Gitai Yahel The School of Marine Sciences Ruppin Academic Center Gitai Yahel (Yahel@Ruppin.ac.il) The School of Marine Sciences and Marine Environment Ruppin Academic Center, Biological Oceanography -12 Revisiting the Redfield ratio and the concept of Ecological stoichiometry Gitai Yahel The School of Marine Sciences Ruppin Academic Center Yahel@Ruppin.ac.il, Tel.(09) 830 4110, Skype gitaiyahel, Web http://Moodle.Ruppin.ac.il

Redfield and the concept of Ecological stoichiometry Gitai Yahel (Yahel@Ruppin.ac.il) The School of Marine Sciences and Marine Environment Ruppin Academic Center, Redfield and the concept of Ecological stoichiometry Redfield A.C. (1934) On the proportions of organic derivations in seawater and their relation to the composition of plankton. In James Johnson Memorial Volume. (ed. R.J. Daniel). University Press of Liverpool, pp. 177-192 Tuesday, May 07, 2019

Original observations Gitai Yahel (Yahel@Ruppin.ac.il) The School of Marine Sciences and Marine Environment Ruppin Academic Center, Original observations “The proportions of carbon, nitrogen, and phosphorus present in the organic material from which the carbonate, nitrate, and phosphate may be supposed to be derived are approximately 140 : 20 : 1 atoms” Western Atlantic Redfield 1934 Seven stations at the Sargasso Sea One station near Main Three water sources: Surface OMZ at ~700 m Deep (below 1500) Redfield 1934 Tuesday, May 07, 2019

Gitai Yahel (Yahel@Ruppin. ac Gitai Yahel (Yahel@Ruppin.ac.il) The School of Marine Sciences and Marine Environment Ruppin Academic Center, Original observations – Correlation between Dissolved Inorganics (Nitrate and Phosphate) Seven stations at the Sargasso Sea One station near Main Three water sources: Surface OMZ at ~700 m Deep (below 1500) Redfield 1934 Tuesday, May 07, 2019

Original observations Gitai Yahel (Yahel@Ruppin.ac.il) The School of Marine Sciences and Marine Environment Ruppin Academic Center, Original observations “It appears to mean that the relative quantities of nitrate-and phosphate occurring in the oceans of the world are just those which are required for the composition of the animals and plants which live in the sea.” “That two compounds of such great importance in the synthesis of living matter are so exactly balanced in the marine environment is a unique fact and one which calls for some explanation,” Seven stations at the Sargasso Sea One station near Main Three water sources: Surface OMZ at ~700 m Deep (below 1500) Redfield 1934 Redfield 1934 Tuesday, May 07, 2019

The Redfield ratio (a reminder) Gitai Yahel (Yahel@Ruppin.ac.il) The School of Marine Sciences and Marine Environment Ruppin Academic Center, The Redfield ratio (a reminder) Redfield Ratio (C:N:P) (molar ratio) = 106:16:1 * average of all living material Redfield 1958 PO4 No3 Average N/P ration in plankton (16) ≈ NO3/PO4 in deep ocean water (15) Not a coincidence! Uptake rate is also ~15:1 N/P Not plankton adaption to the oceanic stoichiometry “The phytoplankton adjust the N:P stoichiometry of the ocean to meet their requirements through nitrogen fixation” Preceded Lovelock’s concept of Gaya World by ~2 decades Redfield et al. argued that the similarity between the average nitrogen-to-phosphorus ratio in plankton (N:P=16 by atoms) and in deep oceanic waters (N:P=15) is neither a coincidence, nor the result of the plankton adapting to the oceanic stoichiometry, but rather that: Tuesday, May 07, 2019

The Redfield ratio II - C:N:P=106:16:1 Gitai Yahel (Yahel@Ruppin.ac.il) The School of Marine Sciences and Marine Environment Ruppin Academic Center, The Redfield ratio II - C:N:P=106:16:1 Ratio of: Available nutrients (inorganic) Nutrient uptake ratio Composition of cells Useful for: Modeling Predicting limiting nutrient Suggests that biology is controlling the chemical constituency of the oceans Can be extended to include other elements e.g., H:O:C:N:P:Fe:VitB12 Reservoirs in relative units to the amount of P in the ocean water (dissolved + Particulate) Phosphorus 40,000 Nitrogen 10,000 Redfield 1958 Tuesday, May 07, 2019

