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Nitrogen–phosphorous interactions in young northern hardwoods indicate P limitation: foliar concentrations and resorption in a factorial N by P addition experiment

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Abstract

Resorption, the process of withdrawing foliar nutrients prior to leaf abscission, is one of the most important nutrient conservation mechanisms in trees. Along with foliar nutrient concentrations, foliar resorption can be used to infer nutrient limitation. We collected green and senesced leaves of five species in early successional stands in the White Mountains of New Hampshire. In unmanipulated controls, foliar N:P ratios ranged from 20 to 31 and litter N:P ratios ranged from 19 to 36. These values suggest P limitation, although this forest type has been assumed to be N-limited. Additionally, N:P resorption ratios in control plots were < 1, reflecting proportionately more conservation of P through resorption than N. Four years into a full-factorial N × P fertilization experiment, N and P additions had increased N and P concentrations in leaves; more importantly, P addition reduced N concentration, possibly indicating alleviation of growth limitation by P. Resorption of P was less proficient (indicated by the concentration of an element in leaf litter) with P addition, as expected. Resorption proficiency and efficiency (the proportion of leaf nutrients resorbed) of N increased with P addition, suggesting increased demand for N with alleviation of P limitation. Resorption of P was more proficient and efficient with N addition, consistent with exacerbated P limitation. Temperate forests on glaciated soils are generally thought to be N-limited, but long-term N × P manipulations in this biome are lacking. Our results suggest that decades of anthropogenic N deposition may have tipped the balance to P limitation in these forests.

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References

  • Aber JD, Goodale CL, Ollinger SV et al (2003) Is nitrogen deposition altering the nitrogen status of northeastern forests? AIBS Bull 53:375–389

    Google Scholar 

  • Adams MB, Loughry LH, Plaugher LL (2003) Experimental forests and ranges of the USDA forest service

  • Aerts R (1990) Nutrient use efficiency in evergreen and deciduous species from heathlands. Oecologia 84:391–397

    Article  PubMed  Google Scholar 

  • Aerts R (1996) Nutrient resorption from senescing leaves of perennials: are there general patterns? J Ecol 84:597–608

    Article  Google Scholar 

  • Aerts R, Chapin FS (1999) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67

    Article  Google Scholar 

  • Ågren GI (2004) The C:N:P stoichiometry of autotrophs—theory and observations. Ecol Lett 7:185–191. https://doi.org/10.1111/j.1461-0248.2004.00567.x

    Article  Google Scholar 

  • Bai Y, Wu J, Clark CM et al (2010) Tradeoffs and thresholds in the effects of nitrogen addition on biodiversity and ecosystem functioning: evidence from inner Mongolia Grasslands. Glob Change Biol 16:358–372

    Article  Google Scholar 

  • Berendse F, Aerts R (1987) Nitrogen-use-efficiency: a biologically meaningful definition? JSTOR 1:293–296

    Google Scholar 

  • Bloom AJ, Chapin FS III, Mooney HA (1985) Resource limitation in plants-an economic analogy. Annu Rev Ecol Syst 16:363–392

    Article  Google Scholar 

  • Buchanan-Wollaston V (1997) The molecular biology of leaf senescence. J Exp Bot 48:181–199

    Article  Google Scholar 

  • Chapin FS, Matson PA, Mooney HA (2002) Terrestrial decomposition. Springer, Berlin

    Google Scholar 

  • Chapin FS III, Matson PA, Vitousek P (2011) Principles of terrestrial ecosystem ecology. Springer, Berlin

    Book  Google Scholar 

  • Danger M, Daufresne T, Lucas F et al (2008) Does Liebig’s law of the minimum scale up from species to communities? Oikos 117:1741–1751

    Article  Google Scholar 

  • Davidson EA, Reis de Carvalho CJ, Vieira IC et al (2004) Nitrogen and phosphorus limitation of biomass growth in a tropical secondary forest. Ecol Appl 14:150–163

    Article  Google Scholar 

  • dos Santos Jr UM, de Carvalho Gonçalves JF, Feldpausch TR (2006) Growth, leaf nutrient concentration and photosynthetic nutrient use efficiency in tropical tree species planted in degraded areas in central Amazonia. For Ecol Manag 226:299–309

