Oecologia

, Volume 181, Issue 2, pp 559–569 | Cite as

Plant-soil feedbacks: a comparative study on the relative importance of soil feedbacks in the greenhouse versus the field

  • Johannes Heinze
  • M. Sitte
  • A. Schindhelm
  • J. Wright
  • J. Joshi
Community ecology – Original research

Abstract

Interactions between plants and soil microorganisms influence individual plant performance and thus plant-community composition. Most studies on such plant-soil feedbacks (PSFs) have been performed under controlled greenhouse conditions, whereas no study has directly compared PSFs under greenhouse and natural field conditions. We grew three grass species that differ in local abundance in grassland communities simultaneously in the greenhouse and field on field-collected soils either previously conditioned by these species or by the general grassland community. As soils in grasslands are typically conditioned by mixes of species through the patchy and heterogeneous plant species’ distributions, we additionally compared the effects of species-specific versus non-specific species conditioning on PSFs in natural and greenhouse conditions. In almost all comparisons PSFs differed between the greenhouse and field. In the greenhouse, plant growth in species-specific and non-specific soils resulted in similar effects with neutral PSFs for the most abundant species and positive PSFs for the less abundant species. In contrast, in the field all grass species tested performed best in non-specific plots, whereas species-specific PSFs were neutral for the most abundant and varied for the less abundant species. This indicates a general beneficial effect of plant diversity on PSFs in the field. Controlled greenhouse conditions might provide valuable insights on the nominal effects of soils on plants. However, the PSFs observed in greenhouse conditions may not be the determining drivers in natural plant communities where their effects may be overwhelmed by the diversity of abiotic and biotic above- and belowground interactions in the field.

Keywords

Grassland Plant performance Experimental environment Community assembly Plant diversity 

Supplementary material

442_2016_3591_MOESM1_ESM.pdf (955 kb)
Supplementary material 1 (PDF 954 kb)

