Estuaries and Coasts

, Volume 41, Issue 4, pp 1102–1117 | Cite as

Quantifying Metabolically Driven pH and Oxygen Fluctuations in US Nearshore Habitats at Diel to Interannual Time Scales

  • Hannes BaumannEmail author
  • Erik M. Smith


We compiled and examined 15 years (2002–2016) of high-frequency monitoring data from the National Estuarine Research Reserve System (NERRS) to characterize diel to interannual variability of pH and dissolved oxygen (DO, % saturation) across 16 diverse, shallow-water habitats along the US Atlantic, Gulf of Mexico, Caribbean, and Pacific coasts. We asked whether these systems exhibit a common pH/DO relationship, whether there were detectable interannual trends in temperature, pH, and DO within and across systems, and how pH/DO dynamics would relate to measured levels of nutrients and chlorophyll. Our analyses confirmed that large, metabolically driven, and thus concurrent fluctuations of pH and DO are a unifying feature of nearshore habitats. Moreover, we derived well-constrained relationships that predict (i) monthly mean pH or (ii) mean diel pH fluctuations across systems based on habitat mean salinity and (i) mean DO or (ii) mean diel DO fluctuations. This suggests that common metabolic principles drive diel to seasonal pH/DO variations within as well as across a diversity of estuarine environments. Yearly pH and DO anomalies did not show monotonous trends over the study period and differed considerably between sites and regions. However, weekly anomalies of means, diel minima, and diel ranges of pH and DO changed significantly over time and were strongly correlated to temperature anomalies. These general patterns lend strong empirical support to the notion that coastal acidification—in addition to being driven by eutrophication and atmospheric CO2 increases—is exacerbated simply by warming, likely via increasing community respiration. Nutrient and chlorophyll dynamics were inversely related in these shallow, well-mixed systems, but higher nutrient levels were still associated with lower pH and lower DO levels in most, but not all, systems. Our analyses emphasize the particular dynamics of nearshore habitats and the critical importance of NERRS and its system-wide monitoring program.


Eutrophication Ecosystem metabolism Oxygen saturation Ocean acidification Multistressor Climate change National Estuarine Research Reserve System (NERRS) 



This study would not have been possible if the NERRS System-Wide Monitoring Program did not exist. Our gratitude to the entirety of the SWMP technical staff for their dedicated and meticulous efforts in maintaining this valuable program for more than two decades cannot be overstated.


This study was partially supported by NSF #1536336 to H.B. and NOAA #NA15NOS4200120 to E. S.

Supplementary material

12237_2017_321_MOESM1_ESM.docx (151 kb)
Table S1 (DOCX 151 kb)


