Advertisement

Plant Ecology

, Volume 219, Issue 4, pp 391–401 | Cite as

Nitrogen fixation ability explains leaf chemistry and arbuscular mycorrhizal responses to fertilization

  • Yadugiri V. Tiruvaimozhi
  • Varun Varma
  • Mahesh Sankaran
Article

Abstract

Atmospheric nitrogen (N) and phosphorus (P) deposition rates are predicted to drastically increase in the coming decades. The ecosystem level consequences of these increases will depend on how plant tissue nutrient concentrations, stoichiometry and investment in nutrient uptake mechanisms such as arbuscular mycorrhizal fungi (AMF) change in response to increased nutrient availability, and how responses differ between plant functional types. Using a factorial nutrient addition experiment with seedlings of multiple N-fixing and non-N-fixing tree species, we examined whether leaf chemistry and AMF responses differ between these dominant woody plant functional groups of tropical savanna and dry forest ecosystems. We found that N-fixers have remarkably stable foliar chemistry that stays constant with external input of nutrients. Non-N-fixers responded to N and N + P addition by increasing both concentrations and total amounts of foliar N, but showed a corresponding decrease in P concentrations while total amounts of foliar P stayed constant, suggesting a ‘dilution’ of tissue P with increased N availability. Non-N-fixers also showed an increase in N:P ratios with N and N + P addition, probably driven by both an increase in N and a decrease in P concentrations. AMF colonization decreased with N + P addition in non-N-fixers and increased with N and N + P addition in N-fixers, suggesting differences in their nutrient acquisition roles in the two plant functional groups. Our results suggest that N-fixers and non-N-fixers can differ significantly in their responses to N and P deposition, with potential consequences for future nutrient and carbon cycling in savanna and dry forest ecosystems.

Keywords

Plant functional group Nutrient deposition Stoichiometry Mycorrhizae Savanna Global change 

