1932

Abstract

Understanding the nature of organic matter flux in the ocean remains a major goal of oceanography because it impacts some of the most important processes in the ocean. Sinking particles are important for carbon dioxide removal from the atmosphere and its movement to the deep ocean. They also feed life below the ocean's productive surface and sustain life in the deep sea, in addition to depositing organic matter on the seafloor. However, the magnitude of all of these processes is dependent on the transformation of sinking particles during their journey through the water column. This review focuses on the movement of organic matter from the surface ocean to the deep sea via the biological carbon pump and examines the processes that prevent this downward movement—namely, attenuation via microbial colonization and zooplankton feeding. It also discusses how the depth-specific interactions among microbes, zooplankton, and aggregates determine carbon export as well as nutrient recycling, which in turn impact ocean production and Earth's climate.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-marine-032122-035153
2023-01-16
2024-06-16
Loading full text...

Full text loading...

/deliver/fulltext/marine/15/1/annurev-marine-032122-035153.html?itemId=/content/journals/10.1146/annurev-marine-032122-035153&mimeType=html&fmt=ahah

Literature Cited

  1. Agassiz A. 1888. Three Cruises of the United States Coast and Geodetic Survey Steamer “Blake” in the Gulf of Mexico, in the Caribbean Sea, and Along the Atlantic Coast of the United States, from 1877 to 1880 London: Sampson Low, Marston, Searle & Rivington
    [Google Scholar]
  2. Alldredge A, Cole JJ, Caron DA. 1986. Production of heterotrophic bacteria inhabiting macroscopic organic aggregates (marine snow) from surface waters. Limnol. Oceanogr. 31:68–78
    [Google Scholar]
  3. Alldredge A, Gotschalk C. 1988. In situ settling behavior of marine snow. Limnol. Oceanogr. 33:339–51
    [Google Scholar]
  4. Alldredge AL, Silver MW. 1988. Characteristics, dynamics and significance of marine snow. Prog. Oceanogr. 20:41–82
    [Google Scholar]
  5. Alonso-González IJ, Arístegui J, Lee C, Calafat A 2010. Regional and temporal variability of sinking organic matter in the subtropical northeast Atlantic Ocean: a biomarker diagnosis. Biogeosciences 7:2101–15
    [Google Scholar]
  6. Anderson TR, Raubenheimer D, Hessen DO, Jensen K, Gentleman WC, Mayor DJ. 2020. Geometric stoichiometry: unifying concepts of animal nutrition to understand how protein-rich diets can be “too much of a good thing. .” Front. Ecol. Evol. 8:196
    [Google Scholar]
  7. Anderson TR, Tang KW. 2010. Carbon cycling and POC turnover in the mesopelagic zone of the ocean: insights from a simple model. Deep-Sea Res. II 57:1581–92
    [Google Scholar]
  8. Armstrong RA, Lee C, Hedges JI, Honjo S, Wakeham SG. 2002. A new, mechanistic model for organic carbon fluxes in the ocean based on the quantitative association of POC with ballast minerals. Deep-Sea Res. II 49:219–36
    [Google Scholar]
  9. Azam F. 1998. Microbial control of oceanic carbon flux: The plot thickens. Science 280:694–96
    [Google Scholar]
  10. Bachmann J, Heimbach T, Hassenrück C, Kopprio GA, Iversen MH et al. 2018. Environmental drivers of free-living versus particle-attached bacterial community composition in the Mauritania upwelling system. Front. Microbiol. 9:2836
    [Google Scholar]
  11. Banse K. 1990. New views on the degradation and disposition of organic particles as collected by sediment traps in the open sea. Deep-Sea Res. A 37:1177–95
    [Google Scholar]
  12. Bianchi D, Galbraith ED, Carozza DA, Mislan KAS, Stock CA. 2013. Intensification of open-ocean oxygen depletion by vertically migrating animals. Nat. Geosci. 6:545–48
    [Google Scholar]
  13. Böckmann S, Koch F, Meyer B, Pausch F, Iversen M et al. 2021. Salp fecal pellets release more bioavailable iron to Southern Ocean phytoplankton than krill fecal pellets. Curr. Biol. 31:2737–46.e3
    [Google Scholar]
  14. Bopp L, Monfray P, Aumont O, Dufresne JL, Le Treut H et al. 2001. Potential impact of climate change on marine export production. Glob. Biogeochem. Cycles 15:81–99
    [Google Scholar]
  15. Boyd PW, Claustre H, Levy M, Siegel DA, Weber T. 2019. Multi-faceted particle pumps drive carbon sequestration in the ocean. Nature 568:327–35
