COMMENTARY COMMENTARY
A carbon for every nitrogen Aron Stubbinsa,1
Biology and the environment interact, one shaping the other (1). In the oceans, the chemistry of seawater and the chemistry of life are intimately linked (2). In 1958, Alfred Redfield (3) noted that the microscopic plankton of the surface ocean contain carbon, nitrogen, and phosphorous atoms in a stoichiometry of ∼105:16:1 and that as these organisms sink and decay, the deep waters of the ocean become enriched in carbon, nitrogen, and phosphorous at the same ratio. This marked the beginnings of ecological stoichiometry, a growing field that is providing novel insight into the ecology and elemental cycles of the planet (4). A study in PNAS provides a new stoichiometric link, reporting that for every nitrogen consumed in the surface Atlantic Ocean, 1.12 carbons are converted from CO2 to dissolved organic carbon (DOC) (5). Carbon sits at the center of the elemental cycles. It is the backbone of the organic molecules that are the principal currency and building blocks of life. Carbon dioxide is the main anthropogenic greenhouse gas responsible for climate change (6). As phytoplankton grow in sunlit surface waters, they incorporate inorganic carbonate from seawater into organic molecules. Much of the organic carbon produced during photosynthesis is rapidly returned to the inorganic pool via respiration, with a small fraction accumulating as net community production (NCP). The carbonates incorporated by phytoplankton are the dissolved equivalent of atmospheric CO2, and, as carbonates are depleted in seawater, they are replenished by inputs of CO2 from the atmosphere. When the organic carbon produced by NCP is transported into the depths of the ocean, it provides a sink for atmospheric CO2 that is termed the biological carbon pump (7). Export to depth in the oceans can be in the form of particulate organic carbon or DOC. Organic particles that sink either are remineralized as they pass through the abyss, relinquishing their carbon back to the water, or survive to be buried at the ocean floor, potentially locking away carbon from the atmosphere for millennia. Other organic molecules dissolve into seawater and are collectively quantified as DOC. The
Fig. 1. New production in the surface ocean leads to the accumulation of 1.12 moles of dissolved organic carbon per mole of nitrate utilized.
diverse molecules that comprise the DOC pool provide sustenance for microbes and constitute significant global stores of carbon in the deep ocean (8). With respect to the latter, radiocarbon dating, natural isotopes, and chemical fingerprinting indicate that the pool of DOC within the ocean represents the NCP of ancient phytoplankton, which, over thousands of years, has accumulated to represent one of the largest organic carbon stores on Earth (9). The organic molecules composing the DOC pool have a C:N of 14 (10), compared with a Redfield C:N of 6.6 for plankton (3). Thus, the C:N of dissolved organics is approximately double the C:N of plankton, making DOC a nitrogenefficient means to sequester carbon in the deep ocean. In the past, changes in the size of the deep ocean DOC store may have driven changes in atmospheric CO2 and paleoclimate (11, 12). Today, the deep ocean DOC store and the atmospheric load of CO2 are of similar magnitude (13). The supply of carbon to the deep relies on phytoplankton and sunlight at the surface, where changes to ocean ecology could influence DOC production, export, and storage over timeframes of relevance to contemporary climate change. However, assessing whether marine DOC will act as a sink for atmospheric CO2 has been hampered by the lack of mechanistic models that predict DOC accumulation in surface waters.
a
Skidaway Institute of Oceanography, Department of Marine Sciences, University of Georgia, Savannah, GA 31411 Author contributions: A.S. wrote the paper. The author declares no conflict of interest. See companion article on page 10497 in issue 38 of volume 113. 1 Email: [email protected].
10736–10738 | PNAS | September 27, 2016 | vol. 113 | no. 39
www.pnas.org/cgi/doi/10.1073/pnas.1612995113
In PNAS, Romera-Castillo et al. identify the utilization of new nitrogen carried up from the deep ocean as a quantitative predictor of DOC production in sunlit surface waters (5). The main supply mechanism of new nitrogen to phytoplankton is via the upwelling, overturn, or mixing of the ocean water column. The amount of new nitrate used by phytoplankton depends upon a number of factors, including the supplies of other potentially limiting essential nutrients (14). By directly calculating new nitrate utilization as the nitrate concentration in deep source waters minus the residual nitrate remaining in the receiving surface waters, RomeraCastillo sidestep these other potential limiting factors to estimate the NCP of new organic carbon based upon the new nitrate utilization term (ΔNO3−) and Redfield’s C:N ratio of 6.6, NCP = New Nitrate Utilization × 6.6.
