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Soil organisms shape the competition between grassland plant species

  • Plant-animal interactions - Original research
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Abstract

Decomposers and arbuscular mycorrhizal fungi (AMF) both determine plant nutrition; however, little is known about their interactive effects on plant communities. We set up a greenhouse experiment to study effects of plant competition (one- and two-species treatments), Collembola (Heteromurus nitidus and Protaphorura armata), and AMF (Glomus intraradices) on the performance (above- and belowground productivity and nutrient uptake) of three grassland plant species (Lolium perenne, Trifolium pratense, and Plantago lanceolata) belonging to three dominant plant functional groups (grasses, legumes, and herbs). Generally, L. perenne benefited from being released from intraspecific competition in the presence of T. pratense and P. lanceolata. However, the presence of AMF increased the competitive strength of P. lanceolata and T. pratense against L. perenne and also modified the effects of Collembola on plant productivity. The colonization of roots by AMF was reduced in treatments with two plant species suggesting that plant infection by AMF was modified by interspecific plant interactions. Collembola did not affect total colonization of roots by AMF, but increased the number of mycorrhizal vesicles in P. lanceolata. AMF and Collembola both enhanced the amount of N and P in plant shoot tissue, but impacts of Collembola were less pronounced in the presence of AMF. Overall, the results suggest that, by differentially affecting the nutrient acquisition and performance of plant species, AMF and Collembola interactively modify plant competition and shape the composition of grassland plant communities. The results suggest that mechanisms shaping plant community composition can only be understood when complex belowground interactions are considered.

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References

  • Aerts R (1999) Interspecific competition in natural plant communities: mechanisms, trade-offs and plant-soil feedbacks. J Exp Bot 50:29–37

    CAS  Google Scholar 

  • Ambler J, Young J (1977) Techniques for determining root length infected by vesicular-arbuscular mycorrhizae. Soil Sci Soc Am J 41:551–556

    Article  Google Scholar 

  • Baar J, Stanton NL (2000) Ectomycorrhizal fungi challenged by saprotrophic basidiomycetes and soil microfungi under different ammonium regimes in vitro. Mycol Res 104:691–697

    Article  Google Scholar 

  • Bardgett RD, Whittaker JB, Frankland JC (1993) The effect of collembolan grazing on fungal activity in differently managed upland pastures: a microcosm study. Biol Fertil Soils 16:255–262

    Article  Google Scholar 

  • Blanke V, Wagner M, Renker C, Lippert H, Michulitz M, Kuhn AJ, Buscot F (2011) Arbuscular mycorrhizas in phosphate polluted soil: interrelations between root colonization and nitrogen. Plant Soil 343:379–392

    Article  CAS  Google Scholar 

  • Cahill JF (1999) Fertilization effects on interactions between above- and belowground competition in an old field. Ecology 80:466–480

    Article  Google Scholar 

  • Chen X, Tu C, Burton MG, Watson DM, Burkley KO, Hu S (2007) Plant nitrogen acquisition and interactions under elevated carbon dioxide: impact of endophytes and mycorrhizae. Glob Change Biol 13:1238–1249

    Article  Google Scholar 

  • Coleman DC, Crossley DA Jr, Hendrix PF (2004) Fundamentals of Soil Ecology, 2nd edn. Elsevier, San Diego

    Google Scholar 

  • Curl EA, Lartey R, Teterson CM (1988) Interactions between root pathogens and soil microarthropods. Agric Ecosyst Environ 24:249–261

    Article  Google Scholar 

  • Eisenhauer N, Scheu S (2008) Earthworms drive the competition between grasses and legumes. Soil Biol Biochem 40:2650–2659

    Article  CAS  Google Scholar 

  • Eisenhauer N, Milcu A, Sabais ACW, Scheu S (2009a) Earthworms and belowground competition effects on plant productivity. Oecologia 161:291–301