    [Google Scholar]
  16. Boyd PW, Newton J. 1999. Does planktonic communities structure determine downward particulate organic carbon flux in different oceanic provinces?. Deep-Sea Res. I 46:63–91
    [Google Scholar]
  17. Boyle EA. 1988. The role of vertical chemical fractionation in controlling late Quaternary atmospheric carbon dioxide. J. Geophys. Res. Oceans 93:15701–14
    [Google Scholar]
  18. Briggs N, Dall'Olmo G, Claustre H 2020. Major role of particle fragmentation in regulating biological sequestration of CO2 by the oceans. Science 367:791–93
    [Google Scholar]
  19. Broecker WS. 1982. Ocean chemistry during glacial time. Geochim. Cosmochim. Acta 46:1689–705
    [Google Scholar]
  20. Broecker WS. 1991. Keeping global change honest. Glob. Biogeochem. Cycles 5:191–92
    [Google Scholar]
  21. Broecker WS, Peng TH. 1974. Gas exchange rates between air and sea. Tellus 26:21–35
    [Google Scholar]
  22. Broecker WS, Peng TH. 1982. Tracers in the Sea Palisades, NY: Eldigio
    [Google Scholar]
  23. Buesseler KO, Lamborg CH, Boyd PW, Lam PJ, Trull TW et al. 2007. Revisiting carbon flux through the ocean's twilight zone. Science 316:567–70
    [Google Scholar]
  24. Buesseler KO, Trull TW, Steinber DK, Silver MW, Siegel DA et al. 2008. VERTIGO (VERtical Transport in the Global Ocean): a study of particle sources and flux attenuation in the North Pacific. Deep-Sea Res. II 55:1522–39
    [Google Scholar]
  25. Burd A, Hansell DA, Steinberg DK, Anderson TR, Arístegui J et al. 2010. Assessing the apparent imbalance between geochemical and biochemical indicators of meso- and bathypelagic biological activity: What the @$#! is wrong with the present calculations of carbon budgets?. Deep-Sea Res. II 57:1557–71
    [Google Scholar]
  26. Cabanes DJE, Norman L, Santos-Echeandía J, Iversen MH, Trimborn S et al. 2017. First evaluation of the role of salp fecal pellets on iron biogeochemistry. Front. Mar. Sci. 3:289
    [Google Scholar]
  27. Cael BB, Bisson K. 2018. Particle flux parameterizations: quantitative and mechanistic similarities and differences. Front. Mar. Sci. 5:395
    [Google Scholar]
  28. Carr ME, Friedrichs MAM, Schmeltz M, Noguchi Aita M, Antoine D et al. 2006. A comparison of global estimates of marine primary production from ocean color. Deep-Sea Res. II 53:741–70
    [Google Scholar]
  29. Carson R. 1951. The Sea Around Us Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  30. Cavan EL, Kawaguchi S, Boyd PW. 2021. Implications for the mesopelagic microbial gardening hypothesis as determined by experimental fragmentation of Antarctic krill fecal pellets. Ecol. Evol. 11:1023–36
    [Google Scholar]
  31. Cavicchioli R, Ripple WJ, Timmis KN, Azam F, Bakken LR et al. 2019. Scientists’ warning to humanity: microorganisms and climate change. Nat. Rev. Microbiol. 17:569–86
    [Google Scholar]
  32. Christiansen S, Hoving HJ, Schütte F, Hauss H, Karstensen J et al. 2018. Particulate matter flux interception in oceanic mesoscale eddies by the polychaete Poeobius sp. Limnol. Oceanogr. 63:2093–109
    [Google Scholar]
  33. Cram JA, Chow CET, Sachdeva R, Needham DM, Parada AE et al. 2014. Seasonal and interannual variability of the marine bacterioplankton community throughout the water column over ten years. ISME J 9:563–80
    [Google Scholar]
  34. Dall'Olmo G, Dingle J, Polimene L, Brewin RJW, Claustre H. 2016. Substantial energy input to the mesopelagic ecosystem from the seasonal mixed-layer pump. Nat. Geosci. 9:820–23
    [Google Scholar]
  35. Daly KL, Wallace DWR, Smith WO, Skoog A, Lara R et al. 1999. Non-Redfield carbon and nitrogen cycling in the Arctic: effects of ecosystem structure and dynamics. J. Geophys. Res. Oceans 104:3185–99
    [Google Scholar]
  36. Datta MS, Sliwerska E, Gore J, Polz MF, Cordero OX. 2016. Microbial interactions lead to rapid micro-scale successions on model marine particles. Nat. Commun. 7:11965
    [Google Scholar]
  37. De La Rocha CL, Passow U 2007. Factors influencing the sinking of POC and the efficiency of the biological carbon pump. Deep-Sea Res. II 54:639–58
    [Google Scholar]
  38. Devol AH, Hartnett HE. 2001. Role of the oxygen-deficient zone in transfer of organic carbon to the deep ocean. Limnol. Oceanogr. 46:1684–90
    [Google Scholar]
