Abstract
Functional balance theory predicts that plants will allocate less carbon belowground when the availability of nutrients is elevated. We tested this prediction in two successional northern hardwood forest stands by quantifying fine root biomass and growth after 5–7 years of treatment in a nitrogen (N) x phosphorus (P) factorial addition experiment. We quantified root responses at two different levels of treatment: the whole-plot scale fertilization and small-patch scale fertilization of ingrowth cores. Fine root biomass was higher in plots receiving P, and fine root growth was highest in plots receiving both N and P. Thus, belowground productivity did not decrease in response to long-term addition of nutrients. We did not find conclusive evidence that elevated availability of one nutrient at the plot scale induced foraging for the other nutrient at the core scale, or that foraging for nutrients at the core scale responded to addition of limiting nutrients. Our observations suggest NP co-limitation of fine root growth and indicate complex interactions of N and P affecting aboveground and belowground production in early successional northern hardwood forest ecosystems.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
Data from this manuscript are available at: fine root ingrowth and biomass: https://doi.org/10.6073/pasta/c51516c8eca9071862db5becec0f4542woody production: https://doi.org/10.6073/pasta/377b1fd44bd88a58e9654ab207e50706leaf litterfall: https://doi.org/10.6073/pasta/8b2975a3a02cbcfb1b0a12ac954576d4 resin available nutrients: https://doi.org/10.6073/pasta/e842c6704690be8e041da48a778583e3soil respiration: https://doi.org/10.6073/pasta/eb37cd72ccaa3e9197c461f0c1c734eb.
References
Ågren GI, Wetterstedt JÅM, Billberger MFK. 2012. Nutrient limitation on terrestrial plant growth—modeling the interaction between nitrogen and phosphorus. New Phytol. 194(4):953–960. https://doi.org/10.1111/j.1469-8137.2012.04116.x.
Alvarez-Clare S, Mack MC, Brooks M. 2013. A direct test of nitrogen and phosphorus limitation to net primary productivity in a lowland tropical wet forest. Ecology 94(7):1540–1551. https://doi.org/10.1890/12-2128.1.
Amrhein V, Greenland S, McShane B. 2019. Scientists rise up against statistical significance. Nature 567(7748):305–307.
Bates D, Mächler M, Bolker B, Walker S. 2015. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67(1):1–48. https://doi.org/10.18637/jss.v067.i01.
Blanes MC, Emmett BA, Viñegla B, Carreira JA. 2012. Alleviation of P limitation makes tree roots competitive for N against microbes in a N-saturated conifer forest: a test through P fertilization and 15N labelling. Soil Biol. Biochem. 48:51–59. https://doi.org/10.1016/j.soilbio.2012.01.012.
Bloom AJ, Chapin FS III, Mooney HA. 1985. Resource limitation in plants-an economic analogy. Ann. Rev. Ecol. Syst. 16(1):363–392.
Burton A, Pregitzer K, Hendrick R. 2000. Relationships between fine root dynamics and nitrogen availability in Michigan northern hardwood forests. Oecologia 125:389–399. https://doi.org/10.1007/s004420000455.
Burton A, Pregitzer K, Ruess R, Hendrick R, Allen M. 2002. Root respiration in north American forests: effects of nitrogen concentration and temperature across biomes. Oecologia 131(4):559–568. https://doi.org/10.1007/s00442-002-0931-7.
Cleland EE, Lind EM, DeCrappeo NM, DeLorenze E, Wilkins RA, Adler PB, Bakker JD, Brown CS, Davies KF, Esch E, Firn J, Gressard S, Gruner DS, Hagenah N, Harpole WS, Hautier Y, Hobbie SE, Hofmockel KS, Kirkman K, Seabloom EW. 2019. Belowground biomass response to nutrient enrichment depends on light limitation across globally distributed grasslands. Ecosystems 22(7):1466–1477. https://doi.org/10.1007/s10021-019-00350-4.
Driscoll CT, Whitall D, Aber J, Boyer E, Castro M, Cronan C, Goodale CL, Groffman P, Hopkinson C, Lambert K, Lawrence G, Ollinger S. 2003. Nitrogen pollution in the northeastern United States: sources, effects, and management options. BioScience 53(4):357. https://doi.org/10.1641/0006-3568(2003)053[0357:NPITNU]2.0.CO;2.
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(12):1135–1142. https://doi.org/10.1111/j.1461-0248.2007.01113.x.
Fahey TJ, Yanai RD, Li S, Mann T. 2021. Multiple element limitation in northern hardwood experiment (MELNHE): soil respiration at hubbard brook experimental forest, bartlett experimental forest and jeffers brook, central NH USA, 2008—present ver 2. Environ. Data Initiat. https://doi.org/10.6073/pasta/eb37cd72ccaa3e9197c461f0c1c734eb.
