Plant and Soil

, Volume 391, Issue 1–2, pp 321–331 | Cite as

Response of belowground communities to short-term phosphorus addition in a phosphorus-limited woodland

  • Uffe N. Nielsen
  • Samantha Prior
  • Brendan Delroy
  • Jennifer K. M. Walker
  • David S. Ellsworth
  • Jeff R. Powell
Regular Article

Abstract

Aims

Soil biota regulate essential ecosystem processes but our understanding of how soil fertility constrains biotic interactions remains limited. We investigated belowground responses to short-term phosphorus (P) fertilization in a P-limited woodland.

Methods

Ten Eucalyptus tereticornis were randomly selected and five fertilized with superphosphate equivalent to 50 kg P ha−1 over 6 months. We estimated aboveground (understory) and belowground plant biomass, and collected samples for soil chemistry, arbuscular mycorrhizal (AM) root colonization, soil fungal abundance and community composition, and extraction of nematodes and microarthropods.

Results

P-fertilization increased root biomass, abundance of non-AM fungi, and abundances of Collembola, and altered fungal community structure, but was associated with a decrease in predatory nematodes. Structural equation modelling indicated that effects on Collembola and fungal abundances were mediated by direct effects of the fertilizer treatment and/or indirect effects via root biomass responses. However, fungal community compositional changes and reductions in predatory nematodes resulted primarily due to fertilization-mediated changes in soil pH.

Conclusion

Our study shows that understory plant communities and soil biota are P-limited at the study site but that some biotic groups appear to be more sensitive to changes in soil pH than to increases in P availability.

Keywords

Cumberland plain woodland Fungi Microarthropods Nematoda Phosphorus fertilization pH 

Supplementary material

11104_2015_2432_MOESM1_ESM.pdf (10 kb)
Supplemental Figure 1Boxplots indicating proportional abundances of DNA sequencing reads in control (ctrl) and fertilized (fert) plots under E. tereticornis. OTU numbers refer to the labels in Table 2. The number in parentheses represents the indicator value for that OTU. The box indicates the interquartile range, the thick line represents the median, and the whiskers extend to either the extremes of the sampled data or to 1.5 times the interquartile range, whichever is closer to the median. (PDF 9 kb)