    Article  PubMed  Google Scholar 

  • Eisenhauer N, König S, Sabais ACW, Renker C, Buscot F, Scheu S (2009b) Impacts of earthworms and arbuscular mycorrhizal fungi (Glomus intraradices) on plant performance are not interrelated. Soil Biol Biochem 41:561–567

    Article  CAS  Google Scholar 

  • Eisenhauer N, Beßler H, Engels C, Gleixner G, Habekost M, Milcu A, Partsch S, Sabais ACW, Scherber C, Steinbeiß S, Weigelt A, Weisser WW, Scheu S (2010) Plant diversity effects on soil microorganisms support the singular hypothesis. Ecology 91:485–496

    Article  PubMed  CAS  Google Scholar 

  • Eisenhauer N, Sabais ACW, Scheu S (2011) Collembola species composition and diversity affects on ecosystem functioning vary with plant functional group. Soil Biol Biochem 43:1697–1704

    Article  CAS  Google Scholar 

  • Endlweber K, Scheu S (2007) Interactions between mycorrhizal fungi and Collembola: effects on root structure of competing plant species. Biol Fertil Soils 43:741–749

    Article  Google Scholar 

  • Endlweber K, Ruess L, Scheu S (2009) Collembola switch diet in presence of plant roots thereby functioning as herbivores. Soil Biol Biochem 41:1151–1154

    Article  CAS  Google Scholar 

  • Finlay RD (1985) Interaction between soil micro-arthropods and endomycorrhizal associations of higher plants. In: Fitter AH (ed) Ecological interactions in soil. Blackwell, Oxford, pp 319–331

    Google Scholar 

  • Fitter AH, Sanders IR (1992) Interactions with the soil fauna. In: Allen MF (ed) Mycorrhizal-functioning, an integrative plant-fungal process. Chapman and Hall, New York, pp 333–354

    Google Scholar 

  • Gange AC (2000) Arbuscular mycorrhizal fungi, Collembola and plant growth. Trends Ecol Evol 15:369–372

    Article  PubMed  Google Scholar 

  • Gange AC, Ayres RL (1999) On the relation between arbuscular mycorrhizal colonization and plant ‘benefit’. Oikos 87:615–621

    Article  Google Scholar 

  • Gange AC, Bower E (1997) Interactions between insects and mycorrhizal fungi. In: Gange AC, Brown VK (eds) Multitrophic interactions in terrestrial systems. Blackwell, Oxford, pp 115–132

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Hawkins HJ, Johansen A, George E (2000) Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant Soil 226:275–285

    Article  CAS  Google Scholar 

  • Hiol FH, Dixon RK, Curl EA (1994) The feeding preference of mycophagous Collembola varies with the ectomycorrhizal symbiont. Mycorrhiza 5:99–103

    Article  Google Scholar 

  • Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GWT, Klironomos JN, Umbanhowar J (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407

    Article  PubMed  Google Scholar 

  • Hopkin SP (1997) Biology of the springtails-insecta: collembola. Oxford University Press, Oxford

    Google Scholar 

  • Hurej M, Debek J, Pomorski RJ (1992) Investigations on damage to sugar beet seedlings by the springtail Onychiurus armatus (Collembola, Onychiuridae) in Lower Silesia (Poland). Acta Entomol Bohemos 89:403–407

    Google Scholar 

  • Ineson P, Leonard MA, Anderson JM (1982) Effect of collembolan grazing upon nitrogen and cation leaching from decomposing leaf litter. Biol Biochem 14:601–605

    Article  Google Scholar 

  • Johnson NC (2010) Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol 185:631–647

    Article  PubMed  CAS  Google Scholar 

  • Kempel A, Schmidt AK, Brandl R, Schädler M (2010) Support from the underground: induced plant resistance depends on arbuscular mycorrhizal fungi. Funct Ecol 24:293–300

    Article  Google Scholar 

  • Klironomos JN, Moutoglis P (1999) Colonization of nonmycorrhizal plants by mycorrhizal neighbours as influenced by the collembolan, Folsomia candida. Biol Fertil Soils 29:277–281

