Biogeochemistry

, Volume 124, Issue 1–3, pp 177–186

Shifting soil resource limitations and ecosystem retrogression across a three million year semi-arid substrate age gradient

Article

Abstract

The current paradigm of plant nutrient limitation during ecosystem development predicts a change from nitrogen (N) limitation when substrates are young to phosphorus (P) limitation when substrates are old. However, there are surprisingly few direct tests of this model. We evaluated this theory experimentally along a three million year semi-arid substrate age gradient using resource additions to intercanopy spaces dominated by the C4 bunchgrass Bouteloua gracilis. Unlike other gradients in subtropical and temperate ecosystems, soil water availability also increases strongly across this semi-arid system due to finer texture with substrate age. We found that aboveground net primary production (ANPP) of B. gracilis was limited by both water and N on the 55 ky substrate; not limited by N, P, or water on the 750 ky substrate; and limited by P alone on the 3000 ky substrate. Notably, measures of foliar nutrient concentration and N:P mass ratios were unable to predict nutrient limitations in these semi-arid systems. In unamended plots, mean ANPP declined dramatically at 3000 ky compared to the younger substrate age sites, presumably due to progressive limitation by P. This decline in ANPP late in ecosystem development is consistent with a reduction in soil total carbon and N storage at this site and provides a mechanism for successional retrogression in ecosystem structure and function. Our results unify biogeochemical theory across disparate ecosystems while illustrating the important water-nutrient interactions in these semi-arid ecosystems to further define the nature of nutrient limitations in terrestrial ecosystems.

Keywords

Chronosequence Nitrogen N:P stoichiometry Phosphorus Piñon–juniper Soil development 

