Estuaries and Coasts

, Volume 37, Supplement 1, pp 31–45 | Cite as

Hydrologic Variability and Its Control of Phytoplankton Community Structure and Function in Two Shallow, Coastal, Lagoonal Ecosystems: The Neuse and New River Estuaries, North Carolina, USA

  • Hans W. Paerl
  • Nathan S. Hall
  • Benjamin L. Peierls
  • Karen L. Rossignol
  • Alan R. Joyner


Hydrologic conditions, especially changes in freshwater input, play an important, and at times dominant, role in determining the structure and function of phytoplankton communities and resultant water quality of estuaries. This is particularly true for microtidal, shallow water, lagoonal estuaries, where water flushing and residence times show large variations in response to changes in freshwater inputs. In coastal North Carolina, there has been an increase in frequency and intensity of extreme climatic (hydrologic) events over the past 15 years, including eight hurricanes, six tropical storms, and several record droughts; these events are forecast to continue in the foreseeable future. Each of the past storms exhibited unique hydrologic and nutrient loading scenarios for two representative and proximate coastal plain lagoonal estuaries, the Neuse and New River estuaries. In this synthesis, we used a 13-year (1998–2011) data set from the Neuse River Estuary, and more recent 4-year (2007–2011) data set from the nearby New River Estuary to examine the effects of these hydrologic events on phytoplankton community biomass and composition. We focused on the ability of specific taxonomic groups to optimize growth under hydrologically variable conditions, including seasonal wet/dry periods, episodic storms, and droughts. Changes in phytoplankton community composition and biomass were strongly modulated by the amounts, duration, and seasonality of freshwater discharge. In both estuaries, phytoplankton total and specific taxonomic group biomass exhibited a distinctive unimodal response to varying flushing rates resulting from both event-scale (i.e., major storms, hurricanes) and more chronic seasonal changes in freshwater input. However, unlike the net negative growth seen at long flushing times for nano-/microphytoplankton, the pigments specific to picophytoplankton (zeaxanthin) still showed positive net growth due to their competitive advantage under nutrient-limited conditions. Along with considerations of seasonality (temperature regimes), these relationships can be used to predict relative changes in phytoplankton community composition in response to hydrologic events and changes therein. Freshwater inputs and droughts, while not manageable in the short term, must be incorporated in water quality management strategies for these and other estuarine and coastal ecosystems faced with increasing frequencies and intensities of tropical cyclones, flooding, and droughts.


