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Reconciliation of the carbon budget in the ocean’s twilight zone

Abstract

Photosynthesis in the surface ocean produces approximately 100 gigatonnes of organic carbon per year, of which 5 to 15 per cent is exported to the deep ocean1,2. The rate at which the sinking carbon is converted into carbon dioxide by heterotrophic organisms at depth is important in controlling oceanic carbon storage3. It remains uncertain, however, to what extent surface ocean carbon supply meets the demand of water-column biota; the discrepancy between known carbon sources and sinks is as much as two orders of magnitude4,5,6,7,8. Here we present field measurements, respiration rate estimates and a steady-state model that allow us to balance carbon sources and sinks to within observational uncertainties at the Porcupine Abyssal Plain site in the eastern North Atlantic Ocean. We find that prokaryotes are responsible for 70 to 92 per cent of the estimated remineralization in the twilight zone (depths of 50 to 1,000 metres) despite the fact that much of the organic carbon is exported in the form of large, fast-sinking particles accessible to larger zooplankton. We suggest that this occurs because zooplankton fragment and ingest half of the fast-sinking particles, of which more than 30 per cent may be released as suspended and slowly sinking matter, stimulating the deep-ocean microbial loop. The synergy between microbes and zooplankton in the twilight zone is important to our understanding of the processes controlling the oceanic carbon sink.

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Figure 1: Sinks and sources of organic carbon to the twilight zone.
Figure 2: Predicted carbon cycle in the twilight zone.

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Acknowledgements

We thank the captain and crew of the RRS Discovery and scientists during D341, especially J. Hunter for executing the ARIES deployments and S. Ward for the PELAGRA deployments. We thank the OSCAR Project Office and BODC for providing data. Finally, we thank T. Cornulier for statistical help. This work was funded by Oceans 2025 and EU FP7-ENV-2010 Collaborative Project 264933 BASIN Basin-Scale Analysis, Synthesis and Integration. C.T. and M.B. were funded by the ANR-POTES program (no. ANR-05-BLAN-0161-01, awarded to C. T.) supported by the Agence Nationale de la Recherche (ANR, France). D.J.M. was funded by NERC (NE/G014744/1).

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Contributions

R.S. and S.L.C.G. designed and conducted the study; R.S.L. was involved in the conceptual development; S.L.C.G., C.T., M.B., M.V.Z., C.M.M. and S.A.H. all contributed data; K.C. was involved in sample analyses; and K.S. coordinated the PELAGRA deployments. T.R.A. and D.J.M. developed the model and implemented it for field data interpretation; S.L.C.G. analysed the data and wrote the manuscript together with R.S., D.J.M. and T.R.A. All authors discussed and commented on the manuscript.

Corresponding authors

Correspondence to Sarah L. C. Giering or Thomas R. Anderson.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Study site and deployments.

a, Current vectors from a vessel-mounted acoustic Doppler current profiler (thin black arrows) overlaid on surface chlorophyll (mg m−3; averaged from 28 July to 8 August 2009). The five sediment traps (PELAGRA; squares) followed the edge of an eddy (thick black arrow). Collection sites for zooplankton (ARIES system, circles) and prokaryotes (CTD, crosses) are marked. b, Lateral advection to the PAP site. Surface particle back-trajectories of the water masses sampled using PELAGRA (grey) and ARIES (black), calculated from satellite-derived near-surface velocities over 3 months. Particles started at the solid circles.

Extended Data Figure 2 DOC supply to the twilight zone.

a, Depth profiles of DOC at the PAP site at four stations during June (grey) and October (black) 2005. Shaded areas represent background concentrations of refractory (R), semi-refractory (SR) and semi-labile (SL) pools based on ref. 29. b, The relationship between AOU and DOC at the four stations. Black and grey circles respectively represent samples collected above and below the mixed layer (here 57 m). DOC recorded below 57 m correlates to AOU (grey line: DOC = −0.26AOU + 62.5; P = 0.01, R2 = 0.53, n = 9). The dotted line represents the theoretical relationship following the Redfield ratio (DOC = −(117/170)AOU + 62.5), which would pertain if all AOU were caused by the respiration of DOC.