    Article  Google Scholar 

  • Elser JJ, Bracken ME, Cleland EE et al (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142

    Article  Google Scholar 

  • Fahey TJ, Battles JJ, Wilson GF (1998) Responses of early successional northern hardwood forests to changes in nutrient availability. Ecol Monogr 68:183–212

    Article  Google Scholar 

  • Fei S, Steiner KC (2007) Evidence for increasing red maple abundance in the eastern United States. For Sci 53:473–477

    Google Scholar 

  • Finzi AC, Austin AT, Cleland EE et al (2011) Responses and feedbacks of coupled biogeochemical cycles to climate change: examples from terrestrial ecosystems. Front Ecol Environ 9:61–67

    Article  Google Scholar 

  • Fisk MC, Ratliff TJ, Goswami S, Yanai RD (2014) Synergistic soil response to nitrogen plus phosphorus fertilization in hardwood forests. Biogeochemistry 118:195–204

    Article  CAS  Google Scholar 

  • Goswami S, Fisk MC, Vadeboncoeur MA et al (2018) Phosphorus limitation of aboveground production in northern hardwood forests. Ecology 99:438–449

    Article  PubMed  Google Scholar 

  • Gradowski T, Thomas SC (2006) Phosphorus limitation of sugar maple growth in central Ontario. For Ecol Manag 226:104–109. https://doi.org/10.1016/j.foreco.2005.12.062

    Article  Google Scholar 

  • Grime JP (1979) Plant strategies and vegetation processes. Plant Strateg Veg Process 206:1176–1177

    Google Scholar 

  • Güsewell S (2004) N:P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266

    Article  Google Scholar 

  • Haase DL, Rose R (1995) Vector analysis and its use for interpreting plant nutrient shifts in response to silvicultural treatments. For Sci 41:54–66

    Google Scholar 

  • Hagen-Thorn A, Varnagiryte I, Nihlgard B, Armolaitis K (2006) Autumn nutrient resorption and losses in four deciduous forest tree species. For Ecol Manag 228:33–39

    Article  Google Scholar 

  • Harpole WS, Ngai JT, Cleland EE et al (2011) Nutrient co-limitation of primary producer communities. Ecol Lett 14:852–862

    Article  Google Scholar 

  • Hedwall P-O, Bergh J, Brunet J (2017) Phosphorus and nitrogen co-limitation of forest ground vegetation under elevated anthropogenic nitrogen deposition. Oecologia 185:317–326. https://doi.org/10.1007/s00442-017-3945-x

    Article  PubMed  PubMed Central  Google Scholar 

  • Ji H, Wen J, Du B et al (2018) Comparison of the nutrient resorption stoichiometry of Quercus variabilis Blume growing in two sites contrasting in soil phosphorus content. Ann For Sci. https://doi.org/10.1007/s13595-018-0727-5

    Article  Google Scholar 

  • Killingbeck KT (1996) Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency. Ecology 77:1716–1727

    Article  Google Scholar 

  • Kobe RK, Lepczyk CA, Iyer M (2005) Resorption efficiency decreases with increasing green leaf nutrients in a global data set. Ecology 86:2780–2792

    Article  Google Scholar 

  • Koerselman W, Meuleman AF (1996) The vegetation N: P ratio: a new tool to detect the nature of nutrient limitation. J Appl Ecol 1:1441–1450

    Article  Google Scholar 

  • Marklein AR, Houlton BZ (2012) Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytol 193:696–704

    Article  CAS  Google Scholar 

  • McGroddy ME, Daufresne T, Hedin LO (2004) Scaling of C:N:P stoichiometry in forests worldwide: implications of terrestrial redfield-type ratios. Ecology 85:2390–2401

    Article  Google Scholar 

  • Menge DN, Field CB (2007) Simulated global changes alter phosphorus demand in annual grassland. Glob Change Biol 13:2582–2591

    Article  Google Scholar 

  • Mohren GMJ, Van Den Burg J, Burger FW (1986) Phosphorus deficiency induced by nitrogen input in Douglas fir in the Netherlands. Plant Soil 95:191–200

