Significance Plankton in the sunlit surface ocean photosynthesize, fixing dissolved CO 2 into particulate organic carbon (POC). This POC sinks and is respired, releasing CO 2 into subsurface waters that are sequestered from the atmosphere. The depth scale over which this regeneration happens strongly affects atmospheric CO 2 , but estimates to date have been sparse and challenging to interpret. We use a new geochemical method to determine POC regeneration depth scales at unprecedented resolution in the South Pacific Ocean, finding shallow regeneration in both oxygen-deficient zone and oligotrophic gyre settings. Our results imply decreased future ocean carbon storage due to gyre expansion and two opposing feedbacks to expanding oxygen-deficient zones, the net effects of which on ocean carbon storage require future research.

Abstract Particulate organic carbon (POC) produced in the surface ocean sinks through the water column and is respired at depth, acting as a primary vector sequestering carbon in the abyssal ocean. Atmospheric carbon dioxide levels are sensitive to the length (depth) scale over which respiration converts POC back to inorganic carbon, because shallower waters exchange with the atmosphere more rapidly than deeper ones. However, estimates of this carbon regeneration length scale and its spatiotemporal variability are limited, hindering the ability to characterize its sensitivity to environmental conditions. Here, we present a zonal section of POC fluxes at high vertical and spatial resolution from the GEOTRACES GP16 transect in the eastern tropical South Pacific, based on normalization to the radiogenic thorium isotope 230Th. We find shallower carbon regeneration length scales than previous estimates for the oligotrophic South Pacific gyre, indicating less efficient carbon transfer to the deep ocean. Carbon regeneration is strongly inhibited within suboxic waters near the Peru coast. Canonical Martin curve power laws inadequately capture POC flux profiles at suboxic stations. We instead fit these profiles using an exponential function with flux preserved at depth, finding shallow regeneration but high POC sequestration below 1,000 m. Both regeneration length scales and POC flux at depth closely track the depths at which oxygen concentrations approach zero. Our findings imply that climate warming will result in reduced ocean carbon storage due to expanding oligotrophic gyres, but opposing effects on ocean carbon storage from expanding suboxic waters will require modeling and future work to disentangle.

The oceanic biological pump encompasses a series of processes by which phytoplankton at the sea surface photosynthetically fix carbon dioxide (CO 2 ) to form particulate organic carbon (POC), a portion of which is exported from the upper ocean and sinks to depth, where it is regenerated by microbial respiration (1, 2). The first two components of the biological pump, primary production and export of POC from the upper ocean, have been sufficiently characterized to enable their parametrization in terms of variables that can be measured by satellites, allowing for comprehensive estimates of their global rates and spatiotemporal variability (3⇓⇓–6). However, the fate of exported POC upon sinking into the ocean interior has proved to be an elusive oceanographic target. Because the time scale that waters are sequestered from the atmosphere increases with depth, the length scale over which POC regeneration occurs exerts a strong control on oceanic carbon storage and atmospheric CO 2 levels (7). Consequently, assessing how environmental conditions influence POC regeneration length scales provides critical insights that can be incorporated into ocean carbon cycle models to improve projections of future oceanic CO 2 uptake, including the response to global warming.

Historical estimates of carbon regeneration in the ocean interior have come from POC flux profiles generated either by compilations of sediment traps (8); by individual free-floating sediment trap profiles, typically with three to six depths in the upper 500 m (9, 10); or by combining 234Th-based euphotic zone POC fluxes with those from bottom-moored sediment traps below 1,500 m (11, 12). POC regeneration length scales are then determined by fitting either power laws (8) or exponential functions (13) to the vertical profiles of POC flux. However, these methods are respectively limited by their spatial resolution, vertical resolution, and integration across different temporal and spatial domains. The methods also provide conflicting results on the spatial patterns of regeneration depths, precluding the development of a comprehensive mechanistic understanding of the processes that control POC regeneration (9, 11).

