Advertisement

Insect-Fungus Interactions in Dead Wood Systems

  • Tone Birkemoe
  • Rannveig M. Jacobsen
  • Anne Sverdrup-Thygeson
  • Peter H. W. Biedermann
Chapter
Part of the Zoological Monographs book series (ZM, volume 1)

Abstract

Fungi can provide insects with nutrients and essential elements, detoxify plant defenses in recently dead wood, and protect or, in contrast, attack and digest insects. Insects can affect fungi through feeding or propagule dispersal. Fungal grazing may induce changes in fungal chemistry, morphology, and growth. Insect-fungus interactions in dead wood span a wide gradient of specificity from indirect interactions through shared habitats to obligate mutualisms. When based on insects reared from polypores, insect-fungi interaction networks may exhibit a degree of specialization similar to that of pollinators and plants , whereas when based on wood-decay fungi isolated from insects sampled at dead wood, the degree of specialization appears closer to animal-mediated seed dispersal. Exchange of dispersal and nutrition is the basis for most obligate insect-fungus mutualisms. Adaptations to these mutualisms seem to have evolved rapidly, and for some insects there has been a feedback between the evolution of fungus farming and sociality. Several recent studies indicate that insect-vectored dispersal might be an important complement to wind dispersal also for non-mutualistic saproxylic fungi, potentially providing targeted dispersal to suitable substrates. We propose a theoretical framework for the effectiveness of insect-vectored spore dispersal. Insect-fungus interactions are an essential component of forest ecosystems, influencing species richness, wood decay, and nutrient cycling. Several aspects of insect-fungus interactions are unknown and require further study, but availability and development of molecular methods may rapidly advance this field of research.

References

  1. Aanen DK, Eggleton P, Rouland-Lefevre C, Guldberg-Froslev T, Rosendahl S, Boomsma JJ (2002) The evolution of fungus-growing termites and their mutualistic fungal symbionts. Proc Natl Acad Sci USA 99(23):14887–14892.  https://doi.org/10.1073/pnas.222313099CrossRefPubMedPubMedCentralGoogle Scholar
  2. Abrahamsson M, Lindbladh M, Ronnberg J (2008) Influence of butt rot on beetle diversity in artificially created high-stumps of Norway spruce. For Ecol Manag 255(8–9):3396–3403.  https://doi.org/10.1016/j.foreco.2008.01.010CrossRefGoogle Scholar
  3. Allison JD, Borden JH, Seybold SJ (2004) A review of the chemical ecology of the Cerambycidae (Coleoptera). Chemoecology 14(3):123–150.  https://doi.org/10.1007/s00049-004-0277-1CrossRefGoogle Scholar
  4. Amburgey TL (1979) Review and checklist of the literature on interactions between wood-inhabiting fungi and subterranean termites: 1960–1978. Sociobiology 4:279–296CrossRefGoogle Scholar
  5. Ayres MP, Wilkens RT, Ruel JJ, Lombardero MJ, Vallery E (2000) Nitrogen budgets of phloem-feeding bark beetles with and without symbiotic fungi. Ecology 81(8):2198–2210.  https://doi.org/10.1890/0012-9658(2000)081[2198,Nbopfb]2.0.Co;2CrossRefGoogle Scholar
  6. Batra LR (1963) Ecology of ambrosia fungi and their dissemination by beetles. Trans KS Acad Sci (1903–) 66(2):213–236CrossRefGoogle Scholar
  7. Batra LR, Michie MD (1963) Pleomorphism in some ambrosia and related fungi. Trans KS Acad Sci (1903–) 66(3):470–481.  https://doi.org/10.2307/3626545CrossRefGoogle Scholar
  8. Beaver RA (1989) Insect-fungus relationships in the bark and ambrosia beetles. In: Wilding N, Collins NM, Hammond PM, Webber JF (eds) Insect-fungus interactions. Academic Press, London, pp 121–143CrossRefGoogle Scholar
