 12regulation of atmospheric pCO2 and Earth’s climate4,5,14,27 Consistent with the 13geological record and the classical ‘Mandala’ of Margalef, our results indicate that 14the relative distribution of diatoms and coccolithophorids is strongly dependent 15upon the mechanisms that supply nutrients into the upper mixed layer of the 16ocean We suggest that this mechanistic connection is majorly responsible for the 17ecological succession and long-term, regime shifts of these two phytoplankton 18functional groups in the ocean If so, these taxonomic shifts, and their associated 19impacts on net air-sea CO2 exchange, would be linked mechanistically to the 20seasonal dynamics of the upper mixed layer, interannual variations in climatic 21forcing22,28, contemporaneous trends in anthropogenic climate warming20,22,27, and 22the historical climate change14,27,29 23METHODS SUMMARY 24Physical, chemical and biological variables were obtained from four Atlantic 25Meridional Transect cruises (50N-50S) Micromolar concentrations of inorganic 10 1nutrients were determined on fresh samples using standard techniques For each 2station, the depth of the nutricline was taken to be the first depth where nitrate 3was detected (> 0.05 μM) Samples for identification and counting of 4phytoplankton were analysed using an inverted microscope (Utermhol’s 5technique) Cell numbers were expressed in terms of carbon using biovolume 6estimates and volume to carbon conversion factors 7The potential of marine phytoplankton to drawdown atmospheric CO2 was 8calculated from the C/D(biomass)-ratio considering the opposing effects of 9photosynthesis and calcification3 We assumed a fixed CaCO3-to-organic C 10production ratio in coccolithophorids of The moles of CO2 released by mole of 11CaCO3 precipitated, also known as ‘Revelle factor’ were calculated from 12analytical equations3 13The numerical simulation of change in ocean nutrient distribution was performed 14using an earth system model of intermediate complexity The model incorporates 15an explicit C cycle model with a parameterization of the biological export 16production limited by the availability of light and nutrients This biogeochemical 17component follows the fate of a macro-nutrient, dissolved organic matter, 18alkalinity and dissolved inorganic carbon Simulated changes in the nutricline 19depth enabled to prognosticate the relative distribution of diatoms and 20coccolithophorids over this century using our empirical relationships 21 221 Volk, T & Hoffert, M I in The Carbon Cycle and Atmospheric CO2: Natural 23 Variations Archean to Present (eds Sundquist, E T & Broecker, W S.) 99– 24 110 (Am Geophys Union, Washington DC, 1985) 11 12 Holligan, P M & Robertson, J E Significance of ocean carbonate budgets for the global carbon cycle Glob Change Biol 2, 85–95 (1996) 33 Frankignoulle, M., Canon, C Gattuso, J-P Marine calcification as a source of carbon dioxide: Positive feedback of increasing atmospheric CO2 Limnol Oceanog 39, 458– (1994) 64 Falkowski, P G., et al The evolution of modern eukaryotic phytoplankton Science 305, 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Revs Geophys 38, 159-189 (2000) 21 22Supplementary Information is linked to the online version of the paper at 23www.nature.com/nature 1 14 1Acknowledgements We thank all those who participated in the collection of data, in particular D 2Harbour for microscopy analyses, and S Costas, A Kahl, E Marón and Y Rosenthal for 3discussion and comments on the manuscript E M provided access to his primary productivity 4data Atlantic Meridional Transect (AMT) data collection was supported by the UK Natural 5Environmental Research Council through the AMT consortium (NER/O/S/2001/00680) P.C was 6supported by Marie Curie Outgoing International Fellowship from the European Union 7Author Contributions P.C., O.S & P.G.F designed the research R.P.H managed the 8phytoplankton database P.C conducted the analysis of phytoplankton data S.D & M.F 9performed the modelling section P.C wrote the paper 10Author Information Reprints and permissions information is available at 11www.nature.com/reprints The authors declare no competing financial interests Correspondence 12and requests for materials should be addressed to P.C (pedro@marine.rutgers.edu) or P.G.F 13(falko@marine.rutgers.edu) 14 15 16 17 18 19 20 15 1Figure Legends 2Figure Phytoplankton distribution in the Atlantic Ocean a, AMT cruises 3track overlain on an annual climatology of chlorophyll showing high values 4where surface nutrients are elevated b, Latitudinal distribution of biomass 5of diatoms (blue) and coccolithophorids (red) c, as b but for number of 6species Solid lines in panels b and c are biomass and number of species 7averaged each 5 of latitude Dashed lines are the range of data values 8Figure Nutricline depth controls the coccolithophorid-to-diatom (C/D) 9ratio Data points are 5 zonal averages of C/D-ratio and nutricline depth 10from four Atlantic latitudinal transects (solid circles) and two coastal 11stations (open circles, see supplementary information) The left Y-axis is 12represented on a log-scale in order to highlight the rapid shift from diatom 13to coccolithophorid dominance in response to the onset of water column 14stratification Colour lines are the least square linear regression models: 15[C/D (biomass) = 0.14 + 0.14 * ND, r2 = 0.78, p < 0.0001], and [C/D 16(diversity) = 0.55 + 0.03 * ND, r2 = 0.83, p < 0.0001] Changes (%) in the 17biological potential for atmospheric CO sequestration were estimated 18from the model equation considering the opposing effects of 19photosynthesis and calcification (thick solid line, see Supplementary 20information for details) Confidence intervals were obtained from the range 21of data values (as shown in Fig 1b, thin solid lines) Note that major 22changes are associated with the stabilisation/destabilisation of water 23column Reduction in pump’s efficiency considering changes in the 24buffering capacity of the ocean’s carbonate system in a future, high CO 25scenario was also displayed (dashed line, see Supplementary 26information) 1 16 1Figure Projected changes in the distribution of diatoms and 2coccolithophorids over this century a, Coccolithophorid to diatom (C/D) 3biomass ratio in year 2000 b, as a but for 2100 (assuming IPCC IS29 CO2 4‘continually increasing’ scenario) 17 1 a b c Figure 1 18 10 11 12 13 14 Figure 19 1 10 Figure  ... stratification increases, the 14upper mixed layer is deprived of nutrients, which leads to a progressive deepening 1 5of the nutricline The depth of the nutricline may thus be used as a proxy of 16nutrient... suggests a strong 19coupling between the position of the nutricline in the water column, the rate of 20nutrient supply into the euphotic layer, and the photosynthetic performance of 21phytoplankton... supply into the upper mixed layer of the ocean In fact, the primary 17productivity of phytoplankton is negatively correlated with the depth of the 1 8nutricline (Supplementary Fig 1) This inverse