References

  1. Altieri MA (1999) The ecological role of biodiversity in agroecosystems. Agric Ecosyst Environ 74:19–31. doi:10.1016/S0167-8809(99)00028-6 CrossRefGoogle Scholar
  2. Aslam TJ, Benton TG, Nielsen UN, Johnson SN (2015) Impacts of eucalypt plantation management on soil faunal communities and nutrient bioavailability: trading function for dependence? Biol Fert Soils (in press)Google Scholar
  3. Bardgett RD (2005) The Biology of Soil: A Community and Ecosystem Approach. Oxford University Press, OxfordCrossRefGoogle Scholar
  4. Bardgett RD, Wardle DA (2010) Aboveground-Belowground Linkages: Biotic Interactions, Ecosystem Processes, and Global Change. Oxford University Press, OxfordGoogle Scholar
  5. Bardgett R, Hopkins D, Usher M (2005) Biological Diversity and Function in Soils. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  6. Bates TR, Lynch JP (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ 19:529–538. doi:10.1111/j.1365-3040.1996.tb00386.x CrossRefGoogle Scholar
  7. Berch SM, Brockley RP, Battigelli J, Hagerman S (2009) Impacts of repeated fertilization on fine roots, mycorrhizas, mesofauna, and soil chemistry under young interior spruce in central British Columbia. Can J For Res 39:889–896. doi:10.1139/X08-204 CrossRefGoogle Scholar
  8. Bongers T (1990) The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83:14–19. doi:10.1007/BF00324627 CrossRefGoogle Scholar
  9. Borch K, Bouma TJ, Lynch JP, Brown KM (1999) Ethylene: a regulator of root architectural responses to soil phosphorus availability. Plant Cell Environ 22:425–431. doi:10.1046/j.1365-3040.1999.00405.x CrossRefGoogle Scholar
  10. Bragg L, Stone G, Imelfort M, Hugenholtz P, Tyson GW (2012) Fast, accurate error-correction of amplicon pyrosequences using Acacia. Nat Methods 9:425–426. doi:10.1038/nmeth.1990 CrossRefPubMedGoogle Scholar
  11. Bray RH, Kurtz LT (1945) Determination of total, organic, and available forms of phosphorus in soils. Soil Sci 59:39–46CrossRefGoogle Scholar
  12. Brussaard L (1997) Biodiversity and ecosystem functioning in soil. Ambio 26:563–570Google Scholar
  13. Bünemann EK, Schwenke GD, Van Zwieten L (2006) Impact of agricultural inputs on soil organisms—a review. Soil Res 44:379–406CrossRefGoogle Scholar
  14. Camenzind T, Hempel S, Homeier J, Horn S, Velescu A, Wilcke W, Rillig MC (2014) Nitrogen and phosphorus additions impact arbuscular mycorrhizal abundance and molecular diversity in a tropical montane forest. Glob Chang Biol 20:3646–3659. doi:10.1111/gcb.12618 CrossRefPubMedGoogle Scholar
  15. Ceulemans T, Stevens CJ, Duchateau L, Jacquemyn H, Gowing DJG, Merckx R, Wallace H, van Rooijen N, Goethem T, Bobbink R, Dorland E, Gaudnik C, Alard D, Corcket E, Muller S, Dise NB, Dupré C, Diekmann M, Honnay O (2014) Soil phosphorus constrains biodiversity across European grasslands. Glob Chang Biol 20:3814–3822. doi:10.1111/gcb.12650 CrossRefPubMedGoogle Scholar
  16. Coates KD, Lilles EB, Astrup R (2013) Competitive interactions across a soil fertility gradient in a multispecies forest. J Ecol 101:806–818. doi:10.1111/1365-2745.12072 CrossRefGoogle Scholar
  17. R Core Development Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/
  18. Crous KY, Ósvaldsson A, Ellsworth DS (2015) Is phosphorus limiting in a mature Eucalyptus woodland? Phosphorus fertilisation stimulates stem growth. doi:10.1007/s11104-015-2426-4
  19. de Vries FT, Thébault E, Liiri M et al (2013) Soil food web properties explain ecosystem services across European land use systems. Proc Natl Acad Sci 110:14296–14301. doi:10.1073/pnas.1305198110 CrossRefPubMedCentralPubMedGoogle Scholar
  20. Doran JW, Werner MR (1990) Management and soil biology. In: Francis CA, Flora CB, King LD (eds) Sustainable Agriculture in Temperate Zones. Wiley, New York, pp 205–230Google Scholar
  21. Dufrêne M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366. doi:10.1890/0012-9615(1997)067[0345:SAAIST]2.0.CO;2 Google Scholar
  22. Dumbrell AJ, Nelson M, Helgason T et al (2009) Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J 4:337–345. doi:10.1038/ismej.2009.122 CrossRefPubMedGoogle Scholar
  23. Edgar RC, Haas BJ, Clemente JC et al (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. doi:10.1093/bioinformatics/btr381 CrossRefPubMedCentralPubMedGoogle Scholar
  24. Ehlers K, Bakken LR, Frostegård Å et al (2010) Phosphorus limitation in a ferralsol: impact on microbial activity and cell internal P pools. Soil Biol Biochem 42:558–566. doi:10.1016/j.soilbio.2009.11.025 CrossRefGoogle Scholar
  25. Elser JJ, Bracken MES, Cleland EE et al (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142. doi:10.1111/j.1461-0248.2007.01113.x CrossRefPubMedGoogle Scholar
  26. Epstein E, Bloom AJ (2005) Inorganic components of plants. In Mineral Nutrition of Plants, 2nd edn. Sinauer Associates, Mass, pp 44–45Google Scholar
