, Volume 175, Issue 2, pp 667–676 | Cite as

Nitrogen availability limits phosphorus uptake in an intertidal macroalga

  • Valerie PeriniEmail author
  • Matthew E. S. Bracken
Ecosystem ecology - Original research


Nutrients such as nitrogen (N) and phosphorus (P) limit primary productivity, and recent anthropogenic activities are changing the availability of these nutrients, leading to alterations in the type and magnitude of nutrient limitation. Recent work highlights the potential for N and P to interact to limit primary production in terrestrial and freshwater systems. However, mechanisms underlying co-limitation are not well described. Documentation of ambient nutrient levels and tissue nutrients of the intertidal macroalga Fucus vesiculosus for 2 years in the southern Gulf of Maine, USA, indicates that N availability may be impacting the ability of F. vesiculosus to access P, despite relatively high ambient P concentrations. To experimentally validate these observations, F. vesiculosus individuals were enriched with N or P for 6 weeks, followed by an uptake experiment to examine how the interactions between these nutrients affected macroalgal N and P uptake efficiency. Results illustrate that exposure of seaweed to different nutrient regimes influenced nutrient uptake efficiency. Notably, seaweeds enriched with N displayed the highest P uptake efficiency at low, biologically relevant, P concentrations. Our results confirm that N availability may be mediating the ability of primary producers to access P. These interactions between limiting nutrients have implications for not only the growth and functioning of primary producers who rely directly on these nutrients but also the entire communities that they support.


Co-limitation Fucus vesiculosus Nutrient limitation Nutrient uptake Stoichiometry 



We thank C. Aguila, K. Benes, J. Douglass, B. Gillis, L. Henry, H. McInerney, I. Rosenthal, A. Saco, and B. Taggart for help with water sampling, seaweed collection, assistance with experiments, and/or tissue sample preparation for elemental analysis. D. Cheney, C. Thornber, and two anonymous reviewers provided valuable feedback on earlier versions of the manuscript. This work was funded by the National Science Foundation (OCE 0961364 to M.E.S.B. and G. Trussell and 0963010 to G. Trussell et al. as part of the Academic Research Infrastructure Recovery and Reinvestment Program). The research described here was completed as part of the requirements for a Master’s degree in Biology at Northeastern University, and this manuscript is contribution number 307 of the Marine Science Center, Northeastern University.


