Advertisement

Ecosystems

pp 1–15 | Cite as

Effects of Mineral Nitrogen Partitioning on Tree–Grass Coexistence in West African Savannas

  • Sarah KonaréEmail author
  • Simon Boudsocq
  • Jacques Gignoux
  • Jean-Christophe Lata
  • Xavier Raynaud
  • Sébastien Barot
Article
  • 50 Downloads

Abstract

Coexistence between trees and grasses in savannas is generally assumed to be due to a combination of partial niche separation for water acquisition and disturbances impacting the demography of trees and grasses. We propose a mechanism of coexistence solely based on the partitioning of the two dominant forms of mineral nitrogen (N), ammonium (NH4+) and nitrate (NO3). We built a mean-field model taking into account the capacity of grasses and trees to alter nitrification fluxes as well as their relative preferences for NH4+ versus NO3. Two models were studied and parameterized for the Lamto savanna (Côte d’Ivoire): In the first model, the nitrification only depends on the quantity of available NH4+, and in the second model the nitrification rate is also controlled by tree and grass biomass. Consistent with coexistence theories, our results show that taking these two forms of mineral N into account can allow coexistence when trees and grasses have contrasting preferences for NH4+ and NO3. Moreover, coexistence is more likely to occur for intermediate nitrification rates. Assuming that grasses are able to inhibit nitrification while trees can stimulate it, as observed in the Lamto savanna, the most likely case of coexistence would be when grasses prefer NH4+ and trees NO3. We propose that mineral N partitioning is a stabilizing coexistence mechanism that occurs in interaction with already described mechanisms based on disturbances by fire and herbivores. This mechanism is likely relevant in many N-limited African savannas with vegetation composition similar to the one at the Lamto site, but should be thoroughly tested through empirical studies and new models taking into account spatiotemporal heterogeneity in nitrification rates.

Keywords

ammonium nitrate nitrification control NH4+ versus NO3 preference resource partitioning savanna tree–grass coexistence 

Notes

Acknowledgements

We thank the Ministry of Higher Education and Scientific Research of Côte d’Ivoire for the PhD grant of SK. This paper is dedicated to the memory of A. Konaré (1965-2017), director general of scientific research and innovation of Côte d’Ivoire.

Supplementary material

10021_2019_365_MOESM1_ESM.pdf (1.5 mb)
Supplementary material 1 (PDF 1509 kb)
10021_2019_365_MOESM2_ESM.jpg (401 kb)
Supplementary material 2 (JPEG 400 kb)
10021_2019_365_MOESM3_ESM.jpg (238 kb)
Supplementary material 3 (JPEG 237 kb)
10021_2019_365_MOESM4_ESM.jpg (297 kb)
Supplementary material 4 (JPEG 296 kb)
10021_2019_365_MOESM5_ESM.jpg (86 kb)
Supplementary material 5 (JPEG 86 kb)
10021_2019_365_MOESM6_ESM.jpg (169 kb)
Supplementary material 6 (JPEG 168 kb)
10021_2019_365_MOESM7_ESM.jpg (169 kb)
Supplementary material 7 (JPEG 168 kb)

