Oecologia

, Volume 156, Issue 3, pp 625–636 | Cite as

Nitrogen preferences and plant-soil feedbacks as influenced by neighbors in the alpine tundra

  • I. W. Ashton
  • A. E. Miller
  • W. D. Bowman
  • K. N. Suding
Community Ecology - Original Paper

Abstract

Plant resource partitioning of chemical forms of nitrogen (N) may be an important factor promoting species coexistence in N-limited ecosystems. Since the microbial community regulates N-form transformations, plant partitioning of N may be related to plant–soil feedbacks. We conducted a 15N tracer addition experiment to study the ability of two alpine plant species, Acomastylis rossii and Deschampsia caespitosa, to partition organic and inorganic forms of N. The species are codominant and associated with strong plant–soil feedbacks that affect N cycling. We manipulated interspecific interactions by removing Acomastylis or Deschampsia from areas where the species were codominant to test if N uptake patterns varied in the presence of the other species. We found that Deschampsia acquired organic and inorganic N more rapidly than Acomastylis, regardless of neighbor treatment. Plant N uptake—specifically ammonium uptake—increased with plant density and the presence of an interspecific neighbor. Interestingly, this change in N uptake was not in the expected direction to reduce niche overlap and instead suggested facilitation of ammonium use. To test if N acquisition patterns were consistent with plant–soil feedbacks, we also compared microbial rhizosphere extracellular enzyme activity in patches dominated by one or the other species and in areas where they grew together. The presence of both species was generally associated with increased rhizosphere extracellular enzyme activity (five of ten enzymes) and a trend towards increased foliar N concentrations. Taken together, these results suggest that feedbacks through the microbial community, either in response to increased plant density or specific plant neighbors, could facilitate coexistence. However, coexistence is promoted via enhanced resource uptake rather than reduced niche overlap. The importance of resource partitioning to reduce the intensity of competitive interactions might vary across systems, particularly as a function of plant-soil feedbacks.

Keywords

Coexistence Foliar nitrogen concentrations Interspecific interactions Neighbor effect Nitrogen uptake patterns Plant resource partitioning Plant–soil feedback 

