Estuaries and Coasts

, Volume 40, Issue 6, pp 1626–1641 | Cite as

Interactive Effects of Physical and Biogeochemical Feedback Processes in a Large Submersed Plant Bed

  • Cassie Gurbisz
  • W. Michael Kemp
  • Jeffrey C. Cornwell
  • Lawrence P. Sanford
  • Michael S. Owens
  • Deborah C. Hinkle
Article

Abstract

Submersed plants are sensitive to nutrient loading because excess algal growth creates light-limiting conditions. However, submersed plant beds can also modify nutrient cycling through feedback loops whereby algal growth is limited and plant growth is enhanced. Whereas most studies on the effect of submersed aquatic vegetation (SAV) beds on nutrient cycling concentrate on either biogeochemical or physical controlling mechanisms, we use a holistic approach that analyzes how these processes interact. We measured a suite of physical and biological processes in a large SAV bed and developed a simple, 1-dimensional reactive transport model to investigate the mechanisms underlying SAV bed effects on nutrient cycling. We observed lower water column concentrations of dissolved inorganic nitrogen and phosphorus (DIN and DIP) inside relative to outside the SAV bed during the summer. Sediment denitrification (mean N2-N flux in August = 46 μmol m−2 h−1) and plant nutrient assimilation (August rates =385 μmol N and 25 μmol P m−2 h−1) were mechanisms of nutrient removal. We also found that the physical structure of the bed decreased advection and tidal dispersion, resulting in increased water residence time that enhanced biologically mediated nutrient loss. These processes create conditions that enable SAV to outcompete other primary producers, as water column nutrient concentrations were low enough to limit algal growth and associated light attenuation, while sediment pore water concentrations were sufficient to satisfy SAV nutrient demand. These findings suggest that interactions between physical and biological feedback processes in SAV beds can play a key role in structuring shallow aquatic ecosystems.

Keywords

Submersed aquatic vegetation Seagrass Feedbacks Biophysical Biogeochemical Interactions 