  27. Ferris H (2010) Form and function: metabolic footprints of nematodes in the soil food web. Eur J Soil Biol 46:97–104. doi:10.1016/j.ejsobi.2010.01.003 CrossRefGoogle Scholar
  28. Foley JA, DeFries R, Asner GP et al (2005) Global consequences of land use. Science 309:570–574. doi:10.1126/science.1111772 CrossRefPubMedGoogle Scholar
  29. Galloway JN, Townsend AR, Erisman JW et al (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892. doi:10.1126/science.1136674 CrossRefPubMedGoogle Scholar
  30. Harpole WS, Tilman D (2007) Grassland species loss resulting from reduced niche dimension. Nature 446:791–793. doi:10.1038/nature05684 CrossRefPubMedGoogle Scholar
  31. Harris KK, Boerner REJ (1990) Effects of belowground grazing by collembola on growth, mycorrhizal infection, and P uptake of Geranium robertianum. Plant Soil 129:203–210. doi:10.1007/BF00032414 Google Scholar
  32. Hooper DU, Bignell DE, Brown VK et al (2000) Interactions between aboveground and belowground biodiversity in terrestrial ecosystems: patterns, mechanisms, and feedbacks. Bioscience 50:1049–1061. doi:10.1641/0006-3568(2000)050[1049:IBAABB]2.0.CO;2 CrossRefGoogle Scholar
  33. Jacobs DF, Timmer VR (2005) Fertilizer-induced changes in rhizosphere electrical conductivity: relation to forest tree seedling root system growth and function. New For 30:147–166. doi:10.1007/s11056-005-6572-z CrossRefGoogle Scholar
  34. Jakobsen I, Abbott LK, Robson AD (1992) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. New Phytol 120:371–380. doi:10.1111/j.1469-8137.1992.tb01077.x CrossRefGoogle Scholar
  35. Jandl R, Kopeszki H, Bruckner A, Hager H (2003) Forest soil chemistry and mesofauna 20 years after an amelioration fertilization. Restor Ecol 11:239–246. doi:10.1046/j.1526-100X.2003.00179.x CrossRefGoogle Scholar
  36. Kluber LA, Carrino-Kyker SR, Coyle KP et al (2012) Mycorrhizal response to experimental pH and P manipulation in acidic hardwood forests. PLoS ONE 7:e48946. doi:10.1371/journal.pone.0048946 CrossRefPubMedCentralPubMedGoogle Scholar
  37. Krashevska V, Sandmann D, Maraun M, Scheu S (2014) Moderate changes in nutrient input alter tropical microbial and protist communities and belowground linkages. ISME J 8:1126–1134. doi:10.1038/ismej.2013.209 CrossRefPubMedCentralPubMedGoogle Scholar
  38. Lavelle P, Spain AV (2001) Soil Ecology. Kluwer Academic Publishers, DordrechtCrossRefGoogle Scholar
  39. Maraun M, Alphei J, Beste P et al (2001) Indirect effects of carbon and nutrient amendments on the soil meso- and microfauna of a beechwood. Biol Fertil Soils 34:222–229. doi:10.1007/s003740100403 Google Scholar
  40. McGonigle TP (1995) The significance of grazing on fungi in nutrient cycling. Can J Bot 73:1370–1376. doi:10.1139/b95-399 CrossRefGoogle Scholar
  41. McGonigle TP, Miller MH, Evans DG et al (1990) A new method which gives an objective measure of colonization of roots by vesicular—arbuscular mycorrhizal fungi. New Phytol 115:495–501. doi:10.1111/j.1469-8137.1990.tb00476.x CrossRefGoogle Scholar
  42. Mulder C, Zwart DD, Van Wijnen HJ et al (2003) Observational and simulated evidence of ecological shifts within the soil nematode community of agroecosystems under conventional and organic farming. Funct Ecol 17:516–525. doi:10.1046/j.1365-2435.2003.00755.x CrossRefGoogle Scholar
  43. Oksanen J, Blanchet FG, Kindt R, et al (2013) vegan: Community Ecology Package. R package version 2.0-10. http://CRAN.R-project.org/package=vegan
  44. Oliver I, Garden D, Greenslade PJ et al (2005) Effects of fertiliser and grazing on the arthropod communities of a native grassland in south-eastern Australia. Agric Ecosyst Environ 109:323–334. doi:10.1016/j.agee.2005.02.022 CrossRefGoogle Scholar
  45. Onanuga AO, Jiang P, Adl S (2011) Effect of phytohormones, phosphorus and potassium on cotton varieties (Gossypium hirsutum) root growth and root activity grown in hydroponic nutrient solution. J Agric Sci 4:93–110. doi:10.5539/jas.v4n3p93 Google Scholar
  46. Peacock AD, Mullen MD, Ringelberg DB et al (2001) Soil microbial community responses to dairy manure or ammonium nitrate applications. Soil Biol Biochem 33:1011–1019. doi:10.1016/S0038-0717(01)00004-9 CrossRefGoogle Scholar
  47. Peñuelas J, Sardans J, Rivas-ubach A, Janssens IA (2012) The human-induced imbalance between C, N and P in Earth’s life system. Glob Chang Biol 18:3–6. doi:10.1111/j.1365-2486.2011.02568.x CrossRefGoogle Scholar
  48. Pruesse E, Quast C, Knittel K et al (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196. doi:10.1093/nar/gkm864 CrossRefPubMedCentralPubMedGoogle Scholar
  49. Pywell RF, Bullock JM, Tallowin JB et al (2007) Enhancing diversity of species-poor grasslands: an experimental assessment of multiple constraints. J Appl Ecol 44:81–94. doi:10.1111/j.1365-2664.2006.01260.x CrossRefGoogle Scholar