References

  1. Ackerly DD (2003) Community assembly, niche conservatism, and adaptive evolution in changing environments. Int J Plant Sci 164:S165–S184CrossRefGoogle Scholar
  2. Aerts R (1999) Interspecific competition in natural plant communities: mechanisms, trade-offs and plant-soil feedbacks. J Exp Bot 50:29–37CrossRefGoogle Scholar
  3. Allison SD, Nielsen C, Hughes RF (2006) Elevated enzyme activities in soils under the invasive nitrogen-fixing tree Falcataria moluccana. Soil Biol Biochem 38:1537–1544CrossRefGoogle Scholar
  4. Anderson RC, Schelfhout S (1980) Phenological patterns among tallgrass prairie plants and their implications for pollinator competition. Am Mid Nat 104:253–263CrossRefGoogle Scholar
  5. Bardgett RD, Smith RS, Shiel RS, Peacock S, Simkin JM., Quirk H, Hobbs PJ (2006) Parasitic plants indirectly regulate below-ground properties in grassland ecosystems. Nature 439:969–972PubMedCrossRefGoogle Scholar
  6. Bertness MD, Callaway R (1994) Positive interactions in communities. Trends Ecol Evol 9:191–193CrossRefGoogle Scholar
  7. Bilbrough CJ, Welker JM, Bowman WD (2000) Early spring nitrogen uptake by snow-covered plants: a comparison of arctic and alpine plant function under the snowpack. Arct Alp Res 32:404–411CrossRefGoogle Scholar
  8. Bowman WD, Steltzer H, Rosenstiel TN, Cleveland CC, Meier CL (2004) Litter effects of two co-occurring alpine species on plant growth, microbial activity and immobilization of nitrogen. Oikos 104:336–344CrossRefGoogle Scholar
  9. Brooker RW, Callaghan TV (1998) The balance between positive and negative plant interactions and its relationship to environmental gradients: a model. Oikos 81:196–207CrossRefGoogle Scholar
  10. Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil-nitrogen—a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842CrossRefGoogle Scholar
  11. Brooks PD, Stark JM, McInteer BB, Preston T (1989) Diffusion method to prepare soil extracts for automated –15 analysis. Soil Sci Soc Am J 53:1707–1711CrossRefGoogle Scholar
  12. Brooks PD, Williams MW, Schmidt SK (1996) Microbial activity under alpine snowpacks, Niwot Ridge, Colorado. Biogeochemistry 32:93–113CrossRefGoogle Scholar
  13. Cabrera ML, Beare MH (1993) Alkaline persulfate oxidation for determining total nitrogen in microbial biomass extracts. Soil Sci Soc Am J 57:1007–1012CrossRefGoogle Scholar
  14. Callaway RM, Brooker RW, Choler P, Kikvidze Z, Lortie CJ, Michalet R, Paolini L, Pugnaire FI, Newingham B, Aschehoug ET, Armas C, Kikodze D, Cook BJ (2002) Positive interactions among alpine plants increase with stress. Nature 417:844–848PubMedCrossRefGoogle Scholar
  15. Castells E, Penuelas J (2003) Is there a feedback between N availability in siliceous and calcareous soils and Cistus albidus leaf chemical composition? Oecologia 136:183–192PubMedCrossRefGoogle Scholar
  16. Chapin FS (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–260CrossRefGoogle Scholar
  17. Chapin FS, Moilanen L, Kielland K (1993) Preferential use of organic nitrogen for growth by a nonmycorrhizal arctic sedge. Nature 361:150–153CrossRefGoogle Scholar
  18. Connell JH (1980) Diversity and the coevolution of competitors, or the Ghost of Competition Past. Oikos 35:131–138CrossRefGoogle Scholar
  19. Craine JM (2006) Competition for nutrients and optimal root allocation. Plant Soil 285:171–185CrossRefGoogle Scholar
  20. Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35–47CrossRefGoogle Scholar
  21. de Kroon H, Mommer L (2006) Root foraging theory put to the test. Trends Ecol Evol 21:113–116PubMedCrossRefGoogle Scholar
  22. Diaz S, Symstad AJ, Chapin FS, Wardle DA, Huenneke LF (2003) Functional diversity revealed by removal experiments. Trends Ecol Evol 18:140–146CrossRefGoogle Scholar
  23. Ehrenfeld JG, Ravit B, Elgersma K (2005) Feedback in the plant-soil system. Annu Rev Environ Resour 30:75–115CrossRefGoogle Scholar
  24. Fargione J, Tilman D (2005) Niche differences in phenology and rooting depth promote coexistence with a dominant C-4 bunchgrass. Oecologia 143:598–606PubMedCrossRefGoogle Scholar
  25. Fargione J, Tilman D, Dybzinski R, Lambers JHR, Clark C, Harpole WS, Knops JMH, Reich PB, Loreau M (2007) From selection to complementarity: shifts in the causes of biodiversity-productivity relationships in a long-term biodiversity experiment. Proc R Soc Lond B Biol Sci 274:871–876CrossRefGoogle Scholar
