Abstract
Coastal upwelling regimes associated with eastern boundary currents are the most biologically productive ecosystems in the ocean. As a result, they play a disproportionately important role in the microbially mediated cycling of marine nutrients. These systems are characterized by strong natural variations in carbon dioxide concentrations, pH, nutrient levels and sea surface temperatures on both seasonal and interannual timescales. Despite this natural variability, changes resulting from human activities are starting to emerge. Carbon dioxide derived from fossil fuel combustion is adding to the acidity of upwelled low-pH waters. Low-oxygen waters associated with coastal upwelling systems are growing in their extent and intensity as a result of a rise in upper ocean temperatures and productivity. And nutrient inputs to the coastal ocean continue to grow. Coastal upwelling systems may prove more resilient to changes resulting from human activities than other ocean ecosystems because of their ability to function under extremely variable conditions. Nevertheless, shifts in primary production, fish yields, nitrogen gain and loss, and the flux of climate-relevant gases could result from the perturbation of these highly productive and dynamic ecosystems.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Chavez, F. P. & Messié, M. A comparison of eastern boundary upwelling ecosystems. Prog. Oceanogr. 83, 80–96 (2009).
Ryther, J. H. Photosynthesis and fish production in the sea. Science 166, 72–77 (1969).
Pauly, D. & Christensen, V. Primary production required to sustain global fisheries. Nature 374, 255–258 (1995).
Chavez, F. P., Ryan, J., Lluch-Cota, S. E. & Ñiquen, M. From anchovies to sardines and back: multidecadal change in the Pacific Ocean. Science 299, 217–221 (2003).
Feely, R. A., Sabine, C. L., Hernandez-Ayon, J. M., Ianson, D. & Hales, B. Evidence for upwelling of corrosive 'acidified' water onto the continental shelf. Science 320, 1490 (2008).
IPCC Climate Change 2007: The Physical Science Basis (eds Solomon, S. et al.) (Cambridge Univ. Press, 2007).
Loucaides, S. et al. Biological and physical forcing of carbonate chemistry in an upwelling filament off northwest Africa: results from a Lagrangian study. Glob. Biogeochem. Cycles 26, http://dx.doi.org/10.1029/2011GB004216 (2012).
Lachkar, Z. & Gruber, N. Response of biological production and air–sea CO2 fluxes to upwelling intensification in the California and Canary Current Systems. J. Mar. Syst. 109-110, 149–160 (2013).
Hauri, C. et al. Spatiotemporal variability and long-term trends of ocean acidification in the California Current System. Biogeosciences 10, 193–216 (2013).
Helly, J. J. & Levin, L. A. Global distribution of naturally occurring marine hypoxia on continental margins. Deep Sea Res. Part I: Oceanogr. Res. Pap. 51, 1159–1168 (2004).
Kuypers, M. M. M. et al. Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc. Natl Acad. Sci. USA 102, 6478–6483 (2005).
Glessmer, M. S., Eden, C. & Oschlies, A. Contribution of oxygen minimum zone waters to the coastal upwelling off Mauritania. Prog. Oceanogr. 83, 143–150 (2009).
Hamersley, M. R. et al. Anaerobic ammonium oxidation contributes significantly to nitrogen loss from the Peruvian oxygen minimum zone. Limnol. Oceanogr. 52, 923–933 (2007).
Ward, B. B. et al. Denitrification as the dominant nitrogen loss process in the Arabian Sea. Nature 461, 78–81 (2009).
Capone, D. G. in Microbial Production and Consumption of Greenhouse Gases: Methane, Nitrogen Oxides, and Halomethanes (eds Rogers, J. E. & Whitman, W. B.) 255–275 (Am. Soc. Microbiol, 1991).
Bange, H. in Nitrogen in the Marine Environment 2nd edn (eds Capone, D. G., Bronk, D., Mulholland, M. & Carpenter, E. J.) 52–93 (Academic Press, 2008).
Bruland, K. W., Rue, E. L. & Smith, G. J. Iron and macronutrients in California coastal upwelling regimes: Implications for diatom blooms. Limnol. Oceanogr. 46, 1661–1674 (2001).
Hutchins, D. A., DiTullio, G. R., Zhang, Y. & Bruland, K. W. An iron limitation mosaic in the California upwelling regime. Limnol. Oceanogr. 43, 1037–1054 (1998).