Phytoplankton Coastal ecosystem Neuse River Estuary New River Estuary Hydrology 


  1. Adolf, J.E., C.L. Yeager, W.D. Miller, M.E. Mallonee, and L.W. Harding. 2006. Environmental forcing of phytoplankton floral composition, biomass, and primary productivity in Chesapeake Bay, USA. Estuarine Coastal and Shelf Science 67: 108–122.CrossRefGoogle Scholar
  2. Alber, M., and J.E. Sheldon. 1999. Use of a date-specific method to examine variability in the flushing times of Georgia estuaries. Estuarine Coastal and Shelf Science 49: 469–482.CrossRefGoogle Scholar
  3. Allan, R.P., and B.J. Soden. 2008. Atmospheric warming and the amplification of precipitation extremes. Science 321: 1481–1484.CrossRefGoogle Scholar
  4. Arar, E.J., W.L. Budde, and T.D. Behymer. 1997. Methods for the determination of chemical substances in marine and environmental matrices. Cincinnati, OH: EPA/600/R-97/072. National Exposure Research Laboratory, U.S. Environmental Protection Agency.Google Scholar
  5. Band, L., and D. Salveston. 2009. Climate Change Committee Report, 180. UNC-Chapel Hill, NC: UNC-Chapel Hill Institute for the Environment.Google Scholar
  6. Bender, M.A., T.R. Knutson, R.E. Tuleya, J.J. Sirutis, G.A. Vecchi, S.T. Garner, and I.M. Held. 2010. Modeled impact of anthropogenic warming on the frequency of intense Atlantic hurricanes. Science 327: 454–458.CrossRefGoogle Scholar
  7. Boesch, D.F., E. Burreson, W. Dennison, E. Houde, M. Kemp, V. Kennedy, R. Newell, K. Paynter, R. Orth, and W. Ulanowicz. 2001. Factors in the decline of coastal ecosystems. Science 293: 629–638.CrossRefGoogle Scholar
  8. Boyer, J.N., R.R. Christian, and D.W. Stanley. 1993. Patterns of phytoplankton primary productivity in the Neuse River Estuary, North Carolina, USA. Marine Ecology Progress Series 97: 287–297.CrossRefGoogle Scholar
  9. Boyer, J.N., D.W. Stanley, and R.R. Christian. 1994. Dynamics of NH4 + and NO3 uptake in the water column of the Neuse River estuary, North Carolina. Estuaries 17: 361–371.CrossRefGoogle Scholar
  10. Brunet, C., J.M. Brylinski, and Y. Lemoine. 1993. In situ variations of xanthophylls diatoxanthin and diadinoxanthin: photadaptation and relationships with a hydrodynamical system in the eastern English Channel. Marine Ecology Progress Series 102: 69–77.CrossRefGoogle Scholar
  11. Burkholder, J., D. Eggleston, H. Glasgow, C. Brownie, R. Reed, G. Janowitz, M. Posey, G. Melia, C. Kinder, R. Corbett, D. Toms, J. Alphin, N. Deamer, and J. Springer. 2004. Comparative impacts of two major hurricane seasons on the Neuse River and western Pamlico Sound ecosystems. Proceedings of the National Academy of Science USA 101: 9291–9296.CrossRefGoogle Scholar
  12. Burkholder, J.M., D.A. Dickey, C.A. Kinder, R.E. Reed, M.A. Mallin, M.R. McIver, L.B. Cahoon, G. Melia, C. Brownie, J. Smith, N. Deamer, J. Springer, H.B. Glasgow, and D. Toms. 2006. Comprehensive trend analysis of nutrients and related variables in a large eutrophic estuary: a decadal study of anthropogenic and climatic influences. Limnology and Oceanography 51: 463–487.CrossRefGoogle Scholar
  13. Buzzelli, C.P., R.A. Luettich Jr., S.P. Powers, C.H. Peterson, J.E. McNinch, J.L. Pinckney, and H.W. Paerl. 2002. Estimating the spatial extent of bottom-water hypoxia and habitat degradation in a shallow estuary. Marine Ecology Progress Series 230: 103–112.CrossRefGoogle Scholar
  14. Christian, R.R., and C.R. Thomas. 2003. Network analysis of nitrogen inputs and cycling in the Neuse River Estuary, North Carolina, USA. Estuaries 26: 815–828.CrossRefGoogle Scholar
  15. Cloern, J.E. 2001. Our evolving conceptual model of the coastal eutrophication problem. Marine Ecology Progress Series 210: 223–253.CrossRefGoogle Scholar
  16. Copeland, B.J., and J. Gray. 1991. Status and trends report of the Albemarle–Pamlico Estuary. In Albemarle–Pamlico Estuarine Study Report 90–01, ed. J. Steel. Raleigh, NC, USA: North Carolina Department of Environment, Health and Natural Resources.Google Scholar