References

  1. An, S., and S.B. Joye. 2001. Enhancement of coupled nitrification-denitrification by benthic photosynthesis in shallow estuarine sediments. Limnology and Oceanography 46: 62–74. doi:10.4319/lo.2001.46.1.0062.CrossRefGoogle Scholar
  2. Aspila, K.I., H. Agemian, and A.S.Y. Chau. 1976. A semi-automated method for the determination of inorganic, organic and total phosphate in sediments. The Analyst 101: 187. doi:10.1039/an9760100187.CrossRefGoogle Scholar
  3. 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. doi:10.1890/10-1510.1.CrossRefGoogle Scholar
  4. Bartoli, M., D. Nizzoli, G. Castaldelli, and P. Viaroli. 2008. Community metabolism and buffering capacity of nitrogen in a Ruppia cirrhosa meadow. Journal of Experimental Marine Biology and Ecology 360: 21–30. doi:10.1016/j.jembe.2008.03.005.CrossRefGoogle Scholar
  5. Bayley, S., V.D. Stotts, P.F. Springer, and J. Steenis. 1978. Changes in submerged aquatic macrophyte populations at the head of Chesapeake Bay, 1958-1975. Estuaries 1: 73–84.CrossRefGoogle Scholar
  6. Burris, J.E. 1981. Effects of oxygen and inorganic carbon concentrations on the photosynthetic quotients of marine-algae. Marine Biology 65: 215–219. doi:10.1007/bf00397114.CrossRefGoogle Scholar
  7. Caffrey, J.M., and W.M. Kemp. 1990. Nitrogen cycling in sediments with estuarine populations of Potamogeton perfoliatus and Zostera marina. Marine Ecology Progress Series 66: 147–160.CrossRefGoogle Scholar
  8. Caffrey, J.M., and W.M. Kemp. 1992. Influence of the submersed plant, Potamogeton perfoliatus, on nitrogen cycling in estuarine sediments. Limnology and Oceanography 37: 1483–1495. doi:10.4319/lo.1992.37.7.1483.CrossRefGoogle Scholar
  9. Caffrey, J.M., M.C. Murrell, K.S. Amacker, J.W. Harper, S. Phipps, and M.S. Woodrey. 2014. Seasonal and inter-annual patterns in primary production, respiration, and net ecosystem metabolism in three estuaries in the northeast Gulf of Mexico. Estuaries and Coasts 37: 222–241. doi:10.1007/s12237-013-9701-5.CrossRefGoogle Scholar
  10. Cerco, C.F. 2000. Phytoplankton kinetics in the Chesapeake Bay eutrophication model. Water Quality and Ecosystem Modeling 1: 5–49.CrossRefGoogle Scholar
  11. Cerco, C.F., and K. Moore. 2001. System-wide submerged aquatic vegetation model for Chesapeake Bay. Estuaries 24: 522–534.CrossRefGoogle Scholar
  12. Cornwell, J.C., W.M. Kemp, and T.M. Kana. 1999. Denitrification in coastal ecosystems: Methods, environmental controls, and ecosystem level controls, a review. Aquatic Ecology 33: 41–54.CrossRefGoogle Scholar
  13. Cornwell, J.C., P.M. Glibert, and M.S. Owens. 2014. Nutrient fluxes from sediments in the San Francisco Bay Delta. Estuaries and Coasts 37: 1120–1133. doi:10.1007/s12237-013-9755-4.CrossRefGoogle Scholar
  14. Dennison, W.C., R.J. Orth, K.A. Moore, J.C. Stevenson, V. Carter, S. Kollar, P.W. Bergstrom, and R.A. Batiuk. 1993. Assessing water quality with submersed aquatic vegetation: Habitat requirements as barometers of Chesapeake Bay health. BioScience 43: 86–94.CrossRefGoogle Scholar
  15. Dettmann, E.H. 2001. Effect of water residence time on annual export and denitrification of nitrogen in estuaries: A model analysis. Estuaries 24: 481. doi:10.2307/1353250.CrossRefGoogle Scholar
  16. Duarte, C.M. 2012. Nutrient concentration of aquatic plants: Across species patterns. Limnology and Oceanography 37: 882–889.CrossRefGoogle Scholar
  17. Duarte, C. M. 1990. Seagrass nutrient content. Marine Ecology Progress Series 67:201–2017Google Scholar
  18. Duarte, C.M., and J. Cebrián. 1996. The fate of marine autotrophic production. Limnology and Oceanography 41: 1758–1766. doi:10.4319/lo.1996.41.8.1758.CrossRefGoogle Scholar
  19. Fonseca, M.S., J.S. Fisher, J.C. Zieman, and G.W. Thayer. 1982. Influence of the seagrass, Zostera marina L., on current flow. Estuarine. Coastal and Shelf Science 15: 351–364. doi:10.1016/0272-7714(82)90046-4.CrossRefGoogle Scholar