References

  1. Aerts R, Chapin FS III (1999) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67Google Scholar
  2. Bloom AJ, Chapin FS III, Mooney HA (1985) Resource limitation in plants—an economic analogy. Annu Rev Ecol Syst 16:363–392CrossRefGoogle Scholar
  3. Bonham CD (1989) Measurements of terrestrial vegetation. Wiley, New YorkGoogle Scholar
  4. Bret-Harte MS, Shaver GR, Zoerner JP, Johnstone JF, Wagner JL, Chavez AS, Gunkelman RF, Lippert SC, Laundre JA (2001) Developmental plasticity allows Betula nana to dominate tundra subjected to an altered environment. Ecol. 82:18–32CrossRefGoogle Scholar
  5. Chapin FS III, Vitousek PM, Van Cleve K (1986) The nature of nutrient limitation in plant communities. Am Nat 127:48–58CrossRefGoogle Scholar
  6. Chapin FS III, Matson PA, Mooney HA (2002) Principles of terrestrial ecosystem ecology. Springer, New YorkGoogle Scholar
  7. Craine JM, Jackson RD (2010) Plant nitrogen and phosphorus limitation in 98 North American grassland soils. Plant Soil 334:73–84CrossRefGoogle Scholar
  8. Craine JM, Morrow C, Stock WD (2008) Nutrient concentration ratios and co-limitation in South African grasslands. New Phytol 179:829–836CrossRefGoogle Scholar
  9. Crews T, Fownes J, Herbert D, Kitayama K, Mueller-Dombois D, Riley R, Scowcroft P, Vitousek PM (1995) Changes in soil phosphorus and ecosystem dynamics across a long soil chronosequence in Hawaii. Ecology 76:1407–1424CrossRefGoogle Scholar
  10. Dodd MB, Lauenroth WK, Welker JM (1998) Differential water resource use by herbaceous and woody plant life-forms in a shortgrass steppe community. Oecologia 117:504–512CrossRefGoogle Scholar
  11. Drenovsky RE, Richards JH (2004) Critical N: P values: predicting nutrient deficiencies in desert shrublands. Plant Soil 259:59–69CrossRefGoogle Scholar
  12. 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 10:1135–1142CrossRefGoogle Scholar
  13. Emerson AA (2010) Atmospheric inputs and plant nutrient uptake along a three million year semi-arid substrate age gradient. Dissertation, Northern Arizona UniversityGoogle Scholar
  14. Epstein HE, Lauenroth WK, Burke IC, Coffin DP (1996) Ecological responses of dominant grasses along two climatic gradients in the Great Plains of the United States. J Veg Sci 7:777–788CrossRefGoogle Scholar
  15. Field CB, Chapin FS III, Matson PA, Mooney HA (1992) Responses of terrestrial ecosystems to the changing atmosphere: a resource-based approach. Annu Rev Ecol Syst 23:201–235CrossRefGoogle Scholar
  16. Fischer DG, Hart SC, LeRoy CJ, Whitham TG (2007) Variation in below-ground carbon fluxes along a Populus hybridization gradient. New Phytol 176:415–425CrossRefGoogle Scholar
  17. Gleason SM, Read J, Ares A, Metcalfe DJ (2009) Phosphorus economics of tropical rainforest species and stands across soil contrasts in Queensland, Australia: understanding the effects of soil specialization and trait plasticity. Funct Ecol 23:1157–1166CrossRefGoogle Scholar
  18. Güsewell S (2004) N: P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266CrossRefGoogle Scholar
  19. Güsewell S, Koerselman W (2002) Variation in nitrogen and phosphorus concentrations in wetland plants. Perspect Ecol Evol Syst 5:37–61CrossRefGoogle Scholar
  20. Harpole SW, 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. doi:10.1111/j.1461-0248.2011.01651.x Google Scholar
  21. Harrington RA, Fownes JH, Vitousek PM (2001) Production and resource use efficiencies in N- and P-limited tropical forests: a comparison of responses to long-term fertilization. Ecosystem 4:646–657CrossRefGoogle Scholar
  22. Hays R, Reid CPP, St. John TV, Coleman DC (1982) Effects of nitrogen and phosphorus on blue grama growth and mycorrhizal infection. Oecologia 54:260–265CrossRefGoogle Scholar
  23. Hooper DU, Johnson L (1999) Nitrogen limitation in dryland ecosystems: responses to geographical and temporal variation in precipitation. Biogeochemistry 46:247–293Google Scholar
  24. Jenny H (1941) Factors of soil formation: a system of quantitative pedology. Dover Publications, New YorkGoogle Scholar
  25. Joern A, Mole S (2005) The plant stress hypothesis and variable responses by blue grama grass (Bouteloua gracilis) to water, mineral nitrogen, and insect herbivory. J Chem Ecol 31:2069–2090CrossRefGoogle Scholar
  26. Kaye JP, Hart SC, Fulé PZ, Covington WW, Moore MM, Kaye MW (2005) Initial carbon, nitrogen, and phosphorus fluxes following ponderosa pine restoration treatments. Ecol Appl 15:1581–1593CrossRefGoogle Scholar
  27. Koerselman W, Meulman AFM (1996) The vegetation N: P ratio: a new tool to detect the nature of nutrient limitation. J Appl Ecol 33:1441–1450CrossRefGoogle Scholar
  28. Lajtha K, Schlesinger WH (1988) The biogeochemistry of phosphorus cycling and phosphorus availability along a desert soil chronosequence. Ecology 69:24–39CrossRefGoogle Scholar