Notes

Acknowledgements

We thank H. C. Manjunatha and family for providing us with land for conducting the experiment, FRLHT who helped raise the seedlings used in this experiment, Mahesh H. K., Bomarai, Mahadev H. K. and other people at Hosur who assisted with field work, and Arockia Catherin who helped with lab work. We are grateful to Anand M. Osuri for his comments on a previous draft of this manuscript. National Centre for Biological Sciences, Bangalore, provided core funding for this study.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 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.  https://doi.org/10.1016/S0065-2504(08)60016-1 CrossRefGoogle Scholar
  2. Allison VJ, Goldberg DE (2002) Species-level versus community-level patterns of mycorrhizal dependence on phosphorus: an example of Simpson’s paradox. Funct Ecol 16:346–352.  https://doi.org/10.1046/j.1365-2435.2002.00627.x CrossRefGoogle Scholar
  3. Allison SD, Vitousek PM (2004) Rapid nutrient cycling in leaf litter from invasive plants in Hawai’i. Oecologia 141:612–619.  https://doi.org/10.1007/s00442-004-1679-z CrossRefPubMedGoogle Scholar
  4. Antoninka A, Reich PB, Johnson NC (2011) Seven years of carbon dioxide enrichment, nitrogen fertilization and plant diversity influence arbuscular mycorrhizal fungi in a grassland ecosystem. New Phytol 192:200–214.  https://doi.org/10.1111/j.1469-8137.2011.03776.x CrossRefPubMedGoogle Scholar
  5. Barbosa ERM, van Langevelde F, Tomlinson KW, Carvalheiro LG, Kirkman K, de Bie S, Prins HHT (2014) Tree species from different functional groups respond differently to environmental changes during establishment. Oecologia 174:1345–1357.  https://doi.org/10.1007/s00442-013-2853-y CrossRefPubMedGoogle Scholar
  6. Bates DM (2010) lme4: mixed-effects modeling with R. Springer, New YorkGoogle Scholar
  7. Bates D, Maechler M, Bolker B, Walker S, Christensen RHB, Singmann H, Dai B, Grothendieck G, Eigen C, Rcpp L (2014) Package “lme4”. R Foundation for Statistical Computing, ViennaGoogle Scholar
  8. Bates D, Maechler M, Bolker B, Walker S, Christensen RHB, Singmann H, Dai B, Grothendieck G, Green P (2017) Package “lme4”. R Foundation for Statistical Computing, ViennaGoogle Scholar
  9. Bobbink R, Hicks K, Galloway J, Spranger T (2010) Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol Appl 20:30–59.  https://doi.org/10.1890/08-1140.1 CrossRefPubMedGoogle Scholar
  10. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White J-SS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135.  https://doi.org/10.1016/j.tree.2008.10.008 CrossRefPubMedGoogle Scholar
  11. Cárate-Tandalla D, Leuschner C, Homeier J (2015) Performance of seedlings of a shade-tolerant tropical tree species after moderate addition of N and P. Front Earth Sci 3:75.  https://doi.org/10.3389/feart.2015.00075 CrossRefGoogle Scholar
  12. Chimphango SBM, Potgieter G, Cramer MD (2015) Differentiation of the biogeochemical niches of legumes and non-legumes in the Cape Floristic Region of South Africa. Plant Ecol 216:1583–1595.  https://doi.org/10.1007/s11258-015-0542-0 CrossRefGoogle Scholar
  13. Cleland EE, Harpole WS (2010) Nitrogen enrichment and plant communities. Ann N Y Acad Sci 1195:46–61.  https://doi.org/10.1111/j.1749-6632.2010.05458.x CrossRefPubMedGoogle Scholar
  14. Egerton-Warburton LM, Johnson NC, Allen EB (2007) Mycorrhizal community dynamics following nitrogen fertilization: a cross site test in five grasslands. Ecol Monogr 77:527–544.  https://doi.org/10.1890/06-1772.1 CrossRefGoogle Scholar
  15. Filippelli GM (2002) The global phosphorus cycle. Rev Mineral Geochem 48:391–425.  https://doi.org/10.2138/rmg.2002.48.10 CrossRefGoogle Scholar
  16. Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892.  https://doi.org/10.1126/science.1136674 CrossRefPubMedGoogle Scholar
  17. Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500.  https://doi.org/10.1111/j.1469-8137.1980.tb04556.x CrossRefGoogle Scholar
  18. Güsewell S (2004) N:P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266.  https://doi.org/10.1111/j.1469-8137.2004.01192.x CrossRefGoogle Scholar
  19. Güsewell S, Koerselman W, Verhoeven JT (2003) Biomass N:P ratios as indicators of nutrient limitation for plant populations in wetlands. Ecol Appl 13:372–384CrossRefGoogle Scholar
  20. Hodge A, Storer K (2015) Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. Plant Soil 386:1–19.  https://doi.org/10.1007/s11104-014-2162-1 CrossRefGoogle Scholar
  21. Huang W, Zhou G, Liu J, Zhang D, Xu Z, Liu S (2012) Effects of elevated carbon dioxide and nitrogen addition on foliar stoichiometry of nitrogen and phosphorus of five tree species in subtropical model forest ecosystems. Environ Pollut 168:113–120.  https://doi.org/10.1016/j.envpol.2012.04.027 CrossRefPubMedGoogle Scholar