[1]
To link new nitrate utilization and NCP to net DOC production (ΔDOC), ΔDOC was calculated as surface water DOC concentration minus the DOC concentration in the deep source water. Building upon the legacy of Alfred Redfield and ecological stoichiometry, RomeraCastillo et al. (5) then defined a new stoichiometry: the Net DOC Production ratio (NDPr) as the ratio of NCP to ΔDOC to be a nearconstant 0.17 throughout the majority of the surface Atlantic Ocean, Atlantic Ocean NDPr = DOC Accumulation=NCP = 0.17.
[2]
Combining Eqs. 1 and 2 provides the following, DOC Accumulation = New Nitrate Utilization × 1.12.
[3]
Over most of the Atlantic Ocean, for every mole of nitrate utilized in sunlit surface waters, just over 1 carbon accumulates as DOC (Fig. 1). This elegantly simple stoichiometric conversion from new nitrogen to DOC production provides a new tool for oceanographers to predict the past and future role of the oceans in carbon storage and offers new insight into the elemental links between chemistry and ocean life. The remarkable constancy of C:N:P stoichiometry observed by Redfield in ocean surface water plankton and dissolved in the ocean’s depths revealed the coupling of chemistry and biology at the time and spatial scales of the global oceans. However, at smaller scales, those of organisms, days, or ecosystems, elemental stoichiometries shift and change (4). With respect to NDPr, an anomaly occurs in the North Atlantic subtropical gyre (NASG), where NDPr is not 0.17, as for the rest of the Atlantic Ocean, but is highly variable, with a mean of >0.8 (5). This anomaly can be interpreted as indicating that >80% of NCP is converted to DOC and raises interesting questions concerning the controls upon DOC accumulation in the ocean. Calculations by Romera-Castillo ruled out a number of explanations for the elevated NDPr observed in the NASG (5). Those explanations addressed include unaccounted for inputs of DOC from rivers, unaccounted for new nitrogen from in situ nitrogen fixation or atmospheric deposition, and the evaporative concentration of DOC. In exploring variability in predicted DOC accumulation, it may prove useful to consider variability, not just in NDPr but also in the canonical Redfield C:N ratio of 6.6 used to calculate NCP (Eq. 2).
1 2 3 4
The elemental stoichiometry of phytoplankton varies with both genotype and phenotype. The nutrient-starved, highly stratified waters of the sunbathed subtropical gyres are inhabited predominantly by cyanobacteria and picoeukaryotes. The biomass of these, the smallest of phytoplankton, has higher C:N values than that of the larger diatoms that thrive in colder, nutrient-rich waters nearer the poles (15), highlighting genetic variability in C:N. Phytoplankton growth in the NASG is nutrientlimited (14). As a general rule, nutrient limitation leads to higher C:nutrient ratios for a given phytoplankton species (4). These genotypic and phenotypic considerations may explain latitudinal patterns in ocean plankton C:N (15). For instance, in cold, nutrientrich waters inhabited by N-rich diatoms, plankton have an average
In PNAS, Romera-Castillo et al. identify the utilization of new nitrogen carried up from the deep ocean as a quantitative predictor of DOC production in sunlit surface waters. C:N of 6, which is enriched in N relative to the canonical Redfield ratio of 6.6. Planktonic matter from the warm, nutrient-limited waters of the subtropical gyres is depleted in N, with a C:N of 7. In warm, upwelling regions, the C:N of plankton is even higher at 7.6. These shifts are modest, suggesting they do not explain the greater variability in NDPr between the NASG (>0.8) and the remaining Atlantic Ocean (0.17). The above considerations concern potential additional sources of DOC to the NASG. Less-efficient removal could also explain the elevated DOC in the ocean’s subtropical gyres. Limitations in the genetic capacity of the bacteria that dominate open ocean gyres may decrease the efficiency with which these bacteria can degrade DOC (8). Incubation studies also show that microbial degradation of DOC accumulated in ocean gyres proceeds only when additions of new bioavailable DOC and inorganic nutrients are made (16), suggesting that, even when the genetic capacity exists, DOC removal in gyres is inefficient due to both bioavailable organic carbon and nutrient limitation of the resident heterotrophic bacteria. Although the complex relationships that lead to DOC accumulation in the gyres remain enigmatic, the newly introduced NDPr highlights the NASG as a region of anomalously nitrogenefficient DOC production. As the ocean gyres are expanding (17), understanding the current and future role of these ecosystems in carbon sequestration is of significant concern. Climate change is also predicted to intensify the upwelling that supplies deep, nutrient-rich waters to the surface ocean (18, 19). Massive quantities of the nitrogen applied by modern agriculture are subsequently exported to the oceans via rivers and atmospheric transport (20). These combined processes could potentially increase DOC accumulation in surface waters. NDPr defines a new quantitative link between the elemental cycles of chemistry and life, postulating nitrate utilization as a fundamental control on DOC accumulation in the surface Atlantic Ocean. In doing so, it offers the power to estimate future DOC accumulation in the ocean and the accompanying removal of CO2 from the atmosphere.
