Nutrient co-limitation of primary producer communities.

Synergistic interactions between multiple limiting resources are common, highlighting the importance of co-limitation as a constraint on primary production. Our concept of resource limitation has shifted over the past two decades from an earlier paradigm of single-resource limitation towards concepts of co-limitation by multiple resources, which are predicted by various theories. Herein, we summarise multiple-resource limitation responses in plant communities using a dataset of 641 studies that applied factorial addition of nitrogen (N) and phosphorus (P) in freshwater, marine and terrestrial systems. We found that more than half of the studies displayed some type of synergistic response to N and P addition. We found support for strict definitions of co-limitation in 28% of the studies: i.e. community biomass responded to only combined N and P addition, or to both N and P when added separately. Our results highlight the importance of interactions between N and P in regulating primary producer community biomass and point to the need for future studies that address the multiple mechanisms that could lead to different types of co-limitation.

[1]  Christopher B. Field,et al.  Plant Responses to Multiple Environmental FactorsPhysiological ecology provides tools for studying how interacting environmental resources control plant growth , 1987 .

[2]  Edward B. Rastetter,et al.  A MODEL OF MULTIPLE-ELEMENT LIMITATION FOR ACCLIMATING VEGETATION' , 1992 .

[3]  Helmut Hillebrand,et al.  Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. , 2007, Ecology letters.

[4]  Philip M. Dixon,et al.  A STATISTICAL TEST TO SHOW NEGLIGIBLE TREND , 2005 .

[5]  William Gregory,et al.  Animal Chemistry; or Organic Chemistry in Its Application to Physiology and Pathology , 1842, The Medico-chirurgical review.

[6]  J. Elser,et al.  The origins of the Redfield nitrogen-to-phosphorus ratio are in a homoeostatic protein-to-rRNA ratio. , 2011, Ecology letters.

[7]  Jacob E. Allgeier,et al.  The frequency and magnitude of non‐additive responses to multiple nutrient enrichment , 2011 .

[8]  Jason T. Ritt,et al.  Some thoughts on the concept of colimitation: Three definitions and the importance of bioavailability , 2008 .

[9]  S. Güsewell,et al.  Competitive interactions between two meadow grasses under nitrogen and phosphorus limitation , 2010 .

[10]  Craig W. Osenberg,et al.  META‐ANALYSIS OF MARINE NUTRIENT‐ENRICHMENT EXPERIMENTS: VARIATION IN THE MAGNITUDE OF NUTRIENT LIMITATION , 1999 .

[11]  Donald L. DeAngelis,et al.  Multiple nutrient limitations in ecological models , 1989 .

[12]  Helmut Hillebrand,et al.  A cross-system synthesis of consumer and nutrient resource control on producer biomass. , 2008, Ecology letters.

[13]  J. Bakker,et al.  NUTRIENT LIMITATION AFTER LONG-TERM NITROGEN FERTILIZER APPLICATION IN CUT GRASSLANDS , 1994 .

[14]  F. Stuart Chapin,et al.  Species composition interacts with fertilizer to control long-term change in tundra productivity , 2001 .

[15]  F. Stuart Chapin,et al.  The Nature of Nutrient Limitation in Plant Communities , 1986, The American Naturalist.

[16]  J. Elser,et al.  Shifts in Lake N:P Stoichiometry and Nutrient Limitation Driven by Atmospheric Nitrogen Deposition , 2009, Science.

[17]  P. Chesson Mechanisms of Maintenance of Species Diversity , 2000 .

[18]  W. L. Nelson,et al.  Soil fertility and fertilizers , 1957 .

[19]  M. Twiss,et al.  Evidence for phosphorus, nitrogen, and iron colimitation of phytoplankton communities in Lake Erie , 2007 .

[20]  Jos T. A. Verhoeven,et al.  BIOMASS N:P RATIOS AS INDICATORS OF NUTRIENT LIMITATION FOR PLANT POPULATIONS IN WETLANDS , 2003 .

[21]  D. Tilman,et al.  Plant Allocation and the Multiple Limitation Hypothesis , 1992, The American Naturalist.

[22]  E. Davidson,et al.  Environmental science: Nutrients in synergy , 2007, Nature.

[23]  H. Paerl,et al.  Controlling Eutrophication: Nitrogen and Phosphorus , 2009, Science.

[24]  Douglas H. Johnson The Insignificance of Statistical Significance Testing , 1999 .

[25]  J. Craine,et al.  Plant nitrogen and phosphorus limitation in 98 North American grassland soils , 2010, Plant and Soil.

[26]  David Tilman,et al.  Niche tradeoffs, neutrality, and community structure: a stochastic theory of resource competition, invasion, and community assembly. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[27]  P. Falkowski,et al.  Multi-nutrient, multi-group model of present and future oceanic phytoplankton communities , 2006 .

