The Biological Productivity of the Ocean: Section 4

Citation: Sigman, D. M. & Hain, M. P. (2012) The Biological Productivity of the Ocean: Section 4. Nature Education Knowledge 3(10):19

Productivity fuels life in the ocean, drives its chemical cycles, and lowers atmospheric carbon dioxide. Nutrient uptake and export interact with circulation to yield distinct ocean regimes.

Aa Aa Aa

Previous Section: How Does Ocean Productivity Affect Atmospheric Carbon Dioxide?

Are Humans Changing Ocean Productivity?

Human activities can directly add significant quantities of major and trace nutrients to some regions of the coastal ocean, unambiguously impacting local productivity. While this enhanced productivity could theoretically benefit the upper trophic levels-including fisheries-a host of effects lead to habitat disturbance. As an example, in the waters surrounding the Mississippi Delta and the Chesapeake Bay, the decomposition of the sedimented organic matter produced by nutrient-enhanced phytoplankton blooms lowers the oxygen content of subsurface waters, driving away fish and other complex organisms that require oxygenated water. Anthropogenically enhanced nutrient inputs to the open ocean occur mostly through the atmosphere. In some regions (e.g., the North Atlantic), atmospheric N and Fe deposition on the open ocean has already been measurably enhanced by human activities (Duce et al. 2008), but this enhancement is not yet sufficient to have a clear impact beyond coastal regions and inland seas.

The human impacts on open ocean productivity are likely to be complex. Global warming associated with the anthropogenic increase in greenhouse gases appears to be strengthening upper ocean stratification, reducing the nutrient supply from below and thus decreasing global ocean productivity (Behrenfeld et al. 2006). At the same time, elevated CO₂ concentrations may have a fertilizing effect on some phytoplankton (CO₂ scarcity can restrict the rate of phytoplankton photosynthesis), while negatively impacting some organisms that produce CaCO₃ hard parts (seawater CO₃^2- concentration largely sets the saturation state of CaCO₃ and decreases under higher CO₂) (Morel et al. 2010). Such changes may alter fisheries substantially, but they are currently much less important than the effects of overfishing.

Purposeful fertilization of N- and P-rich polar surface waters with iron has been proposed as a mechanism for mitigating the anthropogenic rise in atmospheric CO₂ by increasing the biological storage of CO₂ in the deep ocean (Sarmiento et al. 2006). However, fertilizing the modern polar ocean for this purpose appears to yield only modest carbon storage and is likely to have substantial negative impacts, the expenditure of the effort aside. First, even if iron fertilization were to lead to complete consumption of nutrients, it takes too long for the deep waters to cycle through the polar ocean surface to substantially alter the currently rapid rise in atmospheric CO₂ (Peng & Broecker 1991). Second, humans appear incapable of intentionally fertilizing a significant fraction of the Southern Ocean on a continuous basis; with only sporadic fertilization, a substantial portion of the additional CO₂ sequestered in the deep ocean would upwell back to the surface to be released. Third, any modest increase in carbon storage that such fertilization does cause will come at the expense of lower oxygen concentrations in the ocean interior, one climate consequence of which may be enhanced release of the greenhouse gas nitrous oxide to the atmosphere (Jin & Gruber 2003).

Glossary

Alkalinity: Alkalinity is closely related to pH, both describing the acid-base chemistry of water. While there are more complete definitions, alkalinity is the excess of strong base over strong acid in a solution.

Autotroph: As opposed to "heterotroph" and "chemo-autotroph", an organism that has the ability to harvest sunlight as a source of chemical energy.

Benthos: The collective group of organisms that share the sea floor as their habitat. This includes organisms that burrow into the sediments, organisms that permanently attach themselves to the seabed substrate, and organisms that simply rest on the seafloor. These benthic lifestyles are distinct from swimming "nekton" and free floating "plankton".