Vernadsky VI (1998) The Biosphere, trans Langmuir DB (Copernicus, New York), 1st Ed. Redfield AC (1934) On the Proportions of Organic Derivatives in Sea Water and Their Relation to the Composition of Plankton (Univ Press Liverpool, Liverpool, UK). Redfield AC (1958) The biological control of chemical factors in the environment. Am Sci 46(3):205–221. Sterner RW, Elser JJ (2002) Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere (Princeton Univ Press, Princeton), 1st Ed.
Stubbins
PNAS | September 27, 2016 | vol. 113 | no. 39 | 10737
5 Romera-Castillo C, Letscher RT, Hansell DA (2016) Nutrients exert fundamental control on dissolved organic carbon accumulation in the surface Atlantic Ocean. Proc Natl Acad Sci USA 113(38):10497–10502. 6 Intergovernmental Panel on Climate Change (2014) Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, eds Pachauri RK, et al. (Intergov Panel Clim Change, Geneva). 7 Volk T, Hoffert MI (2013) Ocean carbon pumps: Analysis of relative strengths and efficiencies in ocean-driven atmospheric CO2 changes. The Carbon Cycle and Atmospheric CO2: Natural Variations Archean to Present, eds Sundquist ET, Broecker WS (Am Geophys Union, Washington, DC), pp 99–110. 8 Moran MA, et al. (2016) Deciphering ocean carbon in a changing world. Proc Natl Acad Sci USA 113(12):3143–3151. 9 Dittmar T, Stubbins A (2014) Dissolved organic matter in aquatic systems. Treatise on Geochemistry, ed Turekian KK (Elsevier, Oxford), 2nd Ed, pp 125–156. 10 Sipler R, Bronk D (2015) Dynamics of dissolved organic nitrogen. Biogeochemistry of Marine Dissolved Organic Matter, eds Hansell D, Carlson C (Academic, San Diego), 2nd Ed, pp 127–232. 11 Broecker WS (1982) Ocean chemistry during glacial time. Geochim Cosmochim Acta 46(10):1689–1705. 12 Rothman DH, Hayes JM, Summons RE (2003) Dynamics of the Neoproterozoic carbon cycle. Proc Natl Acad Sci USA 100(14):8124–8129. 13 Hansell DA (2013) Recalcitrant dissolved organic carbon fractions. Annu Rev Mar Sci 5:421–445. 14 Moore CM, et al. (2013) Processes and patterns of oceanic nutrient limitation. Nat Geosci 6(9):701–710. 15 Martiny AC, et al. (2013) Strong latitudinal patterns in the elemental ratios of marine plankton and organic matter. Nat Geosci 6(4):279–283. 16 Carlson CA, et al. (2002) Effect of nutrient amendments on bacterioplankton production, community structure, and DOC utilization in the northwestern Sargasso Sea. Aquat Microb Ecol 30(1):19–36. 17 Polovina JJ, Howell EA, Abecassis M (2008) Ocean’s least productive waters are expanding. Geophys Res Lett 35(3):L03618. 18 Sydeman WJ, et al. (2014) Climate change. Climate change and wind intensification in coastal upwelling ecosystems. Science 345(6192):77–80. 19 Wang D, Gouhier TC, Menge BA, Ganguly AR (2015) Intensification and spatial homogenization of coastal upwelling under climate change. Nature 518(7539): 390–394. 20 Gruber N, Galloway JN (2008) An Earth-system perspective of the global nitrogen cycle. Nature 451(7176):293–296.