  22. Johnson NC (1993) Can fertilization of soil select less mutualistic mycorrhizae? Ecol Appl 3:749–757.  https://doi.org/10.2307/1942106 CrossRefPubMedGoogle Scholar
  23. Johnson NC (2010) Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol 185:631–647.  https://doi.org/10.1111/j.1469-8137.2009.03110.x CrossRefPubMedGoogle Scholar
  24. Johnson NC, Angelard C, Sanders IR, Kiers ET (2013) Predicting community and ecosystem outcomes of mycorrhizal responses to global change. Ecol Lett 16:140–153.  https://doi.org/10.1111/ele.12085 CrossRefPubMedGoogle Scholar
  25. Kodandapani N, Cochrane MA, Sukumar R (2008) A comparative analysis of spatial, temporal, and ecological characteristics of forest fires in seasonally dry tropical ecosystems in the Western Ghats, India. For Ecol Manag 256:607–617.  https://doi.org/10.1016/j.foreco.2008.05.006 CrossRefGoogle Scholar
  26. Koerselman W, Meuleman AFM (1996) The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. J Appl Ecol 33:1441–1450.  https://doi.org/10.2307/2404783 CrossRefGoogle Scholar
  27. Koufali E, Voulgari OK, Mamolos AP, Karanika ED, Veresoglou DS (2016) Functional groups’ performances as influenced by nitrogen, phosphorus and nodule inhibition of legumes. J Plant Ecol 9:784–791.  https://doi.org/10.1093/jpe/rtw023 CrossRefGoogle Scholar
  28. Kumar R, Shahabuddin G (2005) Effects of biomass extraction on vegetation structure, diversity and composition of forests in Sariska Tiger Reserve, India. Environ Conserv 32:248.  https://doi.org/10.1017/S0376892905002316 CrossRefGoogle Scholar
  29. Kuznetsova A, Brockhoff PB, Christensen RHB (2015) Package “lmerTest”. R package version, 2(0)Google Scholar
  30. Larimer AL, Bever JD, Clay K (2010) The interactive effects of plant microbial symbionts: a review and meta-analysis. Symbiosis 51:139–148.  https://doi.org/10.1007/s13199-010-0083-1 CrossRefGoogle Scholar
  31. Larimer AL, Clay K, Bever JD (2014) Synergism and context dependency of interactions between arbuscular mycorrhizal fungi and rhizobia with a prairie legume. Ecology 95:1045–1054.  https://doi.org/10.1890/13-0025.1 CrossRefPubMedGoogle Scholar
  32. Lin G, McCormack ML, Guo D (2015) Arbuscular mycorrhizal fungal effects on plant competition and community structure. J Ecol 103:1224–1232.  https://doi.org/10.1111/1365-2745.12429 CrossRefGoogle Scholar
  33. Mahowald N, Jickells TD, Baker AR, Artaxo P, Benitez-Nelson CR, Bergametti G, Bond TC, Chen Y, Cohen DD, Herut B, Kubilay N, Losno R, Luo C, Maenhaut W, McGee KA, Okin GS, Siefert RL, Tsukuda S (2008) Global distribution of atmospheric phosphorus sources, concentrations and deposition rates, and anthropogenic impacts. Global Biogeochem Cycles 22:GB4026.  https://doi.org/10.1029/2008gb003240 CrossRefGoogle Scholar
  34. Matson P, Lohse KA, Hall SJ (2002) The globalization of nitrogen deposition: consequences for terrestrial ecosystems. Ambio 31:113–119.  https://doi.org/10.1579/0044-7447-31.2.113 CrossRefPubMedGoogle Scholar
  35. Mayor JR, Wright SJ, Turner BL (2014) Species-specific responses of foliar nutrients to long-term nitrogen and phosphorus additions in a lowland tropical forest. J Ecol 102:36–44.  https://doi.org/10.1111/1365-2745.12190 CrossRefGoogle Scholar
  36. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142.  https://doi.org/10.1111/j.2041-210x.2012.00261.x CrossRefGoogle Scholar
  37. Novotny AM, Schade JD, Hobbie SE, Kay AD, Kyle M, Reich PB, Elser JJ (2007) Stoichiometric response of nitrogen-fixing and non-fixing dicots to manipulations of CO2, nitrogen, and diversity. Oecologia 151:687–696.  https://doi.org/10.1007/s00442-006-0599-5 CrossRefPubMedGoogle Scholar
  38. Ochoa-Hueso R, Pérez-Corona ME, Manrique E (2013) Impacts of simulated N deposition on plants and mycorrhizae from Spanish semiarid Mediterranean shrublands. Ecosystems 16:838–851.  https://doi.org/10.1007/s10021-013-9655-2 CrossRefGoogle Scholar
  39. Ostertag R (2010) Foliar nitrogen and phosphorus accumulation responses after fertilization: an example from nutrient-limited Hawaiian forests. Plant Soil 334:85–98.  https://doi.org/10.1007/s11104-010-0281-x CrossRefGoogle Scholar
  40. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775.  https://doi.org/10.1038/nrmicro1987 CrossRefPubMedGoogle Scholar
  41. Powers JS, Becklund KK, Gei MG, Iyengar SB, Meyer R, O’Connell CS, Schilling EM, Smith CM, Waring BG, Werden LK (2015) Nutrient addition effects on tropical dry forests: a mini-review from microbial to ecosystem scales. Front Earth Sci 3:34.  https://doi.org/10.3389/feart.2015.00034 CrossRefGoogle Scholar
  42. Reich PB (2014) The world-wide “fast-slow” plant economics spectrum: a traits manifesto. J Ecol 102:275–301.  https://doi.org/10.1111/1365-2745.12211 CrossRefGoogle Scholar