  26. Gersani M, Brown JS, O’Brien EE, Maina GM, Abramsky Z (2001) Tragedy of the commons as a result of root competition. J Ecol 89:660–669CrossRefGoogle Scholar
  27. Gibson DJ, Connolly J, Hartnett DC, Weidenhamer JD (1999) Designs for greenhouse studies of interactions between plants. J Ecol 87:1–16CrossRefGoogle Scholar
  28. Gilbert PM, Lipschultz F, McCarthy JJ, Altabet MA (1982) Isotope-dilution models of uptake and remineralization of ammonium by marine plankton. Limnol Oceanogr 27:639–650Google Scholar
  29. Goldberg D, Scheiner SM (2001) ANOVA and ANCOVA: field competition experiments. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Oxford University Press, Oxford, pp 77–98Google Scholar
  30. Grandy AS, Neff JC, Weintraub MN (2007) Carbon structure and enzyme activities in alpine and forest ecosystems. Soil Biol Biochem 39:2701–2711CrossRefGoogle Scholar
  31. Hairston NG (1980a) Evolution under interspecific competition - field experiments on terrestrial salamanders. Evolution 34:409–420CrossRefGoogle Scholar
  32. Hairston NG (1980b) The experimental test of an analysis of field distributions—competition in terrestrial salamanders. Ecology 61:817–826CrossRefGoogle Scholar
  33. Hauck RD, Bremner JM (1976) Use of tracers for soil and fertilizer nitrogen research. Adv Agron 28:219–266CrossRefGoogle Scholar
  34. Hobbie SE (1992) Effects of plant-species on nutrient cycling. Trends Ecol Evol 7:336–339CrossRefGoogle Scholar
  35. Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter AH (2000) Competition between roots and soil micro-organisms for nutrients from nitrogen-rich patches of varying complexity. J Ecol 88:150–164CrossRefGoogle Scholar
  36. Hutchinson GE (1959) Homage to Santa-Rosalia or why are there so many kinds of animals. Am Nat 93:145–159CrossRefGoogle Scholar
  37. Jackson LE, Schimel JP, Firestone MK (1989) Short-term partitioning of ammonium and nitrate between plants and microbes in an annual grassland. Soil Biol Biochem 21:409–415CrossRefGoogle Scholar
  38. Jedlicka JA, Greenberg R, Perfecto I, Philpottt SM, Dietsch TV (2006) Seasonal shift in the foraging niche of a tropical avian resident: resource competition at work? J Trop Ecol 22:385–395CrossRefGoogle Scholar
  39. Jenkinson DS, Brookes PC, Powlson DS (2004) Measuring soil microbial biomass. Soil Biol Biochem 36:5–7CrossRefGoogle Scholar
  40. Kahmen A, Renker C, Unsicker SB, Buchmann N (2006) Niche complementarity for nitrogen: an explanation for the biodiversity and ecosystem functioning relationship? Ecology 87:1244–1255PubMedCrossRefGoogle Scholar
  41. Kaye JP, Hart SC (1997) Competition for nitrogen between plants and soil microorganisms. Trends Ecol Evol 12:139–143CrossRefGoogle Scholar
  42. Kourtev PS, Ehrenfeld JG, Haggblom M (2002) Exotic plant species alter the microbial community structure and function in the soil. Ecology 83:3152–3166Google Scholar
  43. Levins R (1968) Evolution in changing environments. Princeton University Press, PrincetonGoogle Scholar
  44. Lipson DA, Schmidt SK, Monson RK (1999) Links between microbial population dynamics and nitrogen availability in an alpine ecosystem. Ecology 80:1623–1631CrossRefGoogle Scholar
  45. MacArthur RH (1958) Population ecology of some warblers of northeastern caoniferous forests. Ecology 39:599–619Google Scholar
  46. MacArthur R, Levins R (1967) Limiting similarity convergence and divergence of coexisting species. Am Nat 101:377–385CrossRefGoogle Scholar
  47. McKane RB, Grigal DF, Russelle MP (1990) Spatiotemporal differences in 15N uptake and the organization of an old-field plant community. Ecology 71:1126–1132Google Scholar
  48. 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 415:68–71PubMedCrossRefGoogle Scholar
  49. Miller AE, Bowman WD (2002) Variation in nitrogen-15 natural abundance and nitrogen uptake traits among co-occurring alpine species: do species partition by nitrogen form? Oecologia 130:609–616CrossRefGoogle Scholar
  50. Miller AE, Bowman WD (2003) Alpine plants show species-level differences in the uptake of organic and inorganic nitrogen. Plant Soil 250:283–292CrossRefGoogle Scholar
  51. Miller AE, Bowman WD, Suding KN (2007) Plant uptake of inorganic and organic nitrogen: neighbor identity matters. Ecology 88:1832–1840PubMedCrossRefGoogle Scholar
  52. Monson RK, Mullen R, Bowman WD (2001) Plant nutrient relations In: Bowman WD Seastedt T (eds) Structure and function of an alpine ecosystem. Oxford University Press, Niwot Ridge, pp 198–221Google Scholar