10738 | www.pnas.org/cgi/doi/10.1073/pnas.1612995113
Stubbins
A carbon for every nitrogen Aron Stubbinsa,1
Biology and the environment interact, one shaping the other (1). In the oceans, the chemistry of seawater and the chemistry of life are intimately linked (2). In 1958, Alfred Redfield (3) noted that the microscopic plankton of the surface ocean contain carbon, nitrogen, and phosphorous atoms in a stoichiometry of ∼105:16:1 and that as these organisms sink and decay, the deep waters of the ocean become enriched in carbon, nitrogen, and phosphorous at the same ratio. This marked the beginnings of ecological stoichiometry, a growing field that is providing novel insight into the ecology and elemental cycles of the planet (4). A study in PNAS provides a new stoichiometric link, reporting that for every nitrogen consumed in the surface Atlantic Ocean, 1.12 carbons are converted from CO2 to dissolved organic carbon (DOC) (5). Carbon sits at the center of the elemental cycles. It is the backbone of the organic molecules that are the principal currency and building blocks of life. Carbon dioxide is the main anthropogenic greenhouse gas responsible for climate change (6). As phytoplankton grow in sunlit surface waters, they incorporate inorganic carbonate from seawater into organic molecules. Much of the organic carbon produced during photosynthesis is rapidly returned to the inorganic pool via respiration, with a small fraction accumulating as net community production (NCP). The carbonates incorporated by phytoplankton are the dissolved equivalent of atmospheric CO2, and, as carbonates are depleted in seawater, they are replenished by inputs of CO2 from the atmosphere. When the organic carbon produced by NCP is transported into the depths of the ocean, it provides a sink for atmospheric CO2 that is termed the biological carbon pump (7). Export to depth in the oceans can be in the form of particulate organic carbon or DOC. Organic particles that sink either are remineralized as they pass through the abyss, relinquishing their carbon back to the water, or survive to be buried at the ocean floor, potentially locking away carbon from the atmosphere for millennia. Other organic molecules dissolve into seawater and are collectively quantified as DOC. The
Fig. 1. New production in the surface ocean leads to the accumulation of 1.12 moles of dissolved organic carbon per mole of nitrate utilized.
diverse molecules that comprise the DOC pool provide sustenance for microbes and constitute significant global stores of carbon in the deep ocean (8). With respect to the latter, radiocarbon dating, natural isotopes, and chemical fingerprinting indicate that the pool of DOC within the ocean represents the NCP of ancient phytoplankton, which, over thousands of years, has accumulated to represent one of the largest organic carbon stores on Earth (9). The organic molecules composing the DOC pool have a C:N of 14 (10), compared with a Redfield C:N of 6.6 for plankton (3). Thus, the C:N of dissolved organics is approximately double the C:N of plankton, making DOC a nitrogenefficient means to sequester carbon in the deep ocean. In the past, changes in the size of the deep ocean DOC store may have driven changes in atmospheric CO2 and paleoclimate (11, 12). Today, the deep ocean DOC store and the atmospheric load of CO2 are of similar magnitude (13). The supply of carbon to the deep relies on phytoplankton and sunlight at the surface, where changes to ocean ecology could influence DOC production, export, and storage over timeframes of relevance to contemporary climate change. However, assessing whether marine DOC will act as a sink for atmospheric CO2 has been hampered by the lack of mechanistic models that predict DOC accumulation in surface waters.
a
Skidaway Institute of Oceanography, Department of Marine Sciences, University of Georgia, Savannah, GA 31411 Author contributions: A.S. wrote the paper. The author declares no conflict of interest. See companion article on page 10497 in issue 38 of volume 113. 1 Email: [email protected].
10736–10738 | PNAS | September 27, 2016 | vol. 113 | no. 39
www.pnas.org/cgi/doi/10.1073/pnas.1612995113
In PNAS, Romera-Castillo et al. identify the utilization of new nitrogen carried up from the deep ocean as a quantitative predictor of DOC production in sunlit surface waters (5). The main supply mechanism of new nitrogen to phytoplankton is via the upwelling, overturn, or mixing of the ocean water column. The amount of new nitrate used by phytoplankton depends upon a number of factors, including the supplies of other potentially limiting essential nutrients (14). By directly calculating new nitrate utilization as the nitrate concentration in deep source waters minus the residual nitrate remaining in the receiving surface waters, RomeraCastillo sidestep these other potential limiting factors to estimate the NCP of new organic carbon based upon the new nitrate utilization term (ΔNO3−) and Redfield’s C:N ratio of 6.6, NCP = New Nitrate Utilization × 6.6.