Biological pump: The photosynthetic production, sinking, and deep ocean decomposition of organic matter that cause a vertical gradient of dissolved inorganic carbon in the ocean, in net causing the storage of CO₂ in deep waters and thus lowering atmospheric CO₂. In some cases, the biological pump is taken to involve two components: (1) the rain of soft-tissue organic carbon from the surface to depth, the "soft-tissue pump", and (2) the rain of mineral calcium-carbonate from the surface to depth, the "carbonate pump". The former lowers atmospheric CO₂, while the latter raises it.

Euphotic zone: The upper part of the ocean water column that receives at least 1% of the incident sunlight. The vast majority of photosynthesis in the ocean occurs within this zone.

Export production: The export of organic carbon from a given ecosystem (e.g., the surface mixed layer, the euphotic zone) over a specified time interval.

Fecal pellet: The particulate excretion of zooplankton. Fecal pellets contain substantial amounts of organic carbon and organically-bound nutrients. The sinking of fecal pellets from the surface ocean to depth is one of the main contributors to export production.

Heterotroph: An organism that lives by heterotrophy, in which the organic carbon produced by other organisms is collected and oxidized (or "respired") using a chemical oxidant available in the environment, most commonly oxygen (O₂).

GPP: Gross primary production, the total rate of organic carbon production by autotrophs.

Inorganic carbon: Carbon with the oxidation state +IV, including carbon dioxide (CO₂), carbonic acid (H₂CO₃), bicarbonate ion (HCO₃^-), carbonate ion (CO₃^2-), and carbonate minerals (e.g., calcium carbonate, CaCO₃). Dissolved inorganic carbon (DIC) is the sum of CO₂, H₂CO₃, HCO₃^- and CO₃^2- that are dissolved in water, thereby excluding gas and mineral solids. The ratio among the species of DIC is controlled by pH, with higher pH (lower activity of protons) converting a greater fraction of the CO₂ to HCO₃^- and CO₃^2-.

Microzooplankton: Zooplankton that are small (~ 1-100 µm) and thus can only forage the smallest phytoplankton (of their size or smaller). The body of these small grazers is relatively simple, commonly lacking a complex digestive tract, such that they do not excrete solid fecal pellet but instead release metabolic byproducts back into the water column. For this reason, grazing by microzooplankton promotes nutrient recycling in the surface ocean, thereby raising primary productivity relative to new nutrient supply and export productivity (see "NEP:NPP ratio").

Mixed layer: Or wind-mixed layer, the uppermost skin of the ocean where wind-driven turbulence homogenizes chemical properties of surface water down to the mixed layer depth (MLD). The MLD varies both geographically and seasonally, ranging from a few meters to hundreds of meters.

Nekton: Organisms that swim or are otherwise self-propelled and not largely reliant on ocean viscosity, turbulence, and circulation; for example, fish, whales, and squid. To be distinguished from more or less passively drifting "plankton" and bottom-dwelling "benthos."

NEP: Net ecosystem production, the amount of photosynthesis minus the amount of respiration within a given ecosystem (e.g., the surface mixed layer, the euphotic zone) over a specified time interval. Depending on the ecosystem and the time interval chosen, NEP may closely track the export of organic carbon from the ecosystem (i.e., export production).

NEP:NPP ratio: The ratio between the net ecosystem production and the net production of biomass by phytoplankton (NPP) is a useful measure for nutrient recycling. It has also been named the "f-ratio" (for flux ratio) and represents the fraction of NPP that is supported by new nutrient supply, as opposed to regenerated productivity that is supported by the recycling of nutrients from organic matter within the surface ocean. This ratio is small in the low-nutrient and unproductive subtropical ocean (due to a high degree of recycling) and much greater on the highly productive polar ocean (which has proportionally less recycling).

NPP: Net primary production, which is gross primary production (GPP) minus the autotrophsʼ own rate of respiration; it is thus the rate at which the full metabolism of phytoplankton produces organic matter.

Organic carbon: Carbon that exists in the environment with the oxidation state -IV to +III. Organic carbon is thermodynamically unstable in the presence of the O₂ in the atmosphere and dissolved O₂ in ocean waters (as well as other oxidants, including nitrate and sulfate), such that its biologically mediated oxidation releases energy for life. Organic carbon may exist in particulate or dissolved form.