We determine POC regeneration length scales in the eastern tropical South Pacific by adapting the paleoceanographic 230Th-normalization method (14) to the water column. Our study is the first application of this approach to generate internally consistent, high-resolution POC flux profiles that resolve differences in POC flux characteristics across biogeochemical gradients on annual to multiannual time scales. By analyzing particulate 230Th (230Th p ) and POC collected by in situ filtration, we calculate POC fluxes, integrated across ∼1- to 3-y time scales, at each measurement depth (15, 16) (see Materials and Methods). A recent intercomparison of sediment trap and radiochemical methods at the Bermuda Atlantic Time-Series Station found that 230Th p -normalized POC fluxes agreed (within 2-σ uncertainty) with other radiochemical methods for estimating POC flux in the upper water column (17). In further support of this approach, we find that 230Th p -derived POC fluxes on the GEOTRACES GP16 transect are within uncertainty of nearby annually averaged sediment trap POC fluxes (SI Appendix, Fig. S1).

Samples were collected on the GP16 transect (Research Vessel Thomas G. Thompson, cruise TN303) spanning from Peru to Tahiti (Fig. 1). The GP16 section traversed a strong zonal gradient in upper water column conditions, particularly in productivity and subsurface O 2 (Fig. 1). The Peru oxygen-deficient zone (ODZ) in the eastern portion of the section hosts nanomolar to subnanomolar O 2 levels, making it functionally anoxic (18). Oxygen concentration minima from GP16 were below the detection limit of 1 μmol/kg at stations 1 to 13 (Fig. 1B). Pigment and fluorescence data indicate that there is a transition in microbial community structure moving offshore within the ODZ, from autotrophic at station 9 to heterotrophic at station 11 (19). Our 230Th p -normalized POC flux profiles have sufficient vertical resolution to provide statistically significant constraints on the spatial variability and mechanisms controlling POC regeneration length scales and carbon transfer to the deep ocean across the sharp biogeochemical gradients spanning from the Peru ODZ to the highly oligotrophic South Pacific subtropical gyre (SPSG).

Fig. 1. Cruise track and dissolved oxygen concentrations. (A) TN303 cruise track showing station locations and 2013 annually averaged moderate resolution imaging spectroradiometer satellite-derived net primary productivity (NPP) from the vertically generalized productivity model (3). Locations of historical sediment trap deployments mentioned in the text are shown as stars. (B) Dissolved oxygen concentrations (μmol/kg) on the GP16 section.