    Article  CAS  Google Scholar 

  • NADP Program Office (2017) National Atmospheric Deposition Program

  • Naples BK, Fisk MC (2010) Belowground insights into nutrient limitation in northern hardwood forests. Biogeochemistry 97:109–121

    Article  CAS  Google Scholar 

  • Niinemets Ü, Kull K (2005) Co-limitation of plant primary productivity by nitrogen and phosphorus in a species-rich wooded meadow on calcareous soils. Acta Oecol 28:345–356

    Article  Google Scholar 

  • Ostertag R (2010) Foliar nitrogen and phosphorus accumulation responses after fertilization: an example from nutrient-limited Hawaiian forests. Plant Soil 334:85–98

    Article  CAS  Google Scholar 

  • Rastetter EB, Shaver GR (1992) A model of multiple-element limitation for acclimating vegetation. Ecology 73:1157–1174

    Article  Google Scholar 

  • Rastetter EB, Yanai RD, Thomas RQ et al (2013) Recovery from disturbance requires resynchronization of ecosystem nutrient cycles. Ecol Appl 23:621–642

    Article  CAS  PubMed  Google Scholar 

  • Reed SC, Townsend AR, Davidson EA, Cleveland CC (2012) Stoichiometric patterns in foliar nutrient resorption across multiple scales. New Phytol 196:173–180

    Article  CAS  PubMed  Google Scholar 

  • Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci USA 101:11001–11006

    Article  CAS  PubMed  Google Scholar 

  • Reich PB, Walters MB, Ellsworth DS (1997) From tropics to tundra: global convergence in plant functioning. Proc Natl Acad Sci 94:13730–13734

    Article  CAS  PubMed  Google Scholar 

  • Reich PB, Wright IJ, Cavender-Bares J et al (2003) The evolution of plant functional variation: traits, spectra, and strategies. Int J Plant Sci 164:S143–S164

    Article  Google Scholar 

  • See CR, Yanai RD, Fisk MC et al (2015) Soil nitrogen affects phosphorus recycling: foliar resorption and plant–soil feedbacks in a northern hardwood forest. Ecology 96:2488–2498

    Article  PubMed  Google Scholar 

  • Soudzilovskaia NA, Onipchenko VG, Cornelissen JH, Aerts R (2007) Effects of fertilisation and irrigation on ‘foliar afterlife’in alpine tundra. J Veg Sci 18:755–766

    Article  Google Scholar 

  • Staaf H (1982) Plant nutrient changes in beech leaves during senescence as influenced by site characteristics. ACTA OECOL OECOL PLANT 3:161–170

    Google Scholar 

  • Townsend AR, Cleveland CC, Asner GP, Bustamante M (2007) Controls over foliar N:P ratios in tropical rain forests. Ecology 88:107–118

    Article  PubMed  Google Scholar 

  • Treseder KK, Vitousek PM (2001) Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiian rain forests. Ecology 82:946–954

    Article  Google Scholar 

  • Tripler C, Canham C, Inouye R, Schnurr J (2002) Soil nitrogen availability, plant luxury consumption, and herbivory by white-tailed deer. Oecologia 133:517–524

    Article  CAS  PubMed  Google Scholar 

  • US Environmental Protection Agency Clean Air Markets Division (2017) Clean air status and trends network (CASTNET)

  • Vadeboncoeur MA (2010) Meta-analysis of fertilization experiments indicates multiple limiting nutrients in northeastern deciduous forests. Can J For Res 40:1766–1780

    Article  CAS  Google Scholar 

  • Vadeboncoeur MA, Hamburg SP, Blum JD et al (2012) The quantitative soil pit method for measuring belowground carbon and nitrogen stocks. Soil Sci Soc Am J 76:2241. https://doi.org/10.2136/sssaj2012.0111

    Article  CAS  Google Scholar 

  • Vadeboncoeur MA, Hamburg SP, Yanai RD, Blum JD (2014) Rates of sustainable forest harvest depend on rotation length and weathering of soil minerals. For Ecol Manag 318:194–205