Photosynthesis: The chemical process that uses sunlight as an energy source for the conversion of (oxidized) carbon dioxide to (reduced) organic carbon.

Phytoplankton: Planktonic organisms that are autotrophic and thus generate chemical energy from sunlight through photosynthesis.

Phytoplankton bloom: When environmental conditions improve, autotrophic phytoplankton may grow and divide rapidly, resulting in an increase in biomass and cell numbers and fuelling higher trophic levels. Thus, increasing light (e.g., winter to summer, shoaling of mixed layer depth), nutrient input and low grazing stress encourage the development of blooms. Overall, if net primary production by a given autotroph exceeds the sum of their mortality and grazing losses this organism is said to bloom. The increase of biomass during a bloom provides the feedstock for secondary production by heterotrophic organisms, which ultimately leads to increased grazing stress on the blooming organism. Over the annual cycle a given ocean region typically experiences a complex succession of blooms by specific autotrophic organisms, closely associated with rises in the population of their respective grazers.

Plankton: Organisms that are suspended in and largely drift in ocean water; can be subdivided into (1) (autotrophic) phytoplankton and (2) (heterotrophic) zooplankton and bacteria.

Remineralization: The transformation of organic matter to inorganic constituents (e.g., dissolved inorganic carbon, nitrate, and phosphate). Synonymous with "decomposition," but focusing on the consequence of this process of returning nutrients and other chemical to their dissolved, inorganic form. See also "respiration."

Respiration: The oxidation of organic matter (largely organic carbon being oxidized to carbon dioxide) for the purpose of yielding chemical energy for basic life functions. Often results in the conversion of particulate organic matter back to dissolved inorganic chemicals.

Secondary production (SP): The growth rate of heterotrophic biomass.

Zooplankton: Planktonic organisms that graze upon organic matter, fulfilling their energy requirements by the respiration of organic carbon.

References and Recommended Reading

Altabet, M. A. et al. Climate-related variations in denitrification in the Arabian Sea from sediment ¹⁵N/¹⁴N ratios. Nature 373, 506-509 (1995). doi:10.1038/373506a0

Anbar, A. D. & Knoll, A. H. Proterozoic ocean chemistry and evolution: A bioinorganic bridge? Science 297, 1137-1142 (2002). doi:10.1126/science.1069651

Archer, D. "Biological fluxes in the ocean and atmospheric p_CO2," in Treatise on Geochemistry, Vol. 6, eds. H. D. Holland & K. K. Turekian (Elsevier, 2003) 275-291.

Arrigo, K. R. et al. Phytoplankton community structure and the drawdown of nutrients and CO₂ in the Southern Ocean. Science 283, 365-367 (1999). doi:10.1126/science.283.5400.365

Barbeau, K. et al. Photochemical cycling of iron in the surface ocean mediated by microbial iron(III)-binding ligands. Nature 413, 409-413 (2001). doi:10.1038/35096545

Behrenfeld, M. J. et al. Climate-driven trends in contemporary ocean productivity. Nature 444, 752-755 (2006). doi:10.1038/nature05317

Bender, M. et al. A comparison of 4 methods for determining planktonic community production. Limnology and Oceanography 32, 1085-1098 (1987).

Boyd, P. W. & Ellwood, M. J. The biogeochemical cycle of iron in the ocean. Nature Geoscience 3, 675-682 (2010). doi:10.1038/ngeo964

Boyd, P. W. et al. Mesoscale iron enrichment experiments 1993-2005: Synthesis and future directions. Science 315, 612-617 (2007). doi:10.1126/science.1131669

Brandes, J. A. & Devol, A. H. A global marine-fixed nitrogen isotopic budget: Implications for Holocene nitrogen cycling. Global Biogeochemical Cycles 16, 1120 (2002). doi:10.1029/2001gb001856

Broecker, W. S. Ocean chemistry during glacial time. Geochimica et Cosmochimica Acta 46, 1689-1705 (1982). doi:10.1016/0016-7037(82)90110-7

Buesseler, K. O. The decoupling of production and particulate export in the surface ocean. Global Biogeochemical Cycles 12, 297-310 (1998). doi:10.1029/97gb03366

Chisholm, S. W. et al. A novel free-living prochlorophyte abundant in the oceanic euphotic zone. Nature 334, 340-343 (1988). doi:10.1038/334340a0

Christensen, J. P. Carbon export from continental shelves, denitrification and atmospheric carbon dioxide. Continental Shelf Research 14, 547-576 (1994). doi:10.1016/0278-4343(94)90103-1

Morel, F. M. M. et al. Ocean Acidification: A National Strategy to Meet the Challenges of a Changing Ocean. The National Academic Press, 2010.

