Skip to main content
SpringerLink
Log in

Nitrogen availability limits phosphorus uptake in an intertidal macroalga

  • Ecosystem ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ågren GI, Wetterstedt JA, Billberger MF (2012) Nutrient limitation on terrestrial plant growth—modeling the interaction between nitrogen and phosphorus. New Phytol 194:953–960

    Article  PubMed  Google Scholar 

  • Bari R, Pant BD, Stitt M, Scheible WR (2006) ) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–999

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 104:3719–3724

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bennett EM, Carpenter SR, Caraco NF (2001) Human impact on erodable phosphorus and eutrophication: a global perspective. Bioscience 51:227–234

    Article  Google Scholar 

  • 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 26:603–611

    Article  Google Scholar 

  • Bracken MES (2004) Invertebrate-mediated nutrient loading increases growth of an intertidal macroalga. J Phycol 40:1032–1041

    Article  Google Scholar 

  • Bracken MES, Williams SL (2013) Realistic changes in seaweed biodiversity affect multiple ecosystem functions on a rocky shore. Ecology 94:1944–1954 (in press)

    Article  PubMed  Google Scholar 

  • Bracken MES, Jones E, Williams SL (2011) Herbivores, tidal elevation, and species richness simultaneously mediate nitrate uptake by seaweed assemblages. Ecology 92:1083–1093

    Article  PubMed  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Chapman ARO, Cragie JS (1977) Seasonal growth in Laminaria longicruris: relations with dissolved inorganic nutrients and internal reserves of nitrogen. Mar Biol 40:197–205

    Article  CAS  Google Scholar 

  • 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 57:1–5

    Article  CAS  Google Scholar 

  • Christensen JP, Townsend DW, Montoya JP (1996) Water column nutrients and sedimentary denitrification in the Gulf of Maine. Cont Shelf Res 16:489–515

    Article  Google Scholar 

  • Corwith HL, Wheeler PA (2002) El Niño related variations in nutrient and chlorophyll distributions off Oregon. Prog Oceanogr 54:361–380

    Article  Google Scholar 

  • D’Elia CF, DeBoer JA (1978) Nutritional studies of two red algae. II. kinetics of ammonium and nitrate uptake 1, 2. J Phycol 14:266–272

    Article  Google Scholar 

  • Downing JA (1997) Marine nitrogen:phosphorus stoichiometry and the global N: P cycle. Biogeochemistry 37:237–252

    Article  Google Scholar 

  • 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 10:1135–1142

    Article  PubMed  Google Scholar 

  • Fournier RO, Marra J, Bohrer R, Det MV (1977) Plankton dynamics and nutrient enrichment of the Scotian Shelf. J Fish Res Board Can 34:1004–1018

    Article  CAS  Google Scholar 

  • 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 37:162–171

    Article  CAS  Google Scholar 

  • Fujita RM (1985) The role of nitrogen status in regulating transient ammonium uptake and nitrogen storage by macroalgae. J Exp Mar Biol Ecol 92:283–301

    Article  CAS  Google Scholar 

  • Haines KC, Wheeler PA (1978) Ammonium and nitrate uptake by the marine macrophytes Hypnea musvuformis (Rhodophyta) and Macrocystis pyrifera (Phaeophyta). J Phycol 14:319–324

    Article  CAS  Google Scholar 

  • Hanisak MD (1979) Nitrogen limitation of Codium fragile ssp. tomentosoides as determined by tissue analysis. Mar Biol 50:333–337

    Article  CAS  Google Scholar 

  • 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 14:852–862

    Article  PubMed  Google Scholar 

  • Harrison W (1983) Uptake and recycling of soluble reactive phosphorus by marine microplankton. Mar Ecol Prog Ser 10:127–135

    Article  CAS  Google Scholar 

  • Hemmi A, Jormalainen V (2002) Nutrient enhancement increases performance of a marine herbivore via quality of its food alga. Ecology 83:1052–1064

    Article  Google Scholar 

  • Howarth RW, Marino R (2006) Nitrogen as the limiting nutrient for eutrophication in coastal marine ecosystems: evolving views over three decades. Limnol Oceanogr 51:364–376

    Article  CAS  Google Scholar 

  • Hurd CL, Dring MJ (1990) Phosphate uptake by intertidal algae in relation to zonation and season. Mar Biol 107:281–289

    Article  Google Scholar 

  • Hurd CL, Dring MJ (1991) Desiccation and phosphate uptake by intertidal fucoid algae in relation to zonation. British Phycol J 26:327–333