    Article  Google Scholar 

  • Kreuzer K, Bonkowski M, Langel R, Scheu S (2004) Decomposer animals (Lumbricidae, Collembola) and organic matter distribution affect the performance of Lolium perenne (Poaceae) and Trifolium repens (Fabaceae). Soil Biol Biochem 36:2005–2011

    Article  CAS  Google Scholar 

  • Lodge GM (2000) Competition among seedlings of perennial grasses, subterranean clover, white clover and annual ryegrass in replacement series mixtures. Aust J Agr Res 51:377–383

    Article  Google Scholar 

  • Maina GG, Brown JS, Gersani M (2002) Intra-plant versus inter-plant root competition in beans: avoidance, resource matching or tragedy of the commons. Plant Ecol 160:235–247

    Article  Google Scholar 

  • Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159:89–102

    CAS  Google Scholar 

  • Milcu A, Partsch S, Langel R, Scheu S (2006) The response of decomposers (earthworms, springtails and microorganisms) to variations in species and functional group diversity of plants. Oikos 112:513–524

    Article  Google Scholar 

  • Moore JC, Ingham ER, Coleman DC (1987) Inter-and intraspecific feeding selectivity of Folsomia candida (Willem) (Collembola, Isotomidae) on fungi. Biol Fertil Soils 5:6–12

    Article  Google Scholar 

  • Munoz AE, Weaver RW (1999) Competition between subterranean clover and ryegrass for uptake of N-15-labeled fertilizer. Plant Soil 211:173–178

    Article  CAS  Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161

    Article  Google Scholar 

  • Pieper S, Weigmann G (2008) Interactions between isopods and collembolans modulate the mobilization and transport of nutrients from urban soils. Appl Soil Ecol 39:109–126

    Article  Google Scholar 

  • Reineking A, Langel R, Schikowski J (1993) 15N, 13C-online measurements with an elemental analyser (Carlo Erba, NA 1500), a modified trapping box and a gas isotope mass spectrometer (Finnigan, MAT 251). Isotopes Environ Health Stud 29:169–174

    Article  CAS  Google Scholar 

  • Roscher C, Schumacher J, Baade J, Wilcke W, Gleixner G, Weisser WW, Schmid B, Schulze E-D (2004) The role of biodiversity for element cycling and trophic interactions: an experimental approach in a grassland community. Basic Appl Ecol 5:107–121

    Article  Google Scholar 

  • Rusek J (1998) Biodiversity of Collembola and their functional role in the ecosystem. Biodivers Conserv 7:1207–1219

    Article  Google Scholar 

  • Scherber C, Mwangi P, Schmitz M, Scherer-Lorenzen M, Bessler H, Engels C, Eisenhauer N, Migunova V, Scheu S, Weisser WW, Schulze E-D, Schmid B (2010) Biodiversity and belowground interactions mediate community invasion resistance against a tall herb invader. J Plant Ecol 3:99–108

    Article  Google Scholar 

  • Scheu S, Theenhaus A, Jones TH (1999) Links between the detritivore and the herbivore system: effects of earthworms and Collembola on plant growth and aphid development. Oecologia 119:541–551

    Article  Google Scholar 

  • Scheublin TR, Van Logtestijn RSP, Van der Heijden MGA (2007) Presence and identity of arbuscular mycorrhizal fungi influence competitive interactions between plant species. J Ecol 95:631–638

    Article  CAS  Google Scholar 

  • Schmitz O, Danneberg G, Hundeshagen B, Klingner A, Bothe H (1991) Quantification of vesicular-arbuscular mycorrhiza by biochemical parameters. J Plant Physiol 139:106–114

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, London

    Google Scholar 

  • Stone MJ, Cralle HT, Chandler JM, Bovey RW, Carson KH (1998) Above- and belowground interference of wheat (Triticum aestivum) by Italian ryegrass (Lolium multiflorum). Weed Sci 46:438–441

