Skip to main content
SpringerLink
Log in

Soil conditioning and plant-soil feedbacks in a modified forest ecosystem are soil-context dependent

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

There is potential for altered plant-soil feedback (PSF) to develop in human-modified ecosystems but empirical data to test this idea are limited. Here, we compared the PSF operating in jarrah forest soil restored after bauxite mining in Western Australia with that operating in unmined soil.

Methods

Native seedlings of jarrah (Eucalyptus marginata), acacia (Acacia pulchella), and bossiaea (Bossiaea ornata) were grown in unmined and restored soils to measure conditioning of chemical and biological properties as compared with unplanted control soils. Subsequently, acacia and bossiaea were grown in soils conditioned by their own or by jarrah seedlings to determine the net PSF.

Results

In unmined soil, the three plant species conditioned the chemical properties but had little effect on the biological properties. In comparison, jarrah and bossiaea conditioned different properties of restored soil while acacia did not condition this soil. In unmined soil, neutral PSF was observed, whereas in restored soil, negative PSF was associated with acacia and bossiaea.

Conclusions

Soil conditioning was influenced by soil context and plant species. The net PSF was influenced by soil context, not by plant species and it was different in restored and unmined soils. The results have practical implications for ecosystem restoration after human activities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

(PSF):

Plant-soil feedback

(PLFA):

Phospholipid–fatty acid profile

(CLPP):

Community level physiological profile

(PCO):

Principal co-ordinate analysis

(NCR):

Nematode channel ratio

References

  • Abbott LK, Robson AD (1977) The distribution and abundance of vesicular arbuscular endophytes in some western Australian soils. Aust J Bot 25:515–522

    Article  Google Scholar 

  • Abbott I (1984) Comparisons of spatial pattern, structure, and tree composition between virgin and cut-over jarrah forest in Western Australia. For Ecol Manag 9:101–126

    Article  Google Scholar 

  • Adl SM (2003) The ecology of soil decomposition. CABI Publishing, UK

    Book  Google Scholar 

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  • Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: Guide to software and statistical methods. Institute of Information and Mathematical Sciences (IIMS) Massey University, Auckland

    Google Scholar 

  • Anderson MJ (2010) Detecting multivariate changes in biological assemblages: experimental design and data analysis. Multivariate analysis of complex experimental designs using PERMANOVA+ for PRIMER. Institute of Information and Mathematical Sciences (IIMS) Massey University, Auckland

    Google Scholar 

  • Baeten L, Vanhellemont M, De Frenne P, De Schrijver A, Hermy M, Verheyen K (2010) Plasticity in response to phosphorus and light availability in four forest herbs. Oecologia 163:1021–1032

    Article  PubMed  Google Scholar 

  • Banning NC, Grant CD, Jones DL, Murphy DV (2008) Recovery of soil organic matter, organic matter turnover and nitrogen cycling in a post-mining forest rehabilitation chronosequence. Soil Biol Biochem 40:2021–2031

    Article  CAS  Google Scholar 

  • Bell DT, Heddle EM (1989) Floristic, morphologic and vegetational diversity. In: Dell B, Havel JJ, Malajczuk N (eds) The jarrah forest: a complex Mediterranean ecosystem. Kluwer Academic Publishers, The Netherlands

    Google Scholar 

  • Bell DT (2001) Ecological response syndromes in the flora of southwestern Western Australia: fire resprouters versus reseeders. Bot Rev 67(4):417–440

    Article  Google Scholar 

  • Bertin C, Yang X, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83

    Article  CAS  Google Scholar 

  • Bever JD, Dickie IA, Facelli E, Facelli JM, Klironomos J, Moora M, Rillig MC, Stock WD, Tibbett M, Zobel M (2010) Rooting theories of plant community ecology in microbial interactions. Trends Ecol Evol 25:468–478

    Article  PubMed Central  PubMed  Google Scholar 

  • Bever JD, Platt TG, Morton ER (2012) Microbial populations and community dynamics on plant roots and their feedbacks on plant communities. Annu Rev Microbiol 66:265–283