The Redfield ratio II - C:N:P=106:16:1 Gitai Yahel (Yahel@Ruppin.ac.il) The School of Marine Sciences and Marine Environment Ruppin Academic Center, The Redfield ratio II - C:N:P=106:16:1 Nitrogen fixation and denitrification are biologically mediated P and Fe are controlled by terrestrial processes (aeolian and riverine supply) Thus ocean productivity is ultimately controlled by Fe and P availablity Phosphorus 40,000 Nitrogen 10,000 Redfield 1958 Tuesday, May 07, 2019

These Generalizations are by and large still valid today Gitai Yahel (Yahel@Ruppin.ac.il) The School of Marine Sciences and Marine Environment Ruppin Academic Center, These Generalizations are by and large still valid today Biological N2 fixation and denitrification are the largest sources and sinks in the N cycle with no counterpart in the P cycle Webber and Dutch, Annu. Rev. Marine. Sci. 2012.4:113-141. Tuesday, May 07, 2019

Gitai Yahel (Yahel@Ruppin. ac Gitai Yahel (Yahel@Ruppin.ac.il) The School of Marine Sciences and Marine Environment Ruppin Academic Center, Comparisons between intracellular and dissolved seawater elemental stoichiometry Figure 1 | Comparisons between intracellular and dissolved seawater elemental stoichiometry. a, Representative (circle) and observed range (bar) of elemental ratios in oceanic phytoplankton normalized to carbon (nutrient:C quotas), plotted against mean dissolved seawater ratios. Colours indicate oceanic residence times (see Supplementary Table S1 for data and full list of references). Dark and light grey regions indicate <10-fold and <100-fold excesses and deficiencies relative to nitrogen, which is limiting over much of the ocean (Fig. 3). Elements to the top left of the shaded area are thus in great excess in sea water, and biological processing has little influence on their distribution, whereas some of those in the shaded regions have the potential to become limiting. b–d, Intracellular quotas versus surface dissolved seawater concentrations (normalized to mean ocean nitrate) for three oceanic regions. For clarity, intracellular stoichiometric variability is neglected and only the macronutrients N, P, Si and the scavenged micronutrients, Co, Mn, Fe are indicated (for additional detail and references see Supplementary Fig. S2). Experimental addition of the nutrient indicated in red typically promotes the most immediate (proximal) biological response in each region (Fig. 3), with solid red, dashed and dotted diagonal lines delineating elements that are as deficient as this nutrient, and 10- and 100-fold more replete than this nutrient, respectively. 1. Moore, C. M., Mills, M. M., et al. Processes and patterns of oceanic nutrient limitation. Nature Geoscience 6 (9), 701–710, doi:10.1038/ngeo1765 (2013). a, Representative (circle) and observed range (bar) of elemental ratios in oceanic phytoplankton normalized to carbon (nutrient:C quotas), plotted against mean dissolved seawater ratios. Colours indicate oceanic residence times (see Supplementary Table S1 for data and full list of references). Dark and light grey regions indicate <10-fold and <100-fold excesses and deficiencies relative to nitrogen, which is limiting over much of the ocean Moore et al. Nature Geoscience 6 (9), 701–710, (2013). Tuesday, May 07, 2019

Nitrate is depleted before phosphate is depleted Gitai Yahel (Yahel@Ruppin.ac.il) The School of Marine Sciences and Marine Environment Ruppin Academic Center, The Redfield ratio III “Classic” view (pre 1990s) Recent situation (North pacific) N limited (pre 90s Pacific) P limited (Atlantic) Nitrate is depleted before phosphate is depleted surface plankton, P limitation Inorganic N limitation (deep, old,) 106 CO2 +16 HNO3 + H3PO4 + 78 H2O  C106H175O42N16P1 + 150 O2 106CO2 +16HNO3 + H3PO4 + 122H2O  C106H263O110N16P1 + 138O2 Tuesday, May 07, 2019

The Redfield ratio – current understanding Gitai Yahel (Yahel@Ruppin.ac.il) The School of Marine Sciences and Marine Environment Ruppin Academic Center, The Redfield ratio – current understanding Fixed N:P ratios (NO3/PO4) in the deep water of large water bodies (oceans, large lakes) are usually close to the Redfield ratio mean plankton biomass (16:1) slope = 14.5 Figure 3 Global relationship between NO3 − and PO43− concentrations based on the Global Ocean Data Analysis Project (GLODAP) (Key et al. 2004). Bottle data were binned onto 33 standard depth intervals and onto a 1◦ latitude/longitude grid. Colors delineate the Atlantic (red ), Pacific (blue), and Indian ( yellow) ocean basins. The solid line through the origin has a slope of mean plankton biomass (16:1). The dashed line is the linear regression (slope = 14.5), which is less than the 16:1 ratio of plankton because NO3 − is removed via denitrification in high-nutrient areas and added via remineralization of N2-fixer biomass in low-nutrient areas. Webber and Dutch, Annu. Rev. Marine. Sci. 2012.4:113-141. The regression slope is 14.5 (less than 16) because NO3 − is removed via denitrification in high-nutrient areas and added via remineralization of N2-fixer biomass in low-nutrient areas. Tuesday, May 07, 2019

