Abstract
Collembola are one of the most abundant groups of arthropods, with fungi being an important part of their diet. Collembolan grazing of ectomycorrhizae (ECM) can sever connections between the host root and hyphal networks, interrupting nutrient flow and negatively impacting plant growth. Much of the previous information on interactions between Collembola and ECM has been based on mycelium grown in pure culture, which has artificially high nutrient levels and may lack physical and chemical grazing deterrents seen when ECM form on plant roots. We investigated Collembola feeding preferences by offering naturally occurring ECM, identified by ITS sequencing, to Folsomia candida and Protaphorura armata. We also assessed the gut content fungi of Folsomia collected in a mature Pinus strobus stand. We found that some ECM types, including the Tricholoma aestuans, Piloderma bicolor and the tuburculate ECM of Suillus spraguei, were readily grazed, while Cenococcum geophilum and Lactarius vinaceorufescens were unpalatable. Fungi forming unpalatable ECM were readily grazed when not in symbiosis with the host root.
Similar content being viewed by others
References
Adams E, Salmon J (1972) The mouth-parts and feeding methods of Brachystomella parvula (Schaeffer) (Collembola: Brachystomellidae). Trans R Ent Soc Lond 124:269–286
Agerer R (1987–1996). Color atlas of ectomycorrhizae, lst-9th delivery. Einhorn-Verlag, Schwabisch GmLind
Anslan S, Bahram M, Tedersoo L (2016) Temporal changes in fungal communities associated with guts and appendages of Collembola as based on culturing and high-throughput sequencing. Soil Biol Biochem 96:152–159
Arocena JM, Glowa KR, Massicotte HB (2001) Calcium-rich hypha encrustations on Piloderma. Mycorrhiza 10:209–215
Baumert A, Schumann B, Porzel A, Schmidt J, Strack D (1997) Triterpenoids from Pisolithus tinctorius isolates and ectomycorrhizas. Phytochemistry 45:499–504
Bell AA, Wheeler MH (1986) Biosynthesis and functions of fungal melanins. Annu Rev Phytopathol 24:411–451
Berg MP, Kniese JP, Bedaux JJM, Verhoef HA (1998) Dynamics and stratification of functional groups of micro-and mesoarthropods in the organic layer of a scots pine forest. Biol Fertil Soils 26:268–284
Bessette AE, Roody WC, Bessette AR (2016) Boletes of eastern North America. University Press, Syracuse
Böllmann J, Elmer M, Wöllecke J, Raidl S, Hüttl RF (2010) Defensive strategies of soil fungi to prevent grazing by Folsomia candida (Collembola). Pedobiologia 53:107–114
Booth RG, Anderson JM (1979) The influence of fungal food quality on the growth and fecundity of Folsomia candida (Collembola: Isotomidae). Oecologia 38:317–323
Chahartaghi M, Langel R, Scheu S, Ruess L (2005) Feeding guilds in Collembola based on nitrogen stable isotope ratios. Soil Biol Biochem 37:1718–1725
Christiansen K, Bellinger P (1980) The Collembola of North America, north of the Rio Grande. Grinnelle College, Grinnelle Iowa
Clericuzio M, Gilardoni G, Malagòn O, Vidari G, Vita-Finzi P (2008) Sesquiterpenes of Lactarius and Russula (mushrooms): an update. Nat Prod Commun 3:951–974
Duhamel M, Pel R, Ooms A, Bücking H, Jansa J, Ellers J, Van Straalen NM, Wouda T, Vandenkoornhuyse P, Kiers ET (2013) Do fungivores trigger the transfer of protective metabolites from host plants to arbuscular mycorrhizal hyphae? Ecology 94:2019–2029
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
Fernandez CW, McCormack ML, Hill JM, Pritchard SG, Koide RT (2013) On the persistence of Cenococcum geophilum ectomycorrhizas and its implications for forest carbon and nutrient cycles. Soil Biol Biochem 65:141–143
Folmer O, Black M, Hoeh W, Lutz R, Vrjenhoek R (1994) DNA primers for the amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299