Fahey TJ, Li S, Shan S, Fisk M, Yanai RD, Blum J. 2023. Multiple element limitation in northern hardwood ecosystems (MELNHE): root biomass and growth responses to nitrogen and phosphorus ver 1. Environ. Data Initiat. https://doi.org/10.6073/pasta/c51516c8eca9071862db5becec0f4542.
Fatemi FR, Yanai RD, Hamburg SP, Vadeboncoeur MA, Arthur MA, Briggs RD, Levine CR. 2011. Allometric equations for young northern hardwoods: the importance of age-specific equations for estimating aboveground biomass. Can. J. Forest Res. 41(4):881–891.
Finzi AC. 2009. Decades of atmospheric deposition have not resulted in widespread phosphorus limitation or saturation of tree demand for nitrogen in southern New England. Biogeochemistry 92(3):217–229.
Fisk MC. 2019. Resin-available nutrients in the O horizon in the MELNHE study at hubbard brook experimental forest, Bartlett experimental forest and jeffers brook, central NH USA, 2011-present ver 1. Environ. Data Initiat. https://doi.org/10.6073/pasta/e842c6704690be8e041da48a778583e3.
Fisk MC, Ratliff TJ, Goswami S, Yanai RD. 2014. Synergistic soil response to nitrogen plus phosphorus fertilization in hardwood forests. Biogeochemistry 118:195–204.
Fisk MC, Yanai RD, Fahey TJ. 2022a. Tree DBH response to nitrogen and phosphorus fertilization in the MELNHE study, hubbard brook experimental forest, bartlett experimental forest, and Jeffers Brook ver 1. Environ. Data Initiat. https://doi.org/10.6073/pasta/377b1fd44bd88a58e9654ab207e50706.
Fisk MC, Yanai RD, Hong SD, See CR, Goswami S. 2022b. Litter chemistry and masses for the MELNHE NxP fertilization experiment ver 1. Environ. Data Initiat. https://doi.org/10.6073/pasta/8b2975a3a02cbcfb1b0a12ac954576d4.
Giehl RF, von Wirén N. 2014. Root nutrient foraging. Plant Physiol. 166(2):509–517.
Gleeson SK, Good RE. 2003. Root allocation and multiple nutrient limitation in the New Jersey Pinelands. Ecol. Lett. 6(3):220–227.
Gonzales K, Yanai R. 2019. Nitrogen–phosphorous interactions in young northern hardwoods indicate P limitation: foliar concentrations and resorption in a factorial N by P addition experiment. Oecologia 189(3):829–840. https://doi.org/10.1007/s00442-019-04350-y.
Goswami S, Fisk MC, Vadeboncoeur MA, Garrison-Johnston M, Yanai RD, Fahey TJ. 2018. Phosphorus limitation of aboveground production in northern hardwood forests. Ecology 99(2):438–449. https://doi.org/10.1002/ecy.2100.
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(9):852–862. https://doi.org/10.1111/j.1461-0248.2011.01651.x.
Hendricks JJ, Nadelhoffer KJ, Aber JD. 1993. Assessing the role of fine roots in carbon and nutrient cycling. Trends Ecol. Evolut. 8(5):174–178.
Hermans C, Hammond JP, White PJ, Verbruggen N. 2006. How do plants respond to nutrient shortage by biomass allocation? Trends Plant Sci. 11(12):610–617. https://doi.org/10.1016/j.tplants.2006.10.007.
Hong DS, Gonzales KE, Fahey TJ, Yanai RD. 2022. Foliar nutrient concentrations of six northern hardwood species responded to nitrogen and phosphorus fertilization but did not predict tree growth. PeerJ 10:e13193.
Kloeppel, B. D., Harmon, M. E., & Fahey, T. J. 2007. Estimating aboveground net primary productivity in forest-dominated ecosystems. In T. J. Fahey & A. K. Knapp (Eds.), Principles and standards for measuring primary production (pp. 63–81). Oxford University Press. https://doi.org/10.1093/acprof:oso/9780195168662.003.0005.
Mann, T. 2021. Independent and interactive effects of nitrogen and phosphorus addition on forest soil respiration. [Unpublished MS thesis]. SUNY College of Environmental Science and Forestry.
Metcalfe DB, Williams M, Aragão LEOC, Costa ACLD, Almeida SSD, Braga AP, Gonçalves PHL, Athaydes JD, Junior S, Malhi Y, Meir P. 2007. A method for extracting plant roots from soil which facilitates rapid sample processing without compromising measurement accuracy. New Phytol. 174(3):697–703. https://doi.org/10.1111/j.1469-8137.2007.02032.x.
Nadelhoffer KJ. 2000. The potential effects of nitrogen deposition on fine-root production in forest ecosystems. New Phytol. 147(1):131–139.
NADP Program Office 2017. National atmospheric deposition program.
Naples BK, Fisk MC. 2010. Belowground insights into nutrient limitation in northern hardwood forests. Biogeochemistry 97(2–3):109–121. https://doi.org/10.1007/s10533-009-9354-4.