  1. Barbier, E.B., S.D. Hacker, C. Kennedy, E.W. Koch, A.C. Stier, and B.R. Silliman. 2011. The value of estuarine and coastal ecosystem services. Ecological Monographs 81: 169–193.CrossRefGoogle Scholar
  2. Barton, A., B. Hales, G.G. Waldbusser, C. Langdon, and R.A. Feely. 2012. The Pacific oyster, Crassostrea gigas, shows negative correlation to naturally elevated carbon dioxide levels: implications for near-term ocean acidification effects. Limnology and Oceanography 57: 689–710.CrossRefGoogle Scholar
  3. Bates, N.R., M.H.P. Best, K. Neely, R. Garley, A.G. Dickson, and R.J. Johnson. 2012. Detecting anthropogenic carbon dioxide uptake and ocean acidification in the North Atlantic Ocean. Biogeosciences 9: 2509–2522.CrossRefGoogle Scholar
  4. Baumann, H., R. Wallace, T. Tagliaferri, and C.J. Gobler. 2015. Large natural pH, CO2 and O2 fluctuations in a temperate tidal salt marsh on diel, seasonal and interannual time scales. Estuaries and Coasts 38: 220–231.CrossRefGoogle Scholar
  5. Beck, M.W., K.L. Heck, K.W. Able, D.L. Childers, D.B. Eggleston, B.M. Gillanders, B.S. Halpern, C.G. Hayes, K. Hoshino, and T.J. Minello. 2003. The role of nearshore ecosystems as fish and shellfish nurseries. Issues in Ecology 11: 1–12.Google Scholar
  6. Borges, A.V., and M. Frankignoulle. 2002. Distribution and air-water exchange of carbon dioxide in the Scheldt plume off the Belgian coast. Biogeochemistry 59: 41–67.CrossRefGoogle Scholar
  7. Branch, T.A., B.M. DeJoseph, L.J. Ray, and C.A. Wagner. 2013. Impacts of ocean acidification on marine seafood. Trends in Ecology & Evolution 28: 178–186.CrossRefGoogle Scholar
  8. Breitburg, D.L., D. Hondorp, C. Audemard, R.B. Carnegie, R.B. Burrell, M. Trice, and V. Clark. 2015a. Landscape-level variation in disease susceptibility related to shallow-water hypoxia. PloS One 10: e0116223.CrossRefGoogle Scholar
  9. Breitburg, D.L., J. Salisbury, J.M. Bernhard, W.-J. Cai, S. Dupont, S.C. Doney, K.J. Kroeker, L. Levin, W.C. Long, L.M. Milke, S.H. Miller, B. Phelan, U. Passow, B.A. Seibel, A.E. Todgham, and A.M. Tarrant. 2015b. And on top of all that… coping with ocean acidification in the midst of many stressors. Oceanography 28: 48–61.CrossRefGoogle Scholar
  10. Buskey, E., M. Bundy, M. Ferner, D. Porter, W. Reay, E. Smith, and D. Trueblood. 2015. System-wide monitoring program of the National Estuarine Research Reserve System: research and monitoring to address coastal management issues. In Coastal ocean observing systems: advances and syntheses, ed. Y. Liu, H. Kerkering, R. Weisberg, 392–414. Cambridge, USA: Academic Press.Google Scholar
  11. Caffrey, J.M. 2003. Production, respiration and net ecosystem metabolism in US estuaries. Coastal Monitoring through Partnerships 81: 207–219.CrossRefGoogle Scholar
  12. Cai, W.-J., Y. Wang, J. Krest, and W. Moore. 2003a. The geochemistry of dissolved inorganic carbon in a surficial groundwater aquifer in North Inlet, South Carolina, and the carbon fluxes to the coastal ocean. Geochimica et Cosmochimica Acta 67: 631–639.CrossRefGoogle Scholar
  13. Cai, W.J., Z.A. Wang, and Y. Wang. 2003b. The role of marsh-dominated heterotrophic continental margins in transport of CO2 between the atmosphere, the land-sea interface and the ocean. Geophysical Research Letters 30, 1849.
  14. Cloern, J.E., P.C. Abreu, J. Carstensen, L. Chauvaud, R. Elmgren, J. Grall, H. Greening, J.O.R. Johansson, M. Kahru, and E.T. Sherwood. 2016. Human activities and climate variability drive fast-paced change across the world’s estuarine–coastal ecosystems. Global Change Biology 22: 513–529.CrossRefGoogle Scholar
  15. Conley, D.J., C. Humborg, L. Rahm, O.P. Savchuk, and F. Wulff. 2002. Hypoxia in the Baltic Sea and basin-scale changes in phosphorus biogeochemistry. Environmental Science & Technology 36: 5315–5320.CrossRefGoogle Scholar