  39. DeVries T, Weber T. 2017. The export and fate of organic matter in the ocean: new constraints from combining satellite and oceanographic tracer observations. Glob. Biogeochem. Cycles 31:535–55
    [Google Scholar]
  40. Diercks AR, Asper VL. 1997. In situ settling speeds of marine snow aggregates below the mixed layer: Black Sea and Gulf of Mexico. Deep-Sea Res. I 44:385–98
    [Google Scholar]
  41. Dilling L, Brzezinski MA. 2004. Quantifying marine snow as a food choice for zooplankton using stable silicon isotope tracers. J. Plankton Res. 26:1105–14
    [Google Scholar]
  42. Dilling L, Wilson J, Steinberg D, Alldredge A. 1998. Feeding by the euphausiid Euphausia pacifica and the copepod Calanus pacificus on marine snow. Mar. Ecol. Prog. Ser. 170:189–201
    [Google Scholar]
  43. Dubischar CD, Bathmann UV. 2002. The occurrence of faecal material in relation to different pelagic systems in the Southern Ocean and its importance for vertical flux. Deep-Sea Res. II 49:3229–42
    [Google Scholar]
  44. Ducklow HW, Steinber DK, Buesseler KO. 2001. Upper ocean carbon export and the biological pump. Oceanography 14:450–58
    [Google Scholar]
  45. Emerson S. 2014. Annual net community production and the biological carbon flux in the ocean. Glob. Biogeochem. Cycles 28:14–28
    [Google Scholar]
  46. Engel A, Szlosek J, Abrahamson L, Liu Z, Lee C. 2009. Investigating the effect of ballasting by CaCO3 in Emiliania huxleyi: I. Formation, settling velocities and physical properties of aggregates. Deep-Sea Res. II 56:1396–407
    [Google Scholar]
  47. Etheridge DM, Steele LP, Langenfelds RL, Francey RJ, Barnola JM, Morgan VI. 1996. Natural and anthropogenic changes in atmospheric CO2 over the last 1000 years from air in Antarctic ice and firn. J. Geophys. Res. Atmos. 101:4115–28
    [Google Scholar]
  48. Fadeev E, Rogge A, Ramondenc S, Nöthig EM, Wekerle C et al. 2021. Sea ice presence is linked to higher carbon export and vertical microbial connectivity in the Eurasian Arctic Ocean. Commun. Biol. 4:1255
    [Google Scholar]
  49. Fischer G, Romero O, Toby E, Iversen M, Donner B et al. 2019. Changes in the dust-influenced biological carbon pump in the Canary Current System: implications from a coastal and an offshore sediment trap record off Cape Blanc, Mauritania. Glob. Biogeochem. Cycles 33:1100–28
    [Google Scholar]
  50. Forest A, Tremblay J-É, Gratton Y, Martin J, Gagnon J et al. 2011. Biogenic carbon flows through the planktonic food web of the Amundsen Gulf (Arctic Ocean): a synthesis of field measurements and inverse modeling analyses. Prog. Oceanogr. 91:410–36
    [Google Scholar]
  51. Fortier M, Fortier L, Michel C, Legendre L. 2002. Climatic and biological forcing of the vertical flux of biogenic particles under seasonal Arctic sea ice. Mar. Ecol. Prog. Ser. 225:1–16
    [Google Scholar]
  52. Gehlen M, Bopp L, Emprin N, Aumont O, Heinze C, Ragueneau O. 2006. Reconciling surface ocean productivity, export fluxes and sediment composition in a global biogeochemical ocean model. Biogeosciences 3:521–37
    [Google Scholar]
  53. Gerber RP, Gerber MB. 1979. Ingestion of natural particulate organic matter and subsequent assimilation, respiration and growth by tropical lagoon zooplankton. Mar. Biol. 52:33–43
    [Google Scholar]
  54. Giering SLC, Sanders R, Lampitt RS, Anderson TR, Tamburini C et al. 2014. Reconciliation of the carbon budget in the ocean's twilight zone. Nature 507:480–83
    [Google Scholar]
  55. Gloege L, McKinley GA, Mouw CB, Ciochetto AB. 2017. Global evaluation of particulate organic carbon flux parameterizations and implications for atmospheric pCO2. Glob. Biogeochem. Cycles 31:1192–215
    [Google Scholar]
  56. Goldthwait SA, Carlson CA, Henderson GK, Alldredge AL. 2005. Effects of physical fragmentation on remineralization of marine snow. Mar. Ecol. Prog. Ser. 305:59–65
    [Google Scholar]
  57. Green EP, Dagg MJ. 1997. Mesozooplankton associations with medium to large marine snow aggregates in the northern Gulf of Mexico. J. Plankton Res. 19:435–47
    [Google Scholar]
  58. Grossart HP, Gust G. 2009. Hydrostatic pressure affects physiology and community structure of marine bacteria during settling to 4000 m: an experimental approach. Mar. Ecol. Prog. Ser. 390:97–104
    [Google Scholar]