References

  1. Bartelt-Ryser J, Joshi J, Schmid B, Brandl H, Balser T (2005) Soil feedbacks of plant diversity on soil microbial communities and subsequent plant growth. Perspect Plant Ecol Evol Syst 7:27–49. doi:10.1016/j.ppees.2004.11.002 CrossRefGoogle Scholar
  2. Bauer JT, Mack KML, Bever JD (2015) Plant-soil feedbacks as drivers of succession: evidence from remnant and restored tallgrass prairies. Ecosphere 6:1–12. doi:10.1890/ES14-00480.1 CrossRefGoogle Scholar
  3. Bever JD (1994) Feedback between plants and their soil communities in an old field community. Ecology 75:1965–1977. doi:10.1111/j.1365-2745.2006.01104.x CrossRefGoogle Scholar
  4. Bever JD (2003) Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytol 157:465–473. doi:10.1046/j.1469-8137.2003.00714.x CrossRefGoogle Scholar
  5. Bever JD, Westover KM, Antonovics J (1997) Incorporating the soil community into plant population dynamics: the utility of the feedback approach. J Ecol 85:561–573. doi:10.2307/2960528 CrossRefGoogle Scholar
  6. Bever JD, Dickie IA, Facelli E, Facelli JM, Klironomos JN, 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. doi:10.1016/j.tree.2010.05.004 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bever JD, Mangan SA, Alexander HM (2015) Maintenance of plant species diversity by pathogens. Annu Rev Ecol Evol Syst 46:305–325. doi:10.1146/annurev-ecolsys-112414-054306 CrossRefGoogle Scholar
  8. Bezemer TM, Lawson CS, Hedlund K, Edwards AR, Brook AJ, Igual JM, Mortimer SR, 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. doi:10.1111/j.1365-2745.2006.01158.x CrossRefGoogle Scholar
  9. Bonanomi G, Giannino F, Mazzoleni S (2005) Negative plant-soil feedback and species coexistence. Oikos 111:311–321. doi:10.1111/j.0030-1299.2005.13975.x CrossRefGoogle Scholar
  10. Brinkman EP, van der Putten WH, Bakker E-J, Verhoeven KJF (2010) Plant-soil feedback: experimental approaches, statistical analyses and ecological interpretations. J Ecol 98:1063–1073. doi:10.1111/j.1365-2745.2010.01695.x CrossRefGoogle Scholar
  11. Casper BB, Castelli JP (2007) Evaluating plant-soil feedbacks together with competition in a serpentine grassland. Ecol Lett 10:394–400. doi:10.1111/j.1461-0248.2007.01030.x CrossRefPubMedGoogle Scholar
  12. Casper BB, Bentivenga SP, Ji B, Doherty JH, Edenbern HM, Gustafson DJ (2008) Plant-soil feedback: testing the generality with the same grasses in serpentine and prairie soils. Ecology 89:2154–2164. doi:10.1890/07-1277.1 CrossRefPubMedGoogle Scholar
  13. Chiuffo MC, MacDougall AS, Hierro JL (2015) Native and non-native ruderals experience similar plant-soil feedbacks and neighbor effects in a system where they coexist. Oecologia 179:843–852. doi:10.1007/s00442-015-3399-y CrossRefPubMedGoogle Scholar
  14. Ehrenfeld JG, Ravit B, Elgersma K (2005) Feedback in the plant-soil system. Annu Rev Environ Resour 30:75–115. doi:10.1146/annurev.energy.30.050504.144212 CrossRefGoogle Scholar
  15. Fraser LH, Grime JP (1998) Top-down control and its effect on the biomass and composition of three grasses at high and low soil fertility in outdoor microcosms. Oecologia 113:239–246. doi:10.1007/s004420050374 CrossRefGoogle Scholar
  16. Fricke EC, Tewksbury JJ, Rogers HS (2014) Multiple natural enemies cause distance-dependent mortality at the seed-to-seedling transition. Ecol Lett 17:593–598. doi:10.1111/ele.12261 CrossRefPubMedGoogle Scholar
  17. Grime JP (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111:1169–1194CrossRefGoogle Scholar
  18. Gustafson DJ, Casper BB (2004) Nutrient addition affects AM fungal performance and expression of plant/fungal feedback in three serpentine grasses. Plant Soil 259:9–17. doi:10.1023/B:PLSO.0000020936.56786.a4 CrossRefGoogle Scholar
  19. Heinze J, Bergmann J, Rillig MC, Joshi J (2015a) Negative biotic soil-effects enhance biodiversity by restricting potentially dominant plant species in grasslands. Perspect Plant Ecol Evol Syst 17:227–235. doi:10.1016/j.ppees.2015.03.002 CrossRefGoogle Scholar
  20. Heinze J, Werner T, Weber E, Rillig MC, Joshi J (2015b) Soil biota effects on local abundances of three grass species along a land-use gradient. Oecologia. doi:10.1007/s00442-015-3336-0 PubMedGoogle Scholar
  21. Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211. doi:10.2307/1942661 CrossRefGoogle Scholar
  22. Jackson RB, Canadell J, Ehleringer JR, Mooney HA, Sala OE, Schulze ED (1996) A global analysis of root distributions for terrestrial biomes. Oecologia 108:389–411. doi:10.1007/BF00333714 CrossRefGoogle Scholar
  23. Johnson NC, Wilson GWT, Bowker MA, Wilson JA, Miller RM (2010) Resource limitation is a driver of local adaptation in mycorrhizal symbioses. PNAS 107:2093–2098. doi:10.1073/pnas.0906710107 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 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. Eco Monogr 77:147–162. doi:10.1890/06-0502 CrossRefGoogle Scholar
  25. Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness incommunities. Nature 417:67–70. doi:10.1038/417067a CrossRefPubMedGoogle Scholar
  26. Klotz S, Kühn I, Durka W (2002) BIOLFLOR–eine Datenbank zu biologisch-ökologischen Merkmalen der Gefäßpflanzen in Deutschland. Bundesamt für Naturschutz, Bonn. Schriftenreihe für Vegetationskunde 38Google Scholar