  16. Costanza, R., R. d'Arge, R. de Groot, S. Farber, M. Grasso, B. Hannon, K. Limburg, S. Naeem, R.V. O'Neill, J. Paruelo, R.G. Raskin, P. Sutton, and M. van den Belt. 1997. The value of the world’s ecosystem services and natural capital. Nature 387: 253–260.CrossRefGoogle Scholar
  17. Doney, S.C., V.J. Fabry, R.A. Feely, and J.A. Kleypas. 2009. Ocean acidification: the other CO2 problem. Annual Review of Marine Science 1: 169–192.CrossRefGoogle Scholar
  18. Duarte, C.M., I.E. Hendriks, T.S. Moore, Y.S. Olsen, A. Steckbauer, L. Ramajo, J. Carstensen, J.A. Trotter, and M. McCulloch. 2013. Is ocean acidification an open-ocean syndrome? Understanding anthropogenic impacts on seawater pH. Estuaries and Coasts 36: 221–236.CrossRefGoogle Scholar
  19. Gattuso, J.P., M. Frankignoulle, and R. Wollast. 1998. Carbon and carbonate metabolism in coastal aquatic ecosystems. Annual Review of Ecology and Systematics 29: 405–434.CrossRefGoogle Scholar
  20. Gobler, C.J., and H. Baumann. 2016. Hypoxia and acidification in marine ecosystems: coupled dynamics and effects on ocean life. Biology Letters 12: 20150976.CrossRefGoogle Scholar
  21. Gobler, C.J., E. Depasquale, A. Griffith, and H. Baumann. 2014. Hypoxia and acidification have additive and synergistic negative effects on the growth, survival, and metamorphosis of early life stage bivalves. PloS One 9: e83648.CrossRefGoogle Scholar
  22. Hagy, J.D., W.R. Boynton, C.W. Keefe, and K.V. Wood. 2004. Hypoxia in Chesapeake Bay, 1950–2001: long-term change in relation to nutrient loading and river flow. Estuaries 27: 634–658.CrossRefGoogle Scholar
  23. Harley, C.D.G., A. Randall Hughes, K.M. Hultgren, B.G. Miner, C.J.B. Sorte, C.S. Thornber, L.F. Rodriguez, L. Tomanek, and S.L. Williams. 2006. The impacts of climate change in coastal marine systems. Ecology Letters 9: 228–241.CrossRefGoogle Scholar
  24. Hauri, C., N. Gruber, A. McDonnell, and M. Vogt. 2013. The intensity, duration, and severity of low aragonite saturation state events on the California continental shelf. Geophysical Research Letters 40: 3424–3428.CrossRefGoogle Scholar
  25. Herrmann, M., R.G. Najjar, W.M. Kemp, R.B. Alexander, E.W. Boyer, W.J. Cai, P.C. Griffith, K.D. Kroeger, S.L. McCallister, and R.A. Smith. 2015. Net ecosystem production and organic carbon balance of US East Coast estuaries: a synthesis approach. Global Biogeochemical Cycles 29: 96–111.CrossRefGoogle Scholar
  26. Hofmann, G.E., J.E. Smith, K.S. Johnson, U. Send, L.A. Levin, F. Micheli, A. Paytan, N.N. Price, B. Peterson, Y. Takeshita, P.G. Matson, E.D. Crook, K.J. Kroeker, M.C. Gambi, E.B. Rivest, C.A. Frieder, P.C. Yu, and T.R. Martz. 2011. High-frequency dynamics of ocean pH: a multi-ecosystem comparison. PloS One 6: e28983.CrossRefGoogle Scholar
  27. Holland, A.F., D.M. Sanger, C.P. Gawle, S.B. Lerberg, M.S. Santiago, G.H. Riekerk, L.E. Zimmerman, and G.I. Scott. 2004. Linkages between tidal creek ecosystems and the landscape and demographic attributes of their watersheds. Journal of Experimental Marine Biology and Ecology 298: 151–178.CrossRefGoogle Scholar
  28. Keeling, R.F., A. Körtzinger, and N. Gruber. 2010. Ocean deoxygenation in a warming world. Annual Review of Marine Science 2: 199–229.CrossRefGoogle Scholar
  29. Kemp, W.M., and J.M. Testa. 2011. Metabolic balance between ecosystem production and consumption. In Treatise on estuaries and coastal science, vol. 7, ed. E. Wolansky and D. McLusky, 83–118. Oxford: Elsevier LtdGoogle Scholar
  30. Kneib, R.T. 1997. The role of tidal marshes in the ecology of estuarine nekton. Oceanography and Marine Biology 35: 163–220.Google Scholar
  31. Kristensen, E. 1993. Seasonal variations in benthic community metabolism and nitrogen dynamics in a shallow, organic-poor Danish lagoon. Estuarine, Coastal and Shelf Science 36: 565–586.CrossRefGoogle Scholar