[28]  R. Hecky,et al.  Nutrient limitation of phytoplankton in freshwater and marine environments: A review of recent evidence on the effects of enrichment1 , 1988 .

[29]  D. Altman,et al.  Statistics notes: Measurement error , 1996 .

[30]  D. Tilman,et al.  Recovery of plant diversity following N cessation: effects of recruitment, litter, and elevated N cycling. , 2010, Ecology.

[31]  Martial Bernoux,et al.  Soils, a sink for N2O? A review , 2007 .

[32]  F. Chapin,et al.  Principles of Terrestrial Ecosystem Ecology , 2002, Springer New York.

[33]  Andreas Oschlies,et al.  Chain model of phytoplankton P, N and light colimitation , 2009 .

[34]  M. Rosenzweig Net Primary Productivity of Terrestrial Communities: Prediction from Climatological Data , 1968, The American Naturalist.

[35]  P. M. Gorresen,et al.  A statistical test to show negligible trend: comment. , 2008, Ecology.

[36]  Jessica Gurevitch,et al.  THE META‐ANALYSIS OF RESPONSE RATIOS IN EXPERIMENTAL ECOLOGY , 1999 .

[37]  J. Craine Resource Strategies of Wild Plants , 2009 .

[38]  K. Gross,et al.  Separating the influence of resource 'availability' from resource 'imbalance' on productivity-diversity relationships. , 2009, Ecology letters.

[39]  S. Güsewell High nitrogen : phosphorus ratios reduce nutrient retention and second-year growth of wetland sedges. , 2005, The New phytologist.

[40]  G. E. Hutchinson,et al.  The Balance of Nature and Human Impact: The paradox of the plankton , 2013 .

[41]  D. Schindler,et al.  Eutrophication: more nitrogen data needed. , 2009, Science.

[42]  Samuel L. Tisdale,et al.  Soil Fertility and Fertilizers , 1957 .

[43]  T. Kuhn,et al.  The Structure of Scientific Revolutions. , 1964 .

[44]  J. Huisman,et al.  Biodiversity of plankton by species oscillations and chaos , 1999, Nature.

[45]  V. D. Fageria NUTRIENT INTERACTIONS IN CROP PLANTS , 2001 .

[46]  D. Tilman Resource competition and community structure. , 1983, Monographs in population biology.

[47]  M. Saito,et al.  Zinc‐cobalt colimitation of Phaeocystis antarctica , 2008 .

[48]  R. Sterner On the Phosphorus Limitation Paradigm for Lakes , 2008 .

[49]  D G Altman,et al.  Statistics Notes: Logarithms , 1996, BMJ.

[50]  J. Elser,et al.  Nutrient availability and phytoplankton nutrient limitation across a gradient of atmospheric nitrogen deposition. , 2009, Ecology.

[51]  F. Lucas,et al.  Does Liebig's law of the minimum scale up from species to communities? , 2008 .

[52]  F. Morel,et al.  Colimitation of phytoplankton growth by nickel and nitrogen , 1991 .

[53]  S. Hubbell,et al.  The unified neutral theory of biodiversity and biogeography at age ten. , 2011, Trends in ecology & evolution.

[54]  W. Ta,et al.  Ecosystem responses to water and nitrogen amendment in a California grassland , 2007 .

[55]  P. Vitousek,et al.  Nutrient limitation and soil development: Experimental test of a biogeochemical theory , 1997 .

[56]  J. Syers,et al.  The fate of phosphorus during pedogenesis , 1976 .

[57]  F. Chapin,et al.  Nutrient Manipulations in Terrestrial Ecosystems , 2000 .

[58]  J. Silvertown,et al.  The Park Grass Experiment 1856–2006: its contribution to ecology , 2006 .

[59]  M. B. Kirkham,et al.  On the origin of the theory of mineral nutrition of plants and the law of the minimum , 1999 .

[60]  U. Sommer A comparison of the Droop and the Monod models of nutrient limited growth applied to natural populations of phytoplankton , 1991 .

[61]  H. Mooney,et al.  Resource Limitation in Plants-An Economic Analogy , 1985 .

[62]  Ü. Niinemets,et al.  Co-limitation of plant primary productivity by nitrogen and phosphorus in a species-rich wooded meadow on calcareous soils , 2005 .

[63]  M. Droop SOME THOUGHTS ON NUTRIENT LIMITATION IN ALGAE 1 , 1973 .

[64]  T. Sinclair,et al.  Inadequacy of the Liebig Limiting‐Factor Paradigm for Explaining Varying Crop Yields , 1993 .

[65]  O. Sala,et al.  Long-Term Forage Production of North American Shortgrass Steppe. , 1992, Ecological applications : a publication of the Ecological Society of America.

[66]  S. Levin,et al.  Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton , 2004, Nature.