Global stoichiometric scaling of C, N, and P contents of soil and microbial biomass pools. “Redfield Ratio” in soil microbes: (C:N:P) (molar ratio) = 445:21:1 Figure 1. Global stoichiometric scaling of C, N, and P contents of soil and microbial biomass pools. show more Relationships in plots show variation in A) C∶N ratios B) C∶P ratios C) N∶P ratios of soils, microbial biomass, and combined data. Data were log10 transformed to improve normality and plotted to express size dependent relationships in comparison to the Redfield (1958) ratios (solid black lines). Dashed lines are regression fits for all global soils, with correlation coefficients in plain text and parameters estimated by SMA given in Table 1. Global relationships were compared with fits obtained using different subsets of habitat types, and where slopes were significantly different we plotted fits as dotted lines, with correlation coefficients given in italics. Soil C∶N scaling (A) was different in litter and organic soils (wetland organic, boreal forest, and humic horizons), while forest and pasture soils were different from global relationships in soil and microbial C∶P (B) and soil N∶P (C). SMA regression parameters for these relationships using subsets of our data are given in Table S1. doi:10.1371/journal.pone.0057127.g001 Hartman WH, Richardson CJ (2013) Differential Nutrient Limitation of Soil Microbial Biomass and Metabolic Quotients (qCO2): Is There a Biological Stoichiometry of Soil Microbes?. PLoS ONE 8(3): e57127. doi:10.1371/journal.pone.0057127 http://www.plosone.org/article/info:doi/10.1371/journal.pone.0057127

The Redfield ratio – current understanding Gitai Yahel (Yahel@Ruppin.ac.il) The School of Marine Sciences and Marine Environment Ruppin Academic Center, The Redfield ratio – current understanding Growth requires massive ribosomal (P based) production  low N:P Competition for nutrients and / or lights requires proteins (N) based acquisition and fixation mechanisms high N:P Klausmeier et al. NATURE |VOL 429 | 2004 Growth Coopetition Growth requires massive ribosomal (P based) production  low N:P Competition for nutrients or lights requires (N based) proteins based acquisition and fixation mechanisms high N:P Figure 1 Structural N:P ratio of 29 species of freshwater and marine phytoplankton. The Redfield ratio is shown, as is the theoretical range predicted by the model under the extreme ecological conditions of exponential growth (Opt exp) and competitive equilibrium with light, N and P limiting (Opt I, Opt N and Opt P) conditions. Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton, Klausmeier et al. 2004 NATURE |VOL 429 | 13 MAY 2004 N:P ratios of phytoplanktonic taxa range from 6 to >100 Tuesday, May 07, 2019

