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.
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References
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
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
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
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
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
Bates DM (2010) lme4: mixed-effects modeling with R. Springer, New York
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, Vienna
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, Vienna
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
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
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
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
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
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
Filippelli GM (2002) The global phosphorus cycle. Rev Mineral Geochem 48:391–425. https://doi.org/10.2138/rmg.2002.48.10
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
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
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
Güsewell S, Koerselman W, Verhoeven JT (2003) Biomass N:P ratios as indicators of nutrient limitation for plant populations in wetlands. Ecol Appl 13:372–384
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
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
Johnson NC (1993) Can fertilization of soil select less mutualistic mycorrhizae? Ecol Appl 3:749–757. https://doi.org/10.2307/1942106
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
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
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
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
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
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
Kuznetsova A, Brockhoff PB, Christensen RHB (2015) Package “lmerTest”. R package version, 2(0)
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
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
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
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
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
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
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
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
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
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
Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775. https://doi.org/10.1038/nrmicro1987
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
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
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
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
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
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
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
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
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
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 Research
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
Vierheilig H, Coughlan AP, Wyss U, Piche Y (1998) Ink and vinegar, a simple staining technique for arbuscular mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007
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
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
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
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
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
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
Wright IJ, Reich PB, Westoby M, Ackerly DD (2004) The worldwide leaf economics spectrum. Nature 428:821–827. https://doi.org/10.1038/nature02403
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
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
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.
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Communicated by Christina Birnbaum.
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Tiruvaimozhi, Y.V., Varma, V. & Sankaran, M. Nitrogen fixation ability explains leaf chemistry and arbuscular mycorrhizal responses to fertilization. Plant Ecol 219, 391–401 (2018). https://doi.org/10.1007/s11258-018-0803-9
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DOI: https://doi.org/10.1007/s11258-018-0803-9