References

  1. Abbadie L. 2006. Nitrogen inputs to and outputs from the soil-plant system. In: Abbadie L, Gignoux J, Le Roux X, Lepage M, Eds. Lamto: structure, functioning, and dynamics of a savanna ecosystem. New York: Springer. p 255–75.CrossRefGoogle Scholar
  2. Abbadie L, Gignoux J, Le Roux X, Lepage M, Eds. 2006. Lamto: structure, functioning, and dynamics of a savanna ecosystem. New York: Springer.Google Scholar
  3. Accatino F, De Michele C, Vezzoli R, Donzelli D, Scholes RJ. 2010. Tree–grass co-existence in savanna: Interactions of rain and fire. J Theor Biol 267:235–42.CrossRefGoogle Scholar
  4. Aerts R. 1996. Nutrient resorption from senescing leaves of perennials: are there general patterns? J Ecol 84:597–608.CrossRefGoogle Scholar
  5. Armstrong RA, McGehee R. 1980. Competitive exclusion. Am Nat 115:151–70.CrossRefGoogle Scholar
  6. Ashton IW, Miller AE, Bowman WD, Suding KN. 2010. Niche complementarity due to plasticity in resource use: plant partitioning of chemical N forms. Ecology 91:3252–60.CrossRefGoogle Scholar
  7. Barot S, Gignoux J, Menaut JC. 1999. Demography of a savanna palm tree: predictions from comprehensive spatial patterns analyses. Ecology 80:1987–2005.CrossRefGoogle Scholar
  8. Barot S, Gignoux J. 2004. Mechanisms promoting plant coexistence: can all the proposed processes be reconciled? Oikos 106:185–92.CrossRefGoogle Scholar
  9. Baudena M, Rietkerk M. 2013. Complexity and coexistence in a simple spatial model for arid savanna ecosystems. Theor Ecol 6:131–41.CrossRefGoogle Scholar
  10. Bernhard-Reversat F, Poupon H. 1980. Nitrogen cycling in a soil-tree system in a sahelian savanna. Example of Acacia senegal. In: Rosswall, T. editor. Nitrogen cycling in West African ecosystems. Royal Swedish Academy of Sciences. pp. 363–369.Google Scholar
  11. Bond WJ, Midgley GF. 2000. A proposed CO2-controlled mechanism of woody plant invasion in grasslands and savannas. Glob Change Biol 6:865–9.CrossRefGoogle Scholar
  12. Boudsocq S, Lata JC, Mathieu J, Abbadie L, Barot S. 2009. Modelling approach to analyse the effects of nitrification inhibition on primary production. Funct Ecol 23:220–30.CrossRefGoogle Scholar
  13. Boudsocq S, Niboyet A, Lata JC, Raynaud X, Loeuille N, Mathieu J, Blouin M, Abbadie L, Barot S. 2012. Plant preference for ammonium versus nitrate: a neglected determinant of ecosystem functioning? Am Nat 180:60–9.CrossRefGoogle Scholar
  14. Britto DT, Kronzucker HJ. 2002. NH4 + toxicity in higher plants: a critical review. J Plant Physiol 159:567–84.CrossRefGoogle Scholar
  15. Britto DT, Kronzucker HJ. 2013. Ecological significance and complexity of N-source preference in plants. Ann Bot 112:957–63.CrossRefGoogle Scholar
  16. Chesson P. 2000. Mechanisms of maintenance of species diversity. Ann Rev Ecol Evol Syst 31:343–66.CrossRefGoogle Scholar
  17. D’Antonio CM, Vitousek PM. 1992. Biological invasions by exotic grasses, the grass/fire cycle, and global change. Ann Rev Ecol Syst 23:63–87.CrossRefGoogle Scholar
  18. Donzelli D, De Michele C, Scholes RJ. 2013. Competition between trees and grasses for both soil water and mineral nitrogen in dry savannas. J Theor Biol 332:181–90.CrossRefGoogle Scholar
  19. Ellner SP, Snyder RE, Adler PB, Hooker G. 2019. An expanded modern coexistence theory for empirical applications. Ecol Lett 22:3–18.CrossRefGoogle Scholar
  20. Falkengren-Grerup U, Lakkenborg-Kristensen H. 1994. Importance of ammonium and nitrate to the performance of herb-layer species from deciduous forests in southern sweden. Environ Exp Bot 34:31–8.CrossRefGoogle Scholar
  21. Fang YY, Babourina O, Rengel Z, Yang XE, Pu PM. 2007. Ammonium and nitrate uptake by the floating plant Landoltia punctata. Ann Bot 99:365–70.CrossRefGoogle Scholar