  59. Grossart HP, Ploug H. 2001. Microbial degradation of organic carbon and nitrogen on diatom aggregates. Limnol. Oceanogr. 46:267–77
    [Google Scholar]
  60. Guidi L, Legendre L, Reygondeau G, Uitz J, Stemmann L, Henson SA. 2015. A new look at ocean carbon remineralization for estimating deepwater sequestration. Glob. Biogeochem. Cycles 29:1044–59
    [Google Scholar]
  61. Hach PF, Marchant HK, Krupke A, Riedel T, Meier DV et al. 2020. Rapid microbial diversification of dissolved organic matter in oceanic surface waters leads to carbon sequestration. Sci. Rep. 10:13025
    [Google Scholar]
  62. Hamm CE. 2002. Interactive aggregation and sedimentation of diatoms and clay-sized lithogenic material. Limnol. Oceanogr. 47:1790–95
    [Google Scholar]
  63. Heinze C, Meyer S, Goris N, Anderson L, Steinfeldt R et al. 2015. The ocean carbon sink – impacts, vulnerabilities and challenges. Earth Syst. Dyn. 6:327–58
    [Google Scholar]
  64. Henson SA, Sanders R, Madsen E. 2012. Global patterns in efficiency of particulate organic carbon export and transfer to the deep ocean. Glob. Biogeochem. Cycles 26:GB1028
    [Google Scholar]
  65. Henson SA, Sanders R, Madsen E, Morris PJ, Le Moigne F, Quartly GD 2011. A reduced estimate of the strength of the ocean's biological carbon pump. Geophys. Res. Lett. 38:L04606
    [Google Scholar]
  66. Hernández-Leon S, Ikeda T. 2005. A global assessment of mesozooplankton respiration in the ocean. J. Plankton Res. 27:153–58
    [Google Scholar]
  67. Hofmann M, Schellnhuber HJ. 2009. Oceanic acidification affects marine carbon pump and triggers extended marine oxygen holes. PNAS 106:3017–22
    [Google Scholar]
  68. Indermühle A, Stocker TF, Joos F, Fischer H, Smith HJ et al. 1999. Holocene carbon-cycle dynamics based on CO2 trapped in ice at Taylor Dome, Antarctica. Nature 398:121–26
    [Google Scholar]
  69. Iversen MH, Lampitt RS. 2020. Size does not matter after all: no evidence for a size-sinking relationship for marine snow. Prog. Oceanogr. 189:102445
    [Google Scholar]
  70. Iversen MH, Nowald N, Ploug H, Jackson GA, Fischer G. 2010. High resolution profiles of vertical particulate organic matter export off Cape Blanc, Mauritania: degradation processes and ballasting effects. Deep-Sea Res. I 57:771–84
    [Google Scholar]
  71. Iversen MH, Pakhomov EA, Hunt BPV, van der Jagt H, Wolf-Gladrow D, Klaas C. 2017. Sinkers or floaters? Contribution from salp pellets to the export flux during a large bloom event in the Southern Ocean. Deep-Sea Res. II 138:116–25
    [Google Scholar]
  72. Iversen MH, Ploug H. 2010. Ballast minerals and the sinking carbon flux in the ocean: carbon-specific respiration rates and sinking velocity of marine snow aggregates. Biogeosciences 7:2613–24
    [Google Scholar]
  73. Iversen MH, Ploug H. 2013. Temperature effects on carbon-specific respiration rate and sinking velocity of diatom aggregates – potential implications for deep ocean export processes. Biogeosciences 10:4073–85
    [Google Scholar]
  74. Iversen MH, Poulsen LK. 2007. Coprorhexy, coprophagy, and coprochaly in the copepods Calanus helgolandicus, Pseudocalanus elongatus, and Oithona similis. Mar. Ecol. Prog. Ser. 350:79–89
    [Google Scholar]
  75. Iversen MH, Robert ML. 2015. Ballasting effects of smectite on aggregate formation and export from a natural plankton community. Mar. Chem. 175:18–27
    [Google Scholar]
  76. Jackson GA. 1993. Flux feeding as a mechanism for zooplankton grazing and its implications for vertical particulate flux. Limnol. Oceanogr. 38:1328–31
    [Google Scholar]
  77. Jackson GA, Checkley DM Jr. 2011. Particle size distribution in the upper 100 m water column and their implications for animal feeding in the plankton. Deep-Sea Res. I 58:283–97
    [Google Scholar]
  78. Jiao N, Zheng Q. 2011. The microbial carbon pump: from genes to ecosystems. Appl. Environ. Microbiol. 77:7439–44
    [Google Scholar]
  79. Jónasdóttir SH, Visser AW, Richardson K, Heath MR. 2015. Seasonal copepod lipid pump promotes carbon sequestration in the deep North Atlantic. PNAS 112:12122–26
    [Google Scholar]
  80. Karthäuser C, Ahmerkamp S, Marchant HK, Bristow LA, Hauss H et al. 2021. Small sinking particles control anammox rates in the Peruvian oxygen minimum zone. Nat. Commun. 12:3235
    [Google Scholar]
  81. Kiørboe T. 2001. Formation and fate of marine snow: small-scale processes with large-scale implications. Sci. Mar. 65:57–71