    Article  Google Scholar 

  • Van Heerwaarden LM, Toet S, Aerts R (2003) Nitrogen and phosphorus resorption efficiency and proficiency in six sub-arctic bog species after 4 years of nitrogen fertilization. J Ecol 91:1060–1070

    Article  Google Scholar 

  • Venterink HO, Güsewell S (2010) Competitive interactions between two meadow grasses under nitrogen and phosphorus limitation. Funct Ecol 24:877–886

    Article  Google Scholar 

  • Vergutz L, Manzoni S, Porporato A et al (2012) Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecol Monogr 82:205–220

    Article  Google Scholar 

  • Vitousek PM (1984) Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology 65:285–298

    Article  CAS  Google Scholar 

  • Vitousek PM, Sanford RL Jr (1986) Nutrient cycling in moist tropical forest. Annu Rev Ecol Syst 17:137–167

    Article  Google Scholar 

  • Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecol Appl 20:5–15

    Article  PubMed  Google Scholar 

  • Walker TW, Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15:1–19

    Article  CAS  Google Scholar 

  • Wood Tana E, Deborah Lawrence, Wells Jessie A (2011) Inter-specific variation in foliar nutrients and resorption of nine canopy-tree species in a secondary neotropical rain forest. Biotropica 43:544–551. https://doi.org/10.1111/j.1744-7429.2010.00740.x

    Article  Google Scholar 

  • Wright IJ, Reich PB, Westoby M et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827

    Article  CAS  PubMed  Google Scholar 

  • Yanai RD (1992) Phosphorus budget of a 70-year-old northern hardwood forest. Biogeochemistry 17:1–22

    Article  CAS  Google Scholar 

  • Yang Y, Yanai RD, Fatemi FR et al (2016) Sources of variability in tissue chemistry in northern hardwood species. Can J For Res 46:285–296. https://doi.org/10.1139/cjfr-2015-0302

    Article  CAS  Google Scholar 

  • Yuan ZY, Chen HY (2015) Negative effects of fertilization on plant nutrient resorption. Ecology 96:373–380

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This research was conducted on plots established by Matt Vadeboncoeur, Steve Hamburg, and others almost 15 years ago under funding to Yanai from the National Science Foundation (DEB 0235650). Beginning in 2010, Multiple Element Limitation in Northern Hardwood Ecosystems (http://www.esf.edu/melnhe) was funded (by DEB 0949324 to Yanai), guided by the early vision of Tim Fahey and Melany Fisk. Maintaining the sites and fertilizing them has involved 69 summer interns and 33 graduate students. We are especially grateful to Bali Quintero, Adam Wild, and Nora Yanai, who shot and processed green leaves in August 2014. Jerome Barner, Stephanie Suttenberg, and Alex Kuhn helped collect leaf litter in fall 2014. The paper was improved by comments from Keith Killingbeck, Craig See, and students in FOR 694 at SUNY-ESF. The Bartlett Experimental Forest is owned and operated by the USDA Forest Service. This paper is a product of the Hubbard Brook Long-Term Ecological Research network, funded by the National Science Foundation (DEB 1633026).

Funding

This study was funded by the National Science Foundation (DEB 0235650 and 0949324).

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  1. Kara Gonzales

    Present address: Caltrans, Oakland, CA, USA

Authors and Affiliations

  1. Graduate Program in Environmental Science, State University of New York College of Environmental Science and Forestry, Syracuse, NY, USA

    Kara Gonzales & Ruth Yanai

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  1. Kara Gonzales
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Contributions

The idea for this study was part of a much larger project led by RDY. KEG joined the project in her final semester as an undergraduate student, collecting samples and processing them. As a graduate student, KEG analyzed the data. KEG and RDY interpreted the results, wrote the paper, and enhanced its value through extended revision.

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Correspondence to Kara Gonzales.

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Communicated by Jason P. Kaye.

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Gonzales, K., Yanai, R. Nitrogen–phosphorous interactions in young northern hardwoods indicate P limitation: foliar concentrations and resorption in a factorial N by P addition experiment. Oecologia 189, 829–840 (2019). https://doi.org/10.1007/s00442-019-04350-y

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