, Volume 14, Issue 3, pp 430–444 | Cite as

Long-Term Effects of Adding Nutrients to an Oligotrophic Coastal Environment

  • Anna R. Armitage
  • Thomas A. Frankovich
  • James W. Fourqurean


Management of ecological disturbances requires an understanding of the time scale and dynamics of community responses to disturbance events. To characterize long-term seagrass bed responses to nutrient enrichment, we established six study sites in Florida Bay, USA. In 24 plots (0.25 m2) at each site, we regularly added nitrogen (N) and phosphorus (P) in a factorial design for 7 years. Five of the six sites exhibited strong P limitation. Over the first 2 years, P enrichment increased Thalassia testudinum cover in the three most P-limited sites. After 3 years, Halodule wrightii began to colonize many of the P-addition plots, but the degree of colonization was variable among sites, possibly due to differences in the supply of viable propagules. Thalassia increased its allocation to aboveground tissue in response to P enrichment; Halodule increased in total biomass but did not appear to change its aboveground: belowground tissue allocation. Nutrient enrichment did not cause macroalgal or epiphytic overgrowth of the seagrass. Nitrogen retention in the study plots was variable but relatively low, whereas phosphorus retention was very high, often exceeding 100% of the P added as fertilizer over the course of our experiments. Phosphorus retentions exceeding 100% may have been facilitated by increases in Thalassia aboveground biomass, which promoted the settlement of suspended particulate matter containing phosphorus. Our study demonstrated that low-intensity press disturbance events such as phosphorus enrichment can initiate a slow, ramped successional process that may alter community structure over many years.


aboveground and belowground biomass epiphyte eutrophication macroalgae nutrient press pulse ramp disturbances seagrass 



This research was funded by a grant from the Everglades National Park (ENP) under cooperative agreement 1443CA528001022 and by the Florida Coastal Everglades Long-Term Ecological Research Program funded by the US National Science Foundation (Cooperative Agreement #DEB-9910514). Water column nutrient concentrations were provided by the SERC-FIU Water Quality Monitoring Network which is supported by SFWMD/SERC Cooperative Agreement #4600000352 as well as EPA Agreement #X7-96410603-3. Doug Morrison and Bill Perry facilitated permit issuance and use of ENP facilities. We are grateful to the many people who devoted field and laboratory time to this project. Pursell Technologies Inc. and IMC Global generously donated the nitrogen and phosphorus fertilizers, respectively, for this study. This is contribution number 509 from the Southeast Environmental Research Center at FIU.

Supplementary material

10021_2011_9421_MOESM1_ESM.docx (393 kb)
Supplementary material 1 (DOCX 393 kb)