    [Google Scholar]
  82. Kiørboe T, Tang K, Grossart HP, Ploug H. 2003. Dynamics of microbial communities on marine snow aggregates: colonization, growth, detachment, and grazing mortality of attached bacteria. Appl. Environ. Microbiol. 69:3036–47
    [Google Scholar]
  83. Koski M, Kiørboe T, Takahashi K. 2005. Benthic life in the pelagic: aggregate encounter and degradation rates by pelagic harpacticoid copepods. Limnol. Oceanogr. 50:1254–63
    [Google Scholar]
  84. Kriest I, Oschlies A. 2008. On the treatment of particulate organic matter sinking in large-scale models of marine biogeochemical cycles. Biogeosciences 5:55–72
    [Google Scholar]
  85. Kriest I, Oschlies A, Khatiwala S. 2012. Sensitivity analysis of simple global marine biogeochemical models. Glob. Biogeochem. Cycles 26:GB2029
    [Google Scholar]
  86. Kulk G, Platt T, Dingle J, Jackson T, Jönsson BF et al. 2020. Primary production, an index of climate change in the ocean: satellite-based estimates over two decades. Remote Sens. 12:826
    [Google Scholar]
  87. Kwon EY, Primeau F. 2008. Optimization and sensitivity of a global biogeochemistry ocean model using combined in situ DIC, alkalinity, and phosphate data. J. Geophys. Res. Oceans 113:C08011
    [Google Scholar]
  88. Kwon EY, Primeau F, Sarmiento JL. 2009. The impact of remineralization depth on the air-sea carbon balance. Nat. Geosci. 2:630–35
    [Google Scholar]
  89. Lampitt RS, Hilier WR, Challenor PG. 1993. Seasonal and diel variation in the open ocean concentration of marine snow aggregates. Nature 362:737–39
    [Google Scholar]
  90. Lampitt RS, Noji T, Bodungen BV. 1990. What happens to zooplankton fecal pellets? Implications for material flux. Mar. Biol. 104:15–23
    [Google Scholar]
  91. Lauderdale JM, Cael BB. 2021. Impact of remineralization profile shape on the air-sea carbon balance. Geophys. Res. Lett. 48:e2020GL091746
    [Google Scholar]
  92. Legendre L, Rivkin RB, Weinbauer MG, Guidi L, Uitz J. 2015. The microbial carbon pump concept: potential biogeochemical significance in the globally changing ocean. Prog. Oceanogr. 134:432–50
    [Google Scholar]
  93. Levy M, Bopp L, Karleskind P, Resplandy L, Ethe C, Pinsard F. 2013. Physical pathways for carbon transfers between the surface mixed layer and the ocean interior. Glob. Biogeochem. Cycles 27:1001–12
    [Google Scholar]
  94. Lombard F, Koski M, Kiørboe T. 2013. Copepods use chemical trails to find sinking marine snow aggregates. Limnol. Oceanogr. 58:185–92
    [Google Scholar]
  95. Lutz M, Dunbar R, Caldeira K. 2002. Regional variability in the vertical flux of particulate organic carbon in the ocean interior. Glob. Biogeochem. Cycles 16:11–118
    [Google Scholar]
  96. Marsay CM, Sanders RJ, Henson SA, Pabortsava K, Achterberg EP, Lampitt RS. 2015. Attenuation of sinking particulate organic carbon flux through the mesopelagic ocean. PNAS 112:1089–94
    [Google Scholar]
  97. Martin JH. 1990. Glacial-interglacial CO2 change: the iron hypothesis. Paleoceanography 5:1–13
    [Google Scholar]
  98. Martin JH, Knauer GA, Karl DM, Broenkow WW. 1987. VERTEX: carbon cycling in the northeast Pacific. Deep-Sea Res. A 34:267–85
    [Google Scholar]
  99. Mayor DJ, Sanders R, Giering SLC, Anderson TR. 2014. Microbial gardening in the ocean's twilight zone: Detritivorous metazoans benefit from fragmenting, rather than ingesting, sinking detritus. BioEssays 36:1132–37
    [Google Scholar]
  100. Mestre M, Ruiz-González C, Logares R, Duarte CM, Gasol JM, Montserrat Sala M 2018. Sinking particles promote vertical connectivity in the ocean microbiome. PNAS 115:E6799–807
    [Google Scholar]
  101. Middelburg JJ. 1989. A simple rate model for organic matter decomposition in marine sediments of Kau Bay, Indonesia. Geochim. Cosmochim. Acta 53:1577–81
    [Google Scholar]
  102. Möller KO, St. John M, Temming A, Floeter J, Sell AF et al. 2012. Marine snow, zooplankton and thin layers: indications of a trophic link from small-scale sampling with the Video Plankton Recorder. Mar. Ecol. Prog. Ser. 468:57–69
    [Google Scholar]
  103. Murnane R, Sarmiento J, Le Quéré C 1999. Spatial distribution of air-sea CO2 fluxes and the interhemispheric transport of carbon by the oceans. Glob. Biogeochem. Cycles 13:287–305
    [Google Scholar]