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bezemer TM, Lawson CS, Hedlund K, Edwards AR, Brook AJ, Igual JM, Mortimer SM, van der Putten WH (2006) Plant species and functional group effects on abiotic and microbial soil properties and plant–soil feedback responses in two grasslands. J Ecol 94:893–904

    Article  CAS  Google Scholar 

  • Bleby TM, Colquhoun IJ, Adams MA (2009) Architectural plasticity in young Eucalyptus marginata on restored bauxite mines and adjacent natural forest in south-western Australia. Tree Physiol 29:1033–1045

    Article  PubMed  Google Scholar 

  • Bonanomi G, Rietkerk M, Dekker SC, Mazzoleni S (2005) Negative plant–soil feedback and positive species interaction in an herbaceous plant community. Plant Ecol 181:269–278

    Article  Google Scholar 

  • 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. Ecology 82(1):18–32

    Article  Google Scholar 

  • Brimecombe MJ, De Leij FA, Lynch JM (2001) The effect of root exudates on rhizosphere microbial populations. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the plant-soil interface. Marcel Dekker Editorial, USA

    Google Scholar 

  • Campbell CD, Chapman SJ, Cameron CM, Davidson MS, Potts JM (2003) A rapid microtiter plate method to measure carbon dioxide evolved from carbon substrate amendments so as to determine the physiological profiles of soil microbial communities by using whole soil. Appl Environ Microb 69:3593–3599

    Article  CAS  Google Scholar 

  • Carvalhais LC, Dennis PG, Fedoseyenko D, Hajirezaei MR, Borriss R, von Wirén N (2011) Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency. J Plant Nutr Soil Sc 174:3–11

    Article  CAS  Google Scholar 

  • Coleman DA, Crossley DA, Hendrix PF (2004) Fundamentals of soil ecology 2nd edition. Elsevier Academic Press, Amsterdam

    Google Scholar 

  • Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35–47

    Article  CAS  Google Scholar 

  • De Deyn BG, Raaijmakers EC, van der Putten HW (2004) Plant community development is affected by nutrients and soil biota. J Ecol 92:824–834

    Article  Google Scholar 

  • De Rooij-van der Goes PCEM (1995) The role of plant-parasitic nematodes and soil-borne fungi in the decline of Ammophila arenaria (L.) Link. New Phytol 129:661–669

    Article  Google Scholar 

  • Eviner VT (2004) Plant traits that influence ecosystems processes vary independently among species. Ecology 85:2215–2229

    Article  Google Scholar 

  • Eviner VT, Hawkes CV (2008) Embracing variability in the application of plant–soil interactions to the restoration of communities and ecosystems. Restor Ecol 16(4):713–729

    Article  Google Scholar 

  • George SJ, Tibbett M, Braimbridge MF, Davis SG, Vlahos S, Ryan M (2006) Phosphorus fertiliser placement and seedling success in Australian jarrah forest. In: Fourie A, Tibbett M (eds) Mine Closure. Australian Centre for Geomechanics, Perth

    Google Scholar 

  • George SJ, Kelly RN, Greenwood PF, Tibbett M (2010) Soil carbon and litter development along a reconstructed biodiverse forest chronosequence of south-western Australia. Biogeochemistry 101:197–209

    Article  CAS  Google Scholar 

  • Grierson PF, Adams MA (2000) Plant species affect acid phosphatase, ergosterol and microbial P in a Jarrah (Eucalyptus marginata Donn ex Sm.) forest in south-western Australia. Soil Biol Biochem 32:1817–1827

    Article  CAS  Google Scholar 

  • Harris J (2009) Soil Microbial Communities and Restoration Ecology: facilitators or followers. Science 325:572–574

    Article  Google Scholar 

  • Harrison KA, Bardgett RD (2010) Influence of plant species and soil conditions on plant–soil feedback in mixed grassland communities. J Ecol 98:384–395

    Article  Google Scholar 

  • Hirsch AM, Bauer WD, Bird DM, Cullimore J, Tyler B, Yoder JI (2003) Molecular signals and receptors: controlling rhizosphere interactions between plants and other organisms. Ecology 84(4):858–868