  1. Armitage AR, Fourqurean JW. 2009. Stable isotopes reveal complex changes in trophic relationships following nutrient addition in a coastal marine ecosystem. Estuaries Coasts 32:1152–64.CrossRefGoogle Scholar
  2. Armitage AR, Frankovich TA, Heck KL Jr, Fourqurean JW. 2005. Experimental nutrient enrichment causes complex changes in seagrass, microalgae, and macroalgae community structure in Florida Bay. Estuaries 28:422–34.CrossRefGoogle Scholar
  3. Bargali K. 1997. Role of light, moisture and nutrient availability in replacement of Quercus leucotrichophora by Pinus roxburghii in Central Himalaya. J Trop For Sci 10:262–70.Google Scholar
  4. Boström C, Bonsdorff E. 2000. Zoobenthic community establishment and habitat complexity—the importance of seagrass shoot-density, morphology and physical disturbance for faunal recruitment. Mar Ecol Prog Ser 205:123–38.CrossRefGoogle Scholar
  5. Campbell DR, Rochefort L, Lavoie C. 2003. Determining the immigration potential of plants colonizing disturbed environments: the case of milled peatlands in Quebec. J Appl Ecol 40:78–91.CrossRefGoogle Scholar
  6. de Kanel J, Morse JW. 1978. The chemistry of orthophosphate uptake from seawater on to calcite and aragonite. Geochim Cosmochim Acta 42:1335–40.CrossRefGoogle Scholar
  7. Detenbeck NE, DeVore PW, Niemi GJ, Lima A. 1992. Recovery of temperate stream fish communities from disturbance: a review of case studies and synthesis of theory. Environ Manag 16:33–53.CrossRefGoogle Scholar
  8. Di Carlo G, Kenworthy WJ. 2008. Evaluation of aboveground and belowground biomass recovery in physically disturbed seagrass beds. Oecologia 158:285–98.PubMedCrossRefGoogle Scholar
  9. Dosch JJ, Peterson CJ, Haines BL. 2007. Seed rain during initial colonization of abandoned pastures in the premontane wet forest zone of southern Costa Rica. J Trop Ecol 23:151–9.CrossRefGoogle Scholar
  10. Duarte CM. 1995. Submerged aquatic vegetation in relation to different nutrient regimes. Ophelia 41:87–112.Google Scholar
  11. Dunton KH. 1996. Photosynthetic production and biomass of the subtropical seagrass Halodule wrightii along an estuarine gradient. Estuaries 19:436–47.CrossRefGoogle Scholar
  12. Eckman JE. 1983. Hydrodynamic processes affecting benthic recruitment. Limnol Oceanogr 28:241–57.CrossRefGoogle Scholar
  13. Ferdie M, Fourqurean JW. 2004. Responses of seagrass communities to fertilization along a gradient of relative availability of nitrogen and phosphorus in a carbonate environment. Limnol Oceanogr 49:2082–94.CrossRefGoogle Scholar
  14. Fourqurean JW, Zieman JC. 2002. Nutrient content of the seagrass Thalassia testudinum reveals regional patterns of relative availability of nitrogen and phosphorus in the Florida Keys USA. Biogeochemistry 61:229–45.CrossRefGoogle Scholar
  15. Fourqurean JW, Zieman JC, Powell GVN. 1992a. Phosphorus limitation of primary production in Florida Bay: evidence from C:N:P ratios of the dominant seagrass Thalassia testudinum. Limnol Oceanogr 37:162–71.CrossRefGoogle Scholar
  16. Fourqurean JW, Zieman JC, Powell GVN. 1992b. Relationships between porewater nutrients and seagrasses in a subtropical carbonate environment. Mar Biol 114:57–65.Google Scholar
  17. Fourqurean JW, Powell GVN, Kenworthy WJ, Zieman JC. 1995. The effects of long-term manipulation of nutrient supply on competition between the seagrasses Thalassia testudinum and Halodule wrightii in Florida Bay. Oikos 72:349–58.CrossRefGoogle Scholar
  18. Fourqurean JW, Willsie A, Rose CD, Rutten LM. 2001. Spatial and temporal pattern in seagrass community composition and productivity in south Florida. Mar Biol 138:341–54.CrossRefGoogle Scholar
  19. Fourqurean JW, Muth MF, Boyer JN. 2010. Epiphyte loads on seagrasses and microphytobenthos abundance are not reliable indicators of nutrient availability in oligotrophic coastal ecosystems. Mar Poll Bull 60:971–83.CrossRefGoogle Scholar