  20. Gacia, E., T.C. Granata, and C.M. Duarte. 1999. An approach to measurement of particle flux and sediment retention within seagrass (Posidonia oceanica) meadows. Aquatic Botany 65: 255–268. doi:10.1016/S0304-3770(99)00044-3.CrossRefGoogle Scholar
  21. Gambi, M.C., A.R.M. Nowell, and P.A. Jumars. 1990. Flume observations on flow dynamics in Zostera marina (eelgrass) beds. Marine Ecology Progress Series 61: 159–169. doi:10.3354/meps061159.CrossRefGoogle Scholar
  22. García, R., D. van Oevelen, K. Soetaert, L. Thomsen, H.C. De Stigter, and E. Epping. 2008. Deposition rates, mixing intensity and organic content in two contrasting submarine canyons. Progress in Oceanography 76: 192–215. doi:10.1016/j.pocean.2008.01.001.CrossRefGoogle Scholar
  23. Geyer, W.R., and R.P. Signell. 1992. A reassessment of the role of tidal dispersion in estuaries and bays. Estuaries 15: 97. doi:10.2307/1352684.CrossRefGoogle Scholar
  24. Gruber, R.K., and W.M. Kemp. 2010. Feedback effects in a coastal canopy-forming submersed plant bed. Limnology and Oceanography 55: 2285–2298. doi:10.4319/lo.2010.55.6.2285.CrossRefGoogle Scholar
  25. Gruber, R.K., D.C. Hinkle, and W.M. Kemp. 2011. Spatial patterns in water quality associated with submersed plant beds. Estuaries and Coasts 34: 961–972. doi:10.1007/s12237-010-9368-0.CrossRefGoogle Scholar
  26. Gurbisz, C., and W.M. Kemp. 2014. Unexpected resurgence of a large submersed plant bed in Chesapeake Bay: Analysis of time series data. Limnology and Oceanography 59: 482–494. doi:10.4319/lo.2014.59.2.0482.CrossRefGoogle Scholar
  27. Gurbisz, C., W.M. Kemp, L.P. Sanford, and R.J. Orth. 2016. Mechanisms of storm-related loss and resilience in a large submersed plant bed. Estuaries and Coasts: 39. Estuaries and Coasts: 951–966. doi:10.1007/s12237-016-0074-4.
  28. Havens, K.E., J. Hauxwell, A.C. Tyler, S. Thomas, K.J. McGlathery, J. Cebrian, I. Valiela, A.D. Steinman, and S.J. Hwang. 2001. Complex interactions between autotrophs in shallow marine and freshwater ecosystems: Implications for community responses to nutrient stress. Environmental Pollution 113: 95–107.CrossRefGoogle Scholar
  29. Hemminga, M.A., P.G. Harrison, and F. van Lent. 1991. The balance of nutrient losses and gains in seagrass meadows. Marine Ecology Progress Series 71: 85–96.CrossRefGoogle Scholar
  30. Hesslein, R.H. 1976. An in situ sampler for close interval pore water studies. Limnology and Oceanography 21: 912–914. doi:10.4319/lo.1976.21.6.0912.CrossRefGoogle Scholar
  31. Hofmann, A.F., K. Soetaert, and J.J. Middelburg. 2008. Present nitrogen and carbon dynamics in the Scheldt estuary using a novel 1-D model. Biogeosciences 5: 981–1006. doi:10.5194/bg-5-981-2008.CrossRefGoogle Scholar
  32. Howarth, R.W., M. Hayn, R.M. Marino, N. Ganju, K. Foreman, K. McGlathery, A.E. Giblin, P. Berg, and J.D. Walker. 2013. Metabolism of a nitrogen-enriched coastal marine lagoon during the summertime. Biogeochemistry 118: 1–20. doi:10.1007/s10533-013-9901-x.CrossRefGoogle Scholar
  33. Jordan, T.E., J.C. Cornwell, W.R. Boynton, and J.T. Anderson. 2008. Changes in phosphorus biogeochemistry along an estuarine salinity gradient: The iron conveyer belt. Limnology and Oceanography 53: 172–184. doi:10.4319/lo.2008.53.1.0172.CrossRefGoogle Scholar
  34. Kana, T.M., C. Darkangelo, M.D. Hunt, J.B. Oldham, G.E. Bennett, and J.C. Cornwell. 1994. Membrane inlet mass spectrometer for rapid environmental water samples. Analytical Chemistry 66: 4166–4170.CrossRefGoogle Scholar
  35. Kemp, W.M., W.R. Boynton, and R.R. Twilley. 1984. Influences of submersed vascular plants on ecological processes in upper Chesapeake Bay. In The Estuary as a Filter, ed. V.S. Kennedy, 367–394. New York: Academic Press, Inc.CrossRefGoogle Scholar
  36. Kemp, W.M., M.R. Lewis, and T.W. Jones. 1986. Comparison of methods for measuring production by the submersed macrophyte. Potamogeton perfoliatus L. Limnology and Oceanography 31: 1322–1334. doi:10.4319/lo.1986.31.6.1322.CrossRefGoogle Scholar