  53. Mulvaney RL, Fohringer CL, Bojan VJ, Michlik MM, Herzog LF (1990) A commercial system for automated nitrogen isotope-ratio analysis by the Rittenberg technique. Rev Sci Instrum 61:897–903CrossRefGoogle Scholar
  54. Nadelhoffer K, Shaver G, Fry B, Giblin A, Johnson L, McKane R (1996) –15 natural abundances and N use by tundra plants. Oecologia 107:386–394CrossRefGoogle Scholar
  55. Nordin A, Schmidt IK, Shaver GR (2004) Nitrogen uptake by arctic soil microbes and plants in relation to soil nitrogen supply. Ecology 85:955–962CrossRefGoogle Scholar
  56. Pacala S, Roughgarden J (1982) Resource partitioning and interspecific competition in two 2-species insular Anolis lizard communities. Science 217:444–446PubMedCrossRefGoogle Scholar
  57. Parrish JAD, Bazzaz FA (1976) Underground niche separation in successional plants. Ecology 57:1281–1288CrossRefGoogle Scholar
  58. Parrish JAD, Bazzaz FA (1979) Difference in pollination niche relationships in early and late successional plant-communities. Ecology 60:597–610CrossRefGoogle Scholar
  59. Raab TK, Lipson DA, Monson RK (1996) Non-mycorrhizal uptake of amino acids by roots of the alpine sedge Kobresia myosuroides: implications for the alpine nitrogen cycle. Oecologia 108:488–494CrossRefGoogle Scholar
  60. Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems - a journey towards relevance? New Phytol 157:475–492CrossRefGoogle Scholar
  61. Reynolds HL, Packer A, Bever JD, Clay K (2003) Grassroots ecology: plant-microbe-soil interactions as drivers of plant community structure and dynamics. Ecology 84:2281–2291CrossRefGoogle Scholar
  62. Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315CrossRefGoogle Scholar
  63. Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602CrossRefGoogle Scholar
  64. Schoener TW (1974) Resource partitioning in ecological communities. Science 185:27–39PubMedCrossRefGoogle Scholar
  65. Schoener TW (1989) Food webs from the small to the large. Ecology 70:1559–1589CrossRefGoogle Scholar
  66. Silvertown J (2004) Plant coexistence and the niche. Trends Ecol Evol 19:605–611CrossRefGoogle Scholar
  67. Sinsabaugh RL (1994) Enzymatic analysis of microbial pattern and process. Biol Fert Soils 17:69–74CrossRefGoogle Scholar
  68. Sinsabaugh RL, Saiya-Corka K, Long T, Osgood MP, Neher DA, Zak DR, Norby RJ (2003) Soil microbial activity in a Liquidambar plantation unresponsive to CO2-driven increases in primary production. Appl Soil Ecol 24:263–271CrossRefGoogle Scholar
  69. Somers E, Vanderleyden J, Srinivasan M (2004) Rhizosphere bacterial signalling: A love parade beneath our feet. Crit Rev Microbiol 30:205–240PubMedCrossRefGoogle Scholar
  70. Steltzer H, Bowman WD (1998) Differential influence of plant species on soil nitrogen transformations within moist meadow alpine tundra. Ecosystems 1:464–474CrossRefGoogle Scholar
  71. Suding KN, Larson JR, Thorsos E, Steltzer H, Bowman WD (2004) Species effects on resource supply rates: do they influence competitive interactions? Plant Ecol 175:47–58CrossRefGoogle Scholar
  72. Suding KN, Miller AE, Bechtold H, Bowman WD (2006) The consequence of species loss on ecosystem nitrogen cycling depends on community compensation. Oecologia 149:141–149PubMedCrossRefGoogle Scholar
  73. Theodose TA, Jaeger CH, Bowman WD, Schardt JC (1996) Uptake and allocation of –15 in alpine plants: Implications for the importance of competitive ability in predicting community structure in a stressful environment. Oikos 75:59–66CrossRefGoogle Scholar
  74. Thomson DM (2006) Detecting the effects of introduced species: a case study of competition between Apis and Bombus. Oikos 114:407–418CrossRefGoogle Scholar
  75. Travis JMJ, Brooker RW, Dytham C (2005) The interplay of positive and negative species interactions across an environmental gradient: insights from an individual-based simulation model. Biol Lett 1:5–8PubMedCrossRefGoogle Scholar
  76. Weigelt A, Bol R, Bardgett RD (2005) Preferential uptake of soil nitrogen forms by grassland plant species. Oecologia 142:627–635PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • I. W. Ashton
    • 1
  • A. E. Miller
    • 2
  • W. D. Bowman
    • 3
  • K. N. Suding
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of California, IrvineIrvineUSA
  2. 2.Southwest Alaska NetworkNational Park ServiceAnchorageUSA
  3. 3.Department of Ecology and Evolutionary BiologyUniversity of ColoradoBoulderUSA

Personalised recommendations