Responses of Collembola and Protura to tree girdling – some support for ectomycorrhizal feeding
Keywords:
ectomycorrhiza, food-choice, microarthropods, mycorrhizal fungi, field experimentAbstract
Ectomycorrhizal (EM) fungi are very common in forest soils, but their role as a food resource for fungivorous soil animals is poorly known. We used two tree-girdling experiments in Picea abies forests and one experiment in a Pinus sylvestris forest, all in northern Sweden, to indirectly test if Collembola and Protura in boreal forest soils prefer EM fungi over other fungi. We assumed that tree girdling will stop the flux of carbohydrates to roots and associated fungi, and thereby inhibit growth and long-term survival of EM fungi. After about one year, proturans decreased in abundance after girdling, indicating that they prefer feeding on EM fungi, while most collembolan species seemed to be unaffected by girdling and the presumed reduction in EM fungi. However, the collembolans Mesaphorura macrochaeta, Anurida granaria and Parisotoma notabilis increased in abundance after girdling in one of the three experiments, and Micranurida pygmaea decreased. With the exception of the latter species, this is in accordance with the common opinion that most Collembola prefer saprotrophic fungi over EM fungi, while Protura are at least partly dependent on EM fungi.
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Albers, D., M. Schaefer, & S. Scheu (2006): Incorporation of plant carbon into the soil animal food web of an arable system. – Ecology 87: 235-245.
Bhupinderpal-Singh, A. Nordgren, M. Ottosson-Löfvenius, M. N. Högberg, P.-E. Mellander, P. Högberg (2003): Tree root and soil heterotrophic respiration as revealed by girdling of boreal Scots pine forest: extending observations beyond the first year. – Plant, Cell and Environment 26: 1287–1296.
Bonkowski, M., C. Villenave & B. Griffiths (2009): Rhizosphere fauna: the functional and structural diversity of intimate interactions of soil fauna with plant roots. – Plant Soil 321: 213–233.
Copeland, T. P. & G. Imadaté (1990): Insecta: Protura. In: Dindal, D. L. (Ed.) Soil Biology Guide, pp. 911–933. John Wiley & Sons, New York.
Fjellberg, A. (1980): Identification keys to Norwegian Collembola. – Norsk Entomologisk Förening, Ås, Norway, 152 pp.
Fjellberg, A. (1998): The Collembola of Fennoscandia and Denmark. Part 1: Poduromorpha. – Fauna Entomologica Scandinavica 35: 1–184.
Fjellberg, A. (2007): The Collembola of Fennoscandia and Denmark. Part 1I: Entomobryomorpha and Symphypleona. – Fauna Entomologica Scandinavica 42: 1–264.
Göttlicher, S. G., A. S. F. Taylor, H. Grip, N. R. Betson, E. Valinger, E. & M. N. Högberg (2008): The later spread of tree root systems in boreal forests: estimates based on 15N uptake and distribution of sporocarps of ectomycorrhizal fungi. – Forest Ecology and Management 255: 75–81.
Gunn,A. & J. M. Cherrett (1993): The exploitation of food resources by soil meso- and macroinvertebrates. – Pedobiologia 37: 303–320.
Hiol Hiol, F., R. K. Dixon & E. A. Curl (1994): The feeding preference of mycophagous Collembola varies with the ectomycorrhizal symbiont. – Mycorrhiza 5: 99–103.
Högberg, M. N. & P. Högberg (2002): Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil. – New Phytologist 154: 791–795.
Högberg, P., A. Nordgren, N. Buchmann, A. F. S. Taylor, A. Ekblad, M. N. Högberg, G. Nyberg, M. Ottosson-Löfvenius & D. J. Read (2001): Large-scale forest girdling shows that current photosynthesis drives soil respiration. – Nature 411: 789–792.
Högberg, P., Bhupinderpal-Singh, M. Ottosson-Löfvenius & A. Nordgren (2009): Partitioning of soil respiration into its autotrophic and heterotrophic components by means of tree-girdling in old boreal spruce forest. – Forest Ecology and Management 257: 1764–1767.