  32. Lauvset, S., N. Gruber, P. Landschützer, A. Olsen, and J. Tjiputra. 2015. Trends and drivers in global surface ocean pH over the past 3 decades. Biogeosciences 12: 1285.CrossRefGoogle Scholar
  33. Levin, L., W. Ekau, A. Gooday, F. Jorissen, J. Middelburg, S. Naqvi, C. Neira, N. Rabalais, and J. Zhang. 2009. Effects of natural and human-induced hypoxia on coastal benthos. Biogeosciences 6: 2063–2098.CrossRefGoogle Scholar
  34. Levin, L.A., and D.L. Breitburg. 2015. Linking coasts and seas to address ocean deoxygenation. Nature Climate Change 5: 401–403.CrossRefGoogle Scholar
  35. Long, M.C., C. Deutsch, and T. Ito. 2016. Finding forced trends in oceanic oxygen. Global Biogeochemical Cycles 30: 381–397.CrossRefGoogle Scholar
  36. Melzner, F., J. Thomsen, W. Koeve, A. Oschlies, M. Gutowska, H. Bange, H. Hansen, and A. Körtzinger. 2012. Future ocean acidification will be amplified by hypoxia in coastal habitats. Marine Biology 160: 1875–1888.CrossRefGoogle Scholar
  37. Moore, K.A., and J.C. Jarvis. 2008. Environmental factors affecting recent summertime eelgrass diebacks in the lower Chesapeake Bay: implications for long-term persistence. Journal of Coastal Research 55: 135–147.Google Scholar
  38. Nixon, S.W., S. Granger, B.A. Buckley, M. Lamont, and B. Rowell. 2004. A one hundred and seventeen year coastal water temperature record from Woods Hole, Massachusetts. Estuaries 27: 397–404.CrossRefGoogle Scholar
  39. O’Boyle, S., G. McDermott, T. Noklegaard, and R. Wilkes. 2013. A simple index of trophic status in estuaries and coastal bays based on measurements of pH and dissolved oxygen. Estuaries and Coasts 36: 158–173.CrossRefGoogle Scholar
  40. Oczkowski, A., C.W. Hunt, K. Miller, C. Oviatt, S. Nixon, and L. Smith. 2016. Comparing measures of estuarine ecosystem production in a temperate New England estuary. Estuaries and Coasts 39: 1827–1844.CrossRefGoogle Scholar
  41. Odum, E.P. 1961. The role of tidal marshes in estuarine production. The Conservationist 15: 12–15.Google Scholar
  42. Odum, W.E., E.P. Odum, and H.T. Odum. 1995. Nature’s pulsing paradigm. Estuaries 18: 547–555.CrossRefGoogle Scholar
  43. Porter, D.E., T. Small, D.White, M. Fletcher, A. Norman, D. Swain, and J. Friedmann. 2004. Data management in support of environmental monitoring, research, and coastal management. Journal of Coastal Research 45: 9–16.Google Scholar
  44. Pörtner, H.O. 2012. Integrating climate-related stressor effects on marine organisms: unifying principles linking molecule to ecosystem-level changes. Marine Ecology Progress Series 470: 273–290.CrossRefGoogle Scholar
  45. Provoost, P., S. van Heuven, K. Soetaert, R.W.P.M. Laane, and J.J. Middelburg. 2010. Seasonal and long-term changes in pH in the Dutch coastal zone. Biogeosciences 7: 3869–3878.CrossRefGoogle Scholar
  46. Riley, G.A. 1972. Patterns of production in marine ecosystems. In Ecosystem structure and function, ed. J. A. Wiens, 91–112. Corvallis: University of Oregon Press.Google Scholar
  47. Rockstrom, J., W. Steffen, K. Noone, A. Persson, F.S. Chapin, E.F. Lambin, T.M. Lenton, M. Scheffer, C. Folke, H.J. Schellnhuber, B. Nykvist, C.A. de Wit, T. Hughes, S. van der Leeuw, H. Rodhe, S. Sorlin, P.K. Snyder, R. Costanza, U. Svedin, M. Falkenmark, L. Karlberg, R.W. Corell, V.J. Fabry, J. Hansen, B. Walker, D. Liverman, K. Richardson, P. Crutzen, and J.A. Foley. 2009. A safe operating space for humanity. Nature 461: 472–475.CrossRefGoogle Scholar
  48. Salisbury, J., M. Green, C. Hunt, and J. Campbell. 2008. Coastal acidification by rivers: a new threat to shellfish? Eos, Transactions, American Geophysical Union 89: 513.CrossRefGoogle Scholar