Fountain MT, Hopkin SP (2005) Folsomia candida (Collembola): a “standard” soil arthropod. Annu Rev Entomol 50:201–220
Gange A (2000) Arbuscular mycorrhizal fungi, Collembola and plant growth. Trends Ecol Evol 15:369–372
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes: application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118
Garlaschelli L, Pang Z, Sterner O, Vidari G (1994) New indole derivatives from the fruit bodies of Tricholoma sciodes and T. virgatum. Tetrahedron 50:3571–3574
Harris KK, Boerner REJ (1990) Effects of below-ground grazing by collembola on growth, mycorrhizal infection and P uptake of Geranium robertianum. Plant Soil 129:203–210
Hiol FH, Dixon RK, Curl EA (1994) The feeding preference of mycophagous Collembola varies with the ectomycorrhizal symbiont. Mycorrhiza 5:99–103
Hopkin SP (1997) Biology of the springtails: (Insecta: Collembola). Oxford University Press, New York
Johnson D, Krsek M, Wellington EM, Stott AW, Cole L, Bardgett RD, Read DJ, Leake JR (2005) Soil invertebrates disrupt carbon flow through fungal networks. Science 309:1047–1047
Jørgensen HB, Johansson T, Canbäck B, Hedlund K, Tunlid A (2005) Selective foraging of fungi by collembolans in soil. Biol Lett 1:243–246
Kaneda S, Kaneko N (2004) The feeding preference of a collembolan (Folsomia candida Willem) on ectomycorrhiza (Pisolithus tinctorius (Pers.)) varies with mycelial growth condition and vitality. Appl Soil Ecol 27:1–5
Kanters C, Anderson IC, Johnson D (2015) Chewing up the wood-wide web: selective grazing on ectomycorrhizal fungi by collembola. Forests 6:2560–2570
Kernaghan G, Patriquin G (2015) Diversity and host preference of fungi co-inhabiting Cenococcum mycorrhizae. Fungal Ecol 17:84–95
Kernaghan G, Mayerhofer M, Griffin A (2017) Fungal endophytes of wild and hybrid Vitis leaves and their potential for vineyard biocontrol. Can J Microbiol 63:583–595
Klironomos JN, Kendrick WB (1996) Palatability of microfungi to soil arthropods in relation to the functioning of arbuscular mycorrhizae. Biol Fertil Soils 21:43–52
Klironomos JN, Bednarczuk EM, Neville J (1999) Reproductive significance of feeding on saprobic and arbuscular mycorrhizal fungi by the collembolan, Folsomia candida. Funct Ecol 13:756–761
Kõljalg U, Larsson KH, Abarenkov K, Nilsson RH, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T (2005) UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi. New Phytol 166:1063–1068
Lawrence GB, Hazlett PW, Fernandez IJ, Ouimet R, Bailey SW, Shortle WC, Smith KT, Antidormi MR (2015) Declining acidic deposition begins reversal of forest-soil acidification in the northeastern US and eastern Canada. Environ Sci Technol 49:13103–13111
Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Högberg P, Stenlid J, Finlay RD (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol 173:611–620
Malagòn O, Porta A, Clericuzio M, Gilardoni G, Gozzini D, Vidari G (2014) Structures and biological significance of lactarane sesquiterpenes from the European mushroom Russula nobilis. Phytochemistry 107:126–134
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 39:85–95
Martin F, Plassard C (2001) Nitrogen assimilation by ectomycorrhizal symbiosis. In: Morot-Gaudry J (ed) Nitrogen assimilation by plants: physiological, biochemical and molecular aspects. Science Publishers, Enfield, pp 169–183
Nilsson LO, Giesler R, Bååth E, Wallander H (2005) Growth and biomass of mycorrhizal mycelia in coniferous forests along short natural nutrient gradients. New Phytol 165:613–622
Paul LR, Chapman WK, Chanway CP (2007) Nitrogen fixation associated with Suillus tomentosus tuberculate ectomycorrhizae on Pinus contorta var. latifolia. Ann Bot 99:1101–1109