Klironomos, J. N. & W. B. Kendrick (1996): Palatability of microfungi to soil arthropods in relation to the functioning of arbuscular mycorrhizae. – Biology and Fertility of Soils 21: 43–52.
Klironomos, J. N. & M. Ursic (1998): Density-dependent grazing on the extra-radical hyphal network of the arbuscular mycorrhizal fungus, Glomus intraradices, by the collembolan, Folsomia candida. – Biology and Fertility of Soils 26: 250–253.
Krauss, J. & W. Funke (1999): Extraordinary high density of Protura in a windfall area of young spruce plants. Pedobiologia 43: 44–46.
Larsen, J. & I. Jakobsen (1996): Interactions between a mycophagous Collembola, dry yeast and the external mycelium of an arbuscular mycorrhizal fungus. – Mycorrhiza 6: 259–264.
Leonard, M. A. (1984): Observations on the influence of culture conditions of the fungal feeding preferences of Folsomia candida (Collembola: Isotomidae). – Pedobiologia 26: 361–367.
Malmström, A., T. Persson, J. Bengtsson, K. Gongalsky & K. Ahlström (2009): Dynamics of soil meso- and macrofauna during a 5-year period after clear-cut burning in a boreal forest. – Applied Soil Ecology 43: 61–74.
Maraun, M., H. Martens, S. Migge, A. Theenhaus & S. Scheu (2003): Adding to ‘the enigma of soil animal diversity’: fungal feeders and saprophagous soil invertebrates prefer similar food substrates. – European Journal of Soil Biology 39: 85–95.
Nosek, J. (1977): Proturan synusies and niche separation in the soil. – Ecological Bullentins 25: 138–142. Nosek, J. (1978): Key and diagnoses of proturan genera of the world. Annotationes Zoologicae et Botanicae 122: 1–59.
Olsson, P., S. Linder, R. Giesler & P. Högberg (2005): Fertilization of boreal forest reduces both autotrophic and heterotrophic soil respiration. – Global Change Biology 11: 1745–1753.
Pollierer, M. M., R. Langel, C. Körner, M. Maraun & S. Scheu (2007): The underestimated importance of belowground carbon input for forest soil animal food webs. – Ecology Letters 10: 729–736.
Ponge, J.-F. (2000): Vertical distribution of Collembola (Hexapoda) and their food resources in organic horizons of beech forests. – Biology and Fertility of Soils 32: 508–522.
Remén, C., T. Persson, R. Finlay & K. Ahlström (2008): Responses of oribatid mites to tree girdling and nutrient addition in boreal coniferous forests. – Soil Biology and Biochemistry 40: 2881–2890.
Remén, C., P. Fransson & T. Persson (2010): Population responses of oribatids and enchytraeids to plant- soil microcosms. – Soil Biology and Biochemistry 42: 978–985.
Sadaka-Laulan, N., J.-F. Ponge, M.-F. Roquebert, E. Bury & A. Boumezzough (1998): Feeding preferences of the collembolan Onychiurus sinensis for fungal colonizing holm oak litter (Quercus rotundifolia Lam.). – European Journal of Soil Biology 34: 179–188.
Schneider, K., C. Renker & M. Maraun (2005): Oribatid mite (Acari, Oribatida) feeding on ectomycorrhizal fungi. – Mycorrhiza 16: 67–72.
Smith, S. E. & D. J. Read (1997): Mycorrhizal Symbioses, 2nd edn. – Academic Press, San Diego, 605 pp.
Sturm, H. (1959): Die Nahrung der Proturen. Beobachtungen an Acerentomon doderoi Silv. und Eosentomon transitorium. – Naturwissenschaften 46: 90–91.
Wallander, H., L. Nilsson, D. Hagerberg & E. Bååth (2001): Estimation of the biomass and seasonal growth of external mycelium of ectomycorrhizal fungi in the field. – New Phytologist 151: 753–760.
Wallander, H., L. Nilsson, D. Hagerberg & U. Rosengren (2003): Direct estimates of C:N ratios of ectomycorrhizal mycelia collected from Norway spruce forest soils. – Soil Biology and Biochemistry 35: 997–999.
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