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Oecologia

, Volume 174, Issue 2, pp 471–478 | Cite as

Radish introduction affects soil biota and has a positive impact on the growth of a native plant

Plant-microbe-animal interactions - Original research

Abstract

Introduced plants may out-compete natives by belowground allelopathic effects on soil communities including the symbionts of native plants. We tested for an allelopathic effect of an introduced crucifer, Raphanus sativus, on a common neighboring legume, Lupinus nanus, on the legume’s rhizobium affiliates, and on the broader soil community. In both field observations and a greenhouse experiment, we found that R. sativus decreased the density of nodules on L. nanus roots. However, in the greenhouse experiment, R. sativus soils only decreased the density of small, likely non-beneficial rhizobium nodules. In the same experiment, R. sativus soils decreased fungivorous nematode abundance, though there was no effect of R. sativus introduction on fungal density. In the greenhouse experiment, R. sativus soils had a net positive effect on L. nanus biomass. One explanation of this effect is that R. sativus introduction might alter the mutualistic/parasitic relationship between L. nanus and its rhizobial associates with a net benefit to L. nanus. Our results suggest that introduced brassicas can quickly alter belowground communities, but that the net effect of this on neighboring plants is not necessarily negative.

Keywords

Facilitation Allelopathy Indirect interaction Soil biota Belowground food web 

Notes

Acknowledgments

We would like to thank Jackie Sones and the Bodega Marine Reserve for help in the field as well as University of California, Davis greenhouse staff for greenhouse support. Rick Lankau provided useful discussion of allelopathy and brassicas at an early stage of this project. Ellen Simms, Stephanie Porter, and Allison Berry provided useful discussion on rhizobium-plant interactions. The manuscript was substantially improved after review by Rick Karban, Amanda Hodson, and Taraneh Emam. I. S. P. was funded by a National Science Foundation-Graduate Research Fellowship Program grant during the course of this study. The experiments comply with the current laws of the United States.

Supplementary material

442_2013_2779_MOESM1_ESM.doc (1.3 mb)
Supplementary material 1 (DOC 1306 kb)