Bartlett Experimental Forest Neon/Bart. Bartlett Experimental Forest NEON. (n.d.). Retrieved July 8, 2022, from https://www.neonscience.org/field-sites/bart.
Oliver CD. 1980. Forest development in North America following major disturbances. Forest Ecol. Manag. 3:153–168.
Ostertag R. 2001. Effects of nitrogen and phosphorus availability on fine-root dynamics in Hawaiian montane forest. Ecology 82(2):485–499.
R: The R Project for Statistical Computing. (n.d.). Retrieved August 15, 2021, from https://www.r-project.org/.
Raich JW, Riley RH, Vitousek PM. 1994. Use of root-ingrowth cores to assess nutrient limitations in forest ecosystems. Can. J. Forest Res. 24(10):2135–2138.
Rastetter EB, Yanai RD, Thomas RQ, Vadeboncoeur MA, Fahey TJ, Fisk MC, Kwiatkowski BL, Hamburg SP. 2013. Recovery from disturbance requires resynchronization of ecosystem nutrient cycles. Ecol. Appl. 23(3):621–642.
Shan S, Devens H, Fahey T, Yanai R, Fisk M. 2022. Fine root growth increases in response to nitrogen addition in phosphorus-limited northern hardwood forests. Ecosystems. https://doi.org/10.1007/s10021-021-00735-4.
Simon J, Dannenmann M, Pena R, Gessler A, Rennenberg H. 2017. Nitrogen nutrition of beech forests in a changing climate: importance of plant-soil-microbe water, carbon, and nitrogen interactions. Plant Soil 418(1):89–114. https://doi.org/10.1007/s11104-017-3293-y.
Thornley JHM. 1991. A transport-resistance model of forest growth and partitioning. Ann. Botany 68(3):211–226.
Vadeboncoeur MA. 2010. Meta-analysis of fertilization experiments indicates multiple limiting nutrients in northeastern deciduous forests. Can. J. Forest Res. 40(9):1766–1780. https://doi.org/10.1139/X10-127.
Vitousek PM, Porder S, Houlton BZ, Chadwick OA. 2010. Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecol. Appl. 20(1):5–15. https://doi.org/10.1890/08-0127.1.
Waring BG, Perez-Aviles D, Murray JG, Powers JS. 2019. Plant community responses to stand-level nutrient fertilization in a secondary tropical dry forest. Ecology 100(6):e02691. https://doi.org/10.1002/ecy.2691.
Wright SJ. 2019. Plant responses to nutrient addition experiments conducted in tropical forests. Ecol. Monogr. 89(4):e01382.
Wright SJ, Yavitt JB, Wurzburger N, Turner BL, Tanner EVJ, Sayer EJ, Santiago LS, Kaspari M, Hedin LO, Harms KE, Garcia MN, Corre MD. 2011. Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest. Ecology 92(8):1616–1625.
Wurzburger N, Wright SJ. 2015. Fine-root responses to fertilization reveal multiple nutrient limitation in a lowland tropical forest. Ecology 96(8):2137–2146. https://doi.org/10.1890/14-1362.1.
Yanai RD. 1992. Phosphorus budget of a 70 year-old northern hardwood forest. Biogeochemistry 17(1):1–22.
Yuan ZY, Chen HYH. 2012. A global analysis of fine root production as affected by soil nitrogen and phosphorus. Proc. R. Soc. B: Biol. Sci. 279(1743):3796–3802. https://doi.org/10.1098/rspb.2012.0955.
Zhu F, Yoh M, Gilliam FS, Lu X, Mo J. 2013. Nutrient limitation in three lowland tropical forests in southern china receiving high nitrogen deposition: insights from fine root responses to nutrient additions. Plos One 8(12):e82661. https://doi.org/10.1371/journal.pone.0082661.
Acknowledgements
This research was supported by the NSF Long-Term Ecological Research Program (DEB-1114804) and by NSF (DEB-0949317) and the USDA National Institute of Food and Agriculture (2019-67019-29464). Geoff Wilson and Natalie Cleavitt assisted in field sampling and lab processing, and Erika Mudrak from Cornell Statistical Consulting Unit helped with data analysis. We are also grateful for the cooperation and support of the U.S Forest Service Northern Research Station and the Bartlett Experimental Forest. This project is a contribution to the Hubbard Brook Ecosystem Study.
Author information
Authors and Affiliations
Corresponding author
Additional information
Author Contributions
TJF, MCF, RDY, and SL designed the study. SL and TJF collected the data. SL performed analyses and drafted the manuscript, and TJF, MCF, and RDY contributed substantially to writing and revisions.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Li, S., Fisk, M.C., Yanai, R.D. et al. Co-limitation of Fine Root Growth by Nitrogen and Phosphorus in Early Successional Northern Hardwood Forests. Ecosystems 27, 33–44 (2024). https://doi.org/10.1007/s10021-023-00869-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10021-023-00869-7