  104. Nagata T, Tamburini C, Arístegui J, Baltar F, Bochdansky AB et al. 2010. Emerging concepts on microbial processes in the bathypelagic ocean – ecology, biogeochemistry, and genomics. Deep-Sea Res. II 57:1519–36
    [Google Scholar]
  105. Napp J, Brooks E, Matrai P, Mullin M. 1988. Vertical distribution of marine particles and grazers. II. Relation of grazer distribution to food quality and quantity. Mar. Ecol. Prog. Ser. 50:59–72
    [Google Scholar]
  106. Niemeyer D, Kriest I, Oschlies A. 2019. The effect of marine aggregate parameterisations on nutrients and oxygen minimum zones in a global biogeochemical model. Biogeosciences 16:3095–111
    [Google Scholar]
  107. Noji TT, Estep KW, MacIntyre F, Norrbin F. 1991. Image analysis of faecal material grazed upon by three species of copepods: evidence for coprorhexy, coprophagy and coprochaly. J. Mar. Biol. Assoc. UK 71:465–80
    [Google Scholar]
  108. Nowald N, Fischer G, Ratmeyer V, Iversen MH, Reuter C, Wefer G. 2009. In-situ sinking speed measurements of marine snow aggregates acquired with a settling chamber mounted to the Cherokee ROV. OCEANS 2009 – Europe Piscataway, NJ: IEEE https://doi.org/10.1109/OCEANSE.2009.5278186
    [Crossref] [Google Scholar]
  109. Olli K, Riser CW, Wassmann P, Ratkova T, Arashkevich E, Pasternak A. 2001. Vertical flux of biogenic matter during a Lagrangian study off the NW Spanish continental margin. Prog. Oceanogr. 51:443–66
    [Google Scholar]
  110. Omand MM, D'Asaro EA, Lee CM, Perry MJ, Briggs N et al. 2015. Eddy-driven subduction exports particulate organic carbon from the spring bloom. Science 348:222–25
    [Google Scholar]
  111. Pabortsava K, Lampitt RS, Benson J, Crowe C, McLachlan R et al. 2017. Carbon sequestration in the deep Atlantic enhanced by Saharan dust. Nat. Geosci. 10:189–94
    [Google Scholar]
  112. Parekh P, Follows MJ, Boyle EA. 2005. Decoupling of iron and phosphate in the global ocean. Glob. Biogeochem. Cycles 19:GB2020
    [Google Scholar]
  113. Passow U, Carlson CA. 2012. The biological pump in a high CO2 world. Mar. Ecol. Prog. Ser. 470:249–71
    [Google Scholar]
  114. Passow U, De La Rocha CL. 2006. Accumulation of mineral ballast on organic aggregates. Glob. Biogeochem. Cycles 20:GB1013
    [Google Scholar]
  115. Pauli NC, Flintrop CM, Konrad C, Pakhomov EA, Swoboda S et al. 2021. Krill and salp faecal pellets contribute equally to the carbon flux at the Antarctic Peninsula. Nat. Commun. 12:7168
    [Google Scholar]
  116. Pavia FJ, Anderson RF, Lam PJ, Cael BB, Vivancos SM et al. 2019. Shallow particulate organic carbon regeneration in the South Pacific Ocean. PNAS 116:9753–58
    [Google Scholar]
  117. Pilskaln HG, Lehmann C, Paduan JB, Silber MW. 1998. Spatial and temporal dynamics in marine aggregate abundance, sinking rate and flux: Monterey Bay, central California. Deep-Sea Res. II 45:1803–37
    [Google Scholar]
  118. Ploug H, Grossart HP. 1999. Bacterial production and respiration in suspended aggregates—a matter of the incubation method. Aquat. Microb. Ecol. 20:21–29
    [Google Scholar]
  119. Ploug H, Iversen MH, Fischer G. 2008a. Ballast, sinking velocity, and apparent diffusivity within marine snow and zooplankton fecal pellets: implications for substrate turnover by attached bacteria. Limnol. Oceanogr. 53:1878–86
    [Google Scholar]
  120. Ploug H, Iversen MH, Koski M, Buitenhuis ET. 2008b. Production, oxygen respiration rates, and sinking velocity of copepod fecal pellets: direct measurements of ballasting by opal and calcite. Limnol. Oceanogr. 53:469–76
    [Google Scholar]
  121. Poulsen LK, Iversen MH. 2008. Degradation of copepod fecal pellets: key role of protozooplankton. Mar. Ecol. Prog. Ser. 367:1–13
    [Google Scholar]
  122. Poulsen LK, Kiørboe T. 2005. Coprophagy and coprorhexy in the copepods Acartia tonas and Temora longicornis: clearance rates and feeding behaviour. Mar. Ecol. Prog. Ser. 299:217–27
    [Google Scholar]
  123. Poulsen LK, Moldrup M, Berge T, Hansen PJ. 2011. Feeding on copepod fecal pellets: a new trophic role of dinoflagellates as detritivores. Mar. Ecol. Prog. Ser. 441:65–78
    [Google Scholar]
  124. Primeau F. 2005. Characterizing transport between the surface mixed layer and the ocean interior with a forward and adjoint global ocean transport model. J. Phys. Oceanogr. 35:545–64
