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Latitudinal Gradient in the Respiration Quotient and the Implications for Ocean Oxygen Availability

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Latitudinal Gradient in the Respiration Quotient and the Implications for Ocean Oxygen Availability Latitudinal gradient in the respiration quotient and the implications for ocean oxygen availability Allison R. Morenoa, Catherine A. Garciab, Alyse A. Larkinb, Jenna A. Leeb, Wei-Lei Wangb, J. Keith Mooreb, Francois W. Primeaub, and Adam C. Martinya,b,1 aDepartment of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697; and bDepartment of Earth System Science, University of California, Irvine, CA 92697 Edited by Donald E. Canfield, Institute of Biology and Nordic Center for Earth Evolution, University of Southern Denmark, Odense M., Denmark, and approved July 28, 2020 (received for review March 23, 2020) + → + [3] Climate-driven depletion of ocean oxygen strongly impacts the y NH3 2y O2 y HNO3 y H2O, global cycles of carbon and nutrients as well as the survival of many animal species. One of the main uncertainties in predicting yielding the total respiration quotient (rΣ−O2:C) describing the changes to marine oxygen levels is the regulation of the biological full oxidation of particulate organic matter, respiration demand associated with the biological pump. Derived from the Redfield ratio, the molar ratio of oxygen to organic car- ( + 1 + ) x 4 z 2y bon consumed during respiration (i.e., the respiration quotient, rΣ− = . [4] O2:C x rÀO2:C) is consistently assumed constant but rarely, if ever, mea- sured. Using a prognostic Earth system model, we show that a 0.1 The respiration quotient is commonly prescribed within models increase in the respiration quotient from 1.0 leads to a 2.3% de- to be static. Alfred Redfield implicitly assumed that all plank- cline in global oxygen, a large expansion of low-oxygen zones, tonic organic carbon consisted of carbohydrates (setting z to additional water column denitrification of 38 Tg N/y, and the loss zero), and thus, r−O2:C = 1.0 and rΣ−O2:C = 1.3 (7). Carbohydrates of fixed nitrogen and carbon production in the ocean. We then r represent a somewhat oxidized form of organic carbon, and other present direct chemical measurements of ÀO2:C using a Pacific macromolecules (especially lipids) are further reduced with higher Ocean meridional transect crossing all major surface biome types. r− . Nevertheless, theoretical estimations of phytoplankton bio- r O2:C ENVIRONMENTAL SCIENCES The observed ÀO2:C has a positive correlation with temperature, mass chemistry independently predicted the respiration quotient and regional mean values differ significantly from Redfield pro- to be ∼1.1 with limited biological variation (8, 9). Finally, a re- portions. Finally, an independent global inverse model analysis cent analysis using satellite-derived macromolecular composition constrained with nutrients, oxygen, and carbon concentrations of phytoplankton and gridded nutrient data were unable to detect r supports a positive temperature dependence of ÀO2:C in exported any systematic geospatial variation (10). Based on these consider- organic matter. We provide evidence against the common assump- ations, ocean biogeochemical models and theories assume a tion of a static biological link between the respiration of organic constant respiration quotient, although they disagree on the exact carbon and the consumption of oxygen. Furthermore, the model value (6). simulations suggest that a changing respiration quotient will im- There is also evidence suggesting substantial variation in the pact multiple biogeochemical cycles and that future warming can respiration quotient. First, the macromolecular composition of lead to more intense deoxygenation than previously anticipated. Redfield ratio | CESM | inverse modeling | elemental stoichiometry | Significance photosynthetic quotient The loss of ocean oxygen caused by climate warming is a se- he oceans are currently experiencing deoxygenation and an rious environmental issue and could lead to major declines Texpansion of oxygen minimum zones (1) with potentially dev- in animal habitats. However, current Earth system models astating impacts on marine life (2). Warming induced changes in struggle in explaining observed trends in global ocean oxygen. oxygen solubility as well as circulation-driven ventilation rates are Using a model, we demonstrate that marine oxygen concen- considered the primary drivers of deoxygenation (3). However, trations depend sensitively on a rarely considered quantity current models are unable to reproduce observed shifts in ocean known as the respiration quotient to prescribe the oxygen oxygen concentrations (4). consumed per mole of organic carbon respired. Using a combi- One of the main uncertainties in predicting ocean oxygen levels nation of direct chemical measurements across major biomes in is the regulation of the biological respiration demand (5). The the eastern Pacific Ocean plus changes in the global distribution respiration quotient describes the molar ratio of oxygen to organic of oxygen and carbon, we show how the respiration quotient carbon consumed during respiration and is thus controlled by the increases systematically with temperature. The findings imply oxidation state of organic material (signified by z)(6), that we can experience more intense declines in ocean oxygen with warming. ()() + ()+ 1 → + Cx H2O w NH3 yHzH3PO4 x z O2 xCO2 yNH3 Author contributions: A.R.M., F.W.P., and A.C.M. designed research; A.R.M., C.A.G., 4 A.A.L., J.A.L., W.