Bruland, K. W., Rue, E. L., Smith, G. J. & DiTullio, G. R. Iron, macronutrients and diatom blooms in the Peru upwelling regime: brown and blue waters of Peru. Mar. Chem. 93, 81–103 (2005).
Hutchins, D. A. et al. Phytoplankton iron limitation in the Humboldt current and Peru upwelling. Limnol. Oceanogr. 47, 997–1011 (2002).
Hutchins, D. A. & Bruland, K. W. Iron-limited growth and Si:N uptake ratio in a coastal upwelling regime. Nature 393, 561–564 (1998).
Deutsch, C., Sarmiento, J. L., Sigman, D. M., Gruber, N. & Dunne, J. P. Spatial coupling of nitrogen inputs and losses in the ocean. Nature 445, 163–167, (2007).
Bonnet, S. et al. Nutrient limitation of primary productivity in the southeast Pacific (BIOSOPE cruise). Biogeosciences 5, 215–225 (2008).
Barber, R. T. & Chavez, F. P. Biological consequences of El Nino. Science 222, 1203–1210 (1983).
Lavaniegos, B. E. & Ohman, M. D. Coherence of long-term variations of zooplankton in two sectors of the California current system. Prog. Oceanogr. 75, 42–69 (2007).
McGowan, J. A., Cayan, D. R. & Dorman, L. R. M. Climate: Ocean variability and ecosystem response in the Northeast Pacific. Science 281, 210–217 (1998).
Gruber, N. et al. Eddy-induced reduction of biological production in eastern boundary upwelling systems. Nature Geosci. 4, 787–792 (2011).
Hofmann, G. E. et al. The effect of ocean acidification on calcifying organisms in marine ecosystems: an organism to ecosystem perspective. Annu. Rev. Ecol. Evol. Systemat. 41, 127–147 (2010).
Gruber, N. et al. Rapid progression of ocean acidification in the California current system. Science 337, 220–223 (2012).
Stramma, L., Johnson, G. C., Sprintall, J. & Mohrholz, V. Expanding oxygen-minimum zones in the tropical oceans. Science 320, 655–658 (2008).
Bograd, S. J. et al. Oxygen declines and the shoaling of the hypoxic boundary in the California Current. Geophys. Res. Lett. 35, L12607 (2008).
Cocco, V. et al. Oxygen and indicators of stress for marine life in multi-model global warming projections. Biogeosciences 10, 1849–1868 (2013).
Dugdale, R., Goering, J., Barber, R., Smith, R. & Packard, T. Denitrification and hydrogen sulfide in the Peru upwelling region during 1976. Deep Sea Res. 24, 601–608 (1977).
Brüchert, V. et al. in Past and Present Water Column Anoxia 161–193 (Springer, 2006).
Chan, F. et al. Emergence of anoxia in the California current large marine ecosystem. Science 319, 920–920 (2008).
California Current Acidification Network. http://c-can.msi.ucsb.edu/news/hypoxic-conditions-found-off-southern-washington-coast-update (2012).
Rykaczewski, R. R. & Dunne, J. P. Enhanced nutrient supply to the California current ecosystem with global warming and increased stratification in an earth system model. Geophys. Res. Lett. 37, L21606 (2010).
Duce, R. A. et al. Impacts of atmospheric anthropogenic nitrogen on the open ocean. Science 320, 893–897 (2008).
Doney, S. C. The growing human footprint on coastal and open-ocean biogeochemistry. Science 328, 1512–1516 (2010).
Bakun, A., Field, D. B., Redondo-Rodriguez, A. & Weeks, S. J. Greenhouse gas, upwelling-favorable winds, and the future of coastal ocean upwelling ecosystems. Glob. Change Biol. 16, 1213–1228 (2010).
Gutiérrez, D. et al. Coastal cooling and increased productivity in the main upwelling zone off Peru since the mid-twentieth century. Geophys. Res. Lett. 38, L07603 (2011).
Santos, F., Gomez Gesteira, M., Decastro, M. & Alvarez, I. Differences in coastal and oceanic SST trends due to the strengthening of coastal upwelling along the Benguela current system. Contin. Shelf Res. 34, 79–86 (2011).
Di Lorenzo, E., Miller, A. J., Schneider, N. & McWilliams, J. C. The warming of the California current system: Dynamics and ecosystem implications. J. Phys. Oceanogr. 35, 336–362 (2005).