  17. De Senerpont Domis, L.N., W.M. Mooij, and J. Huisman. 2007. Climate-induced shifts in an experimental phytoplankton community: a mechanistic approach. Hydrobiologia 584: 403–413.CrossRefGoogle Scholar
  18. Elliott, J.A., S.J. Thackeray, C. Huntingford, and R.G. Jones. 2005. Combining a regional climate model with a phytoplankton community model to predict future changes in phytoplankton in lakes. Freshwater Biology 50: 1404–141.CrossRefGoogle Scholar
  19. Elmgren, R., and U. Larsson. 2001. Nitrogen and the Baltic Sea: Managing nitrogen in relation to phosphorus. The scientific world, Special edition (S2):371–377. Leiden, the Netherlands: Balkema Publishers.Google Scholar
  20. Ensign, S.H., J.N. Halls, and M.A. Mallin. 2004. Application of digital bathymetry data in an analysis of flushing times of two North Carolina Estuaries. Computers and Geosciences 30: 501–511.CrossRefGoogle Scholar
  21. Gaulke, A.K., M.S. Wetz, and H.W. Paerl. 2010. Picophytoplankton: a major contributor to planktonic biomass and primary production in a eutrophic, river-dominated estuary. Estuarine Coastal and Shelf Science 90: 45–54.CrossRefGoogle Scholar
  22. Hall, N.S., and H.W. Paerl. 2011. Vertical migration patterns of phytoflagellates in relation to light and nutrient availability in a shallow, microtidal estuary. Marine Ecology Progress Series 425: 1–19.CrossRefGoogle Scholar
  23. Hall, M.J., H.F.P. Van den Boogaard, R.C. Fernando, and A.E. Mynett. 2004. The construction of confidence intervals for frequency analysis using resampling techniques. Hydrology and Earth System Sciences 8: 235–246.CrossRefGoogle Scholar
  24. Hall, N.S., R.W. Litaker, E. Fensin, J.E. Adolf, A.R. Place, and H.W. Paerl. 2008. Environmental factors contributing to the development and demise of a toxic dinoflagellate (Karlodinium veneficum) bloom in a shallow, eutrophic, lagoonal estuary. Estuaries and Coasts 31: 402–418.CrossRefGoogle Scholar
  25. Hall, N.S., B.L. Peierls, H.W. Paerl, A.C. Whipple, and K.L. Rossignol. 2013. Effects of climatic variability on phytoplankton community structure and bloom development in the eutrophic, microtidal, New River Estuary, North Carolina, USA. Estuarine Coastal and Shelf Science 117: 70–82.CrossRefGoogle Scholar
  26. Hoek, C.V., D.G. Mann, and H.M. Jahns. 1997. Algae, an introduction to phycology. Cambridge, UK: Cambridge University Press.Google Scholar
  27. Holland, G.J., and P.J. Webster. 2007. Heightened tropical cyclone activity in the North Atlantic: natural variability of climate trend? Philosophical Transactions of the Royal Society A. doi:10.1098/rsta.2007.2083.Google Scholar
  28. Holmes, R.M., A. Aminot, R. Kérouel, B.A. Hooker, and B.J. Peterson. 1999. A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Canadian Journal of Fisheries and Aquatic Sciences 56: 1801–1808.CrossRefGoogle Scholar
  29. Howarth, R.W. 2008. Coastal nitrogen pollution: a review of sources and trends globally and regionally. Harmful Algae 8: 14–20.CrossRefGoogle Scholar
  30. IPCC. 2007. Climate change 2007: Synthesis report. Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. In Core writing team, ed. R.K. Pachauri and A. Reisinger, 104. Geneva, Switzerland: IPCC.Google Scholar
  31. IPCC. 2012. Managing the risks of extreme events and disasters to advance climate change adaptation. In A special report of Working Groups I and II of the Intergovernmental Panel on Climate Change, ed. C.B. Field, V. Barros, T.F. Stocker, D. Qin, D.J. Dokken, K.L. Ebi, M.D. Mastrandrea, K.J. Mach, G.-K. Plattner, S.K. Allen, M. Tignor, and P.M. Midgley, 582. Cambridge, UK: Cambridge University Press.Google Scholar
  32. Kemp, A.C., B.P. Horton, J.P. Donnelly, M.E. Mann, M. Vermeer, and S. Rahmstorf. 2011. Climate related sea-level variations over the past two millennia. Proceedings of the National Academy of Sciences 108: 11017–11022.CrossRefGoogle Scholar
  33. Kennish, M., and H.W. Paerl. 2010. Coastal Lagoons: Critical Habitats of Environmental Change. CRC Marine Science Series, CRC Press: Boca Raton, FL.CrossRefGoogle Scholar