-L.W., J.K.M., F.W.P., and A.C.M. performed research; J.K.M. contributed 1 new reagents/analytic tools; A.R.M., F.W.P., and A.C.M. analyzed data; and A.R.M. and A.C.M. wrote the paper. + H3PO4 + ()w + z H2O, 2 The authors declare no competing interest. [1] This article is a PNAS Direct Submission. Published under the PNAS license. ( + 1 ) 1 x 4 z To whom correspondence may be addressed. Email: [email protected]. r−O2:C = , [2] x This article contains supporting information online at https://www.pnas.org/lookup/suppl/ doi:10.1073/pnas.2004986117/-/DCSupplemental. with an additional oxygen demand due to nitrification, www.pnas.org/cgi/doi/10.1073/pnas.2004986117 PNAS Latest Articles | 1of7 Downloaded by guest on October 1, 2021 plankton differs across lineages (11) and physiological states (12) To directly quantify the respiration quotient, we combined leading to a large predicted biological variation in the respiration field measurements of particulate organic carbon (POC) and the quotient (SI Appendix, Fig. S1). Second, a limited set of full el- required oxygen demand for respiration across a meridional emental analyses of particulate organic matter provides support transect in the eastern Pacific Ocean. POC was estimated by for variation in the carbon oxidation state (13, 14). Third, end- combustion and the release of CO2 using an elemental analyzer. member mixing models of oxygen and DIC concentrations along To quantify the oxygen required for complete respiration of isopycnal surfaces suggest large variance in r−O2:C between ocean POC, we modified and calibrated a method commonly used for basins (15). However, this method can have large biases (16). measuring the particulate chemical oxygen demand (PCOD) in Fourth, global inverse model studies find large-scale gradients in wastewater (20). We then estimated the respiration quotient ( ) r−O2:P and rC : P for the regeneration of organic matter (17, 18). r−O2:C by taking the ratio of PCOD and POC across 198 sta- Simply dividing these two ratios suggests that rΣ−O2:C could range tions along the Pacific Ocean line P18 (SI Appendix, Table S2). between 0.7 and 2.1. Such independent studies challenge the Sea surface temperature steadily decreased from 29.5 to ∼0°C notion of a static link between the oxygen and carbon cycles, but (Fig. 2A). A deep nutricline was detected in multiple regions the drivers, magnitude, and regional differences of the respira- marking the location of oligotrophic conditions (Fig. 2B). Nitrate tion quotient are unknown. was mostly drawn down to detection limit in several regions, Here we report the outcome from a set of prognostic ocean whereas residual phosphate was present throughout the eastern biogeochemical model simulations, direct chemical measurements Pacific Ocean (SI Appendix, Fig. S4). As a result, N* was low in of the respiration quotient from diverse biomes, and a global in- most of the tropical and subtropical regions but rose with the verse model analysis to address the following research questions: high nutrient supply in the Southern Ocean (Fig. 2C). As such, 1) what are the global biogeochemical implications of a changing our samples covered a broad range of environmental conditions r−O2:C, 2) what is the regional average and variation in r−O2:C,and across the eastern Pacific Ocean. 3) does the regional variation in r−O2:C systematically relate to We observed distinct but highly correlated particulate organic specific environmental conditions? matter (POM) concentration levels across the regions. [POC] 2 and [PCOD] were tightly correlated (r Pearson = 0.93, P < 0.0001) Results (Fig. 2 D and E) and showed parallel regional shifts. Thus, our A change in the respiration quotient can have widespread im- optimized PCOD assay accurately reflects the amount of oxygen pacts on ocean oxygen, nitrogen, and carbon cycle processes. We required to oxidize all nonnitrogenous compounds making up conducted sensitivity simulations with a prognostic global ocean marine particulate organic matter. [POC] and [PCOD] were low biogeochemical model (19). The Community Earth System Model in regions with a deeper nutricline (1, Central American Coast (CESM) allowed for variation and dynamical feedbacks between [CAMR]; 2, North Pacific Equatorial Counter Current [PNEC]; the carbon, nitrogen, oxygen, and phosphorus cycles and included 3, Transitional Pacific Equatorial Divergence [TPEQ]; and 5, the regulation of primary production, carbon export, and an South Pacific Gyre [SPSG]), slightly higher in equatorial Pacific oxygen-dependent water column and sediment denitrification. We Ocean waters (4, Pacific Equatorial Divergence [PEQD]), and varied r−O2:C between 0.7 and 1.3 to test for potential biogeo- very high in the Southern Ocean regions (6, Southern Subtrop- chemical impacts of a changing respiration quotient.
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