Cullen, J. J. The deep chlorophyll maximum: Comparing vertical profiles of chlorophyll a. Canadian Journal of Fisheries and Aquatic Sciences 39, 791-803 (1982). doi:10.1139/f82-108

Dalsgaard, T., Thamdrup, B. & Canfield, D. E. Anaerobic ammonium oxidation (anammox) in the marine environment. Research in Microbiology 156, 457-464 (2005). doi:10.1016/j.resmic.2005.01.011

de Baar, H. J. W. von Liebig's Law of the Minimum and plankton ecology (1899-1991). Progress in Oceanography 33, 347-386 (1994). doi:10.1016/0079-6611(94)90022-1

Deutsch, C. et al. Isotopic constraints on glacial/interglacial changes in the oceanic nitrogen budget. Global Biogeochemical Cycles 18, GB4012 (2004). doi:10.1029/2003gb002189

Deutsch, C. et al. Spatial coupling of nitrogen inputs and losses in the ocean. Nature 445, 163-167 (2007). doi:10.1038/nature05392

Duce, R. A. et al. Impacts of atmospheric anthropogenic nitrogen on the open ocean. Science 320, 893-897 (2008). doi:10.1126/science.1150369

Dugdale, R. C. & Goering, J. J. Uptake of new and regenerated forms of nitrogen in primary productivity. Limnology and Oceanography 12, 196-206 (1967).

Emerson, S. & Hedges, J. "Sediment diagenesis and benthic flux," in Treatise on Geochemistry, Vol. 6, eds. H. D. Holland & K. K. Turekian (Elsevier, 2003) 293-319.

Eppley, R. W. & Peterson, B. J. Particulate organic matter flux and planktonic new production in the deep ocean. Nature 282, 677-680 (1979). doi:10.1038/282677a0

Falkowski, P. G. Evolution of the nitrogen cycle and its influence on the biological sequestration of CO₂ in the ocean. Nature 387, 272-275 (1997). doi:10.1038/387272a0

Francois, R. et al. Contribution of Southern Ocean surface-water stratification to low atmospheric CO₂ concentrations during the last glacial period. Nature 389, 929-935 (1997).

Froelich, P. N. et al. The marine phosphorus cycle. American Journal of Science 282, 474-511 (1982).

Ganeshram, R. S. et al. Large changes in oceanic nutrient inventories from glacial to interglacial periods. Nature 376, 755-758 (1995). doi:10.1038/376755a0

Geider, R. J., MacIntyre, H. L. & Kana, T. M. Dynamic model of phytoplankton growth and acclimation: Responses of the balanced growth rate and the chlorophyll a:carbon ratio to light, nutrient-limitation and temperature. Marine Ecology-Progress Series 148, 187-200 (1997). doi:10.3354/meps148187

Hansell, D. A. et al. Dissolved organic matter in the ocean: A controversy stimulates new insights. Oceanography 22, 202-211 (2009).

Jaccard, S. L. et al. Glacial/interglacial changes in subarctic North Pacific stratification. Science 308, 1003-1006 (2005). doi:10.1126/science.1108696

Jin, X. & Gruber, N. Offsetting the radiative benefit of ocean iron fertilization by enhancing N₂O emissions. Geophysical Research Letters 30, 2249 (2003). doi:10.1029/2003gl018458

Johnson, K. S., Gordon, R. M. & Coale, K. H. What controls dissolved iron concentrations in the world ocean? Marine Chemistry 57, 137-161 (1997). doi:10.1016/s0304-4203(97)00043-1

Kennett, J. P. Cenozoic evolution of Antarctic glaciation, the circum-Antarctic Ocean, and their impact on global paleoceanography. Journal of Geophysical Research-Oceans and Atmospheres 82, 3843-3860 (1977). doi:10.1029/JC082i027p03843

Kilham, P. & Hecky, R. E. Comparative ecology of marine and fresh-water phytoplankton. Limnology and Oceanography 33, 776-795 (1988).