Paul LR, Chapman WK, Chanway CP (2012) Diazotrophic bacteria reside inside Suillus tomentosus/Pinus contorta tuberculate ectomycorrhizae. Botany 91:48–52
Ponge JF (2000) Vertical distribution of Collembola (Hexapoda) and their food resources in organic horizons of beech forests. Biol Fertil Soils 32:508–522
Ponge JF, Arpin P, Sondag F, Delecour F (1997) Soil fauna and site assessment in beech stands of the Belgian Ardennes. Can J For Res 27:2053–2064
Potapov AM, Tiunov AV (2016) Stable isotope composition of mycophagous collembolans versus mycotrophic plants: do soil invertebrates feed on mycorrhizal fungi? Soil Biol Biochem 93:115–118
Potapov MB, Bu Y, Huang CW, Gao Y, Luan YX (2010) Generic switch-over during ontogenesis in Dimorphacanthella gen. N. (Collembola, Isotomidae) with barcoding evidence. ZooKeys 73:13
Scheu S, Folger M (2004) Single and mixed diets in Collembola: effects on reproduction and stable isotope fractionation. Funct Ecol 18:94–102
Schultz PA (1991) Grazing preferences of two collembolan species, Folsomia candida and Proisotoma minuta, for ectomycorrhizal fungi. Pedobiologia 35:313–325
Setälä H (1995) Growth of birch and pine seedlings in relation to grazing by soil fauna on ectomycorrhizal fungi. Ecology 76:1844–1851
Shaw PJA (1988) A consistent hierarchy of fungal feeding preferences of the Collembola Onychiurus armatus. Pedobiologia 31:179–187
Stadler M, Sterner O (1998) Production of bioactive secondary metabolites in the fruit bodies of macrofungi as a response to injury. Phytochemistry 49:1013–1019
Sterner O, Bergman R, Kihlberg J, Wickberg B (1985) The sesquiterpenes of Lactarius vellereus and their role in a proposed chemical defense system. J Nat Prod 48:279–288
Toledo AV, Franco MEE, Lopez SMY, Troncozo MI, Saparrat MCN, Balatti PA (2017) Melanins in fungi: types, localization and putative biological roles. Physiol Mol Plant Pathol 99:2–6
Trappe JM (1962) Cenococcum graniforme - its distribution, ecology, mycorrhiza formation, and inherent variation. Ph.D. Thesis, University of Washington
Usher MB, Booth W, Sparkes KE (1982) A review of progress in understanding the organisation of communities of soil arthropods. Pedobiologia 23:126–144
van der Linde S, Suz LM, Orme CD, Cox F, Andreae H, Asi E, Atkinson B, Benham S, Carroll C, Cools N, De Vos B (2018) Environment and host as large-scale controls of ectomycorrhizal fungi. Nature 6:1
Waksman SA (1922) A method for counting the number of fungi in the soil. J Bacteriol 7:339
Wallander H, Massicotte HB, Nylund JE (1997) Seasonal variation in protein, ergosterol and chitin in five morphotypes of Pinus sylvestris L. ectomycorrhizae in a mature Swedish forest. Soil Biol Biochem 29:45–53
Warnock AJ, Fitter AH, Usher MB (1982) The influence of a springtail Folsomia candida (Insecta, Collembola) on the mycorrhizal association of Leek Allium porum and the vesicular-arbuscular mycorrhizal endophyte Glomus fasciculatus. New Phytol 90:285–292
White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (ed) PCR Protocols: a guide to methods and applications. Academic Press, New York, pp 315–322
Acknowledgements
We thank Amanda Griffin for help with graphics, Jeff Battigelli for expert identification of Collembola, and the Natural Sciences and Engineering Research Council of Canada (NSERC) for funding.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
LeFait, A., Gailey, J. & Kernaghan, G. Fungal species selection during ectomycorrhizal grazing by Collembola. Symbiosis 78, 87–95 (2019). https://doi.org/10.1007/s13199-018-00596-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13199-018-00596-x