  22. February EC, Higgins SI, Bond WJ, Swemmer L. 2013. Influence of competition and rainfall manipulation on the growth responses of savanna trees and grasses. Ecology 94:1155–64.CrossRefGoogle Scholar
  23. Forde BG, Clarkson DT. 1999. Nitrate and ammonium nutrition of plants: physiological and molecular perspectives. Adv Bot Res 30:1–90.CrossRefGoogle Scholar
  24. Gignoux J, Lahoreau G, Julliard R, Barot S. 2009. Establishment and early persistence of tree seedlings in an annually burned savanna. J Ecol 97:484–95.CrossRefGoogle Scholar
  25. Hardin G. 1960. The competitive exclusion principle. Science 131:1292–7.CrossRefGoogle Scholar
  26. Harrison KA, Bol R, Bardgett RD. 2007. Preferences for different nitrogen forms by coexisting plant species and soil microbes. Ecology 88:989–99.CrossRefGoogle Scholar
  27. Higgins SI, Bond WJ, Trollope WSW. 2000. Fire, resprouting and variability: a recipe for grass-tree coexistence in savanna. J Ecol 88:213–29.CrossRefGoogle Scholar
  28. Higgins SI, Scheiter S, Sankaran M. 2010. The stability of African savannas: insights from the indirect estimation of the parameters of a dynamic model. Ecology 91:1682–92.CrossRefGoogle Scholar
  29. Hochberg ME, Menaut JC, Gignoux J. 1994. The influences of tree biology and fire in the spatial structure of the West African savannah. J Ecol 82:217–26.CrossRefGoogle Scholar
  30. Holdo RM, Nippert JB, Mack MC. 2018. Rooting depth varies differentially in trees and grasses as a function of mean annual rainfall in an African savanna. Oecologia 186:269–80.CrossRefGoogle Scholar
  31. Holt RD. 2008. Perspectives on resource pulses. Ecology 89:671–81.CrossRefGoogle Scholar
  32. Houlton BZ, Sigman DM, Schuur EAG, Hedin LO. 2007. A climate-driven switch in plant nitrogen acquisition within tropical forest communities. Proc Natl Acad Sci 104:8902–6.CrossRefGoogle Scholar
  33. Huangfu C, Li H, Chen X, Liu H, Wang H, Yang D. 2016. Response of an invasive plant, Flaveria bidentis, to nitrogen addition: a test of form-preference uptake. Biol Invasions 18:3365–80.CrossRefGoogle Scholar
  34. Jeltsch F, Weber GE, Grimm V. 2000. Ecological buffering mechanisms in savannas: a unifying theory of long-term tree–grass coexistence. Plant Ecol 161:161–71.CrossRefGoogle Scholar
  35. Jumpponen A, Högberg P, Huss-Danell K, Mulder CPH. 2002. Interspecific and spatial differences in nitrogen uptake in monocultures and two-species mixtures in north European grasslands. Funct Ecol 16:454–61.CrossRefGoogle Scholar
  36. Kahmen A, Renker C, Unsicker SB, Buchmann N. 2006. Niche complementarity for nitrogen: an explanation for the biodiversity and ecosystem functioning relationship? Ecology 87:1244–55.CrossRefGoogle Scholar
  37. Konnerup D, Brix H. 2010. Nitrogen nutrition of Canna indica: Effects of ammonium versus nitrate on growth, biomass allocation, photosynthesis, nitrate reductase activity and N uptake rates. Aquat Bot 92:142–8.CrossRefGoogle Scholar
  38. Lata JC. 1999. Interactions between microbial processes, nutrient cycle and grass cover functioning: Study of soil nitrification under the Gramineae Hyparrhenia diplandra in a wet tropical savanna of Côte d’Ivoire. France: University of Paris VI. PhD ThesisGoogle Scholar
  39. Lata JC, Guillaume K, Degrange V, Abbadie L, Lensi R. 2000. Relationships between root density of the African grass Hyparrhenia diplandra and nitrification at the decimetric scale: an inhibition-stimulation balance hypothesis. Proc R Soc B 267:595–600.CrossRefGoogle Scholar
  40. Lata JC, Degrange V, Raynaud X, Maron PA, Lensi R, Abbadie L. 2004. Grass populations control nitrification in savanna soils. Funct Ecol 18:605–11.CrossRefGoogle Scholar