  20. Frankovich TA, Fourqurean JW. 1997. Seagrass epiphyte loads along a nutrient availability gradient, Florida Bay, USA. Mar Ecol Prog Ser 159:37–50.CrossRefGoogle Scholar
  21. Gallegos ME, Merino M, Rodriguez A, Marbà N, Duarte CM. 1994. Growth patterns and demography of pioneer Caribbean seagrasses Halodule wrightii and Syringodium filiforme. Mar Ecol Prog Ser 109:99–104.CrossRefGoogle Scholar
  22. Grime JP. 1977. Evidence for existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111:1169–94.CrossRefGoogle Scholar
  23. Haase J, Brandl R, Scheu S, Schadler M. 2008. Above- and belowground interactions are mediated by nutrient availability. Ecology 89:3072–81.CrossRefGoogle Scholar
  24. Hauxwell J, Cebrian J, Furlong C, Valiela I. 2001. Macroalgal canopies contribute to eelgrass (Zostera marina) decline in temperate estuarine ecosystems. Ecology 82:1007–22.Google Scholar
  25. Heck KL Jr, Valentine JF, Pennock JR, Chaplin G, Spitzer PM. 2006. Effects of nutrient enrichment and grazing on shoalgrass Halodule wrightii and its epiphytes: results of a field experiment. Mar Ecol Prog Ser 326:145–56.CrossRefGoogle Scholar
  26. Herbert DA, Fourqurean JW. 2008. Ecosystem structure and function still altered two decades after short-term fertilization of a seagrass meadow. Ecosystems 11:688–700.CrossRefGoogle Scholar
  27. Holmer M, Carta C, Andersen FØ. 2006. Biogeochemical implications for phosphorus cycling in sandy and muddy rhizosphere sediments of Zostera marina meadows (Denmark). Mar Ecol Prog Ser 320:141–51.CrossRefGoogle Scholar
  28. Hughes AR, Bando KJ, Rodriguez LF, Williams SL. 2004. Relative effects of grazers and nutrients on seagrasses: a meta-analysis approach. Mar Ecol Prog Ser 282:87–99.CrossRefGoogle Scholar
  29. Jeffrey SW, Humphrey GF. 1975. New spectrophotometric equations for determining chlorophylls a, b, c 1, and c 2 in higher plants, algae and natural phytoplankton. Biochemie und Physiologie der Pflanzen 167:191–4.Google Scholar
  30. Johnson NC, Rowland DL, Corkidi L, Allen EB. 2008. Plant winners and losers during grassland N-eutrophication differ in biomass allocation and mycorrhizas. Ecology 89:2868–78.PubMedCrossRefGoogle Scholar
  31. Kennedy H, Beggins J, Duarte CM, Fourqurean JW, Holmer M, Marbà N, Middelburg JJ. 2010. Seagrass sediments as a global carbon sink: isotopic constraints. Global Biogeochem Cycles 24: GB4026. doi: 10.1029/2010GB003848.
  32. Lake PS. 2000. Disturbance, patchiness, and diversity in streams. J N Am Benth Soc 19:573–92.CrossRefGoogle Scholar
  33. Lee K-S, Dunton KH. 1999. Inorganic nitrogen acquisition in the seagrass Thalassia testudinum: development of a whole-plant nitrogen budget. Limnol Oceanogr 44:1204–15.CrossRefGoogle Scholar
  34. Lee K-S, Dunton KH. 2000. Effects of nitrogen enrichment on biomass allocation, growth, and leaf morphology of the seagrass Thalassia testudinum. Mar Ecol Prog Ser 196:39–48.CrossRefGoogle Scholar
  35. Long MH, McGlathery KJ, Zieman JC, Berg P. 2008. The role of organic acid exudates in liberating phosphorus from seagrass-vegetated carbonate sediments. Limnol Oceanogr 53:2616–26.CrossRefGoogle Scholar
  36. Lotze HK, Worm B, Sommer U. 2000. Propagule banks, herbivory and nutrient supply control population development and dominance patterns in macroalgal blooms. Oikos 89:46–58.CrossRefGoogle Scholar
  37. Martinetto P, Teichberg M, Valiela I. 2006. Coupling of estuarine benthic and pelagic food webs to land-derived nitrogen sources in Waquoit Bay, Massachusetts, USA. Mar Ecol Prog Ser 307:37–48.CrossRefGoogle Scholar
  38. McGlathery KJ. 2001. Macroalgal blooms contribute to the decline of seagrass in nutrient-enriched coastal waters. J Phycol 37:453–6.CrossRefGoogle Scholar
