Abstract
Mycorrhizal fungi influence plant nutrition and therefore likely modify competition between plants. By affecting mycorrhiza formation and nutrient availability of plants, Collembola may influence competitive interactions of plant roots. We investigated the effect of Collembola (Protaphorura fimata Gisin), a mycorrhizal fungus (Glomus intraradices Schenck and Smith), and their interaction on plant growth and root structure of two plant species, Lolium perenne L. (perennial ryegrass) and Trifolium repens L. (white clover). In a laboratory experiment, two individuals of each plant species were grown either in monoculture or in competition to the respective other plant species. Overall, L. perenne built up more biomass than T. repens. The clover competed poorly with grass, whereas the L. perenne grew less in presence of conspecifics. In particular, presence of conspecifics in the grass and presence of grass in clover reduced shoot and root biomass, root length, number of root tips, and root volume. Collembola reduced shoot biomass in L. perenne, enhanced root length and number of root tips, but reduced root diameter and volume. The effects of Collembola on T. repens were less pronounced, but Collembola enhanced root length and number of root tips. In contrast to our hypothesis, changes in plant biomass and root structure in the presence of Collembola were not associated with a reduction in mycorrhizal formation. Presumably, Collembola affected root structure via changes in the amount of nutrients available and their spatial distribution.
Similar content being viewed by others
References
Aerts R (1999) Interspecific competition in natural plant communities: mechanisms, trade-offs and plant-soil feedbacks. J Exp Bot 50:29–37
Bakonyi G, Posta K, Kiss I, Fabian M, Nagy P, Nosek JN (2002) Density-dependent regulation of arbuscular mycorrhiza by Collembola. Soil Biol Biochem 34:661–664
Bardgett RD, Chan KF (1999) Experimental evidence that soil fauna enhance nutrient mineralization and plant nutrient uptake in montane grassland ecosystems. Soil Biol Biochem 31:1007–1014
Blanke V, Renker C, Wagner M, Fullner K, Held M, Kuhn A J, Buscot F (2005) Nitrogen supply affects arbuscular mycorrhizal colonization of Artemisia vulgaris in a phosphate-polluted field site. New Phytol 166:981–992
Cole L, Staddon PL, Sleep D, Bardgett RD (2004) Soil animals influence microbial abundance, but not plant- microbial competition for soil organic nitrogen. Funct Ecol 18:631–640
Cragg RG, Bardgett RD (2001) How changes in soil faunal diversity and composition within a trophic group influence decomposition processes. Soil Biol Biochem 33:2073–2081
Ek H, Sjögren M, Arnebrant K, Söderström B (1994) Extramatrical mycelial growth, biomass allocation and nitrogen uptake in ectomycorrhizal systems in response to collembolan grazing. Appl Soil Ecol 1:155–169
Endlweber K, Scheu S (2006) Effects of Collembola on root properties of two competing ruderal plant species. Soil Biol Biochem 38: 2025–2031
Filser J (2002) The role of Collembola in carbon and nitrogen cycling in soil. Pedobiologia 46:234–245
Gange A (2000) Arbuscular mycorrhizal fungi, Collembola and plant growth. Trends Ecol Evol 15:369–372
Gersani M, Abramsky Z, Falik O (1998) Density-dependent habitat selection in plants. Evol Ecol 12:223–234
Gersani M, Brown JS, O’Brien EE, Maina GM, Abramsky Z (2001) Tragedy of the commons as a result of root competition. J Ecol 89:660–669
Giovannetti M, Mosse B (1980) Evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500
Hamel C, Furlan V, Smith DL (1992) Mycorrhizal effects on interspecific plant competition and nitrogen transfer in legume grass mixtures. Crop Sci 32:991–996
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
Harrison MJ (1997) The arbuscular mycorrhizal symbiosis: an underground association. Trends Plant Sci 2:54–60
Hawkins HJ, George E (2001) Reduced N-15-nitrogen transport through arbuscular mycorrhizal hyphae to Triticum aestivum L. supplied with ammonium vs. nitrate nutrition. Ann Bot (London) 87:303–311
Hawkins HJ, Johansen A, George E (2000) Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant Soil 226:275–285
Hodge A, Robinson D, Griffiths BS, Fitter AH (1999) Why plants bother: root proliferation results in increased nitrogen capture from an organic patch when two grasses compete. Plant Cell Environ 22:811–820
Huber-Sannwald E, Pyke DA, Caldwell MM (1996) Morphological plasticity following species-specific recognition and competition in two perennial grasses. Am J Bot 83:919–931
Javelle A, Chalot M, Soderstrom B, Botton B (1999) Ammonium and methylamine transport by the ectomycorrhizal fungus Paxillus involutus and ectomycorrhizas. FEMS Microbiol Ecol 30:355–366
Joner EJ, Leyval C (2001) Influence of arbuscular mycorrhiza on clover and ryegrass grown together in a soil spiked with polycyclic aromatic hydrocarbons. Mycorrhiza 10:155–159
Kaiser PA, Lussenhop J (1991) Collembolan effects on establishment of vesicular–arbuscular mycorrhizae in soybean (Glycine max). Soil Biol Biochem 23:307–308
Kandeler E, Kampichler C, Joergensen RG, Molter K (1999) Effects of mesofauna in a spruce forest on soil microbial communities and N cycling in field mesocosms. Soil Biol Biochem 31:1783–1792
Keeney DR, Nelson DW (1982) Nitrogen—inorganic forms. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis. Part 2—chemical and microbiological properties, 2nd edn. American Society of Agronomy, Soil Science Society of America, Madison, Wisconsin, USA, pp 643–698
Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301
Klironomos JN, Ursic M (1998) Density-dependent grazing on the extraradical hyphal network of the arbuscular mycorrhizal fungus, Glomus intraradices, by the collembolan, Folsomia candida. Biol Fertil Soils 26:250–253
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
Lodge GM (2000) Competition among seedlings of perennial grasses, subterranean clover, white clover and annual ryegrass in replacement series mixtures. Aust J Agric Res 51:377–383
Lucero DW, Grieu P, Guckert A (1999) Effects of water deficit and plant interaction on morphological growth parameters and yield of white clover (Trifolium repens L.) and ryegrass (Lolium perenne L.) mixtures. Eur J Agron 11:167–177
Lussenhop J (1992) Mechanisms of microarthropod microbial interactions in soil. Adv Ecol Res 23:1–33
Lussenhop J (1993) Effects of two Collembola species on nodule occupancy by two Bradyrhizobium japonicum strains. Soil Biol Biochem 25:775–780
Lussenhop J (1996) Collembola as mediators of microbial symbiont effects upon soybean. Soil Biol Biochem 28:363–369
Lussenhop J, Bassirirad H (2005) Collembola effects on plant mass and nitrogen acquisition by ash seedlings (Fraxinus pennsylvanica). Soil Biol Biochem 37:645–650
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
Mantelin S, Touraine B (2004) Plant growth-promoting bacteria and nitrate availability: impacts on root development and nitrate uptake. J Exp Bot 55:27–34
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
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
Munoz AE, Weaver RW (1999) Competition between subterranean clover and ryegrass for uptake of N-15-labeled fertilizer. Plant Soil 211:173–178
O’Brien EE, Gersani M, Brown JS (2005) Root proliferation and seed yield in response to spatial heterogeneity of below-ground competition. New Phytol 168:401–412
Olsen SR, Sommers LE (1982) Phosphorus. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis. Part 2—chemical and microbiological properties, 2nd edn. American Society of Agronomy, Soil Science Society of America, Madison, Wisconsin, USA, pp 403–430
Partsch S, Milcu A, Scheu S (2006) The role of decomposer animals (Lumbricidae, Collembola) for plant performance in model grassland systems of different diversity. Ecology (in press)
Petersen H (2000) Collembola populations in an organic crop rotation: population dynamics and metabolism after conversion from clover–grass ley to spring barley. Pedobiologia 44:502–515
Rajaniemi TK, Reynolds HL (2004) Root foraging for patchy resources in eight herbaceous plant species. Oecologia 141:519–525
Rogers JB, Laidlaw AS, Christie P (2001) The role of arbuscular mycorrhizal fungi in the transfer of nutrients between white clover and perennial ryegrass. Chemosphere 42:153–159
Rubio G, Walk T, Ge ZY, Yan XL, Liao H, Lynch JP (2001) Root gravitropism and below-ground competition among neighbouring plants: a modelling approach. Ann Bot (London) 88:929–940
Sabatini MA, Innocenti G (2000) Functional relationships between Collembola and plant pathogenic fungi of agricultural soils. Pedobiologia 44:467–475
Salamon JA, Schaefer M, Alphei J, Schmid B, Scheu S (2004) Effects of plant diversity on Collembola in an experimental grassland ecosystem. Oikos 106:51–60
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
Schreiner RP, Bethlenfalvay GJ (2003) Crop residue and Collembola interact to determine the growth of mycorrhizal pea plants. Biol Fertil Soils 39:1–8
Sjursen H, Holmstrup M (2004) Direct measurement of ammonium excretion in soil microarthropods. Funct Ecol 18:612–615
Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, London
Smith MD, Hartnett DC, Wilson GWT (1999) Interacting influence of mycorrhizal symbiosis and competition on plant diversity in tallgrass prairie. Oecologia 121:574–582
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
Sung K, Kim J, Munster CL, Corapcioglu MY, Park S, Drew MC, Chang YY (2006) A simple approach to modelling microbial biomass in the rhizosphere. Ecol Model 190:227–286
Theenhaus A, Scheu S, Schaefer M (1999) Contramensal interactions between two collembolan species: effects on population development and on soil processes. Funct Ecol 13:238–246
Tiunov AV, Scheu S (2005) Arbuscular mycorrhiza and Collembola interact in affecting community composition of saprotrophic microfungi. Oecologia 142:636–642
Van Der Heijden MGA (2004) Arbuscular mycorrhizal fungi as support systems for seedling establishment in grassland. Ecol Lett 7:293–303
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
Visser S, Parkinson D, Hassal M (1987) Fungi associated with Onychiurus subtenius (Collembola) in an aspen woodland. Can J Bot 65:635–642
Zhang HM, Forde BG (2000) Regulation of Arabidopsis root development by nitrate availability. J Exp Bot 51:51–59
Acknowledgments
We thank the UFZ Leipzig-Halle for providing the soil. Special thanks are given to Katja Domes for her help during the experiment. We acknowledge the financial support by the German Science Foundation (DFG).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Endlweber, K., Scheu, S. Interactions between mycorrhizal fungi and Collembola: effects on root structure of competing plant species. Biol Fertil Soils 43, 741–749 (2007). https://doi.org/10.1007/s00374-006-0157-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-006-0157-7