  9. Becker G (1964) Termiten-anlockende Wirkung einiger bei Basidiomyceten-Angriff in Holz entstehender Verbindungen. Holzforschung-Int J Biol Chem Phys Technol Wood 18(6):168–172.  https://doi.org/10.1515/hfsg.1964.18.6.168Google Scholar
  10. Becker G (1965) Versuche über den Einfluß von Braunfäulepilzen auf Wahl und Ausnutzung der Holznahrung durch Termiten. Mater Organismen 1:95–156Google Scholar
  11. Becker G, Kerner-Gang W (1963) Schädigung und Förderung von Termiten durch Schimmelpilze. Z Angew Entomol 53:429–448CrossRefGoogle Scholar
  12. Biedermann PHW (2012) The evolution of cooperation in ambrosia beetles. University of BernGoogle Scholar
  13. Biedermann PHW, Kaltenpoth M (2014) New synthesis: the chemistry of partner choice in insect-microbe mutualisms. J Chem Ecol 40(2):99–99.  https://doi.org/10.1007/s10886-014-0382-8CrossRefPubMedPubMedCentralGoogle Scholar
  14. Biedermann PHW, Rohlfs M (2017) Evolutionary feedbacks between insect sociality and microbial management. Curr Opin Insect Sci 22:92–100PubMedCrossRefPubMedCentralGoogle Scholar
  15. Biedermann PHW, Taborsky M (2011) Larval helpers and age polyethism in ambrosia beetles. Proc Natl Acad Sci USA 108(41):17064–17069.  https://doi.org/10.1073/pnas.1107758108CrossRefPubMedPubMedCentralGoogle Scholar
  16. Birkemoe T (2002) Structural infestations of ants (Hymenoptera, Formicidae) in southern Norway. Norw J Entomol 49:139–142Google Scholar
  17. Blackwell M, Bridges JR, Moser JC, Perry TJ (1986) Hyperphoretic dispersal of a Pyxidiophora anamorph. Science 232(4753):993–995.  https://doi.org/10.1126/science.232.4753.993CrossRefPubMedPubMedCentralGoogle Scholar
  18. Blanchette RA, Shaw CG (1978) Associations among bacteria, yeasts, and basidiomycetes during wood decay. Phytopathology 68(4):631–637CrossRefGoogle Scholar
  19. Blüthgen N, Menzel F, Hovestadt T, Fiala B, Blüthgen N (2007) Specialization, constraints, and conflicting interests in mutualistic networks. Curr Biol 17(4):341–346.  https://doi.org/10.1016/j.cub.2006.12.039CrossRefPubMedPubMedCentralGoogle Scholar
  20. Boddy L (2000) Interspecific combative interactions between wood-decaying basidiomycetes. FEMS Microbiol Ecol 31(3):185–194PubMedCrossRefPubMedCentralGoogle Scholar
  21. Boddy L (2001) Fungal community ecology and wood decomposition processes in angiosperms: from standing tree to complete decay of coarse woody debris. Ecol Bull 49:43–56Google Scholar
  22. Boddy L, Jones TH (2008) Chapter 9: Interactions between basidiomycota and invertebrates. In: Lynne Boddy JCF, Pieter van W (eds) British Mycological Society Symposia Series, vol 28. Academic Press, London, pp 155–179. doi: https://doi.org/10.1016/S0275-0287(08)80011-2CrossRefGoogle Scholar
  23. Boddy L, Hynes J, Bebber DP, Fricker MD (2009) Saprotrophic cord systems: dispersal mechanisms in space and time. Mycoscience 50(1):9–19CrossRefGoogle Scholar
  24. Boucher DH, James S, Keeler KH (1982) The ecology of mutualism. Annu Rev Ecol Syst 13(1):315–347.  https://doi.org/10.1146/annurev.es.13.110182.001531CrossRefGoogle Scholar
  25. Bourke AFG (2011) Principles of social evolution. Oxford series in ecology and evolution. Oxford University Press, OxfordCrossRefGoogle Scholar
  26. Bracewell RR, Six DL (2015) Experimental evidence of bark beetle adaptation to a fungal symbiont. Ecol Evol 5(21):5109–5119.  https://doi.org/10.1002/ece3.1772CrossRefPubMedPubMedCentralGoogle Scholar
  27. Bronstein JL (2015) Mutualism. OUP, OxfordGoogle Scholar