[1]
To link new nitrate utilization and NCP to net DOC production (ΔDOC), ΔDOC was calculated as surface water DOC concentration minus the DOC concentration in the deep source water. Building upon the legacy of Alfred Redfield and ecological stoichiometry, RomeraCastillo et al. (5) then defined a new stoichiometry: the Net DOC Production ratio (NDPr) as the ratio of NCP to ΔDOC to be a nearconstant 0.17 throughout the majority of the surface Atlantic Ocean, Atlantic Ocean NDPr = DOC Accumulation=NCP = 0.17.
[2]
Combining Eqs. 1 and 2 provides the following, DOC Accumulation = New Nitrate Utilization × 1.12.
[3]
Over most of the Atlantic Ocean, for every mole of nitrate utilized in sunlit surface waters, just over 1 carbon accumulates as DOC (Fig. 1). This elegantly simple stoichiometric conversion from new nitrogen to DOC production provides a new tool for oceanographers to predict the past and future role of the oceans in carbon storage and offers new insight into the elemental links between chemistry and ocean life. The remarkable constancy of C:N:P stoichiometry observed by Redfield in ocean surface water plankton and dissolved in the ocean’s depths revealed the coupling of chemistry and biology at the time and spatial scales of the global oceans. However, at smaller scales, those of organisms, days, or ecosystems, elemental stoichiometries shift and change (4). With respect to NDPr, an anomaly occurs in the North Atlantic subtropical gyre (NASG), where NDPr is not 0.17, as for the rest of the Atlantic Ocean, but is highly variable, with a mean of >0.8 (5). This anomaly can be interpreted as indicating that >80% of NCP is converted to DOC and raises interesting questions concerning the controls upon DOC accumulation in the ocean. Calculations by Romera-Castillo ruled out a number of explanations for the elevated NDPr observed in the NASG (5). Those explanations addressed include unaccounted for inputs of DOC from rivers, unaccounted for new nitrogen from in situ nitrogen fixation or atmospheric deposition, and the evaporative concentration of DOC. In exploring variability in predicted DOC accumulation, it may prove useful to consider variability, not just in NDPr but also in the canonical Redfield C:N ratio of 6.6 used to calculate NCP (Eq. 2).
1 2 3 4
The elemental stoichiometry of phytoplankton varies with both genotype and phenotype. The nutrient-starved, highly stratified waters of the sunbathed subtropical gyres are inhabited predominantly by cyanobacteria and picoeukaryotes. The biomass of these, the smallest of phytoplankton, has higher C:N values than that of the larger diatoms that thrive in colder, nutrient-rich waters nearer the poles (15), highlighting genetic variability in C:N. Phytoplankton growth in the NASG is nutrientlimited (14). As a general rule, nutrient limitation leads to higher C:nutrient ratios for a given phytoplankton species (4). These genotypic and phenotypic considerations may explain latitudinal patterns in ocean plankton C:N (15). For instance, in cold, nutrientrich waters inhabited by N-rich diatoms, plankton have an average
In PNAS, Romera-Castillo et al. identify the utilization of new nitrogen carried up from the deep ocean as a quantitative predictor of DOC production in sunlit surface waters. C:N of 6, which is enriched in N relative to the canonical Redfield ratio of 6.6. Planktonic matter from the warm, nutrient-limited waters of the subtropical gyres is depleted in N, with a C:N of 7. In warm, upwelling regions, the C:N of plankton is even higher at 7.6. These shifts are modest, suggesting they do not explain the greater variability in NDPr between the NASG (>0.8) and the remaining Atlantic Ocean (0.17). The above considerations concern potential additional sources of DOC to the NASG. Less-efficient removal could also explain the elevated DOC in the ocean’s subtropical gyres. Limitations in the genetic capacity of the bacteria that dominate open ocean gyres may decrease the efficiency with which these bacteria can degrade DOC (8). Incubation studies also show that microbial degradation of DOC accumulated in ocean gyres proceeds only when additions of new bioavailable DOC and inorganic nutrients are made (16), suggesting that, even when the genetic capacity exists, DOC removal in gyres is inefficient due to both bioavailable organic carbon and nutrient limitation of the resident heterotrophic bacteria. Although the complex relationships that lead to DOC accumulation in the gyres remain enigmatic, the newly introduced NDPr highlights the NASG as a region of anomalously nitrogenefficient DOC production. As the ocean gyres are expanding (17), understanding the current and future role of these ecosystems in carbon sequestration is of significant concern. Climate change is also predicted to intensify the upwelling that supplies deep, nutrient-rich waters to the surface ocean (18, 19). Massive quantities of the nitrogen applied by modern agriculture are subsequently exported to the oceans via rivers and atmospheric transport (20). These combined processes could potentially increase DOC accumulation in surface waters. NDPr defines a new quantitative link between the elemental cycles of chemistry and life, postulating nitrate utilization as a fundamental control on DOC accumulation in the surface Atlantic Ocean. In doing so, it offers the power to estimate future DOC accumulation in the ocean and the accompanying removal of CO2 from the atmosphere.