  27. Kneis D, Knoesche R, Bronstert A (2006) Analysis and simulation of nutrient retention and management for a lowland river-lake system. Hydrol Earth Syst Sci 10:575–588CrossRefGoogle Scholar
  28. Kulmatiski A, Kardol P (2008) Getting plant-soil feedbacks out of the greenhouse: experimental and conceptual approaches. In: Lüttge U, Beyschlag W, Murata J (eds) Progress in botany 69. Springer, Heidelberg, pp 449–472. doi:10.1007/978-3-540-72954-9_18
  29. Kulmatiski A, Beard KH, Stevens JR, Cobbold SM (2008) Plant-soil feedbacks: a meta-analytic review. Ecol Lett 11:980–992. doi:10.1111/j.1461-0248.2008.01209.x CrossRefPubMedGoogle Scholar
  30. Kulmatiski A, Heavilin J, Beard KH (2011) Testing predictions of a three-species plant-soil feedback model. J Ecol 99:542–550. doi:10.1111/j.1365-2745.2010.01784.x Google Scholar
  31. 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 466:752–755. doi:10.1038/nature09273 CrossRefPubMedGoogle Scholar
  32. McConnaughay KDM, Berntson GM, Bazzaz FA (1993) Limitations to CO2-induced growth enhancement in pot studies. Oecologia 94:550–557. doi:10.1007/BF00566971 CrossRefGoogle Scholar
  33. Mokany K, Raison RJ, Prokushkin AS (2006) Critical analysis of root:shoot ratios in terrestrial biomes. Glob Change Biol 12:84–96. doi:10.1111/j.1365-2486.2005.001043.x CrossRefGoogle Scholar
  34. Morris WF, Hufbauer RA, Agrawal AA, Bever JD, Borowitz VA, Gilbert GS, Maron JL, Mitchell CE, Parker IM, Power AG, Torchin ME, Vàzquez DP (2007) Direct and interactive effects of enemies and mutualists on plant performance: a meta-analysis. Ecology 88:1021–1029. doi:10.1890/06-0442 CrossRefPubMedGoogle Scholar
  35. Müller KE, Tilman D, Fornara DA, Hobbie SE (2013) Root depth distribution and the diversity–productivity relationship in a long-term grassland experiment. Ecology 94:787–793. doi:10.1890/12-1399.1 CrossRefGoogle Scholar
  36. Mwangi PN, Schmitz M, Scherber C, Roscher C, Schumacher J, Scherer-Lorenzen M, Weisser WW, Schmid B (2007) Niche pre-emption increases with species richness in experimental plant communities. J Ecol 95:65–78. doi:10.1111/j.1365-2745.2006.01189.x CrossRefGoogle Scholar
  37. Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA Circular 939:1–19. Government Printing Office, Washington, DCGoogle Scholar
  38. Peltzer DA (2001) Plant responses to competition and soil origin across a prairie–forest boundary. J Ecol 89:176–185. doi:10.1046/j.1365-2745.2001.00544.x CrossRefGoogle Scholar
  39. Petermann JS, Fergus AJF, Turnbull LA, Schmid B (2008) Janzen–Connell effects are widespread and strong enough to maintain diversity in grasslands. Ecology 89:2399–2406. doi:10.1890/07-2056.1 CrossRefPubMedGoogle Scholar
  40. Pizano C, Mangan SC, Graham JH, Kitajima K (2014) Habitat-specific positive and negative effects of soil biota on seedling growth in a fragmented tropical montane landscape. Oikos 123:846–856. doi:10.1111/oik.01032 CrossRefGoogle Scholar
  41. Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol 193:30–50. doi:10.1111/j.1469-8137.2011.03952.x CrossRefPubMedGoogle Scholar
  42. R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  43. Reinhart KO (2012) The organization of plant communities: negative plant-soil feedbacks and semiarid grasslands. Ecology 93:2377–2385. doi:10.1890/12-0486.1 CrossRefPubMedGoogle Scholar
  44. Rottstock T, Joshi J, Kummer V, Fischer M (2014) Higher plant diversity promotes higher diversity of fungal pathogens, while it decreases pathogen infection per plant. Ecology 95:1907–1917. doi:10.1890/13-2317.1 CrossRefPubMedGoogle Scholar
  45. Solaiman MZ, Hirata H (1997) Effect of arbuscular mycorrhizal fungi inoculation of rice seedlings at the nursery stage upon performance in the paddy field and greenhouse. Plant Soil 191:1–12. doi:10.1023/A:1004238028617 CrossRefGoogle Scholar
  46. Soliveres S, Maestre FT, Ulbrich W, Manning P, Boch S, Bowker MA, Prati D, Delgado-Baquerizo M, Quero JL, Schöning I, Gallardo A, Weisser W, Müller J, Socher SA, García-Gómez M, Ochoa V, Schulze ED, Fischer M, Allen E (2015) Intransitive competition is widespread in plant communities and maintains their species richness. Ecol Lett 18:790–798. doi:10.1111/ele.12456 CrossRefPubMedGoogle Scholar
  47. 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 99:945–953. doi:10.1111/j.1365-2745.2011.01815 CrossRefGoogle Scholar
  48. van der Putten WH, Kowalchuk GA, Brinkman EP, Doodeman GTA, van der Kaaij RM, Kamp AFD, Menting FBJ, Veenendaal EM (2007) Soil feedback of exotic savanna grass relates to pathogen absence and mycorrhizal selectivity. Ecology 88:978–988. doi:10.1890/06-1051 CrossRefPubMedGoogle Scholar
  49. 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, the present and future challenges. J Ecol 101:265–276. doi:10.1111/1365-2745.12054 CrossRefGoogle Scholar
  50. Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633. doi:10.1126/science.1094875 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Johannes Heinze
    • 1
    • 2
  • M. Sitte
    • 1
  • A. Schindhelm
    • 1
    • 3
  • J. Wright
    • 4
  • J. Joshi
    • 1
    • 2
  1. 1.Institute for Biochemistry and Biology, Biodiversity Research/BotanyUniversity of PotsdamPotsdamGermany
  2. 2.Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB)BerlinGermany
  3. 3.Institute of BiologyFreie Universität BerlinBerlinGermany
  4. 4.Biology DepartmentDuke UniversityDurhamUSA

Personalised recommendations