  28. Brune A (2014) Symbiotic digestion of lignocellulose in termite guts. Nat Rev Microbiol 12(3):168–180.  https://doi.org/10.1038/nrmicro3182CrossRefPubMedPubMedCentralGoogle Scholar
  29. Buchner P (1965) Endosymbiosis of animals with plant-like microorganisms. Wiley Interscience, New YorkGoogle Scholar
  30. Castello J, Shaw C, Furniss M (1976) Isolation of Cryptoporus volvatus and Fomes pinicola from Dendroctonus pseudotsugae. Phytopathology 66(12):1431–1434CrossRefGoogle Scholar
  31. Castrillo LA, Griggs MH, Vandenberg JD (2016) Competition between biological control fungi and fungal symbionts of ambrosia beetles Xylosandrus crassiusculus and X. germanus (Coleoptera: Curculionidae): mycelial interactions and impact on beetle brood production. Biol Control 103:138–146.  https://doi.org/10.1016/j.biocontrol.2016.09.005CrossRefGoogle Scholar
  32. Cease KR, Juzwik J (2001) Predominant nitidulid species (Coleoptera: Nitidulidae) associated with spring oak wilt mats in Minnesota. Can J For Res 31(4):635–643CrossRefGoogle Scholar
  33. Ceja-Navarro JA, Nguyen NH, Karaoz U, Gross SR, Herman DJ, Andersen GL, Bruns TD, Pett-Ridge J, Blackwell M, Brodie EL (2014) Compartmentalized microbial composition, oxygen gradients and nitrogen fixation in the gut of Odontotaenius disjunctus. ISME J 8(1):6–18.  https://doi.org/10.1038/ismej.2013.134CrossRefPubMedPubMedCentralGoogle Scholar
  34. Chapela IH, Boddy L (1988) Fungal colonization of attached beech branches 2. Spatial and temporal organization of fungal communities arising from latent invaders in bark and functional sapwood, under different moisture regimes. New Phytol 110(1):47–57.  https://doi.org/10.1111/j.1469-8137.1988.tb00236.xCrossRefGoogle Scholar
  35. Chen Y, Hansen LD, Brown JJ (2002) Nesting sites of the carpenter ant, Camponotus vicinus (Mayr) (Hymenoptera: Formicidae) in Northern Idaho. Environ Entomol 31(6):1037–1042.  https://doi.org/10.1603/0046-225X-31.6.1037CrossRefGoogle Scholar
  36. Clark AJ, Block K (1959) The absence of sterol synthesis in insects. J Biol Chem 234:2578–2582PubMedGoogle Scholar
  37. Coates D, Rayner A (1985) Fungal population and community development in cut beech logs. New Phytol 101(1):153–171CrossRefGoogle Scholar
  38. Cobb TP, Hannam KD, Kishchuk BE, Langor DW, Quideau SA, Spence JR (2010) Wood-feeding beetles and soil nutrient cycling in burned forests: implications of post-fire salvage logging. Agric For Entomol 12(1):9–18.  https://doi.org/10.1111/j.1461-9563.2009.00440.xCrossRefGoogle Scholar
  39. Cornelius ML, Daigle DJ, Connick Jr WJ, Parker A, Wunch K (2002) Responses of Coptotermes formosanus and Reticulitermes flavipes (Isoptera: Rhinotermitidae) to three types of wood rot fungi cultured on different substrates. J Econ Entomol 95(1):121–128.  https://doi.org/10.1603/0022-0493-95.1.121CrossRefPubMedPubMedCentralGoogle Scholar
  40. Cornwell WK, Cornelissen JHC, Allison SD, Bauhus J, Eggleton P, Preston CM, Scarff F, Weedon JT, Wirth C, Zanne AE (2009) Plant traits and wood fates across the globe: rotted, burned, or consumed? Glob Change Biol 15(10):2431–2449.  https://doi.org/10.1111/j.1365-2486.2009.01916.xCrossRefGoogle Scholar
  41. Cramer JM, Mesquita RC, Williamson GB (2007) Forest fragmentation differentially affects seed dispersal of large and small-seeded tropical trees. Biol Conserv 137(3):415–423CrossRefGoogle Scholar
  42. Crowther TW, A'Bear AD (2012) Impacts of grazing soil fauna on decomposer fungi are species-specific and density-dependent. Fungal Ecol 5(2):277–281.  https://doi.org/10.1016/j.funeco.2011.07.006CrossRefGoogle Scholar