  43. Rillig MC (2004) Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecol Lett 7:740–754.  https://doi.org/10.1111/j.1461-0248.2004.00620.x CrossRefGoogle Scholar
  44. Sagar R, Singh JS (2004) Local plant species depletion in a tropical dry deciduous forest of northern India. Environ Conserv 31:55–62.  https://doi.org/10.1017/S0376892904001031 CrossRefGoogle Scholar
  45. Scheublin TR, Ridgway KP, Young JPW, van der Heijden MGA (2004) Nonlegumes, legumes, and root nodules harbor different arbuscular mycorrhizal fungal communities. Appl Environ Microbiol 70:6240–6246.  https://doi.org/10.1128/AEM.70.10.6240-6246.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Shantz AA, Lemoine NP, Burkepile DE (2016) Nutrient loading alters the performance of key nutrient exchange mutualisms. Ecol Lett 19:20–28.  https://doi.org/10.1111/ele.12538 CrossRefPubMedGoogle Scholar
  47. Sistla SA, Appling AP, Lewandowska AM, Taylor BN, Wolf AA (2015) Stoichiometric flexibility in response to fertilization along gradients of environmental and organismal nutrient richness. Oikos 124:949–959.  https://doi.org/10.1111/oik.02385 CrossRefGoogle Scholar
  48. Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–355.  https://doi.org/10.1111/j.1469-8137.2004.01159.x CrossRefGoogle Scholar
  49. Treseder KK, Allen MF (2000) Mycorrhizal fungi have a potential role in soil carbon storage under elevated CO2 and nitrogen deposition. New Phytol 147:189–200.  https://doi.org/10.1046/j.1469-8137.2000.00690.x CrossRefGoogle Scholar
  50. Varma V (2016) Direct and indirect effects of nutrient deposition on woody vegetation dynamics of tropical dry forests. Dissertation, National Centre for Biological Sciences, Tata Institute of Fundamental ResearchGoogle Scholar
  51. Varma V, Catherin AM, Sankaran M (2017) Effects of increased N and P availability on biomass allocation and root carbohydrate reserves differ between N-fixing and non-N-fixing savanna tree seedlings. bioRxiv.  https://doi.org/10.1101/224188 Google Scholar
  52. Vierheilig H, Coughlan AP, Wyss U, Piche Y (1998) Ink and vinegar, a simple staining technique for arbuscular mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007PubMedPubMedCentralGoogle Scholar
  53. Vierheilig H, Schweiger P, Brundrett M (2005) An overview of methods for the detection and observation of arbuscular mycorrhizal fungi in roots. Physiol Plant 125:393–404.  https://doi.org/10.1111/j.1399-3054.2005.00564.x Google Scholar
  54. Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NB, Sprent JI (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57:1–45.  https://doi.org/10.1023/A:101579842 CrossRefGoogle Scholar
  55. Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecol Appl 20:5–15.  https://doi.org/10.1890/08-0127.1 CrossRefPubMedGoogle Scholar
  56. Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall D (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633.  https://doi.org/10.1126/science.1094875 CrossRefPubMedGoogle Scholar
  57. Waters CN, Zalasiewicz J, Summerhayes C, Barnosky AD, Poirier C, Gauszka A, Cearreta A, Edgeworth M, Ellis EC, Ellis M, Jeandel C, Leinfelder R, McNeill JR, de Richter DB, Steffen W, Syvitski J, Vidas D, Wagreich M, Williams M, Zhisheng A, Grinevald J, Odada E, Oreskes N, Wolfe AP (2016) The Anthropocene is functionally and stratigraphically distinct from the Holocene. Science.  https://doi.org/10.1126/science.aad2622 PubMedCentralGoogle Scholar
  58. Witkowski ETF (1989) Effects of nutrients on the distribution of dry mass, nitrogen and phosphorus in seedlings of Protea repens (L.) L. (Proteaceae). New Phytol 112:481–487.  https://doi.org/10.1111/j.1469-8137.1989.tb00341.x CrossRefPubMedGoogle Scholar
  59. Wright IJ, Reich PB, Westoby M, Ackerly DD (2004) The worldwide leaf economics spectrum. Nature 428:821–827.  https://doi.org/10.1038/nature02403 CrossRefPubMedGoogle Scholar
  60. Xia J, Wan S (2008) Global response patterns of terrestrial plant species to nitrogen addition. New Phytol 179:428–439.  https://doi.org/10.1111/j.1469-8137.2008.02488.x CrossRefPubMedGoogle Scholar
  61. Yang Y, Luo Y, Lu M, Schädel C, Han W (2011) Terrestrial C:N stoichiometry in response to elevated CO2 and N addition: a synthesis of two meta-analyses. Plant Soil 343:393–400.  https://doi.org/10.1007/s11104-011-0736-8 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Ecology and Evolution GroupNational Centre for Biological Sciences (NCBS), Tata Institute of Fundamental Research (TIFR), GKVK CampusBangaloreIndia
  2. 2.Department of BiosciencesUniversity of ExeterExeterUK
  3. 3.Faculty of Biological Sciences, School of BiologyUniversity of LeedsLeedsUK

Personalised recommendations