    [Google Scholar]
  125. Puigcorbé V, Benitez-Nelson CR, Masqué P, Verdeny E, White AE et al. 2015. Small phytoplankton drive high summertime carbon and nutrient export in the Gulf of California and eastern tropical North Pacific. Glob. Biogeochem. Cycles 29:1309–32
    [Google Scholar]
  126. Reinthaler T, van Aken H, Veth C, Arístegui J, Robinson C et al. 2006. Prokaryotic respiration and production in the meso- and bathypelagic realm of the eastern and western North Atlantic basin. Limnol. Oceanogr. 51:1262–73
    [Google Scholar]
  127. Richardson TL, Jackson GA. 2007. Small phytoplankton and carbon export from the surface ocean. Science 315:838–40
    [Google Scholar]
  128. Sabatini M, Kiørboe T. 1994. Egg production, growth and development of the cyclopoid copepod Oithona similis. J. Plankton Res. 16:1329–51
    [Google Scholar]
  129. Sarmiento JL, Gruber N. 2006. Ocean Biogeochemical Dynamics Princeton, NJ: Princeton Univ. Press
    [Google Scholar]
  130. Sarmiento JL, Sundquist ET. 1992. Revised budget for the oceanic uptake of anthropogenic carbon dioxide. Nature 356:589–93
    [Google Scholar]
  131. Sarmiento JL, Toggweiler JR. 1984. A new model for the role of the oceans in determining atmospheric . Nature 308:621–24
    [Google Scholar]
  132. Sarthou G, Vincent D, Christaki U, Obernosterer I, Timmermans KR, Brussaard CPD. 2008. The fate of biogenic iron during a phytoplankton bloom induced by natural fertilisation: impact of copepod grazing. Deep-Sea Res. II 55:734–51
    [Google Scholar]
  133. Schmidt K, Atkinson A, Steigenberger S, Fielding S, Lindsay MCM et al. 2011. Seabed foraging by Antarctic krill: implications for stock assessment, bentho-pelagic coupling, and the vertical transfer of iron. Limnol. Oceanogr. 56:1411–28
    [Google Scholar]
  134. Schnetzer A, Steinberg DK. 2002. Active transport of particulate organic carbon and nitrogen by vertically migrating zooplankton in the Sargasso Sea. Mar. Ecol. Prog. Ser. 234:71–84
    [Google Scholar]
  135. Schwinger J, Goris N, Tjiputra JF, Kriest I, Bentsen M et al. 2016. Evaluation of NorESM-OC (versions 1 and 1.2), the ocean carbon-cycle stand-alone configuration of the Norwegian Earth System Model (NorESM1). Geosci. Model Dev. 9:2589–622
    [Google Scholar]
  136. Siegel DA, Buesseler KO, Doney SC, Sailley SF, Behrenfeld MJ, Boyd PW. 2014. Global assessment of ocean carbon export by combining satellite observations and food-web models. Glob. Biogeochem. Cycles 28:181–96
    [Google Scholar]
  137. Siegenthaler U, Wenk T. 1984. Rapid atmospheric CO2 variations and ocean circulation. Nature 308:624–26
    [Google Scholar]
  138. Silver MW, Bruland KW. 1981. Differential feeding and fecal pellet composition of salps and pteropods, and the possible origin of the deep-water flora and olive-green “cells. .” Mar. Biol. 62:263–73
    [Google Scholar]
  139. Silver MW, Shanks AL, Trent JD. 1978. Marine snow: microplankton habitat and source of small-scale patchiness in pelagic populations. Science 201:371–73
    [Google Scholar]
  140. Steinberg DK. 1995. Diet of copepods (Scolpalatum vorax) associated with mesopelagic detritus (giant larvacean houses) in Monterey Bay, California. Mar. Biol. 122:571–84
    [Google Scholar]
  141. Steinberg DK, Cope JS, Wilson SE, Kobari T. 2008. A comparison of mesopelagic mesozooplankton community structure in the subtropical and subarctic North Pacific Ocean. Deep-Sea Res. II 55:1615–35
    [Google Scholar]
  142. Steinberg DK, Goldthwait SA, Hansell DA. 2002. Zooplankton vertical migration and the active transport of dissolved organic and inorganic nitrogen in the Sargasso Sea. Deep-Sea Res. I 49:1445–61
    [Google Scholar]
  143. Steinberg DK, Landry MR. 2017. Zooplankton and the ocean carbon cycle. Annu. Rev. Mar. Sci. 9:413–44
    [Google Scholar]
  144. Steinberg DK, Silver MW, Pilskaln CH, Coale SL, Paduan JB. 1994. Midwater zooplankton communities on pelagic detritus (giant larvacean houses) in Monterey Bay, California. Limnol. Oceanogr. 39:1606–20
    [Google Scholar]
  145. Stemmann L, Jackson GA, Ianson D. 2004. A vertical model of particle size distributions and fluxes in the midwater column that includes biological and physical processes—part I: model formulation. Deep-Sea Res. I 51:865–84
    [Google Scholar]