    Article  Google Scholar 

  • Hobbie SE (1992) Effects of plant species on nutrient cycling. Trends Ecol Evol 7(10):336–339

    Article  CAS  PubMed  Google Scholar 

  • Hooper DJ, Hallmann J, Subbotin SA (2005) Methods for extraction, processing and detection of plant and soil nematodes. In: Luc M, Sikora RA, Bridge J (eds) Plant parasitic nematodes in subtropical and tropical agriculture, 2nd edn. CAB Publishing, UK

    Google Scholar 

  • Hopper SD (2009) OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically buffered, infertile landscapes. Plant Soil 322:49–86

    Article  CAS  Google Scholar 

  • Jasper AD (2007) Beneficial soil microorganisms of the jarrah forest and their recovery in bauxite mine restoration in South Western Australia. Restor Ecol 15(4):S74–S84

    Article  Google Scholar 

  • Jones DL (1998) Organic acids in the rhizosphere – a critical review. Plant Soil 205:25–44

    Article  CAS  Google Scholar 

  • Jordan NR, Larson DL, Huerd SC (2008) Soil modification by invasive plants: effects on native and invasive species of mixed-grass prairies. Biol Invasions 10:177–190

    Article  Google Scholar 

  • Kardol P, Cornips NJ, van Kempen MML, Bakx-Schotman JMT, van der Putten WH (2007) Microbe-mediated plant-soil feedback causes historical contingency effects in plant community assembly. Ecol Monogr 77(2):147–162

    Article  Google Scholar 

  • Koch JM (2007) Alcoa’s mining and restoration process in south-western Australia. Restor Ecol 15(4):S11–S16

    Article  Google Scholar 

  • Kulmatiski A, Beard HK, Stevens RJ, Cobbold MS (2008) Plant-soil feedbacks: a meta-analytical review. Ecol Lett 11:980–992

    Article  PubMed  Google Scholar 

  • Kulmatiski A, Beard KH (2011) Long-term plant growth legacies overwhelm short-term plant growth effects on soil microbial community structure. Soil Biol Biochem 43:823–830

    Article  CAS  Google Scholar 

  • Lalor EL, Cookson WR, Murphy DV (2007) Comparison of two methods that assess soil community level physiological profiles in a forest ecosystem. Soil Biol Biochem 39:454–462

    Article  CAS  Google Scholar 

  • Lambers H, Raven JA, Shaver GR, Smith SE (2007) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol. doi:10.1016/j.tree.2007.10.008

    Google Scholar 

  • Lavelle P, Spain AV (2003) Soil Ecology. Kluwer Academic Publishers, USA

    Google Scholar 

  • Malajczuk N, McComb AJ (1977) Root exudates from Eucalyptus calophylla R.Br. and Eucalyptus marginata Donn. ex Sm. seedlings and their effect on Phytophthora cinnamomi Rands. Aust J Bot 25:501–514

    Article  CAS  Google Scholar 

  • Malajczuk N (1979) The microflora of unsuberized roots of Eucalyptus calophylla R. Br. and Eucalyptus marginata Donn ex Sm. seedlings grown in soils suppressive and conducive to Phytophthora cinnamomi Rands. II Mycorrhizal roots and associated microflora. Aust J Bot 27:255–272

    Article  Google Scholar 

  • Malajczuk N, McComb AJ (1979) The microflora of unsuberized roots of Eucalyptus calophylla R.Br. and Eucalyptus marginata Donn ex Sm. seedlings grown in soil suppressive and conducive to Phytophthora cinnamomi Rands. I Rhizosphere bacteria, actinomycetes and fungi. Aust J Bot 27:235–254

    Article  Google Scholar 

  • Mangan SA, Schnitzer SA, Herre EA, Mack KML, Valencia MC, Sanchez EI, Bever JD, (2010) Negative plant–soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466 doi: 10.1038/nature09273

  • Manning P, Morrison SA, Bonkowski M, Bardgett RD (2008) Nitrogen enrichment modifies plant community structure via changes to plant-soil feedback. Oecologia 157:661–673