  29. Laliberté E, Turner BL, Costes T, Pearse SJ, Wyrwoll K, Zemunik G, Lambers H (2012) Experimental assessment of nutrient limitation along a 2-million-year dune chronosequence in the south-western Australia biodiversity hotspot. J Ecol 100:631–642CrossRefGoogle Scholar
  30. Lauenroth WK, Sala OE (1992) Long-term forage production of North American shortgrass steppe. Ecol Appl 2:397–403CrossRefGoogle Scholar
  31. Looney CE, Sullivan BW, Kolb TE, Kane JM, Hart SC (2011) Pinyon pine (Pinus edulis) mortality and response to water addition across a three million year substrate age gradient in northern Arizona, USA. Plant Soil 357:89–102CrossRefGoogle Scholar
  32. Neff JC, Reynolds R, Sanford RL Jr, Fernandez D, Lamothe P (2006) Controls of bedrock geochemistry on soil and plant nutrients in southeastern Utah. Ecosystem 9:879–893CrossRefGoogle Scholar
  33. Ostertag R (2010) Foliar nitrogen and phosphorus accumulation responses after fertilization: an example from nutrient-limited Hawaiian forests. Plant Soil 334:85–98CrossRefGoogle Scholar
  34. Parkinson JA, Allen SE (1975) A wet oxidation procedure suitable for the determination of nitrogen and mineral nutrients in biological material. Commun Soil Sci Plant Anal 6:1–11CrossRefGoogle Scholar
  35. Peltzer DA, Wardle DA, Allison VJ, Baisden WT, Bardgett RD, Chadwick OA, Condron LM, Parfitt RL, Porder S, Richardson SJ, Turner BL, Vitousek PM, Walker J, Walker LR (2010) Understanding ecosystem retrogression. Ecol Monogr 80:509–529CrossRefGoogle Scholar
  36. Poorter H, Nagel O (2000) The role of biomass allocation in the growth response of plants to different light, CO2, nutrients and water: a quantitative review. Aust J Plant Physiol 27:595–607CrossRefGoogle Scholar
  37. Sala OE, Lauenroth WK (1982) Small rainfall events: an ecological role in semiarid regions. Oecologia 53:301–304CrossRefGoogle Scholar
  38. Schlesinger WH, Bernhardt ES (2013) Biogeochemistry: an analysis of global change. Springer, NetherlandsCrossRefGoogle Scholar
  39. Seliskar DM, Gallagher JL, Burdick DM, Mutz LA (2002) The regulation of ecosystem functions by ecotypic variation in the dominant plant: a Spartina alterniflora salt-marsh case study. J Ecol 90:1–11CrossRefGoogle Scholar
  40. Selmants PC (2007) Carbon, nitrogen, and phosphorus dynamics across a three million year substrate age gradient in northern Arizona, USA. PhD Dissertation, Northern Arizona UniversityGoogle Scholar
  41. Selmants PC, Hart SC (2008) Substrate age and tree islands influence carbon and nitrogen dynamics across a retrogressive semiarid chronosequence. Global Biogeochem Cycles 22:GB1021. doi:10.1029/2007GB003062 CrossRefGoogle Scholar
  42. Selmants PC, Hart SC (2010) Phosphorus and soil development: does the Walker and Syers model apply to semiarid ecosystems? Ecology 91:474–484CrossRefGoogle Scholar
  43. Sheppard PR, Comrie AC, Packtin GD, Angersbach K, Hughes MK (2002) The climate of the US Southwest. Clim Res 21:219–238CrossRefGoogle Scholar
  44. Smoliak S (1986) Influence of climatic conditions on production of Stipa-Bouteloua prairie over a 50-year period. J Range Manag 39:100–103CrossRefGoogle Scholar
  45. Tanaka KL, Shoemaker EM, Ulrich GE, Wolfe EW (1986) Migration of volcanism in the San Francisco volcanic field, Arizona. Geol Soc Am Bull 97:129–141CrossRefGoogle Scholar
  46. Thompson K, Parkinson JA, Band S, Spencer RE (1997) A comparative study of leaf nutrient concentrations in a regional herbaceous flora. New Phytol 136:679–689CrossRefGoogle Scholar
  47. Vitousek PM (2004) Nutrient cycling and limitation: Hawai’i as a model system. Princeton University Press, NJGoogle Scholar
  48. Vitousek PM, Farrington H (1997) Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry 37:63–75CrossRefGoogle Scholar
  49. Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115CrossRefGoogle Scholar
  50. Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20:5–15CrossRefGoogle Scholar
  51. Walker TW, Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15:1–19CrossRefGoogle Scholar
  52. Wardle DA, Walker LR, Bardgett RD (2004) Ecosystem properties and forest decline in contrasting long-term chronosequences. Science 305:509–513CrossRefGoogle Scholar
  53. Wassen MJ, Olde Venterink HGM, de Swart EOAM (1995) Nutrient concentrations in mire vegetation as a measure of nutrient limitation in mire ecosystems. J Veg Sci 6:5–16CrossRefGoogle Scholar
  54. Yuan ZY, Chen HY (2012) A global analysis of fine root production as affected by soil nitrogen and phosphorus. Proc R Soc B 279:3796–3802CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.School of ForestryNorthern Arizona UniversityFlagstaffUSA
  2. 2.Natural History Museum of DenmarkUniversity of CopenhagenCopenhagen KDenmark
  3. 3.Life & Environmental Sciences and Sierra Nevada Research InstituteUniversity of CaliforniaMercedUSA

Personalised recommendations