  39. MCSM. 2001. Monroe County Stormwater Management Master Plan; Vol. 1; Sect. 2.3; Pollution loads targets and analysis.Google Scholar
  40. Micheli F. 1999. Eutrophication, fisheries, and consumer-resource dynamics in marine pelagic ecosystems. Science 285:1396–8.PubMedCrossRefGoogle Scholar
  41. Morris EP, Peralta G, Brun FG, van Duren L, Bouma TJ, Perez-Llorens JL. 2008. Interaction between hydrodynamics and seagrass canopy structure: spatially explicit effects on ammonium uptake rates. Limnol Oceanogr 53:1531–9.CrossRefGoogle Scholar
  42. Mutchler T, Sullivan MJ, Fry B. 2004. Potential of 14N isotope enrichment to resolve ambiguities in coastal trophic relationships. Mar Ecol Prog Ser 266:27–33.CrossRefGoogle Scholar
  43. Perez M, Duarte CM, Romero J, Sand-Jensen K, Alcoverro T. 1994. Growth plasticity in Cymodocea nodosa stands: the importance of nutrient supply. Aquat Bot 47:249–64.CrossRefGoogle Scholar
  44. Pickett STA, Kolasa J, Armesto JJ, Collins SL. 1989. The ecological concept of disturbance and its expression at various hierarchical levels. Oikos 54:129–36.CrossRefGoogle Scholar
  45. Powell GVN, Kenworthy WJ, Fourqurean JW. 1989. Experimental evidence for nutrient limitation of seagrass growth in a tropical estuary with restricted circulation. Bull Mar Sci 44:324–40.Google Scholar
  46. Reed DC, Raimondi PT, Carr MH, Goldwasser L. 2000. The role of dispersal and disturbance in determining spatial heterogeneity in sedentary organisms. Ecology 81:2011–26.CrossRefGoogle Scholar
  47. Robbins BD, Bell SS. 2000. Dynamics of a subtidal seagrass landscape: seasonal and annual change in relation to water depth. Ecology 81:1193–205.CrossRefGoogle Scholar
  48. Rose CD, Dawes CJ. 1999. Effects of community structure on the seagrass Thalassia testudinum. Mar Ecol Prog Ser 184:83–95.CrossRefGoogle Scholar
  49. Sheridan P. 2004. Recovery of floral and faunal communities after placement of dredged material on seagrasses in Laguna Madre, Texas. Estuar Coast Shelf Sci 59:441–58.CrossRefGoogle Scholar
  50. Short FT. 1983. The seagrass, Zostera marina L.: plant morphology and bed structure in relation to sediment ammonium in Izembek Lagoon, Alaska. Aquat Bot 16:149–61.CrossRefGoogle Scholar
  51. Siemann E, Rogers WE. 2003. Changes in light and nitrogen availability under pioneer trees may indirectly facilitate tree invasions of grasslands. J Ecol 91:923–31.CrossRefGoogle Scholar
  52. Tilman D. 1987. Secondary succession and the pattern of plant dominance along experimental nitrogen gradients. Ecol Monogr 57:189–214.CrossRefGoogle Scholar
  53. Tilman D, Wedin D. 1991. Dynamics of nitrogen competition between successional grasses. Ecology 72:1038–49.CrossRefGoogle Scholar
  54. Valiela I, McClelland J, Hauxwell J, Behr PJ, Hersh D, Foreman K. 1997. Macroalgal blooms in shallow estuaries: controls and ecophysiological and ecosystem consequences. Limnol Oceanogr 42:1105–18.CrossRefGoogle Scholar
  55. Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman DG. 1997. Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–50.Google Scholar
  56. Welschmeyer NA. 1994. Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol Oceanogr 39:1985–92.CrossRefGoogle Scholar
  57. Zieman JC, Fourqurean JW, Iverson RL. 1989. Distribution, abundance and productivity of seagrasses and macroalgae in Florida Bay. Bull Mar Sci 44:292–311.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Anna R. Armitage
    • 1
    • 2
  • Thomas A. Frankovich
    • 3
  • James W. Fourqurean
    • 3
  1. 1.Department of Biological Sciences and Southeast Environmental Research CenterFlorida International UniversityMiamiUSA
  2. 2.Department of Marine BiologyTexas A&M University at GalvestonGalvestonUSA
  3. 3.Marine Sciences Program, Department of Biological Sciences and Southeast Environmental Research CenterFlorida International UniversityNorth MiamiUSA

Personalised recommendations