Vernadsky VI (1998) The Biosphere, trans Langmuir DB (Copernicus, New York), 1st Ed. Redfield AC (1934) On the Proportions of Organic Derivatives in Sea Water and Their Relation to the Composition of Plankton (Univ Press Liverpool, Liverpool, UK). Redfield AC (1958) The biological control of chemical factors in the environment. Am Sci 46(3):205–221. Sterner RW, Elser JJ (2002) Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere (Princeton Univ Press, Princeton), 1st Ed.
Stubbins
PNAS | September 27, 2016 | vol. 113 | no. 39 | 10737
5 Romera-Castillo C, Letscher RT, Hansell DA (2016) Nutrients exert fundamental control on dissolved organic carbon accumulation in the surface Atlantic Ocean. Proc Natl Acad Sci USA 113(38):10497–10502. 6 Intergovernmental Panel on Climate Change (2014) Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, eds Pachauri RK, et al. (Intergov Panel Clim Change, Geneva). 7 Volk T, Hoffert MI (2013) Ocean carbon pumps: Analysis of relative strengths and efficiencies in ocean-driven atmospheric CO2 changes. The Carbon Cycle and Atmospheric CO2: Natural Variations Archean to Present, eds Sundquist ET, Broecker WS (Am Geophys Union, Washington, DC), pp 99–110. 8 Moran MA, et al. (2016) Deciphering ocean carbon in a changing world. Proc Natl Acad Sci USA 113(12):3143–3151. 9 Dittmar T, Stubbins A (2014) Dissolved organic matter in aquatic systems. Treatise on Geochemistry, ed Turekian KK (Elsevier, Oxford), 2nd Ed, pp 125–156. 10 Sipler R, Bronk D (2015) Dynamics of dissolved organic nitrogen. Biogeochemistry of Marine Dissolved Organic Matter, eds Hansell D, Carlson C (Academic, San Diego), 2nd Ed, pp 127–232. 11 Broecker WS (1982) Ocean chemistry during glacial time. Geochim Cosmochim Acta 46(10):1689–1705. 12 Rothman DH, Hayes JM, Summons RE (2003) Dynamics of the Neoproterozoic carbon cycle. Proc Natl Acad Sci USA 100(14):8124–8129. 13 Hansell DA (2013) Recalcitrant dissolved organic carbon fractions. Annu Rev Mar Sci 5:421–445. 14 Moore CM, et al. (2013) Processes and patterns of oceanic nutrient limitation. Nat Geosci 6(9):701–710. 15 Martiny AC, et al. (2013) Strong latitudinal patterns in the elemental ratios of marine plankton and organic matter. Nat Geosci 6(4):279–283. 16 Carlson CA, et al. (2002) Effect of nutrient amendments on bacterioplankton production, community structure, and DOC utilization in the northwestern Sargasso Sea. Aquat Microb Ecol 30(1):19–36. 17 Polovina JJ, Howell EA, Abecassis M (2008) Ocean’s least productive waters are expanding. Geophys Res Lett 35(3):L03618. 18 Sydeman WJ, et al. (2014) Climate change. Climate change and wind intensification in coastal upwelling ecosystems. Science 345(6192):77–80. 19 Wang D, Gouhier TC, Menge BA, Ganguly AR (2015) Intensification and spatial homogenization of coastal upwelling under climate change. Nature 518(7539): 390–394. 20 Gruber N, Galloway JN (2008) An Earth-system perspective of the global nitrogen cycle. Nature 451(7176):293–296.
10738 | www.pnas.org/cgi/doi/10.1073/pnas.1612995113
Stubbins