Pardo, P. C., Padín, X. A., Gilcoto, M., Farina-Busto, L. & Pérez, F. F. Evolution of upwelling systems coupled to the long-term variability in sea surface temperature and Ekman transport. Clim. Res. 48, 231–246 (2011).
Wang, M., Overland, J. E. & Bond, N. A. Climate projections for selected large marine ecosystems. J. Mar. Syst. 79, 258–266 (2010).
Ackerman, D. & Schiff, K. Modeling storm water mass emissions to the Southern California Bight. J. Environ. Eng. 129, 308–317 (2003).
Nohara, D., Kitoh, A., Hosaka, M. & Oki, T. Impact of climate change on river discharge projected by multimodel ensemble. J. Hydrometeorol. 7, 1076–1089 (2006).
Neuer, S. et al. Dust deposition pulses to the eastern subtropical North Atlantic gyre: does ocean's biogeochemistry respond? Glob. Biogeochem. Cycles 18, GB4020 (2004).
Mahowald, N. M. et al. Atmospheric iron deposition: global distribution, variability, and human perturbations. Annu. Rev. Mar. Sci. 1, 245–278 (2009).
Galloway, J. N. et al. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320, 889 (2008).
Doney, S. C. et al. Impact of anthropogenic atmospheric nitrogen and sulfur deposition on ocean acidification and the inorganic carbon system. Proc. Natl Acad. Sci. USA 104, 14580–14585 (2007).
Gruber, N. & Galloway, J. N. An Earth-system perspective of the global nitrogen cycle. Nature 451, 293–296 (2008).
Hutchins, D. A., Fu, F-X., Webb, E. A. & Tagliabue, A. Taxon-specific response of marine nitrogen fixers to elevated carbon dioxide concentrations. Nature Geosci. 6, 790–795 (2013).
Krishnamurthy, A., Moore, J. K., Mahowald, N., Luo, C. & Zender, C. S. Impacts of atmospheric nutrient inputs on marine biogeochemistry. J. Geophys. Res. Biogeosci. 115, G01006 (2010).
Mills, M., Ridame, C., Davey, M., LaRoche, J. & Geider, R. J. Iron and phosphorus co-limit nitrogen fixation in the Eastern Tropical North Atlantic. Nature 429, 292–294 (2004).
Hinga, K. R. Effects of pH on coastal marine phytoplankton. Mar. Ecol. Prog. Ser. 238, 300 (2002).
Gao, K. et al. Rising CO2 and increased light exposure synergistically reduce marine primary productivity. Nature Clim. Change 2, 519–523 (2012).
Hutchins, D. A., Mulholland, M. R. & Fu, F. Nutrient cycles and marine microbes in a CO2-enriched ocean. Oceanography 22, 128–145 (2009).
Riebesell, U. et al. Enhanced biological carbon consumption in a high CO2 ocean. Nature 450, 545–548 (2007).
Oschlies, A., Schulz, K. G., Riebesell, U. & Schmittner, A. Simulated 21st century's increase in oceanic suboxia by CO2-enhanced biotic carbon export. Glob. Biogeochem. Cycles 22, GB4008 (2008).
Caron, D. A. & Hutchins, D. A. The effects of changing climate on microzooplankton community structure and grazing: drivers, predictions and knowledge gaps. J. Plankton Res. 35, 235–252 (2013).
Farıas, L., Fernández, C., Faúndez, J., Cornejo, M. & Alcaman, M. Chemolithoautotrophic production mediating the cycling of the greenhouse gases N2O and CH4 in an upwelling ecosystem. Biogeosciences 6, 3053–3069 (2009).
Monteiro, P. et al. Variability of natural hypoxia and methane in a coastal upwelling system: oceanic physics or shelf biology? Geophys. Res. Lett. 33, L16614 (2006).
Kock, A., Gebhardt, S. & Bange, H. Methane emissions from the upwelling area off Mauritania (NW Africa). Biogeosciences 5, 1119–1125 (2008).
Naqvi, S. et al. Marine hypoxia/anoxia as a source of CH4 and N2O. Biogeosciences 7, 2159–2190 (2010).
Shi, D., Xu, Y., Hopkinson, B. M. & Morel, F. M. M. Effect of ocean acidification on iron availability to marine phytoplankton. Science 327, 676–679 (2010).