Materials and Methods Particulate Sample Collection. Particulate samples on the GP16 section were collected via in situ filtration using McLane pumps (WTS-LV) with two flow paths. Each flow path was equipped with a 142-mm-diameter filter holder containing baffles to ensure homogenous particle distributions on the filters (32). The holders both had a 51-μm Sefar Polyester mesh prefilter, followed by either paired acid-leached, precombusted quartz-fiber Whatman QM-A filters with a 1-μm pore size, or acid-leached paired Pall Supor800 0.8-μm polyethersulfone filters (33). Blank filters were simultaneously deployed with the pumps on each cast, either on specially adapted filter holders disconnected from pumped water flow or in polypropylene containers zip-tied to the frame of a pump. The blank filters were in contact with ambient seawater at pump depth for the entire cast. These dipped blanks were used for background corrections of POC and Th isotopes. Previous publications (33, 34) have provided more detailed documentation of the collection of in situ pumped particles on the TN303 cruise. Sample Analysis. Measurement techniques for dissolved oxygen (35), POC (33), and Th isotopes (36) on the GP16 section have been previously documented. We provide here a brief overview containing the salient details of the measurements techniques, but refer readers to the publications containing the original data for complete methods. Dissolved oxygen was determined via modified Winkler titration, according to standard procedures established in the WOCE, CLIVAR, and GO-SHIP Repeat Hydrography programs (https://www.go-ship.org/HydroMan.html). The detection limit for discrete oxygen samples was 1 μmol/L, with ∼0.1% precision (35). The finalized oxygen dataset is archived online at the Biological and Chemical Oceanography Data Management Office (BCO-DMO, https://www.bco-dmo.org/dataset/503145), as well as the GEOTRACES Intermediate Data Product (37). POC in the 0.8- to 51-μm small-size fraction (SSF) was measured on two 12-mm-diameter punches taken from the top QM-A filter, representing ∼20 L of pumped seawater. The filters were dried at sea, fumed with concentrated hydrochloric acid (HCl) to remove inorganic carbon, and then dried again before the punches were taken. SSF POC was measured using a FlashEA 1112 Carbon/Nitrogen Analyzer using a Dynamic Flash Combustion technique. Dipped blank QM-A filters (n = 47) were used for blank subtraction, and the SD of the dipped blank measurements was assigned as the uncertainty for SSF POC measurements. POC data are available online at BCO-DMO (https://www.bco-dmo.org/dataset/668083) and the GEOTRACES Intermediate Data Product (37). Particulate 230Th (230Th p ) was measured in two laboratories: Lamont-Doherty Earth Observatory (LDEO), and University of Minnesota (UMN). Intercalibration showed no detectable differences between the methods of the two laboratories. At LDEO, one-fourth–filter aliquots were placed in 60-mL Savillex jars, a 229Th-233Pa spike and 25 mg of purified iron carrier were added, and the filters sat overnight in concentrated HNO 3 at room temperature. The filters were then completely digested in concentrated perchloric acid (HClO 4 ) to dissolve the polyethersulfone material. Particles were subsequently digested in concentrated HNO 3 and HF, followed by iron coprecipitation. Thorium fractions were isolated using anion exchange chromatography (Bio-Rad AG1-X8, 100 to 200 μm). Measurements of 230Th and 232Th were made on a Thermo Element XR inductively coupled plasma mass spectrometer (ICP-MS) instrument, using an Aridus desolvating nebulizer for sample introduction to improve sensitivity (38). Full details of the LDEO method have been published previously (36, 39). At UMN, one-eighth–filter aliquots were folded into 30-mL Teflon beakers, a 229Th-233Pa spike was added, and filters were submerged in 7N HNO 3 and 10 drops of concentrated HF. The beakers were capped and heated under pressure for 10 h at 200 °F to leach/digest the samples. After heating, the leach solution was quantitatively transferred to a separate 30-mL Teflon beaker, and five drops of concentrated HClO 4 were added. The leach solution was dried down and taken up in 2N HCl, followed by iron hydroxide coprecipitation. The precipitate was dissolved, dried down, and taken up again in 7N HNO 3 , which was then loaded onto Bio-Rad AG1-X8 100- to 200-μm mesh resin for separation of Th fractions via anion exchange chromatography. Thorium isotope measurements were made on a Thermo Neptune multicollector ICP-MS instrument (40, 41). In both laboratories, measured 230Th and 232Th were blank corrected using average dipped blank values. Errors in measured 230Th include uncertainties from ICP-MS counting statistics, spike concentrations, and blank corrections. Particulate 230Th and 232Th data are archived at BCO-DMO (https://www.bco-dmo.org/dataset/676231) and in the GEOTRACES Intermediate Data Product (37). More details on the measurements techniques in this study can be found in SI Appendix, Supplementary Information Text. Application of 230Th normalization to POC fluxes. 