    Article  Google Scholar 

  • Lobban CS, Harrison PJ (1994) Seaweed ecology and physiology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Loladze I, Elser JJ (2011) The origins of the Redfield nitrogen-to-phosphorus ratio are in a homoeostatic protein-to-rRNA ratio. Ecol Lett 14:244–250

    Article  PubMed  Google Scholar 

  • Mann KH (1973) Seaweeds: their productivity and strategy for growth. Science 182:975–981

    Article  CAS  PubMed  Google Scholar 

  • 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 40:525–542

    CAS  Google Scholar 

  • 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 142:261–272

    Article  CAS  Google Scholar 

  • Pedersen MF, Borum J (1997) Nutrient control of estuarine macroalgae: growth strategy and the balance between nitrogen requirements and uptake. Mar Ecol Progr Ser 161:155–163

    Article  Google Scholar 

  • 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 399:103–115

    Article  CAS  Google Scholar 

  • 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, Boston

  • 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 57:2536–2546

    Article  CAS  Google Scholar 

  • Phillips JC, Hurd CL (2004) Kinetics of nitrate, ammonium and urea uptake by four intertidal seaweeds from New Zealand. J Phycol 40:534–545

    Article  CAS  Google Scholar 

  • Rausch C, Bucher M (2002) Molecular mechanisms of phosphate transport in plants. Planta 216:23–37

    Article  CAS  PubMed  Google Scholar 

  • Rhee GY (1974) Phosphate uptake under nitrate limitation by Scenedesmus sp. and its ecological implications. J Phycol 10:470–475

    CAS  Google Scholar 

  • 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 16:181–194

    Article  CAS  Google Scholar 

  • Ryther JH, Dunstan WM (1971) Nitrogen, phosphorus, and eutrophication in the coastal marine environment. Science 171:1008–1013

    Article  CAS  PubMed  Google Scholar 

  • Saito MA, Goepfert TJ, Ritt JT (2008) Some thoughts on the concept of colimitation: three definitions and the importance of bioavailability. Limol Oceanogr 53:276

    Article  CAS  Google Scholar 

  • Stephenson TA, Stephenson A (1949) The universal features of zonation between tide-marks on rocky coasts. J Ecol 37:289–305

    Article  Google Scholar 

  • Sterner RW, Elser JJ (2002) Ecological stoichiometry : the biology of elements from molecules to the biosphere. Princeton University Press, Princeton

    Google Scholar 

  • 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 53:1169–1180

    Article  CAS  Google Scholar 

  • Thomas TE, Harrison PJ (1985) Effect of nitrogen supply on nitrogen uptake, accumulation and assimilation in Porphyra perforata (Rhodophyta). Mar Biol 85:269–278

    Article  CAS  Google Scholar 

  • Topinka JA (1978) Nitrogen uptake by Fucus spiralis (Phaeophyceae). J Phycol 14:241–247

    Article  CAS  Google Scholar 

  • Townsend DW (1991) Influences of oceanographic processes on the biological productivity of the Gulf of Maine. Rev Aquat Sci 5:211–230

    Google Scholar 

  • 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 7:737–750

    Google Scholar 

  • Wallentinus I (1984) Comparisons of nutrient uptake rates for Baltic macroalgae with different thallus morphologies. Mar Biol 80:215–225

    Article  CAS  Google Scholar 

  • 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 28:1–6

    Article  CAS  Google Scholar 

  • Wheeler PA, North WJ (1981) Nitrogen supply, tissue composition and frond growth rates for Macrocystis pyrifera off the coast of Southern California. Mar Biol 64:59–69

    Article  CAS  Google Scholar 

  • 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 96:15336–15341

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

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.

Author information

Author notes

  1. Matthew E. S. Bracken

    Present address: Department of Ecology and Evolutionary Biology, University of California, 321 Steinhaus Hall, Irvine, CA, 92697-2525, USA

Authors and Affiliations

  1. Marine Science Center, Northeastern University, 430 Nahant Road, Nahant, MA, 01908, USA

    Valerie Perini & Matthew E. S. Bracken

Authors
  1. Valerie Perini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matthew E. S. Bracken
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Valerie Perini.

Additional information

Communicated by Craig A. Layman.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Perini, V., Bracken, M.E.S. Nitrogen availability limits phosphorus uptake in an intertidal macroalga. Oecologia 175, 667–676 (2014). https://doi.org/10.1007/s00442-014-2914-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-014-2914-x

Keywords

Search

Navigation