Kohfeld, K. E. et al. Role of marine biology in glacial-interglacial CO₂ cycles. Science 308, 74-78 (2005). doi:10.1126/science.1105375

Landry, M. R. & Hassett, R. P. Estimating the grazing impact of marine micro-zooplankton. Marine Biology 67, 283-288 (1982). doi:10.1007/bf00397668

Maldonado, M. T. et al. Co-limitation of phytoplankton growth by light and Fe during winter in the NE subarctic Pacific Ocean. Deep-Sea Research Part II-Topical Studies in Oceanography 46, 2475-2485 (1999). doi:10.1016/s0967-0645(99)00072-7

Martin, J. H. & Fitzwater, S. E. Iron-deficiency limits phytoplankton growth in the Northeast Pacific Subarctic. Nature 331, 341-343 (1988). doi:10.1038/331341a0

Martin, J. H. et al. VERTEX: Phytoplankton/iron studies in the Gulf of Alaska. Deep-Sea Research Part A: Oceanographic Research Papers 36, 649-680 (1989). doi:10.1016/0198-0149(89)90144-1

Martin, J. H. et al. VERTEX: Carbon cycling in the northeast Pacific. Deep-Sea Research Part A: Oceanographic Research Papers 34, 267-285 (1987). doi:10.1016/0198-0149(87)90086-0

Martin, J. H. Glacial-interglacial CO₂ change: The iron hypothesis. Paleoceanography 5, 1-13 (1990). doi:10.1029/PA005i001p00001

Martinez-Garcia, A. et al. Southern Ocean dust-climate coupling over the past four million years. Nature 476, 312-315 (2011). doi:10.1038/nature10310

Michaels, A. F. & Silver, M. W. Primary production, sinking fluxes and the microbial food web. Deep-Sea Research Part A: Oceanographic Research Papers 35, 473-490 (1988). doi:10.1016/0198-0149(88)90126-4

Mitchell, B. G. et al. Light limitation of phytoplankton biomass and macronutrient utilization in the Southern Ocean. Limnology and Oceanography 36, 1662-1677 (1991).

Morel, F. M. M. The co-evolution of phytoplankton and trace element cycles in the oceans. Geobiology 6, 318-324 (2008).

Morel, F. M. M., Milligan, A. J. & Saito, M. A. "Marine bioinorganic chemistry: The role of trace metals in the oceanic cycles of major nutrients," in Treatise on Geochemistry, Vol. 6, eds. H. D. Holland & K. K. Turekian (Elsevier, 2003) 113-143.

Morel, F. M. M., Rueter, J. G. & Price, N. M. Iron nutrition of phytoplankton and its possible importance in the ecology of ocean regions with high nutrient and low biomass. Oceanography 4, 56-61 (1991).

Mortlock, R. A. et al. Evidence for lower productivity in the Antarctic during the last glaciation. Nature 351, 220-223 (1991). doi:10.1038/351220a0

Palter, J. B. et al. Fueling export production: Nutrient return pathways from the deep ocean and their dependence on the Meridional Overturning Circulation. Biogeosciences 7, 3549-3568 (1991). doi:10.5194/bg-7-3549-2010

Peng, T. H. & Broecker, W. S. Dynamic limitations on the Antarctic iron fertilization strategy. Nature 349, 227-229 (1991). doi:10.1038/349227a0

Rau, G. H., Arthur, M. A. & Dean, W. E. ¹⁵N/¹⁴N variations in Cretaceous Atlantic sedimentary sequences: Implication for past changes in marine nitrogen biogeochemistry. Earth and Planetary Science Letters 82, 269-279 (1987). doi:10.1016/0012-821x(87)90201-9

Redfield, A. C. The biological control of chemical factors in the environment. American Scientist 46, 205-221 (1958).