  37. Kemp, W.M., P. Sampou, J. Caffrey, M. Mayer, K. Henriksen, and W.R. Boynton. 1990. Ammonium recycling versus denitrification in Chesapeake Bay sediments. Limnology and Oceanography 35: 1545–1563. doi:10.4319/lo.1990.35.7.1545.CrossRefGoogle Scholar
  38. Kemp, W.M., W.R. Boynton, J.E. Adolf, D.F. Boesch, W.C. Boicourt, G. Brush, J.C. Cornwell, T.R. Fisher, P.M. Glibert, J.D. Hagy, L.W. Harding, E.D. Houde, D.G. Kimmel, W.D. Miller, R.I.E. Newell, M.R. Roman, E.M. Smith, and J.C. Stevenson. 2005. Eutrophication of Chesapeake Bay: Historical trends and ecological interactions. Marine Ecology Progress Series 303: 1–29. doi:10.3354/meps303001.CrossRefGoogle Scholar
  39. Koch, E.W. 2001. Beyond light: Physical, geological, and geochemical parameters as possible submersed aquatic vegetation habitat requirements. Estuaries 24: 1–17.CrossRefGoogle Scholar
  40. Lightbody, A.F., and H.M. Nepf. 2006. Prediction of velocity profiles and longitudinal dispersion in emergent salt marsh vegetation. Limnology and Oceanography 51: 218–228. doi:10.4319/lo.2006.51.1.0218.CrossRefGoogle Scholar
  41. Luhar, M., and H.M. Nepf. 2013. From the blade scale to the reach scale: A characterization of aquatic vegetative drag. Advances in Water Resources: 51. Elsevier Ltd: 305–316. doi:10.1016/j.advwatres.2012.02.002.
  42. Luhar, M., J. Rominger, and H. Nepf. 2008. Interaction between flow, transport and vegetation spatial structure. Environmental Fluid Mechanics 8: 423–439. doi:10.1007/s10652-008-9080-9.CrossRefGoogle Scholar
  43. Lyubchich, V., B.R. Gray, and Y.R. Gel. 2015. Multilevel random slope approach and nonparametric inference for river temperature, under haphazard sampling. In Approaches to Climate Science, ed. Machine Learning and Data Mining, 137–145. London: Springer International Publishing. doi:10.1007/978-3-319-17220-0_13.Google Scholar
  44. Marino, R., and R.W. Howarth. 1993. Atmospheric oxygen exchange in the Hudson River: Dome measurements and comparison with other natural waters. Estuaries 16: 433–455.CrossRefGoogle Scholar
  45. McGlathery, K.J., K. Sundbäck, and I.C. Anderson. 2007. Eutrophication in shallow coastal bays and lagoons: The role of plants in the coastal filter. Marine Ecology Progress Series 348: 1–18. doi:10.3354/meps07132.CrossRefGoogle Scholar
  46. Murphy, E., M. Ghisalberti, and H. Nepf. 2007. Model and laboratory study of dispersion in flows with submerged vegetation. Water Resources Research 43: 1–12. doi:10.1029/2006WR005229.CrossRefGoogle Scholar
  47. Nepf, H.M., C.G. Mugnier, and R.A. Zavistoski. 1997. The effects of vegetation on longitudinal dispersion. Estuarine, Coastal and Shelf Science 44: 675–684. doi:10.1006/ecss.1996.0169.CrossRefGoogle Scholar
  48. Nepf, H., M. Ghisalberti, B. White, and E. Murphy. 2007. Retention time and dispersion associated with submerged aquatic canopies. Water Resources Research 43: 1–10. doi:10.1029/2006WR005362.CrossRefGoogle Scholar
  49. Nixon, S.W., J.W. Ammerman, L.P. Atkinson, V.M. Berounsky, G. Billen, W.C. Boicourt, W.R. Boynton, T.M. Church, D.M. Ditoro, R. Elmgren, J.H. Garber, A.E. Giblin, R.A. Jahnke, N.J.P. Owens, M.E.Q. Pilson, and S.P. Seitzinger. 1996. The fate of nitrogen and phosphorus at the land-sea margin of the North Atlantic Ocean. Biogeochemistry 35: 141–180.CrossRefGoogle Scholar
  50. Odum, H. T. 1956. Primary production in flowing waters. Limnology and Oceanography 1:102–117Google Scholar
  51. Orth, R.J., and K.A. Moore. 1983. Chesapeake Bay: An unprecedented decline in submerged aquatic vegetation. Science 222: 51–53.CrossRefGoogle Scholar
  52. Orth, R.J., M.R. Williams, S.R. Marion, D.J. Wilcox, T.J.B. Carruthers, K.A. Moore, W.M. Kemp, et al. 2010. Long-term trends in submersed aquatic vegetation (SAV) in Chesapeake Bay, USA, related to water quality. Estuaries and Coasts 33: 1144–1163. doi:10.1007/s12237-010-9311-4.CrossRefGoogle Scholar