230Th normalization is a widely used method in paleoceanography for correcting sediment mass accumulation rates for syndepositional redistribution (42, 43). Most 230Th in seawater is produced in the water column by the decay of 234U. Uranium is highly soluble in seawater, stabilized as carbonate complexes (44, 45) with a residence time of hundreds of thousands of years (46). As such, uranium is conservative in seawater, with only minor (parts per thousand) spatial variations in concentration as a function of salinity, allowing for the prediction of oceanic uranium concentrations from salinity (47, 48). These uranium–salinity relationships are used to predict the activity of the major uranium isotope, 238U, which is multiplied by the seawater 234U/238U activity ratio of 1.1468 (49) to estimate 234U. Thus, the production rate of 230Th integrated to a depth horizon z can be predicted anywhere in the water column: P ( T 230 h ) z = ∫ 0 z λ 230 U 234 d z . Unlike its parent 234U, 230Th is highly insoluble in seawater. Upon production by 234U decay, 230Th rapidly adsorbs to particles, with a scavenging residence time of 20 to 40 y (50), much shorter than both its half-life [75,584 y (51)] and the time scale of whole-ocean mixing. The removal of 230Th from a given location is potentially driven by two processes: scavenging removal by particles, and lateral redistribution by advective-diffusive fluxes. Where the latter can be either ignored or corrected, the concentrations of both dissolved and particulate 230Th are expected to increase linearly with depth in a process known as reversible scavenging (52). In this formulation, the integrated production of 230Th to a depth z is balanced in one dimension by its downward export on particles sinking through that depth. The equation for calculating 230Th p -normalized POC fluxes is nearly identical to that used in paleoceanography to determine vertical constituent fluxes: P O C F l u x = P ( T 230 h ) z * [ P O C ] [ T 230 h ] p , where the integrated production rate is in μBq⋅m−2⋅d−1, [230Th] p is the activity of particulate 230Th in μBq⋅m−3, and [POC] is the concentration of POC in mmol⋅m−3. The resulting POC fluxes we report (Dataset S1) are in units of mmol⋅m−2⋅d−1. We calculate POC fluxes on particles in the 0.8- to 51-μm SSF. Due to low 230Th activity on particles >51 μm, larger filter aliquots were required for analysis than could be routinely measured across the entire section. The actual size of sinking particles carrying 230Th downward to balance its water column production is unknown. However, scavenging removal of 230Th is a two-step process involving adsorption of 230Th onto small particles, which subsequently undergo repeated cycles of aggregation into larger “sinking” particles and disaggregation into smaller “suspended” particles (53, 54). Thus, provided that the aggregation-sinking process is in equilibrium on the time scales of 230Th removal, the POC fluxes recorded by 230Th p normalization on 0.8- to 51-μm particles will be valid. Statistical procedures. Power laws of form F z = F z 0 ( z z 0 ) − b were fit to POC flux profiles at each station (Fig. 3) using data only at or above 1,000 m. Because the depths of the mixed layer, the deep chlorophyll maximum, and the oxycline varied between stations (SI Appendix, Fig. S2), we used the depth of maximum POC flux at each station as the reference depth z 0 rather than interpolating onto a common reference depth (e.g., the base of the euphotic zone or 100 m) across all stations. We show in SI Appendix, Supplementary Information Text that our findings are not sensitive to the choice of reference depth. For Fig. 4 A and B, data from the suboxic stations at the depths where oxygen concentrations were near zero (60 to 600 m) were grouped, as were data from the oxic stations over the same depth range. Three correlation tests were performed—Pearson’s correlation, Spearman’s rank correlation, and Kendall’s rank correlation (also known as Kendall’s tau)—and associated P values were computed for both groups of data (55). By any usual significance threshold, fluxes from suboxic depths of the suboxic stations are not significantly correlated with depth, whereas fluxes from the same depths of the oxic stations significantly decrease with depth. To quantify the differences between the flux–depth relationships in the oxic versus suboxic stations, we estimated uncertainty in the parameters of the exponential fits using a bootstrap analysis (56). For each group of stations, we generated 10,000 replicate datasets via resampling with replacement and then fit the functional form F z = F z 0 ⁡ exp ( − z L ) + F ∞ via nonlinear least-squares regression to each replicate. These 10,000 estimates for each parameter are shown in Fig. 4 C and D for F ∞ and L, respectively. Based on the intersection of these parameters’ estimated probability distributions, we can state with 98% and 90% confidence, respectively, that F ∞ is larger and that L is smaller for the suboxic data than for the oxic data. The median L for the suboxic data is 56 m and the median L for the oxic data is 102 m. The median F ∞ for the suboxic data is 0.36 mmol⋅m−2⋅d−1 and the median F ∞ for the oxic data is 0.093 mmol⋅m−2⋅d−1.

Acknowledgments We thank the captain and crew of the Research Vessel Thomas G. Thompson during the TN303 cruise. The pump team led by Dan Ohnemus was responsible for the collection of the particulate samples used in this study. We thank Kassandra Costa for comments on an early draft of the paper, as well as two anonymous reviewers and the handling editor for constructive feedback. This work was funded by US National Science Foundation Awards OCE-1233688 (to R.F.A.), OCE-1233903 (to R.L.E.), and OCE-1518110 (to P.J.L.), and by the NSF Graduate Research Fellowship DGE-16-44869 (to F.J.P.).

Footnotes Author contributions: F.J.P., R.F.A., P.J.L., and R.L.E. designed research; F.J.P., B.B.C., S.M.V., M.Q.F., Y.L., P.Z., and H.C. performed research; F.J.P., B.B.C., M.Q.F., and P.Z. analyzed data; and F.J.P. wrote the paper with input from R.F.A., P.J.L., and B.B.C.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

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