  34. Lebo, M.E., H.W. Paerl, and B.L. Peierls. 2012. Evaluation of progress in achieving TMDL mandated nitrogen reductions in the Neuse River Basin, North Carolina. Environmental Management 49: 253–266.CrossRefGoogle Scholar
  35. Lenihan, H., and C.H. Peterson. 1998. How habitat degradation through fishery disturbance enhances impacts of hypoxia on oyster reefs. Ecological Applications 8: 128–140.CrossRefGoogle Scholar
  36. Litaker, W., C.S. Duke, B.E. Kenney, and J. Ramus. 1987. Short-term environmental variability and phytoplankton abundance in a shallow tidal estuary: i. Winter and summer. Marine Biology 96: 115–121.CrossRefGoogle Scholar
  37. Lucas, L.V., J.K. Thompson, and L.R. Brown. 2009. Why are diverse relationships observed between phytoplankton biomass and transport time? Limnology and Oceanography 54: 381–390.CrossRefGoogle Scholar
  38. Luettich Jr., R.A., J.E. McNinch, H.W. Paerl, C.H. Peterson, J.T. Wells, M. Alperin, C.S. Martens, and J.L. Pinckney. 2000. Neuse River Estuary modeling and monitoring project stage: 1. Hydrography and circulation, water column nutrients and productivity, sedimentary processes and benthic–pelagic coupling, 172. Raleigh, NC: Report UNC-WRRI-2000-325B, Water Resources Research Institute of the University of North Carolina.Google Scholar
  39. Mallin, M.A., and H.W. Paerl. 1992. Effects of variable irradiance on phytoplankton productivity in shallow estuaries. Limnology and Oceanography 37: 54–62.CrossRefGoogle Scholar
  40. Mallin, M.A., H.W. Paerl, J. Rudek, and P.W. Bates. 1993. Regulation of estuarine primary production by watershed rainfall and river flow. Marine Ecology Progress Series 93: 199–203.CrossRefGoogle Scholar
  41. Mallin, M.A., L.B. Cahoon, M.R. McIver, D.C. Parsons, and G.C. Shank. 1997. Nutrient limitation and eutrophication potential in the Cape Fear and New River Estuaries. Report No. 313. Raleigh, NC: Water Resources Research Institute of the University of North Carolina.Google Scholar
  42. Mallin, M.A., M.R. McIver, H.A. Wells, D.C. Parsons, and V.L. Johnson. 2005. Reversal of eutrophication following sewage treatment upgrades in the New River Estuary, North Carolina. Estuaries 28: 750–760.CrossRefGoogle Scholar
  43. National Research Council (NRC). 2000. Clean coastal waters: Understanding and reducing the effects of nutrient pollution. Washington, DC: National Academy Press.Google Scholar
  44. North Carolina Department of Environment and Natural Resources (NCDENR), Division of Water Quality. 2001a. White Oak Basinwide Water Quality Plan. Raleigh, NC: NCDENR.Google Scholar
  45. North Carolina Department of Environment and Natural Resources (NCDENR), Division of Water Quality. 2001b. Phase II of the total maximum daily load for total nitrogen to the Neuse River Estuary, North Carolina. Raleigh, NC: NCDENR.Google Scholar
  46. North Carolina Department of Environment and Natural Resources (NCDENR), Division of Water Resources. 2012. Drought Monitor History 2000–2012. Accessed 1 October 2012.
  47. North Carolina Department of Environment, Health, and Natural Resources (NCDEHNR), Division of Environmental Management. 1990. New River, Onslow County. Nutrient Control Measures and Water Quality Characteristics for 1986–1989. Raleigh, NC: NCDEHNR Report No. 90–04.Google Scholar
  48. Paerl, H.W., and J. Huisman. 2008. Blooms like it hot. Science 320: 57–58.CrossRefGoogle Scholar
  49. Paerl, H.W., and M.F. Piehler. 2008. Nitrogen and marine eutrophication. In Nitrogen in the marine environment, 2nd ed, ed. D.G. Capone, M. Mulholland, and E. Carpenter, 529–567. Orlando, FL: Academic Press.CrossRefGoogle Scholar
  50. Paerl, H.W., M.A. Mallin, C.A. Donahue, M. Go, and B.L. Peierls. 1995. Nitrogen loading sources and eutrophication of the Neuse River estuary, NC: Direct and indirect roles of atmospheric deposition. University of North Carolina Water Resources Research Institute Report No. 291. 119 p.Google Scholar
  51. Paerl, H.W., J.L. Pinckney, J.M. Fear, and B.L. Peierls. 1998. Ecosystem responses to internal and watershed organic matter loading: consequences for hypoxia in the eutrophying Neuse River Estuary, North Carolina, USA. Marine Ecology Progress Series 166: 17–25.CrossRefGoogle Scholar