  41. Le Roux X, Abbadie L, Fritz H, Leriche H. 2006. Modification of the savanna functioning by herbivores. In: Abbadie L, Gignoux J, Le Roux X, Lepage M, Eds. Lamto: Structure, functioning, and dynamics of a savanna ecosystem. New York: Springer. p 185–98.CrossRefGoogle Scholar
  42. Ludwig F, de Kroon H, Prins HHT, Berendse F. 2001. Effects of nutrients and shade on tree–grass interactions in an East African savanna. J Veg Sci 12:579–88.CrossRefGoogle Scholar
  43. Maire V, Gross N, Da Silveira Pontes L, Picon-Cochard C, Soussana JF. 2009. Trade-off between root nitrogen acquisition and shoot nitrogen utilization across 13 co-occurring pasture grass species. Funct Ecol 23:668–79.CrossRefGoogle Scholar
  44. Marschner H. 2008. Mineral nutrition of higher plants. 2nd edn. London: Acad Press.Google Scholar
  45. McKane RB, Johnson LC, Shaver GR, Nadelhoffer KJ, Rastetter EB, Fry B, Giblin AE, Kielland K, Kwiatkowski BL, Laundre JA, Murray G. 2002. Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415:68–71.CrossRefGoogle Scholar
  46. Menaut JC, César J. 1979. Structure and primary productivity of Lamto savannas, Ivory Coast. Ecology 60:1197–210.CrossRefGoogle Scholar
  47. Miller AE, Bowman WD. 2002. Variations in nitrogen-15 natural abundance and nitrogen uptake traits among co-occuring alpine species: do species partition by nitrogen form? Oecologia 130:609–16.CrossRefGoogle Scholar
  48. Mordelet P, Menaut JC, Mariotti A. 1997. Tree and grass rooting patterns in an African humid savanna. J Veg Sci 8:65–70.CrossRefGoogle Scholar
  49. Nacry P, Bouguyon E, Gojon A. 2013. Nitrogen acquisition by roots: physiological and developmental mechanisms ensuring plant adaptation to a fluctuating resource. Plant Soil 370:1–29.CrossRefGoogle Scholar
  50. Perry LG, Neuhauser C, Galatowitsch SM. 2003. Founder control and coexistence in a simple model of asymmetric competition for light. J Theor Biol 222:425–36.CrossRefGoogle Scholar
  51. R Development Core Team. 2014. R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria.Google Scholar
  52. Rastetter EB, Agren GI. 2002. Changes in individual allometry can lead to species coexistence without niche separation. Ecosystems 5:789–801.CrossRefGoogle Scholar
  53. Rossiter-Rachor NA, Setterfield SA, Douglas MM, Hutley LB, Cook GD, Schmidt S. 2009. Invasive Andropogon gayanus (gamba grass) is an ecosystem transformer of nitrogen relations in Australian savanna. Ecol Appl 19:1546–60.CrossRefGoogle Scholar
  54. Rossiter-Rachor NA, Setterfield SA, Hutley LB, McMaster D, Schmidt S, Douglas MM. 2017. Invasive Andropogon gayanus (Gamba grass) alters decomposition and nitrogen fluxes in an Australian tropical savanna. Sci Rep 7:11705.CrossRefGoogle Scholar
  55. Salsac L, Chaillou S, Morot-Gaudry JF, Lesaint C, Jolivet E. 1987. Nitrate and ammonium nutrition in plants. Plant Physiol Biochem 25:805–12.Google Scholar
  56. Sankaran M, Ratnam J, Hanan NP. 2004. Tree–grass coexistence in savannas revisited-insights from an examination of assumptions and mechanisms invoked in existing models. Ecol Lett 7:480–90.CrossRefGoogle Scholar
  57. Sankaran M, Hanan NP, Scholes RJ, Ratnam J, Augustine DJ, Cade BS, Gignoux J, Higgins SI, Le Roux X, Ludwig F, Ardo J, Banyikwa F, Bronn A, Bucini G, Caylor KK, Coughenour MB, Diouf A, Ekaya W, Feral CJ, February EC, Frost PGH, Hiernaux P, Hrabar H, Metzger KL, Prins HHT, Ringrose S, Sea W, Tews J, Worden J, Zambatis N. 2005. Determinants of woody cover in African savannas. Nature 438:846–9.CrossRefGoogle Scholar
  58. Sankaran M, Ratnam J, Hanan N. 2008. Woody cover in African savannas: the role of resources, fire and herbivory. Glob Ecol Biogeogr 17:236–45.CrossRefGoogle Scholar
  59. Schenk HJ, Jackson RB. 2002. Rooting depths, lateral root spreads and below-ground/above-ground allometries of plants in water-limited ecosystems. J Ecol 90:480–94.CrossRefGoogle Scholar