  50. Read DJ (1991) Mycorrhizas in ecosystems - Nature’s response to the ‘Law of the minimum’. In: Hawksworth DL (ed) Frontiers in mycology. CAB International, Regensburg, pp 101–130Google Scholar
  51. Richardson AE, Hocking PJ, Simpson RJ, George TS (2009) Plant mechanisms to optimise access to soil phosphorus. Crop Pasture Sci 60:124–143CrossRefGoogle Scholar
  52. Rillig MC, Field CB, Allen MF (1999) Soil biota responses to long-term atmospheric CO2 enrichment in two California annual grasslands. Oecologia 119:572–577. doi:10.1007/s004420050821 CrossRefGoogle Scholar
  53. Roberts DW (2007) labdsv: Ordination and multivariate analysis for ecology. R package version 1.6-1. http://CRAN.R-project.org/package=labdsv
  54. Rosseel Y (2012) lavaan: an R package for structural equation modeling. J Stat Softw 48:1–36. URL http://www.jstatsoft.org/v48/i02/
  55. Rousk J, Bååth E, Brookes PC et al (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351. doi:10.1038/ismej.2010.58 CrossRefPubMedGoogle Scholar
  56. Ruess L, Michelsen A, Schmidt IK, Jonasson S (1999) Simulated climate change affecting microorganisms, nematode density and biodiversity in subarctic soils. Plant Soil 212:63–73. doi:10.1023/A:1004567816355 CrossRefGoogle Scholar
  57. Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. doi:10.1128/AEM. 01541-09 CrossRefPubMedCentralPubMedGoogle Scholar
  58. Schon N, Mackay A, Gray R, Minor M (2011) Influence of phosphorus inputs and sheep treading on soil macrofauna and mesofauna in hill pastures. N Z J Agric Res 54:83–96. doi:10.1080/00288233.2011.558904 CrossRefGoogle Scholar
  59. Siciliano SD, Palmer AS, Winsley T et al (2014) Soil fertility is associated with fungal and bacterial richness, whereas pH is associated with community composition in polar soil microbial communities. Soil Biol Biochem 78:10–20. doi:10.1016/j.soilbio.2014.07.005 CrossRefGoogle Scholar
  60. Sjursen H, Michelsen A, Jonasson S (2005) Effects of long-term soil warming and fertilisation on microarthropod abundances in three sub-arctic ecosystems. Appl Soil Ecol 30:148–161. doi:10.1016/j.apsoil.2005.02.013 CrossRefGoogle Scholar
  61. Steinaker DF, Wilson SD (2008) Scale and density dependent relationships among roots, mycorrhizal fungi and collembola in grassland and forest. Oikos 117:703–710. doi:10.1111/j.0030-1299.2008.16452.x CrossRefGoogle Scholar
  62. Tabaglio V, Gavazzi C, Menta C (2009) Physico-chemical indicators and microarthropod communities as influenced by no-till, conventional tillage and nitrogen fertilisation after four years of continuous maize. Soil Tillage Res 105:135–142. doi:10.1016/j.still.2009.06.006 CrossRefGoogle Scholar
  63. Thiele-Bruhn S, Bloem J, de Vries FT et al (2012) Linking soil biodiversity and agricultural soil management. Curr Opin Environ Sustain 4:523–528. doi:10.1016/j.cosust.2012.06.004 CrossRefGoogle Scholar
  64. Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–355. doi:10.1111/j.1469-8137.2004.01159.x CrossRefGoogle Scholar
  65. Treseder KK, Allen MF (2002) Direct nitrogen and phosphorus limitation of arbuscular mycorrhizal fungi: a model and field test. New Phytol 155:507–515. doi:10.1046/j.1469-8137.2002.00470.x CrossRefGoogle Scholar
  66. van der Wal A, Geerts RHEM, Korevaar H et al (2009) Dissimilar response of plant and soil biota communities to long-term nutrient addition in grasslands. Biol Fertil Soils 45:663–667. doi:10.1007/s00374-009-0371-1 CrossRefGoogle Scholar
  67. Vierheilig H, Coughlan AP, Wyss U, Piche Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007PubMedCentralPubMedGoogle Scholar
  68. Vilkamaa P, Huhta V (1986) Effects of fertilization and pH on communities of Collembola in pine forest soil. Ann Zool Fenn 167–174Google Scholar
  69. Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecol Appl 20:5–15. doi:10.1890/08-0127.1 CrossRefPubMedGoogle Scholar
  70. Wagg C, Bender SF, Widmer F, van der Heijden MGA (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci 111:5266–5270. doi:10.1073/pnas.1320054111 CrossRefPubMedCentralPubMedGoogle Scholar
  71. Walker JKM, Phillips LA, Jones MD (2014) Ectomycorrhizal fungal hyphae communities vary more along a pH and nitrogen gradient than between decayed wood and mineral soil microsites. Botany 92:453–463. doi:10.1139/cjb-2013-0239 CrossRefGoogle Scholar
  72. Wassen MJ, Venterink HO, Lapshina ED, Tanneberger F (2005) Endangered plants persist under phosphorus limitation. Nature 437:547–550. doi:10.1038/nature03950 CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Uffe N. Nielsen
    • 1
    • 2
  • Samantha Prior
    • 1
    • 2
  • Brendan Delroy
    • 1
    • 2
  • Jennifer K. M. Walker
    • 1
  • David S. Ellsworth
    • 1
  • Jeff R. Powell
    • 1
  1. 1.Hawkesbury Institute for the EnvironmentUniversity of Western SydneyPenrithAustralia
  2. 2.School of Science and HealthUniversity of Western SydneyPenrithAustralia

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