  1. Ågren GI, Wetterstedt JA, Billberger MF (2012) Nutrient limitation on terrestrial plant growth—modeling the interaction between nitrogen and phosphorus. New Phytol 194:953–960PubMedCrossRefGoogle Scholar
  2. Bari R, Pant BD, Stitt M, Scheible WR (2006) ) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–999PubMedCentralPubMedCrossRefGoogle Scholar
  3. Barth JA, Menge BA, Lubchenco J, Chan F, Bane JM, Kirincich AR, McManus MA, Nielsen KJ, Pierce SD, Washburn L (2007) Delayed upwelling alters nearshore coastal ocean ecosystems in the northern California current. Proc Nat Acad Sci USA 104:3719–3724PubMedCentralPubMedCrossRefGoogle Scholar
  4. Bennett EM, Carpenter SR, Caraco NF (2001) Human impact on erodable phosphorus and eutrophication: a global perspective. Bioscience 51:227–234CrossRefGoogle Scholar
  5. Björnsäter B, Wheeler PA (1990) Effect of nitrogen and phosphorus supply on growth and tissue composition of Ulva fenestrata and Enteromorpha intestinalis (Ulvales, Chlorophyta). J Phycol 26:603–611CrossRefGoogle Scholar
  6. Bracken MES (2004) Invertebrate-mediated nutrient loading increases growth of an intertidal macroalga. J Phycol 40:1032–1041CrossRefGoogle Scholar
  7. Bracken MES, Williams SL (2013) Realistic changes in seaweed biodiversity affect multiple ecosystem functions on a rocky shore. Ecology 94:1944–1954 (in press)PubMedCrossRefGoogle Scholar
  8. Bracken MES, Jones E, Williams SL (2011) Herbivores, tidal elevation, and species richness simultaneously mediate nitrate uptake by seaweed assemblages. Ecology 92:1083–1093PubMedCrossRefGoogle Scholar
  9. Burnham KP, Anderson DR (2002) Model selection and inference: a practical information-theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  10. Chapman ARO, Cragie JS (1977) Seasonal growth in Laminaria longicruris: relations with dissolved inorganic nutrients and internal reserves of nitrogen. Mar Biol 40:197–205CrossRefGoogle Scholar
  11. Chapman ARO, Lindley JE (1980) Seasonal growth of Laminaria solidungula in the Canadian High Arctic in relation to irradiance and dissolved nutrient concentrations. Mar Biol 57:1–5CrossRefGoogle Scholar
  12. Christensen JP, Townsend DW, Montoya JP (1996) Water column nutrients and sedimentary denitrification in the Gulf of Maine. Cont Shelf Res 16:489–515CrossRefGoogle Scholar
  13. Corwith HL, Wheeler PA (2002) El Niño related variations in nutrient and chlorophyll distributions off Oregon. Prog Oceanogr 54:361–380CrossRefGoogle Scholar
  14. D’Elia CF, DeBoer JA (1978) Nutritional studies of two red algae. II. kinetics of ammonium and nitrate uptake 1, 2. J Phycol 14:266–272CrossRefGoogle Scholar
  15. Downing JA (1997) Marine nitrogen:phosphorus stoichiometry and the global N: P cycle. Biogeochemistry 37:237–252CrossRefGoogle Scholar
  16. Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142PubMedCrossRefGoogle Scholar
  17. Fournier RO, Marra J, Bohrer R, Det MV (1977) Plankton dynamics and nutrient enrichment of the Scotian Shelf. J Fish Res Board Can 34:1004–1018CrossRefGoogle Scholar
  18. Fourqurean JW, Zieman JC (1992) Phosphorus limitation of primary production in Florida Bay: evidence from C:N: P ratios of the dominant seagrass Thalassia testudinum. Limnol Oceanogr 37:162–171CrossRefGoogle Scholar
  19. Fujita RM (1985) The role of nitrogen status in regulating transient ammonium uptake and nitrogen storage by macroalgae. J Exp Mar Biol Ecol 92:283–301CrossRefGoogle Scholar
  20. Haines KC, Wheeler PA (1978) Ammonium and nitrate uptake by the marine macrophytes Hypnea musvuformis (Rhodophyta) and Macrocystis pyrifera (Phaeophyta). J Phycol 14:319–324CrossRefGoogle Scholar
  21. Hanisak MD (1979) Nitrogen limitation of Codium fragile ssp. tomentosoides as determined by tissue analysis. Mar Biol 50:333–337CrossRefGoogle Scholar
  22. Harpole WS, Ngai JT, Cleland EE, Seabloom EW, Borer ET, Bracken MES, Elser JJ, Gruner DS, Hillebrand H, Shurin JB, Smith JE (2011) Nutrient co-limitation of primary producer communities. Ecol Lett 14:852–862PubMedCrossRefGoogle Scholar
  23. Harrison W (1983) Uptake and recycling of soluble reactive phosphorus by marine microplankton. Mar Ecol Prog Ser 10:127–135CrossRefGoogle Scholar
  24. Hemmi A, Jormalainen V (2002) Nutrient enhancement increases performance of a marine herbivore via quality of its food alga. Ecology 83:1052–1064CrossRefGoogle Scholar
  25. Howarth RW, Marino R (2006) Nitrogen as the limiting nutrient for eutrophication in coastal marine ecosystems: evolving views over three decades. Limnol Oceanogr 51:364–376CrossRefGoogle Scholar
  26. Hurd CL, Dring MJ (1990) Phosphate uptake by intertidal algae in relation to zonation and season. Mar Biol 107:281–289CrossRefGoogle Scholar
  27. Hurd CL, Dring MJ (1991) Desiccation and phosphate uptake by intertidal fucoid algae in relation to zonation. British Phycol J 26:327–333CrossRefGoogle Scholar