Ren, H. et al. Foraminiferal isotope evidence of reduced nitrogen fixation in the Ice Age Atlantic Ocean. Science 323, 244-248 (2009). doi:10.1126/science.1165787

Ruttenberg, K. C. Reassessment of the oceanic residence time of phosphorous. Chemical Geology 107, 405-409 (1993). doi:10.1016/0009-2541(93)90220-d

Sarmiento, J. L. & Bender, M. Carbon biogeochemistry and climate change. Photosynthesis Research 39, 209-234 (1994). doi:10.1007/bf00014585

Sarmiento, J. L. et al. High-latitude controls of thermocline nutrients and low latitude biological productivity. Nature 427, 56-60 (2004). doi:10.1038/nature02127

Sarmiento, J. L. & Toggweiler, J. R. A new model for the role of the oceans in determining atmospheric pCO₂. Nature 308, 621-624 (1984).

Sarmiento, J. L., Gnanadesikan, A. & Gruber, N. Carbon Sequestration by Patch Fertilization: A Comprehensive Assessment Using Coupled Physical-Ecological-Biogeochemical Models. Final Report. Princeton, NJ: DOE Office of Biological and Environmental Research, 2006.

Sarmiento, J. L. & Gruber, N. Ocean Biogeochemical Cycles. Princeton, NJ: Princeton University Press, 2006.

Schindler, D. W. Evolution of phosphorus limitation in lakes. Science 195, 260-262 (1977). doi:10.1126/science.195.4275.260

Siegel, D. A., Doney, S. C. & Yoder, J. A. The North Atlantic spring phytoplankton bloom and Sverdrup's critical depth hypothesis. Science 296, 730-733 (2002). doi:10.1126/science.1069174

Sigman, D. M. & Boyle, E. A. Glacial/interglacial variations in atmospheric carbon dioxide. Nature 407, 859-869 (2000). doi: 10.1038/35038000

Sigman, D. M., Hain, M. P. & Haug, G. H. The polar ocean and glacial cycles in atmospheric CO₂ concentration. Nature 466, 47-55 (2010). doi:10.1038/nature09149

Smith, R. C. Remote sensing and depth distribution of ocean chlorophyll. Marine Ecology-Progress Series 5, 359-361 (1981). doi:10.3354/meps005359

Sunda, W. G. & Huntsman, S. A. Interrelated influence of iron, light and cell size on marine phytoplankton growth. Nature 390, 389-392 (1997). doi:10.1038/37093

Treguer, P. et al. The silica balance in the world ocean: A reestimate. Science 268, 375-379 (1995). doi:10.1126/science.268.5209.375

Tyrrell, T. The relative influences of nitrogen and phosphorus on oceanic primary production. Nature 400, 525-531 (1999). doi:10.1038/22941

VanCappellen, P. & Ingall, E. D. Redox stabilization of the atmosphere and oceans by phosphorus-limited marine productivity. Science 271, 493-496 (1996). doi:10.1126/science.271.5248.493

Volk, T. & Hoffert, M. I. "Ocean carbon pumps: Analysis of relative strengths and efficiencies in ocean-driven atmospheric CO₂ changes," in The Carbon Cycle and Atmospheric CO₂: Natural Variations Archaean to Present, Geophysical Monograph Series, Vol. 32, eds. E. T. Sundquist & W. S. Broeker. (American Geophysical Union, 1985) 99-110. ()

Watson, A. J. et al. Effect of iron supply on Southern Ocean CO₂ uptake and implications for glacial atmospheric CO₂. Nature 407, 730-733 (2000). doi:10.1038/35037561

Waterbury, J. B. et al. Widespread occurrence of a unicellular, marine, planktonic, cyanobacterium. Nature 277, 293-294 (1979). doi:10.1038/277293a0

Weber, T. S. & Deutsch, C. Ocean nutrient ratios governed by plankton biogeography. Nature 467, 550-554 (2010). doi:10.1038/nature09403