    Article  CAS  PubMed  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants 2nd edition. Academic, Great Britain

    Google Scholar 

  • Martin BC, George SJ, Price CA, Ryan MH, Tibbett M (2014) The role of root exuded low molecular weight organic anions in facilitating petroleum hydrocarbon degradation: current knowledge and future directions. Sci Total Environ 472:642–653

    Article  CAS  PubMed  Google Scholar 

  • Miki T (2012) Microbe-mediated plant-soil feedback and its roles in a changing world. Ecol Res 27:509–520

    Article  CAS  Google Scholar 

  • Mills EK, Bever DJ (1998) Maintenance of diversity within plant communities: soil pathogens as agents of negative feedback. Ecology 79(5):1595–1601

    Article  Google Scholar 

  • Monk D, Pate JS, Loneragan WA (1981) Biology of Acacia pulchella R.Br. with special reference to symbiotic nitrogen fixation. Aust J Bot 29:579–592

    Article  CAS  Google Scholar 

  • Nautiyal CS, Srivastava S, Chauhan PS (2008) Rhizosphere colonization: molecular determinants from plant-microbe coexistence perspective. In: Nautiyal CS, Dion P (eds) Molecular mechanisms of plant and microbe coexistence. Springer, Germany

    Chapter  Google Scholar 

  • Neumann G, Römheld V (1999) Root excretion of carboxylic acids and protons in phosphorus-deficient plants. Plant Soil 211:121–130

    Article  CAS  Google Scholar 

  • Neumann G, Römheld V (2001) The release of root exudates as affected by the plant’s physiological status. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the plant-soil interface. Marcel Dekker Editorial, USA

    Google Scholar 

  • Neumann G (2007) Root exudates and nutrient cycling. In: Marschner P, Rengel Z (eds) Nutrient cycling in terrestrial ecosystems. Springer, Germany

    Google Scholar 

  • Pang J, Ryan MH, Tibbett M, Cawthray GR, Siddique KHM, Bolland MDA, Denton MD, Lambers H (2010) Variation in morphological and physiological parameters in herbaceous perennial legumes in response to phosphorus supply. Plant Soil 331:241–255

    Article  CAS  Google Scholar 

  • Pernilla BE, van der Putten WH, Bakker EJ, Verhoeven KJF (2010) Plant–soil feedback: experimental approaches, statistical analyses and ecological interpretations. J Ecol 98:1063–1073

    Article  Google Scholar 

  • Rayment GE, Higginson FR (1992) Australian laboratory handbook of soil and water chemical methods: Australian soil and land survey handbook Vol. 3. Inkata Press, Australia

    Google Scholar 

  • 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(9):2281–2291

    Article  Google Scholar 

  • Sardans J, Peñuelas J (2013) Plant-soil interactions in Mediterranean forest and shrublands: impacts of climatic change. Plant Soil 365:1–33

    Article  CAS  Google Scholar 

  • te Beest M, Stevens N, Olff N, van der Putten WH (2009) Plant–soil feedback induces shifts in biomass allocation in the invasive plant Chromolaena odorata. J Ecol 97:1281–1290

    Article  Google Scholar 

  • Tibbett M (2010) Large-scale mine site restoration of Australian eucalypt forests after bauxite mining: soil management and ecosystem development. In: Batty LC, Hallberg K (eds) Ecology of industrial pollution. Cambridge University Press, UK

    Google Scholar 

  • Treonis AM, Ostle NJ, Stott AW, Primrose R, Grayston SJ, Ineson P (2004) Identification of groups of metabolically-active rhizosphere microorganisms by stable isotope probing of PLFAs. Soil Biol Biochem 36:533–537

    Article  CAS  Google Scholar 

  • Uren NC (2001) Types, amounts, and possible functions of compounds released into the rhizosphere by soil-grown plants. In: Pinton R, Varanini Z, Nannipieri P (eds) The Rhizosphere: Biochemistry and organic substances at the soil-plant interface. Marcel Dekker Editorial, USA

