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

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

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

    Article  Google 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)

  3. Bardgett RD (2005) The Biology of Soil: A Community and Ecosystem Approach. Oxford University Press, Oxford

    Book  Google Scholar 

  4. Bardgett RD, Wardle DA (2010) Aboveground-Belowground Linkages: Biotic Interactions, Ecosystem Processes, and Global Change. Oxford University Press, Oxford

    Google Scholar 

  5. Bardgett R, Hopkins D, Usher M (2005) Biological Diversity and Function in Soils. Cambridge University Press, Cambridge

    Book  Google 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

    Article  CAS  Google 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

    Article  CAS  Google 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

    Article  Google 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

    Article  CAS  Google 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

    Article  CAS  PubMed  Google Scholar 

  11. Bray RH, Kurtz LT (1945) Determination of total, organic, and available forms of phosphorus in soils. Soil Sci 59:39–46

    Article  CAS  Google Scholar 

  12. Brussaard L (1997) Biodiversity and ecosystem functioning in soil. Ambio 26:563–570

    Google Scholar 

  13. Bünemann EK, Schwenke GD, Van Zwieten L (2006) Impact of agricultural inputs on soil organisms—a review. Soil Res 44:379–406

    Article  Google 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

    Article  PubMed  Google 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

    Article  PubMed  Google 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

    Article  Google 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

    Article  PubMed Central  PubMed  Google 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 205–230

    Google 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

    Article  PubMed  Google 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

    Article  PubMed Central  CAS  PubMed  Google 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

    Article  CAS  Google 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

    Article  PubMed  Google Scholar 

  26. Epstein E, Bloom AJ (2005) Inorganic components of plants. In Mineral Nutrition of Plants, 2nd edn. Sinauer Associates, Mass, pp 44–45

    Google 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

    Article  Google 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

    Article  CAS  PubMed  Google 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

    Article  CAS  PubMed  Google Scholar 

  30. Harpole WS, Tilman D (2007) Grassland species loss resulting from reduced niche dimension. Nature 446:791–793. doi:10.1038/nature05684

    Article  CAS  PubMed  Google 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

    CAS  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

    Article  Google 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

    Article  Google 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

    Article  CAS  Google 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

    Article  Google 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

    Article  PubMed Central  CAS  PubMed  Google 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  38. Lavelle P, Spain AV (2001) Soil Ecology. Kluwer Academic Publishers, Dordrecht

    Book  Google 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

    CAS  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

    Article  Google 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

    Article  Google 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

    Article  Google 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

    Article  Google 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

    Article  CAS  Google 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

    Article  Google 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

    Article  PubMed Central  CAS  PubMed  Google 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

    Article  CAS  Google 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 101–130

    Google Scholar 

  51. Richardson AE, Hocking PJ, Simpson RJ, George TS (2009) Plant mechanisms to optimise access to soil phosphorus. Crop Pasture Sci 60:124–143

    Article  CAS  Google 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

    Article  Google 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

    Article  PubMed  Google 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

    Article  CAS  Google 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

    Article  PubMed Central  CAS  PubMed  Google 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

    Article  Google 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

    Article  CAS  Google 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

    Article  Google 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

    Article  Google 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

    Article  Google 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

    Article  Google 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

    Article  Google 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

    Article  Google 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

    Article  Google 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 64:5004–5007

    PubMed Central  CAS  PubMed  Google Scholar 

  68. Vilkamaa P, Huhta V (1986) Effects of fertilization and pH on communities of Collembola in pine forest soil. Ann Zool Fenn 167–174

  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

    Article  PubMed  Google 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

    Article  PubMed Central  CAS  PubMed  Google 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

    Article  Google 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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Dr Kaushal Tewari and Sarah Beck provided technical assistance with sample processing. This work was supported by the Australian Reseach Council Discovery Grants scheme (DP110105102 and DP130102501). EucFACE is supported by the Australian Commonwealth government in collaboration with the University of Western Sydney. This is part of a TERN Super-site facility. EucFACE was built as an initiative of the Australian government as part of the Nation-building Economic Stimulus Package.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Jeff R. Powell.

Additional information

Uffe N. Nielsen and Jeff R. Powell contributed equally to this work.

Responsible Editor: Sven Marhan.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplemental Figure 1

Boxplots 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)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Nielsen, U.N., Prior, S., Delroy, B. et al. Response of belowground communities to short-term phosphorus addition in a phosphorus-limited woodland. Plant Soil 391, 321–331 (2015). https://doi.org/10.1007/s11104-015-2432-6

Download citation

Keywords

  • Cumberland plain woodland
  • Fungi
  • Microarthropods
  • Nematoda
  • Phosphorus fertilization
  • pH