The Redfield ratio – current understanding Gitai Yahel (Yahel@Ruppin.ac.il) The School of Marine Sciences and Marine Environment Ruppin Academic Center, The Redfield ratio – current understanding Webber and Dutch, Annu. Rev. Marine. Sci. 2012.4:113-141. It is not clear what the 16:1 ratio represents? Ecosystem averaging? Circulation mixing? Growth requires massive ribosomal (P based) production  low N:P Competition for nutrients or lights requires (N based) proteins based acquisition and fixation mechanisms high N:P Figure 1 Structural N:P ratio of 29 species of freshwater and marine phytoplankton. The Redfield ratio is shown, as is the theoretical range predicted by the model under the extreme ecological conditions of exponential growth (Opt exp) and competitive equilibrium with light, N and P limiting (Opt I, Opt N and Opt P) conditions. Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton, Klausmeier et al. 2004 NATURE |VOL 429 | 13 MAY 2004 At least four mechanisms have been proposed to explain variability in C/N/P ratios in surface communities. The first mechanism suggests that the taxonomic composition of a community will influence its elemental stoichiometry. Indeed, several studies have measured low nutrient drawdown and C/P and N/P ratios for diatoms9, 15, 16, whereas cultures of marine Cyanobacteria have C/P and N/P ratios greater than the Redfield ratio6. The second mechanism relates the nutrient supply ratio (that is, the stoichiometry of the environment) to cellular elemental stoichiometry. Depending on the nutrient supply ratio, laboratory phytoplankton strains exhibit a range of equilibrium cellular N/P ratios17, but the importance of this mechanism for open-ocean communities has yet to be determined. The third mechanism is that the elemental stoichiometry within a cell is controlled by the biochemical allocation of resources to different growth strategies and is referred to as the growth rate hypothesis18, 19. Fast-growing cells may have a lower N/P ratio due to a larger investment in P-rich ribosomes. The fourth mechanism is that dead plankton material or detritus can accumulate in ocean waters and thus influence the observed particulate elemental ratios. Unfortunately, our quantitative knowledge of detritus concentrations 20 and elemental composition 21 in the open ocean is woefully inadequate. From: Strong latitudinal patterns in the elemental ratios of marine plankton and organic matter Adam C. Martiny, Chau T. A. Pham, Francois W. Primeau, Jasper A. Vrugt, J. Keith Moore, Simon A. Levin & Michael W. Lomas Nature Geoscience  6, 279–283  (2013)  doi:10.1038/ngeo1757 a physiological optimum? a balance between growth (low N:P) and competition (high N:P)? (iron) limitation on nitrogen fixation Note that the later hypothesis suggests that in an iron replete ocean the “Redfield ratio” may be much higher Tuesday, May 07, 2019

The Redfield ratio – Large regional differences Gitai Yahel (Yahel@Ruppin.ac.il) The School of Marine Sciences and Marine Environment Ruppin Academic Center, The Redfield ratio – Large regional differences Weber and Deutsch 2010 Southern Ocean High nitrate Low Iron Oxygenated  Low N fixation Low nitrification Diatom dominate Ecosystem vs. Circulation averaging? Figure 3 | (upper panel in my slide) Diagnosed nutrient export ratios. Spatial pattern of N/P exp, derived in model 2 by diagnosing the export of NO3 and PO4 independently. Figure 1 (lower right panel in my slide) Observed N* distribution in the Southern Ocean. a, Zonal mean section of N* ([NO3]+16[PO4] ), with potential density anomaly contours (thin lines) and schematic large-scale meridional overturning circulation patterns (arrows). Upwelling circumpolar deep water (CDW) is driven across the Antarctic polar front (APF) and the sub-Antarctic front (SAF) by Ekman transport, and subsides in the polar frontal zone (PFZ) to form Antarctic intermediate water (AAIW) and sub-Antarctic mode water (SAMW). Tuesday, May 07, 2019

The Redfield ratio – current understanding Gitai Yahel (Yahel@Ruppin.ac.il) The School of Marine Sciences and Marine Environment Ruppin Academic Center, The Redfield ratio – current understanding High N:P “To reconcile the biological and geochemical perspectives on Redfield N/P ratios, some process is required to effectively average out the wide variations in N/P at the organism level (N/Porg) and maintain the covariation of NO3 and PO4 observed in sea water.” Weber and Deutsch (2010) Ecosystem vs. Circulation averaging? Diatom dominate Low N:P Southern Ocean communities comprise diatoms with a low N/P ratio (11:1) and a remaining population with a high average N/P ratio (20). Large-scale variability in nutrient uptake ratios stems primarily from the relative abundance of species Weber and Deutsch 2010 Tuesday, May 07, 2019

The Redfield ratio – current understanding Gitai Yahel (Yahel@Ruppin.ac.il) The School of Marine Sciences and Marine Environment Ruppin Academic Center, The Redfield ratio – current understanding “To reconcile the biological and geochemical perspectives on Redfield N/P ratios, some process is required to effectively average out the wide variations in N/P at the organism level (N/Porg) and maintain the covariation of NO3 and PO4 observed in sea water.” Weber and Deutsch (2010) Ecosystem vs. Circulation averaging? Diatom dominate Southern Ocean communities comprise diatoms with a low N/P ratio (11:1) and a remaining population with a high average N/P ratio (20). Large-scale variability in nutrient uptake ratios stems primarily from the relative abundance of species Growth requires massive ribosomal (P based) production  low N:P Competition for nutrients or lights requires (N based) proteins based acquisition and fixation mechanisms high N:P Figure 1 Structural N:P ratio of 29 species of freshwater and marine phytoplankton. The Redfield ratio is shown, as is the theoretical range predicted by the model under the extreme ecological conditions of exponential growth (Opt exp) and competitive equilibrium with light, N and P limiting (Opt I, Opt N and Opt P) conditions. Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton, Klausmeier et al. 2004 NATURE |VOL 429 | 13 MAY 2004 Weber and Deutsch 2010 Tuesday, May 07, 2019