    Google Scholar 

  • van der Putten WH (2000) Pathogen-driven forest diversity. Nature 404:232–233

    Article  PubMed  Google Scholar 

  • van der Putten WH, Peters BAM (1997) How soil-borne pathogens may affect plant competition. Ecology 78(6):1785–1795

    Article  Google Scholar 

  • van der Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, Kardol P, Klironomos JN, Kulmatiski A, Schweitzer JA, Suding KN, van de Voorde TFJ, Wardle DA (2013) Plant-soil feedbacks: the past, present and future challenges. J Ecol 101(2):265–276

    Article  Google Scholar 

  • van der Stoel CD, van der Putten WH, Duyts H (2002) Development of a negative plant-soil feedback in the extension zone of the clonal grass Ammophila arenaria following root formation and nematode colonization. J Ecol 90:978–988

    Article  Google Scholar 

  • van de Voorde TFJ, van der Putten WH, Bezemer TM (2011) Intra- and interspecific plant–soil interactions, soil legacies and priority effects during old-field succession. J Ecol. doi:10.1111/j.1365-2745.2011.01815

    Google Scholar 

  • Ward SC (2000) Soil development on restored bauxite mines in south-west Australia. Aust J Soil Res 38(2):453

    Article  Google Scholar 

  • White DC, Davies WM, Nickels JS, Kings JD, Bobbie RJ (1979) Determination of the sedimentary microbial biomass by extractible lipid phosphate. Oecologia 40:51–62

    Article  Google Scholar 

  • Yeates GW, Bongers M, de Goede RG, Freckman DW, Georgieva SS (1993) Feeding habits in soil nematode families and genera – An outline for soil ecologists. J Nematol 25(3):315–331

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yeates GW (2003) Nematodes as soil indicators: functional and biodiversity aspects. Biol Fertil Soils 37:199–210

    Google Scholar 

  • Zavaleta-Mejía E, Kaloshian I (2012) Plant-nematode interactions. In: Manzanilla-López RH, Marbán-Mendoza N (eds) Practical Plant Nematology. Biblioteca básica de Agricultura, México

    Google Scholar 

  • Zelles L, Bai QY (1993) Fractionation of fatty acids derived from soil lipids by soil phase extraction and their quantitative analysis by GC–MS. Soil Biol Biochem 25:495–507

    Article  CAS  Google Scholar 

  • Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review. Biol Fertil Soils 29:111–129

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank The Mexican National Council for Science and Technology (CONACYT), John Koch (ALCOA World Alumina Australia) and Tim Morald (University of Western Australia - UWA) for their support and help with field work, Michael Smirke (UWA) for his technical support during laboratory work, Deborah Lin, Khalil Kariman and Alonso Calvo Araya (UWA) for their help during the experiment, Vivien Vanstone, Sarah Collins and staff (DAFWA) for help with nematode extraction as well as Jackie Nobbs (SARDI) for training on the identification of nematode trophic groups. Finally, we thank Richard Hobbs (UWA) and Ken Dodds (ChemCentre – WA) for their support to complete the PLFA analyses.

Author information

Authors and Affiliations

  1. School of Earth and Environment, University of Western Australia, M087, 35 Stirling Hwy, Crawley, WA, 6009, Australia

    Martha Orozco-Aceves & Mark Tibbett

  2. School of Plant Biology, University of Western Australia, M090, 35 Stirling Hwy, Crawley, WA, 6009, Australia

    Rachel J. Standish

  3. Cranfield Soil and Agrifood Institute, Cranfield University, Cranfield, Bedfordshire, MK43 0AL, UK

    Mark Tibbett

Authors
  1. Martha Orozco-Aceves
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rachel J. Standish
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mark Tibbett
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mark Tibbett.

Additional information

Responsible Editor: Jeff R. Powell.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Orozco-Aceves, M., Standish, R.J. & Tibbett, M. Soil conditioning and plant-soil feedbacks in a modified forest ecosystem are soil-context dependent. Plant Soil 390, 183–194 (2015). https://doi.org/10.1007/s11104-015-2390-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-015-2390-z

Keywords

Search

Navigation