  146. Stukel MR, Aluwihare LI, Barbeau KA, Chekalyuk AM, Goericke R et al. 2017. Mesoscale ocean fronts enhance carbon export due to gravitational sinking and subduction. PNAS 114:1252–57
    [Google Scholar]
  147. Suess E. 1980. Particulate organic carbon flux in the oceans—surface productivity and oxygen utilization. Nature 288:260–63
    [Google Scholar]
  148. Svensen C, Wexel Riser C, Reigstad M, Seuthe L 2012. Degradation of copepod faecal pellets in the upper layer: role of microbial community and Calanus finmarchicus. Mar. Ecol. Prog. Ser. 462:39–49
    [Google Scholar]
  149. Tamburini C, Garcin J, Ragot M, Bianchi A. 2002. Biopolymer hydrolysis and bacterial production under ambient hydrostatic pressure through a 2000 m water column in the NW Mediterranean. Deep-Sea Res. II 49:2109–23
    [Google Scholar]
  150. Tamburini C, Goutx M, Guigue C, Garel M, Lefevre D et al. 2009. Effects of hydrostatic pressure on microbial alteration of sinking fecal pellets. Deep-Sea Res. II 56:1533–46
    [Google Scholar]
  151. Tamelander T. 2013. Community composition and extracellular enzyme activity of bacteria associated with suspended and sinking particles in contrasting arctic and sub-arctic marine environments. Aquat. Microb. Ecol. 69:211–21
    [Google Scholar]
  152. Thiele S, Fuchs BM, Amann R, Iversen MH. 2015. Colonization in the photic zone and subsequent changes during sinking determine bacterial community composition in marine snow. Appl. Environ. Microbiol. 81:1463–71
    [Google Scholar]
  153. Turley CM, Mackie PJ. 1994. Biogeochemical significance of attached and free-living bacteria and the flux of particles in the NE Atlantic Ocean. Mar. Ecol. Prog. Ser. 115:191–203
    [Google Scholar]
  154. Turner JT. 2015. Zooplankton fecal pellets, marine snow, phytodetritus and the ocean's biological pump. Prog. Oceanogr. 130:205–48
    [Google Scholar]
  155. van der Jagt H, Wiedmann I, Hildebrandt N, Niehoff B, Iversen MH. 2020. Aggregate feeding by the copepods Calanus and Pseudocalanus controls carbon flux attenuation in the Arctic shelf sea during the productive period. Front. Mar. Sci. 7:733
    [Google Scholar]
  156. van Mooy BAS, Keil RG, Devol AH 2002. Impact of suboxia on sinking particulate organic carbon: enhanced carbon flux and preferential degradation of amino acids via denitrification. Geochim. Cosmochim. Acta 66:457–65
    [Google Scholar]
  157. Volk T, Hoffert MI 1985. 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 ET Sundquist, WS Broecker 99–110 Washington, DC: Am. Geophys. Union
    [Google Scholar]
  158. Wassmann P, Olli K, Wexel Riser C, Svensen C 2003. Ecosystem function, biodiversity and vertical flux regulation in the twilight zone. Marine Science Frontiers for Europe G Wefer, F Lamy, F Mantoura 279–87 Berlin: Springer
    [Google Scholar]
  159. Whitmore BM, Ohman MD. 2021. Zooglider-measured association of zooplankton with the fine-scale vertical prey field. Limnol. Oceanogr. 66:3811–27
    [Google Scholar]
  160. Wiedmann I, Ceballos-Romero E, Villa-Alfageme M, Renner AHH, Dybwad C et al. 2020. Arctic observations identify phytoplankton community composition as driver of carbon flux attenuation. Geophys. Res. Lett. 47:e2020GL087465
    [Google Scholar]
  161. Wilson SE, Steinberg DK, Buesseler KO. 2008. Changes in fecal pellet characteristics with depth as indicators of zooplankton repackaging of particles in the mesopelagic zone of the subtropical and subarctic North Pacific Ocean. Deep-Sea Res. II 55:1636–47
    [Google Scholar]
  162. Wotton RS. 1994. Particulate and dissolved organic matter as food. The Biology of Particles in Aquatic Systems RS Wotton 235–88 Boca Raton, FL: CRC. , 2nd ed..
    [Google Scholar]
  163. Yamamoto A, Abe-Ouchi A, Yamanaka Y. 2018. Long-term response of oceanic carbon uptake to global warming via physical and biological pumps. Biogeosciences 15:4163–80
    [Google Scholar]
  164. Yamanaka Y, Tajika E. 1996. The role of the vertical fluxes of particulate organic matter and calcite in the oceanic carbon cycle: studies using an ocean biogeochemical general circulation model. Glob. Biogeochem. Cycles 10:361–82
    [Google Scholar]
/content/journals/10.1146/annurev-marine-032122-035153
Loading
/content/journals/10.1146/annurev-marine-032122-035153
Loading

Data & Media loading...

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error