Ecosystem and circulation averaging Webber and Dutch, Annu. Rev. Marine. Sci. 2012.4:113-141. Tuesday, May 07, 2019

Gitai Yahel (Yahel@Ruppin. ac Gitai Yahel (Yahel@Ruppin.ac.il) The School of Marine Sciences and Marine Environment Ruppin Academic Center, Oceanic nitrogen reservoir regulated by plankton diversity and ocean circulation The average nitrogen-to-phosphorus ratio of marine phytoplankton (16N:1P) is closely matched to the nutrient content of mean ocean waters (14.3N:1P). This condition is thought to arise from biological control over the ocean’s nitrogen budget, in which removal of bioavailable nitrogen by denitrifying bacteria ensures widespread selection for diazotrophic phytoplankton that replenish this essential nutrient when it limits the growth of other species. Here we show that in the context of a realistic ocean circulation model, and a uniform N:P ratio of plankton biomass, this feedback mechanism yields an oceanic nitrate deficit more than double its observed value. The critical missing phenomenon is diversity in the metabolic N:P requirement of phytoplankton, which has recently been shown to exhibit large-scale patterns associated with species composition. When we model these variations, such that diazotrophs compete with high N:P communities in subtropical regions, the ocean nitrogen inventory rises and may even exceed the average N:P ratio of plankton. The latter condition, previously considered impossible, is prevented in the modern ocean by shallow circulations that communicate stoichiometric signals from remote biomes dominated by diatoms with low N:P ratios. Large-scale patterns of plankton diversity and the circulation pathways connecting them are thus key factors determining the availability of fixed nitrogen in the ocean. Figure 4 | Influence of individual surface regions on SN/SP. a, Values of DSN/SP represent the change in steady-state SN/SP (from the Redfield case) prompted by introducing the grid cell’s deviation of RO from 16 (Supplementary Fig. 4), while holding RO516 elsewhere (see Methods). Tuesday, May 07, 2019

Variation in elemental stoichiometry of marine environments Gitai Yahel (Yahel@Ruppin.ac.il) The School of Marine Sciences and Marine Environment Ruppin Academic Center, Variation in elemental stoichiometry of marine environments From: Strong latitudinal patterns in the elemental ratios of marine plankton and organic matter Adam C. Martiny, Chau T. A. Pham, Francois W. Primeau, Jasper A. Vrugt, J. Keith Moore, Simon A. Levin & Michael W. Lomas Nature Geoscience  6, 279–283  (2013)  doi:10.1038/ngeo1757 Each histogram shows the frequency of stations (0–100%) with a N/P or C/P ratio within the specified range. The red asterisks specify the lognormal average and n specifies the number of stations in each histogram. a, The N/P and C/P ratios of all stations in this study. b, The N/P and C/P ratio binned by latitude. c, The N/P and C/P ratio binned by nitrate concentrations. The nitrate concentration is the average concentration in the top 50 m at a specific station. Please note the unequal bin size in the histogram. Tuesday, May 07, 2019

Diversity in the metabolic N:P requirement of phytoplankton Redfield revisited The average N:P ratio of marine phytoplankton (16:1) is closely matched to the nutrient content of mean ocean waters (14.3:1) Biological control over the ocean’s nitrogen budget via denitrification (by bacteria) that select for diazotrophic phytoplankton Diversity in the metabolic N:P requirement of phytoplankton Large-scale patterns associated with species composition Circulation averaging is responsible for the relatively uniform N:P ratio of the world ocean Tuesday, May 07, 2019

Tuesday, May 07, 2019

Table 1. Summary of SMA regressions of log10-transformed C, N, and P contents in soil and microbial pools, along with predictors of soil C mineralization (CO2) and microbial metabolism (qCO2). Hartman WH, Richardson CJ (2013) Differential Nutrient Limitation of Soil Microbial Biomass and Metabolic Quotients (qCO2): Is There a Biological Stoichiometry of Soil Microbes?. PLoS ONE 8(3): e57127. doi:10.1371/journal.pone.0057127 http://www.plosone.org/article/info:doi/10.1371/journal.pone.0057127