  52. Paerl, H.W., J.D. Bales, L.W. Ausley, C.P. Buzzelli, L.B. Crowder, L.A. Eby, J.M. Fear, M. Go, B.L. Peierls, T.L. Richardson, and J.S. Ramus. 2001. Ecosystem impacts of 3 sequential hurricanes (Dennis, Floyd and Irene) on the US's largest lagoonal estuary, Pamlico Sound, NC. Proceedings of the National Academy of Science USA 98(10): 5655–5660.CrossRefGoogle Scholar
  53. Paerl, H.W., L.M. Valdes, J.L. Pinckney, M.F. Piehler, J. Dyble, and P.H. Moisander. 2003. Phytoplankton photopigments as indicators of estuarine and coastal eutrophication. BioScience 53: 953–964.CrossRefGoogle Scholar
  54. Paerl, H.W.J., J.L. Dyble, L.M. Pinckney, D.F. Valdes, P.H. Millie, J.T. Moisander, B. Morris, B. Bendis, and M.F. Piehler. 2005. Using microalgal indicators to assess human and climactically-induced ecological change in estuaries. In Proceedings of the estuarine indicators workshop, ed. S. Bartone, 145–174. Boca Raton, Florida: CRC Press, Orlando, FL.Google Scholar
  55. Paerl, H.W., L.M. Valdes, J.E. Adolf, B.M. Peierls, and L.W. Harding Jr. 2006a. Anthropogenic and climatic influences on the eutrophication of large estuarine ecosystems. Limnology and Oceanography 51: 448–462.CrossRefGoogle Scholar
  56. Paerl, H.W., L.M. Valdes, A.R. Joyner, B.L. Peierls, C.P. Buzzelli, M.F. Piehler, S.R. Riggs, R.R. Christian, J.S. Ramus, E.J. Clesceri, L.A. Eby, L.W. Crowder, and R.A. Luettich. 2006b. Ecological response to hurricane events in the Pamlico Sound System, NC and implications for assessment and management in a regime of increased frequency. Estuaries and Coasts 29: 1033–1045.CrossRefGoogle Scholar
  57. Paerl, H.W., L.M. Valdes, A.R. Joyner, and V. Winkelmann. 2007. Phytoplankton indicators of ecological change in the nutrient and climatically-impacted Neuse River–Pamlico Sound System, North Carolina. Ecological Applications 17(5): 88–101.CrossRefGoogle Scholar
  58. Paerl, H.W., K.L. Rossignol, N.S. Hall, B.L. Peierls, and M.S. Wetz. 2010. Phytoplankton community indicators of short- and long-term ecological change in the anthropogenically and climatically impacted Neuse River Estuary, North Carolina, USA. Estuaries and Coasts 33: 485–497.CrossRefGoogle Scholar
  59. Peierls, B.L., R.R. Christian, and H.W. Paerl. 2003. Water quality and phytoplankton as indicators of hurricane impacts on large estuarine ecosystems. Estuaries 26: 1329–1343.CrossRefGoogle Scholar
  60. Peierls, B.L., N.S. Hall, and H.W. Paerl. 2012. Non-monotonic responses of phytoplankton biomass accumulation to hydrologic variability: a comparison of two coastal plain North Carolina estuaries. Estuaries and Coasts 35: 1376–1392.CrossRefGoogle Scholar
  61. Pietrafesa, L.J., G.S. Janowitz, T-Y. Chao, T.H. Weisberg, F. Askari, and E. Noble. 1996. The physical oceanography of Pamlico Sound. UNC Sea Grant Publication UNC-WP-86-5, 125 pp.Google Scholar
  62. Pinckney, J.L., D.F. Millie, K.E. Howe, H.W. Paerl, and J. Hurley. 1996. Flow scintillation counting of 14C labeled microalgal photosynthetic pigments. Journal of Plankton Research 18: 1867–1880.CrossRefGoogle Scholar
  63. Pinckney, J.L., H.W. Paerl, M.B. Harrington, and K.E. Howe. 1998. Annual cycles of phytoplankton community structure and bloom dynamics in the Neuse River Estuary, NC (USA). Marine Biology 131: 371–382.CrossRefGoogle Scholar
  64. Pinckney, J.L., H.W. Paerl, and M.B. Harrington. 1999. Responses of the phytoplankton community growth rate to nutrient pulses in variable estuarine environments. Journal of Phycology 35: 1455–1463.CrossRefGoogle Scholar
  65. Pinckney, J.L., T.L. Richardson, D.F. Millie, and H.W. Paerl. 2001. Application of photopigment biomarkers for quantifying microalgal community composition and in situ growth rates. Organic Geochemistry 32: 585–595.CrossRefGoogle Scholar
  66. Reynolds, C.S. 2006. The ecology of phytoplankton (Ecology, biodiversity and conservation). Cambridge, UK: Cambridge University Press.Google Scholar