Eppley, R. W. & Peterson, B. J. Particulate organic matter flux and planktonic new production in the deep ocean. Nature 282, 677–680 (1979).
Ward, B. B., Arp, D. J. & Klotz, M. G. in Nitrification, 416 (Am. Soc. Microbiol., 2011).
Ward, B. B. in Nitrification (eds Ward, B. B., Arp, D. J. & Klotz, M. G.) 326–346 (Am. Soc. Microbiol., 2011).
Ward, B. B., Glover, H. E. & Lipschultz, F. Chemoautotrophic activity and nitrification in the oxygen minimum zone off Peru. Deep Sea Res. 36, 1031–1051 (1989).
Freing, A., Wallace, D. W. R. & Bange, H. W. Global oceanic production of nitrous oxide. Phil. Trans. R. Soc. B 367, 1245–1255 (2012).
Beman, J. M. et al. Global declines in oceanic nitrification rates as a consequence of ocean acidification. Proc. Natl Acad. Sci. USA 108, 208–213 (2011).
Rudd, J. W. M., Kelly, C. A., Schindler, D. W. & Turner, M. A. Disruption of the nitrogen cycle in acidified lakes. Science 240, 1515–1517 (1988).
Lam, P. et al. Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proc. Natl Acad. Sci. USA 106, 4752 (2009).
Kalvelage, T. et al. Nitrogen cycling driven by organic matter export in the South Pacific oxygen minimum zone. Nature Geosci. 6, 228–234 (2013).
Hamersley, M. R. et al. Nitrogen fixation within the water column associated with two hypoxic basins in the Southern California Bight. Aquat. Microb. Ecol. 63, 193–205 (2011).
Fernandez, C., Farıas, L. & Ulloa, O. Nitrogen fixation in denitrified marine waters. PLoS ONE 6, e20539 (2011).
Ramos, A. G. et al. Bloom of the marine diazotrophic cyanobacterium Trichodesmium erythraeum in the Northwest African Upwelling. Mar. Ecol. Prog. Ser. 301, 303–305 (2005).
Sohm, J. A., Webb, E. A. & Capone, D. G. Emerging patterns of marine nitrogen fixation. Nature Rev. Microbiol. 9 499–508 (2011).
Breitbarth, E., Oschlies, A. & LaRoche, J. Physiological constraints on the global distribution of Trichodesmium: effect of temperature on diazotrophy. Biogeosciences 4, 53–61 (2007).
Boyd, P. W., Strzepek, R., Fu, F-X. & Hutchins, D. A. Environmental control of open ocean phytoplankton groups: now and in the future. Limnol. Oceanogr. 55, 1353–1376 (2010).
Acknowledgements
Support was provided by the USC Dornsife 2020 Research Clusters Fund to D.G.C. and D.A.H., US National Science Foundation grants OCE 0850801 and 0934073 to D.G.C. and OCE 117030687 and 1260490 to D.A.H., and University of Southern California Sea Grant funding to D.A.H. We acknowledge the critical input of N. Gruber which greatly improved the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplemental Table 1
Interactive environmental change factors affecting coastal upwelling systems. The distinction between drivers and impacts is not necessarily straightforward. (PDF 158 kb)
Rights and permissions
About this article
Cite this article
Capone, D., Hutchins, D. Microbial biogeochemistry of coastal upwelling regimes in a changing ocean. Nature Geosci 6, 711–717 (2013). https://doi.org/10.1038/ngeo1916
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/ngeo1916
This article is cited by
-
Short-term acidification promotes diverse iron acquisition and conservation mechanisms in upwelling-associated phytoplankton
Nature Communications (2023)
-
Biological matter enhanced iron release from shallow marine bioturbated sediments: a case study of Late Cretaceous sandstone, northern Saudi Arabia
International Journal of Earth Sciences (2023)
-
Nitrogen fixation rates in the Guinea Dome and the equatorial upwelling regions in the Atlantic Ocean
Biogeochemistry (2023)
-
Spatio-temporal variation of nitrate based on Landsat 8 in Playa Colorada bay, Sinaloa, Mexico
Environmental Monitoring and Assessment (2023)
-
Ocean-wide comparisons of mesopelagic planktonic community structures
ISME Communications (2023)