References

  1. Barbour MG, Craig RB, Drysdale FR, Ghiselin MT (1973) Coastal ecology-Bodega Head. University of California Press, BerkeleyGoogle Scholar
  2. Bever JD (2002) Negative feedback within a mutualism: host-specific growth of mycorrhizal fungi reduces plant benefit. Proc R Soc Lond Ser B-Biol Sci 269:2595–2601CrossRefGoogle Scholar
  3. Bolan NS (1991) A critical review on the role of mycorrhizal fungi in the uptake of phosphorus by plants. Plant Soil 134:189–207CrossRefGoogle Scholar
  4. Caldwell MM, Dawson TE, Richards JH (1998) Hydraulic lift: consequences of water efflux from the roots of plants. Oecologia 113:151–161CrossRefGoogle Scholar
  5. Callaway RM (1995) Positive interactions among plants. Bot Rev 61:306–349CrossRefGoogle Scholar
  6. Callaway RM, Walker LR (1997) Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78:1958–1965CrossRefGoogle Scholar
  7. Callaway RM, Nadkarni NM, Mahall BE (1991) Facilitation and interference of Quercus douglasii on understory productivity in central California. Ecology 72:1484–1499CrossRefGoogle Scholar
  8. Callaway RM et al (2008) Novel weapons: invasive plant suppresses fungal mutualists in America but not in its native Europe. Ecology 89:1043–1055PubMedCrossRefGoogle Scholar
  9. Denison RF (2000) Legume sanctions and the evolution of symbiotic cooperation by rhizobia. Am Nat 156:567–576CrossRefGoogle Scholar
  10. Denison RF, Kiers ET (2004) Lifestyle alternatives for rhizobia: mutualism, parasitism, and forgoing symbiosis. FEMS Microbiol Lett 237:187–193PubMedCrossRefGoogle Scholar
  11. Ehlers BK, Grondahl E, Ronfort J, Bataillon T (2012) “Menage a trois”: the presence/absence of thyme shapes the mutualistic interaction between the host plant Medicago truncatula (Fabaceae) and its symbiotic bacterium Sinorhizobium meliloti. Ecol Evol 2:1676–1681PubMedCentralPubMedCrossRefGoogle Scholar
  12. Ferris H, Matute MM (2003) Structural and functional succession in the nematode fauna of a soil food web. Appl Soil Ecol 23:93–110CrossRefGoogle Scholar
  13. Halkier BA, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57:303–333PubMedCrossRefGoogle Scholar
  14. Hanssen JF, Thingsta Tf, Goksoyr J (1974) Evaluation of hyphal lengths and fungal biomass in soil by a membrane-filter technique. Oikos 25:102–107CrossRefGoogle Scholar
  15. Haramoto ER, Gallandt ER (2004) Brassica cover cropping for weed management: a review. Renew Agric Food Syst 19:187–194CrossRefGoogle Scholar
  16. Hardarson G, Zapata F, Danso SKA (1984) Effect of plant genotype and nitrogen fertilizer on symbiotic nitrogen fixation by soybean cultivars. Plant Soil 82:397–405CrossRefGoogle Scholar
  17. Hierro JL, Callaway RM (2003) Allelopathy and exotic plant invasion. Plant Soil 256:29–39CrossRefGoogle Scholar
  18. Hirrel MC, Mehravaran H, Gerdemann JW (1978) Vesicular-arbuscular mycorrhizae in Chenopodiaceae and Cruciferae—do they occur? Can J Bot-Rev Can Bot 56:2813–2817Google Scholar
  19. Jaffee BA, Bastow JL, Strong DR (2007) Suppression of nematodes in a coastal grassland soil. Biol Fertil Soils 44:19–26CrossRefGoogle Scholar
  20. Kabouw P, van der Putten WH, van Dam NM, Biere A (2010) Effects of intraspecific variation in white cabbage (Brassica oleracea var. capitata) on soil organisms. Plant Soil 336:509–518CrossRefGoogle Scholar
  21. Lankau R (2010) Soil microbial communities alter allelopathic competition between Alliaria petiolata and a native species. Biol Invasions 12:2059–2068CrossRefGoogle Scholar
  22. Lankau RA, Wheeler E, Bennett AE, Strauss SY (2010) Plant-soil feedbacks contribute to an intransitive competitive network that promotes both genetic and species diversity. J Ecol 99:176–185CrossRefGoogle Scholar
  23. Maraun M, Martens H, Migge S, Theenhaus A, Scheu S (2003) Adding to ‘the enigma of soil animal diversity’: fungal feeders and saprophagous soil invertebrates prefer similar food substrates. Eur J Soil Biol 39:85–95CrossRefGoogle Scholar
  24. Maron JL, Connors PG (1996) A native nitrogen-fixing shrub facilitates weed invasion. Oecologia 105:302–312CrossRefGoogle Scholar
  25. Marvier MA (1998) Parasite impacts on host communities: plant parasitism in a California coastal prairie. Ecology 79:2616–2623Google Scholar
  26. Mitchell RJ (2001) Path analysis: pollination. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments, 2nd edn. Oxford University Press, OxfordGoogle Scholar
  27. O’Connell T, Bolger T (1998) Intraspecific aggregation ‘probability niches’ and the diversity of soil microarthropod assemblages. Appl Soil Ecol 9:63–67CrossRefGoogle Scholar
  28. Panetsos CA, Baker HG (1968) Origin of variation in wild Raphanus sativus (Cruciferae) in California. Genetica 38:243–274CrossRefGoogle Scholar
  29. Pinheiro J, Bates D, DebRoy S, Sarkar D, The R Core Development Team (2009) nlme: Linear and nonlinear mixed effects models. R package version 3.1–93Google Scholar
  30. Porter SS, Rice KJ (2013) Trade-offs, spatial heterogeneity, and the maintenance of microbial diversity. Evolution 67:599–608PubMedCrossRefGoogle Scholar
  31. R Core Development Team (2008) R v. 2.10.1. The R FoundationGoogle Scholar
  32. Ridley CE, Ellstrand NC (2009) Evolution of enhanced reproduction in the hybrid-derived invasive, California wild radish (Raphanus sativus). Biol Invasions 11:2251–2264CrossRefGoogle Scholar
  33. Sachs JL, Simms EL (2008) The origins of uncooperative rhizobia. Oikos 117:961–966CrossRefGoogle Scholar
  34. Sanon A et al (2009) Changes in soil diversity and global activities following invasions of the exotic invasive plant, Amaranthus viridis L., decrease the growth of native sahelian Acacia species. FEMS Microbiol Ecol 70:118–131PubMedCrossRefGoogle Scholar
  35. Simms EL, Taylor DL (2002) Partner choice in nitrogen-fixation mutualisms of legumes and rhizobia. Integr Comp Biol 42:369–380PubMedCrossRefGoogle Scholar
  36. Simms EL et al (2006) An empirical test of partner choice mechanisms in a wild legume-rhizobium interaction. Proc R Soc B-Biol Sci 273:77–81Google Scholar
  37. Stinson KA et al (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol 4:727–731CrossRefGoogle Scholar
  38. van der Beek JG, Poleij LM, Zijlstra C, Janssen R, Janssen GJW (1998) Variation in virulence within Meloidogyne chitwoodi, M. fallax, and M. hapla on Solanum spp. Phytopathology 88:658–665PubMedCrossRefGoogle Scholar
  39. 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
  40. Wardle DA, Yeates GW (1993) The dual importance of competition and predation as regulatory forces in terrestrial—ecosystems evidence from decomposer food-webs. Oecologia 93:303–306CrossRefGoogle Scholar
  41. West AW (1988) Specimen preparation, stain type, and extraction and observation procedures as factors in the estimation of soil mycelial lengths and volumes by light microscopy. Biol Fertil Soils 7:88–94CrossRefGoogle Scholar
  42. Williamson VM, Hussey RS (1996) Nematode pathogenesis and resistance in plants. Plant Cell 8:1735–1745PubMedCentralPubMedGoogle Scholar
  43. Yeates GW, Bongers T, Degoede RGM, Freckman DW, Georgieva SS (1993) Feeding habits in soil nematode families and genera—an outline for soil ecologists. J Nematol 25:315–331PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Ian S. Pearse
    • 1
    • 2
  • Justin L. Bastow
    • 3
  • Alia Tsang
    • 1
  1. 1.Department of EntomologyUniversity of California, DavisDavisUSA
  2. 2.Laboratory of OrnithologyCornell UniversityIthacaUSA
  3. 3.Department of BiologyEastern Washington UniversityCheneyUSA

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