  53. Owens, M.S., and J.C. Cornwell. 2016. The benthic exchange of O2, N2, dissolved nutrients using small core incubations. Journal of Visualized Experiments (114): e54098. doi:10.3791/54098.
  54. Parsons, T. R., Y. Maita, and C. M. Lalli. 1984. A manual of chemical and biological methods for seawater analysis. Pergamon Press Inc., Oxford, 173 pp.Google Scholar
  55. Pinheiro, J.C., and D.M. Bates. 2000. Mixed-effects models in S and S-PLUS. Statistics and Computing. New York: Springer-Verlag. doi:10.1007/b98882.CrossRefGoogle Scholar
  56. Risgaard-Petersen, N., and L.D.M. Ottosen. 2000. Nitrogen cycling in two temperate Zostera marina beds: Seasonal variation. Marine Ecology Progress Series 198: 93–107. doi:10.3354/meps198093.
  57. Risgaard-Petersen, N., M.H. Nicolaisen, N.P. Revsbech, and B.A. Lomstein. 2004. Competition between ammonia-oxidizing bacteria and benthic microalgae. Applied and Environmental Microbiology 70: 5528–5537. doi:10.1128/AEM.70.9.5528-5537.2004.CrossRefGoogle Scholar
  58. Rybicki, N.B., H.L. Jenter, V. Carter, R.A. Baltzer, and M. Turtora. 1997. Observations of tidal flux between a submersed aquatic plant stand and the adjacent channel in the Potomac River near Washington, D.C. Limnology and Oceanography 42: 307–317. doi:10.4319/lo.1997.42.2.0307.CrossRefGoogle Scholar
  59. Rysgaard, S., N. Risgaard-Petersen, and N. Peter Sloth. 1996. Nitrification, denitrification, and nitrate ammonification in sediments of two coastal lagoons in Southern France. Hydrobiologia 329: 133–141. doi:10.1007/BF00034553.CrossRefGoogle Scholar
  60. Seitzinger, S., J.A. Harrison, J.K. Bohlke, A.F. Bouwman, R. Lowrance, B. Peterson, C. Tobias, and G. Van Drecht. 2006. Denitrification across landscaes and waterscapes: A synthesis. Ecological Applications 16: 2064–2090. doi:10.1890/1051-0761(2006)016[2064:DALAWA]2.0.CO;2.CrossRefGoogle Scholar
  61. Soetaert, K., and F. Meysman. 2012. Reactive transport in aquatic ecosystems: Rapid model prototyping in the open source software R. Environmental Modelling & Software 32: 49–60.CrossRefGoogle Scholar
  62. Testa, J. M., D.C. Brady, D.M. Di Toro, W.R. Boynton, J.C. Cornwell, and W.M. Kemp. 2013. Sediment flux modeling: Simulating nitrogen, phosphorus, and silica cycles. Estuarine, Coastal and Shelf Science: 131. Elsevier Ltd: 245–263. doi:10.1016/j.ecss.2013.06.014.
  63. Valiela, I., J. Mcclelland, J. Hauxwell, P.J. Behr, D. Hersh, and K. Foreman. 1997. Macroalgal blooms in shallow estuaries: Controls and ecophysiological and ecosystem consequences. Limnology and Oceanography 42: 1105–1118. doi:10.4319/lo.1997.42.5_part_2.1105.CrossRefGoogle Scholar
  64. Waycott, M., C.M. Duarte, T.J.B. Carruthers, R.J. Orth, W.C. Dennison, S. Olyarnik, A. Calladine, J.W. Fourqurean, K.L. Heck, A.R. Hughes, G.A. Kendrick, W.J. Kenworthy, F.T. Short, and S.L. Williams. 2009. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences of the United States of America 106: 12377–12381. doi:10.1073/pnas.0905620106.CrossRefGoogle Scholar
  65. Welsh, D.T., M. Bartoli, D. Nizzoli, G. Castaldelli, S.A. Riou, and P. Viaroli. 2000. Denitrification, nitrogen fixation, community primary productivity and inorganic-N and oxygen fluxes in an intertidal Zostera noltii meadow. Marine Ecology Progress Series 208: 65–77. doi:10.3354/meps208065.CrossRefGoogle Scholar
  66. Zimmerman, J.T.F. 1976. Mixing and flushing of tidal embayments in the western Dutch Wadden Sea, Part II: Analysis of mixing processes. Netherlands Journal of Sea Research 10: 397–439.CrossRefGoogle Scholar

Copyright information

© Coastal and Estuarine Research Federation 2017

Authors and Affiliations

  1. 1.National Socio-Environmental Synthesis CenterAnnapolisUSA
  2. 2.University of Maryland Center for Environmental Science Horn Point LaboratoryCambridgeUSA

Personalised recommendations