  49. Salisbury, J., D. Vandemark, C. Hunt, J. Campbell, B. Jonsson, A. Mahadevan, W. McGillis, and H. Xue. 2009. Episodic riverine influence on surface DIC in the coastal Gulf of Maine. Estuarine, Coastal and Shelf Science 82: 108–118.CrossRefGoogle Scholar
  50. Soetaert, K., A.F. Hofmann, J.J. Middelburg, F.J.R. Meysman, and J. Greenwood. 2007. The effect of biogeochemical processes on pH. Marine Chemistry 105: 30–51.CrossRefGoogle Scholar
  51. Turner, R.E., N.N. Rabalais, and D. Justic. 2008. Gulf of Mexico hypoxia: alternate states and a legacy. Environmental Science & Technology 42: 2323–2327.CrossRefGoogle Scholar
  52. Van Dolah, R.F., G.H. Riekerk, D.C. Bergquist, J. Felber, D.E. Chestnut, and A.F. Holland. 2008. Estuarine habitat quality reflects urbanization at large spatial scales in South Carolina’s coastal zone. Science of the Total Environment 390: 142–154.CrossRefGoogle Scholar
  53. Vaquer-Sunyer, R., and C.M. Duarte. 2011. Temperature effects on oxygen thresholds for hypoxia in marine benthic organisms. Global Change Biology 17: 1788–1797.CrossRefGoogle Scholar
  54. Waldbusser, G.G., and J.E. Salisbury. 2014. Ocean acidification in the coastal zone from an organism’s perspective: multiple system parameters, frequency domains, and habitats. Annual Review of Marine Science 6: 221–247.CrossRefGoogle Scholar
  55. Wallace, R.B., H. Baumann, J.S. Grear, R.C. Aller, and C.J. Gobler. 2014. Coastal ocean acidification: the other eutrophication problem. Estuarine, Coastal and Shelf Science 148: 1–13.CrossRefGoogle Scholar
  56. Wang, Z.A., and W.-J. Cai. 2004. Carbon dioxide degassing and inorganic carbon export from a marsh-dominated estuary (the Duplin River): a marsh CO2 pump. Limnology and Oceanography 49: 341–354.CrossRefGoogle Scholar
  57. Wenner, E., D. Sanger, M. Arendt, A.F. Holland, and Y. Chen. 2004. Variability in dissolved oxygen and other water-quality variables within the national estuarine research reserve system. Journal of Coastal Research 45: 17–38.Google Scholar
  58. Wenner, E.L., and M. Geist. 2001. The National Estuarine Research Reserves program to monitor and preserve estuarine waters. Coastal Management 29: 1–17.CrossRefGoogle Scholar
  59. Wootton, J.T., C.A. Pfister, and J.D. Forester. 2008. Dynamic patterns and ecological impacts of declining ocean pH in a high-resolution multi-year dataset. Proceedings of the National Academy of Sciences 105: 18848–18853.CrossRefGoogle Scholar
  60. Yvon-Durocher, G., J.I. Jones, M. Trimmer, G. Woodward, and J.M. Montoya. 2010. Warming alters the metabolic balance of ecosystems. Philosophical Transactions of the Royal Society of London B: Biological Sciences 365: 2117–2126.CrossRefGoogle Scholar
  61. Zhang, J., D. Gilbert, A.J. Gooday, L. Levin, S.W.A. Naqvi, J.J. Middelburg, M. Scranton, W. Ekau, A. Peña, B. Dewitte, T. Oguz, P.M.S. Monteiro, E. Urban, N.N. Rabalais, V. Ittekkot, W.M. Kemp, O. Ulloa, R. Elmgren, E. Escobar-Briones, and A.K. Van der Plas. 2010. Natural and human-induced hypoxia and consequences for coastal areas: synthesis and future development. Biogeosciences 7: 1443–1467.CrossRefGoogle Scholar
  62. Zimmerman, R.C., V.J. Hill, and C.L. Gallegos. 2015. Predicting effects of ocean warming, acidification, and water quality on Chesapeake region eelgrass. Limnology and Oceanography 60: 1781–1804.CrossRefGoogle Scholar
  63. Zimmerman, R.C., and J.N. Kremer. 1984. Episodic nutrient supply to a kelp forest ecosystem in Southern California. Journal of Marine Research 42: 591–604.CrossRefGoogle Scholar

Copyright information

© Coastal and Estuarine Research Federation 2017

Authors and Affiliations

  1. 1.Department of Marine SciencesUniversity of ConnecticutGrotonUSA
  2. 2.North Inlet-Winyah Bay National Estuarine Research Reserve, Baruch Marine Field LaboratoryUniversity of South CarolinaGeorgetownUSA

Personalised recommendations