  67. Rothenberger, M.B., J.M. Burkholder, and T.R. Wentworth. 2009. Use of long-term data and multivariate ordination techniques to identify environmental factors governing estuarine phytoplankton species dynamics. Limnology and Oceanography 54: 2107–2127.CrossRefGoogle Scholar
  68. Rudek, J., H.W. Paerl, M.A. Mallin, and P.W. Bates. 1991. Seasonal and hydrological control of phytoplankton nutrient limitation in the lower Neuse River Estuary, North Carolina. Marine Ecology Progress Series 75: 133–142.CrossRefGoogle Scholar
  69. Sheldon, J.E., and M. Alber. 2006. The calculation of estuarine turnover times using freshwater fraction and tidal prism models: a critical evaluation. Estuaries and Coasts 29: 133–146.CrossRefGoogle Scholar
  70. Stow, C.A., M.E. Borsuk, and D.W. Stanley. 2001. Long-term changes in watershed nutrient inputs and riverine exports in the Neuse River, North Carolina. Water Research 35: 1489–1499.CrossRefGoogle Scholar
  71. Sunda, W.G., E. Graneli, and C.J. Gobler. 2006. Positive feedback and the development and persistence of ecosystem disruptive algal blooms. Journal of Phycology 42: 963–974.CrossRefGoogle Scholar
  72. Tester, P.M., S.M. Varnam, M.E. Culver, D.L. Eslinger, R.P. Stumpf, R.N. Swift, J.K. Yungel, M.D. Black, and R.W. Litaker. 2003. Airborne detection of ecosystem responses to an extreme event: phytoplankton displacement and abundance after hurricane induced flooding in the Albemarle–Pamlico Sound system. Estuaries 26: 1353–1364.CrossRefGoogle Scholar
  73. Tomas, C.R., J. Peterson, and A.O. Tatters. 2007. Harmful algal species from Wilson Bay, New River, North Carolina: Composition, nutrient bioassay and HPLC pigment analyses, 31. Raleigh, NC: North Carolina Water Resources Research Institute Report No. 369.Google Scholar
  74. Trenberth, K.E. 2005. The impact of climate change and variability on heavy precipitation, floods, and droughts. In Encyclopedia of hydrological sciences, ed. M.G. Anderson, 1–11. Chichester, UK: John Wiley and Sons.Google Scholar
  75. Twomey, L.J., M.F. Piehler, and H.W. Paerl. 2005. Phytoplankton uptake of ammonium, nitrate, and urea in the Neuse River Estuary, NC, USA. Hydrobiologia 533: 123–134.CrossRefGoogle Scholar
  76. Valdes-Weaver, L.M., M.F. Piehler, J.L. Pinckney, K.E. Howe, K. Rossignol, and H.W. Paerl. 2006. Long-term temporal and spatial trends in phytoplankton biomass and class-level taxonomic composition in the hydrologically variable Neuse–Pamlico estuarine continuum, NC, USA. Limnology and Oceanography 51(3): 1410–1420.CrossRefGoogle Scholar
  77. Van Heukelem, L., A. Lewitus, T. Kana, and N. Craft. 1994. Improved separations of phytoplankton pigments using temperature-controlled high performance liquid chromatography. Marine Ecology Progress Series 114: 303–313.CrossRefGoogle Scholar
  78. Vitousek, P.M., H.A. Mooney, J. Lubchenko, and J.M. Mellilo. 1997. Human domination of Earth’s ecosystem. Science 277: 494–499.CrossRefGoogle Scholar
  79. Vörösmarty, C.J., P. Green, J. Salisbury, and R.B. Lammers. 2000. Global water resources: vulnerability from climate change and population growth. Science 289: 284–288.CrossRefGoogle Scholar
  80. Webster, P.J., G.J. Holland, J.A. Curry, and H.R. Chang. 2005. Changes in tropical cyclone number, duration, and intensity in a warming environment. Science 309: 1844–1846.CrossRefGoogle Scholar
  81. Welschmeyer, N.A. 1994. Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnology and Oceanography 39: 1985–1992.CrossRefGoogle Scholar
  82. Wetz, M.S., E.A. Hutchinson, R.S. Lunetta, H.W. Paerl, and J.C. Taylor. 2011. Severe droughts reduce estuarine primary productivity with cascading effects on higher trophic levels. Limnology and Oceanography 56: 627–638.CrossRefGoogle Scholar

Copyright information

© Coastal and Estuarine Research Federation 2013

Authors and Affiliations

  • Hans W. Paerl
    • 1
  • Nathan S. Hall
    • 1
  • Benjamin L. Peierls
    • 1
  • Karen L. Rossignol
    • 1
  • Alan R. Joyner
    • 1
  1. 1.Institute of Marine SciencesUniversity of North Carolina at Chapel HillChapel HillUSA

Personalised recommendations