  28. Lobban CS, Harrison PJ (1994) Seaweed ecology and physiology. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  29. Loladze I, Elser JJ (2011) The origins of the Redfield nitrogen-to-phosphorus ratio are in a homoeostatic protein-to-rRNA ratio. Ecol Lett 14:244–250PubMedCrossRefGoogle Scholar
  30. Mann KH (1973) Seaweeds: their productivity and strategy for growth. Science 182:975–981PubMedCrossRefGoogle Scholar
  31. Pastuszak M, Wright W, Patanjo D (1982) One year of nutrient distribution in the Georges Bank region in relation to hydrography, 1975–1976. J Mar Res 40:525–542Google Scholar
  32. Pedersen MF, Borum J (1996) Nutrient control of algal growth in estuarine waters. Nutrient limitation and the importance of nitrogen requirements and nitrogen storage among phytoplankton and species of macroalgae. Mar Ecol Progr Ser 142:261–272CrossRefGoogle Scholar
  33. Pedersen MF, Borum J (1997) Nutrient control of estuarine macroalgae: growth strategy and the balance between nitrogen requirements and uptake. Mar Ecol Progr Ser 161:155–163CrossRefGoogle Scholar
  34. Pedersen MF, Borum J, Fotel FL (2010) Phosphorus dynamics and limitation of fast- and slow-growing temperate seaweeds in Oslofjord, Norway. Mar Ecol Progr Ser 399:103–115CrossRefGoogle Scholar
  35. Perini V (2013) The role of seasonality, seaweed traits and seaweed herbivore interactions in nutrient cycling in the southern Gulf of Maine. Master’s thesis, Northeastern University, BostonGoogle Scholar
  36. Petrie B, Yeats P (2000) Annual and interannual variability of nutrients and their estimated fluxes in the Scotian Shelf—Gulf of Maine region. Can J Fish Aquat Sci 57:2536–2546CrossRefGoogle Scholar
  37. Phillips JC, Hurd CL (2004) Kinetics of nitrate, ammonium and urea uptake by four intertidal seaweeds from New Zealand. J Phycol 40:534–545CrossRefGoogle Scholar
  38. Rausch C, Bucher M (2002) Molecular mechanisms of phosphate transport in plants. Planta 216:23–37PubMedCrossRefGoogle Scholar
  39. Rhee GY (1974) Phosphate uptake under nitrate limitation by Scenedesmus sp. and its ecological implications. J Phycol 10:470–475Google Scholar
  40. Runcie JW, Ritchie RJ, Larkum AW (2004) Uptake kinetics and assimilation of phosphorus by Catenella nipae and Ulva lactuca can be used to indicate ambient phosphate availability. J Appl Phycol 16:181–194CrossRefGoogle Scholar
  41. Ryther JH, Dunstan WM (1971) Nitrogen, phosphorus, and eutrophication in the coastal marine environment. Science 171:1008–1013PubMedCrossRefGoogle Scholar
  42. Saito MA, Goepfert TJ, Ritt JT (2008) Some thoughts on the concept of colimitation: three definitions and the importance of bioavailability. Limol Oceanogr 53:276CrossRefGoogle Scholar
  43. Stephenson TA, Stephenson A (1949) The universal features of zonation between tide-marks on rocky coasts. J Ecol 37:289–305CrossRefGoogle Scholar
  44. Sterner RW, Elser JJ (2002) Ecological stoichiometry : the biology of elements from molecules to the biosphere. Princeton University Press, PrincetonGoogle Scholar
  45. Sterner RW, Andersen T, Elser JJ, Hessen DO, Hood JM, McCauley E, Urabe J (2008) Scale-dependent carbon:nitrogen:phosphorus seston stoichiometry in marine and freshwaters. Limnol Oceanogr 53:1169–1180CrossRefGoogle Scholar
  46. Thomas TE, Harrison PJ (1985) Effect of nitrogen supply on nitrogen uptake, accumulation and assimilation in Porphyra perforata (Rhodophyta). Mar Biol 85:269–278CrossRefGoogle Scholar
  47. Topinka JA (1978) Nitrogen uptake by Fucus spiralis (Phaeophyceae). J Phycol 14:241–247CrossRefGoogle Scholar
  48. Townsend DW (1991) Influences of oceanographic processes on the biological productivity of the Gulf of Maine. Rev Aquat Sci 5:211–230Google Scholar
  49. 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 7:737–750Google Scholar
  50. Wallentinus I (1984) Comparisons of nutrient uptake rates for Baltic macroalgae with different thallus morphologies. Mar Biol 80:215–225CrossRefGoogle Scholar
  51. Wheeler PA, Bjornsater BR (1992) Seasonal fluctuations in tissue nitrogen, phosphorous, and N:P for five macroalgal species common to the Pacific Northwest coast. J Phycol 28:1–6CrossRefGoogle Scholar
  52. Wheeler PA, North WJ (1981) Nitrogen supply, tissue composition and frond growth rates for Macrocystis pyrifera off the coast of Southern California. Mar Biol 64:59–69CrossRefGoogle Scholar
  53. Wykoff DD, Grossman AR, Weeks DP, Usuda H, Shimogawara K (1999) Psr1, a nuclear localized protein that regulates phosphorus metabolism in Chlamydomonas. Proc Natl Acad Sci USA 96:15336–15341PubMedCentralPubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Marine Science CenterNortheastern UniversityNahantUSA
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of CaliforniaIrvineUSA

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