    CAS  Google Scholar 

  • Tiunov AV, Scheu S (2005) Arbuscular mycorrhiza and Collembola interact in affecting community composition of saprotrophic microfungi. Oecologia 142:636–642

    Article  PubMed  Google Scholar 

  • Van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72

    Article  Google Scholar 

  • Van der Heijden MGA, Wiemken A, Sanders IR (2003) Different arbuscular mycorrhizal fungi alter coexistence and resource distribution between co-occurring plant. New Phytol 157:569–578

    Article  Google Scholar 

  • Vierheilig H, Piché Y (1998) A modified procedure for staining arbuscular mycorrhizal fungi in roots. J Plant Nutr Soil Sci 161:601–602

    Article  CAS  Google Scholar 

  • Wagg C, Stadler M, Schmid B, Van der Heijden MAG (2011) Mycorrhizal fungal identity and diversity relaxes plant–plant competition. Ecology 92:1030–1313

    Article  Google Scholar 

  • Warnock AJ, Fitter AH, Usher MB (1982) The influence of springtail Folsomia candida (Insecta, Collembola) on the mycorrhizal association of leek Allium porrum and the vesicular-arbuscular mycorrhizal endophyte Glomus fasciculatus. New Phytol 90:285–292

    Article  Google Scholar 

  • Weigelt A, Schumacher J, Walther T, Bartelheimer M, Steinlein T, Beyschlag W (2007) Identifying mechanisms of competition in multi-species communities. J Ecol 95:53–64

    Article  Google Scholar 

  • Wurst S, Dugassa-Gobena D, Langel R, Bonkowski M, Scheu S (2004) Combined effects of earthworms and vesicular-arbuscular mycorrhizas on plant and aphid performance. New Phytol 163:169–176

    Article  Google Scholar 

Download references

Acknowledgments

This work was funded by the Deutsche Forschungsgemeinschaft (FOR 456; The Jena Experiment). We thank all the people who helped to set up and maintain the experiment, in particular V. Eißfeller and C. M. U. Pusch for transplanting plant seedlings into the microcosms, and T. Volovei for watering of the experimental containers. Comments of two anonymous reviewers improved the manuscript. N. Eisenhauer is grateful for a postdoctoral scholarship by the Deutsche Forschungsgemeinschaft (Ei 862/1-1).

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  1. Nico Eisenhauer

    Present address: Technische Universität München, Department of Ecology and Ecosystem Management, Hans-Carl-von-Carlowitz-Platz 2, 85354, Freising, Germany

Authors and Affiliations

  1. Institute of Zoology, Darmstadt University of Technology, Schnittspahnstr. 3, 64287, Darmstadt, Germany

    Alexander C. W. Sabais

  2. Department of Forest Resources, University of Minnesota, 1530 Cleveland Ave. N., St. Paul, MN, 55108, USA

    Nico Eisenhauer

  3. Department of Soil Ecology, UFZ, Helmholtz Centre for Environmental Research, Theodor-Lieser-Straße 4, 06120, Halle, Germany

    Stephan König, Carsten Renker & François Buscot

  4. Natural History Museum Mainz, Reichklarastraße 10, 55116, Mainz, Germany

    Carsten Renker

  5. Institute of Biology, University of Leipzig, Johannis-Allee 21-23, 04103, Leipzig, Germany

    François Buscot

  6. J.F. Blumenbach Institute of Zoology and Anthropology, Georg August University Göttingen, Berliner Str. 28, 37073, Göttingen, Germany

    Stefan Scheu

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  1. Alexander C. W. Sabais
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Correspondence to Nico Eisenhauer.

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Communicated by Diethart Matthies.

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Sabais, A.C.W., Eisenhauer, N., König, S. et al. Soil organisms shape the competition between grassland plant species. Oecologia 170, 1021–1032 (2012). https://doi.org/10.1007/s00442-012-2375-z

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