  60. Scholes RJ, Archer SR. 1997. Tree–grass interactions in savannas. Ann Rev Ecol Syst 28:517–44.CrossRefGoogle Scholar
  61. Silvertown J. 2004. Plant coexistence and the niche. Trends Ecol Evol 19:605–11.CrossRefGoogle Scholar
  62. Soetaert K, Petzoldt T, Woodrow S. 2010. Solving differential equations in R: Package deSolve. J Stat Softw 33:1–25.Google Scholar
  63. Srikanthasamy T, Leloup J, N’Dri AB, Barot S, Gervaix J, Koné AW, Koffi KF, Le Roux X, Raynaud X, Lata JC. 2018. Contrasting effects of grasses and trees on microbial N-cycling in an African humid savanna. Soil Biol Biochem 117:153–63.CrossRefGoogle Scholar
  64. Staver AC, Archibald S, Levin SA. 2011a. The global extent and determinants of savanna and forest as alternative biome states. Science 334:230–2.CrossRefGoogle Scholar
  65. Staver AC, Archibald S, Levin S. 2011b. Tree cover in sub-Saharan Africa: rainfall and fire constrain forest and savanna as alternative stable states. Ecology 92:1063–72.CrossRefGoogle Scholar
  66. Subbarao GV, Rondon M, Ito O, Ishikawa T, Rao IM, Nakahara K, Lascano C, Berry WL. 2007. Biological nitrification inhibition (BNI)—is it a widespread phenomenon? Plant Soil 294:5–18.CrossRefGoogle Scholar
  67. Subbarao GV, Nakahara K, Hurtado MP, Ono H, Moreta DE, Salcedo AF, Yoshihashi AT, Ishikawa T, Ishitani M, Ohnishi-Kameyama M, Yoshida M, Rondon M, Rao IM, Lascano CE, Berry WL, Ito O. 2009. Evidence for biological nitrification inhibition in Brachiaria pastures. Proc Natl Acad Sci 106:17302–7.CrossRefGoogle Scholar
  68. Subbarao GV, Yoshihashi T, Worthington M, Nakahara K, Ando Y, Sahrawat KL, Rao IM, Lata JC, Kishii M, Braun HJ. 2015. Suppression of soil nitrification by plants. Plant Science 233:155–64.CrossRefGoogle Scholar
  69. Tavernier V. 2003. Interactions entre structures racinaires et cycle de l’azote en savane africaine. PhD Thesis, INA-P-G Paris, France.Google Scholar
  70. Van Heerwaarden LM, Toet S, Aerts R. 2003. Current measures of nutrient resorption efficiency lead to a substantial underestimation of real resorption efficiency: facts and solutions. Oikos 101:664–9.CrossRefGoogle Scholar
  71. Van Langevelde F, Van De Vijver CADM, Kumar L, Van De Koppel J, De Ridder N, Van Andel J, Skidmore AK, Hearne JW, Stroosnijder L, Bond WJ, Prins HHT, Rietkerk M. 2003. Effects of fire and herbivory on the stability of savanna ecosystems. Ecology 84:337–50.CrossRefGoogle Scholar
  72. Villecourt P, Roose E. 1978. Charge en azote et en éléments minéraux majeurs des eaux de pluie, de pluviolessivage et de drainage dans la savane de Lamto (Côte d’Ivoire). Revue d’Ecologie et de Biologie du Sol 15:1–20.Google Scholar
  73. Walker BH, Noy-Meir I. 1982. Aspects of stability and resilience of savanna ecosystems. In: Huntley BJ, Walker BH, Eds. Ecology of tropical savannas. Berlin: Springer. p 556–90.CrossRefGoogle Scholar
  74. Walter H. 1971. Ecology of tropical and subtropical vegetation. Edinburgh: Oliver & Boyd.Google Scholar
  75. Ward D. 2005. Do we understand the causes of bush encroachment in African savannas? Afr J Range Forage Sci 22:101–5.CrossRefGoogle Scholar
  76. Ward D, Wiegand K, Getzin S. 2013. Walter’s two-layer hypothesis revisited: back to the roots!. Oecologia 172:617–30.CrossRefGoogle Scholar
  77. Wolfram Research. 2017. Mathematica, Version 10.0. Wolfram Research Champaign IL.Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Sorbonne Université, IRD, CNRS, INRA, UPEC, Univ Paris Diderot, Institute of Ecology and Environmental Sciences, iEES ParisParisFrance
  2. 2.Eco&Sols, INRA, CIRAD, IRD, Montpellier SupaAgroUniv MontpellierMontpellierFrance
  3. 3.Department of Geoecology and Geochemistry, Institute of Natural ResourcesTomsk Polytechnic UniversityTomskRussia

Personalised recommendations