Extended Data Figure 3 Zooplankton depth distribution.

a, b, Zooplankton biomass (>200 μm) during deployment periods 1 and 2 at the PAP site. Taxonomic groups are colour-coded as shown. c, d, Biomass of migratory zooplankton during deployment periods 1 and 2. Biomasses of community and migratory zooplankton are represented for daytime (right) and night time (left). The shaded area represents the mixed layer.

Extended Data Figure 4 Steps for calculating prokaryotic respiration.

a, Depth profiles of the leucine-to-carbon conversion factor (LeuCF) measured in the eastern North Atlantic (circles47, triangles48 and diamonds49) and the North Pacific (grey squares50). The average LeuCF below 50 m was 0.44 kg C mol−1 Leu (±0.27 s.d., n = 21). b, Depth profiles of prokaryotic growth efficiency (PGE) measured for the twilight zone across the North Atlantic (open triangles48, asterisk51, crosses52, filled triangles53 and filled circles54). The solid blue line shows the median PGE (0.08, n = 26), and the blue shaded area shows the interquartile range (0.04–0.12). Error bars, s.e.m. as reported in original studies. c, Flow diagram of calculation of prokaryotic respiration using bootstrapping. The output gives 100,000 estimates of prokaryotic respiration, which are used to compute the uncertainty in the final estimate.

Extended Data Figure 5 Twilight-zone carbon budget with different depth horizons.

a, Organic matter supply via dissolved matter (black area), active transport (mid grey area) and total supply including particles (light grey area), compared with zooplankton respiration (dashed red line) and community respiration (prokaryotes plus zooplankton; solid red line). bd, Comparison of net supply of organic carbon (sum of active flux, DOC and ΔPOC) with respiration by prokaryotes (PR) and non-migratory zooplankton (ZR) in the entire twilight zone (50–1,000 m; b), the upper twilight zone (50–150 m; c) and the lower twilight zone (150–1,000 m; d). Error bars represent upper and lower estimates (see text).

Extended Data Figure 6 Twilight-zone carbon model.

a, Flow diagram. Recycling pathways by attached prokaryotes, detritivores and the microbial loop (DOC and free-living prokaryotes). Fluxes to small coloured circles or hexagons enter sinking detritus (D1; orange circles), suspended detritus (D2; red circles), DOC (yellow circles) or CO2 (blue hexagons). b, Modelled sources and sinks of carbon. Net inputs of POC and DOC from the mixed layer (ML) versus respiration by the twilight-zone food web (‘Overall’; left); sources (D1 and D2 represent sinking and suspended POC, respectively) and sinks of detritus (middle); and sources and sinks of DOC (right). P, prokaryotes.

Extended Data Figure 7 Sensitivity analysis for predicted respiration rates.

Predicted zooplankton respiration (ZR; mg C m−2 d−1; excluding microzooplankton) and prokaryotic respiration (PR; mg C m−2 d−1) for varying parameters. The fraction of sinking POC consumed by attached prokaryotes (ψB; remainder consumed by detritivorous zooplankton) was varied between 0.1 and 0.9 (standard model value, 0.5). The fraction of grazed POC that is lost to suspended POC owing to sloppy feeding by detritivores (λH) was varied between 0.1 and 0.5 (standard value, 0.3). PGE (ωfl) was assigned values of 0.04 (a, b), 0.08 (c, d) and 0.12 (e, f). Red areas show the estimated range based on field data.

Extended Data Figure 8 Twilight-zone carbon budgets based on ‘carbon demand’.

Budgets were compiled by comparing loss of POC (ΔPOC; black) with carbon demand (ingestion) by zooplankton (dark grey) and prokaryotes (light grey) in the North Atlantic (PAP; this study) and twice at each of two stations in the Pacific (ALOHA and K2; ref. 6). The imbalance of these budgets contrasts with our final budget (Fig. 1d) based on respiration. Error bars show analytical errors for POC flux and upper and lower estimates for carbon demands based on a range of conversion factors (see methods reported in ref. 6 for details).

Extended Data Table 1 Deployment details
Extended Data Table 2 Model parameters and default values

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Giering, S., Sanders, R., Lampitt, R. et al. Reconciliation of the carbon budget in the ocean’s twilight zone. Nature 507, 480–483 (2014). https://doi.org/10.1038/nature13123

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