  43. Crowther TW, Boddy L, Jones TH (2011a) Outcomes of fungal interactions are determined by soil invertebrate grazers. Ecol Lett 14(11):1134–1142PubMedCrossRefPubMedCentralGoogle Scholar
  44. Crowther TW, Boddy L, Jones TH (2011b) Species-specific effects of soil fauna on fungal foraging and decomposition. Oecologia 167(2):535–545PubMedCrossRefPubMedCentralGoogle Scholar
  45. Crowther TW, Boddy L, Jones TH (2012) Functional and ecological consequences of saprotrophic fungus-grazer interactions. ISME J 6(11):1992–2001.  https://doi.org/10.1038/ismej.2012.53CrossRefPubMedPubMedCentralGoogle Scholar
  46. Dahlberg A, Stokland J (2004) Vedlevande arters krav på substrat - sammanställning och analys av 3 600 arter. Skogsstyrelsen, Rapport:7–04Google Scholar
  47. Davis T (2014) The ecology of yeasts in the bark beetle holobiont: a century of research revisited. Microb Ecol:1–10.  https://doi.org/10.1007/s00248-014-0479-1
  48. De Fine Licht HH, Biedermann PHW (2012) Patterns of functional enzyme activity in fungus farming ambrosia beetles. Front Zool 9(1):13.  https://doi.org/10.1186/1742-9994-9-13CrossRefPubMedPubMedCentralGoogle Scholar
  49. Dighton J (2003) Fungi in ecosystem processes. CRC, Boca RatonCrossRefGoogle Scholar
  50. Doebeli M, Knowlton N (1998) The evolution of interspecific mutualisms. Proc Natl Acad Sci Biol 95(15):8676–8680CrossRefGoogle Scholar
  51. Dowd PF (1992) Insect fungal symbionts - a promising source of detoxifying enzymes. J Ind Microbiol 9(3–4):149–161CrossRefGoogle Scholar
  52. Drenkhan T, Kasanen R, Vainio EJ (2016) Phlebiopsis gigantea and associated viruses survive passing through the digestive tract of Hylobius abietis. Biocontrol Sci Technol 26(3):320–330CrossRefGoogle Scholar
  53. Dybas HS (1976) The larval characters of featherwing and limulodid beetles and their family relationships in the Staphylinoidea (Coleoptera: Ptilidae and Limulodidae). Fieldiana Zool 70:29–78Google Scholar
  54. Dyer HC, Boddy L, Preston-Meek CM (1992) Effect of the nematode Panagrellus redivivus on growth and enzyme production by Phanerochaete velutina and Stereum hirsutum. Mycol Res 96(12):1019–1028.  https://doi.org/10.1016/S0953-7562(09)80110-XCrossRefGoogle Scholar
  55. Fäldt J, Jonsell M, Nordlander G, Borg-Karlson A-K (1999) Volatiles of bracket fungi Fomitopsis pinicola and Fomes fomentarius and their functions as insect attractants. J Chem Ecol 25(3):567–590.  https://doi.org/10.1023/a:1020958005023CrossRefGoogle Scholar
  56. Farrell BD, Sequeira AS, O'Meara BC, Normark BB, Chung JH, Jordal BH (2001) The evolution of agriculture in beetles (Curculionidae : Scolytinae and Platypodinae). Evolution 55(10):2011–2027PubMedCrossRefGoogle Scholar
  57. Filipiak M (2018) Nutrient dynamics in decomposing dead wood in the context of wood eater requirements: the ecological stoichiometry of saproxylophagous insects. In: Ulyshen MD (ed) Saproxylic insects: diversity, ecology and conservation. Springer, Heidelberg, pp 429–469Google Scholar
  58. Filipiak M, Weiner J (2014) How to make a beetle out of wood: multi-elemental stoichiometry of wood decay, xylophagy and fungivory. PLoS One 9(12):e115104.  https://doi.org/10.1371/journal.pone.0115104CrossRefPubMedPubMedCentralGoogle Scholar
  59. Filipiak M, Weiner J (2017) Nutritional dynamics during the development of xylophagous beetles related to changes in the stoichiometry of 11 elements. Physiol Entomol 42(1):73–84.  https://doi.org/10.1111/phen.12168CrossRefGoogle Scholar
  60. Filipiak M, Sobczyk Ł, Weiner J (2016) Fungal transformation of tree stumps into a suitable resource for xylophagous beetles via changes in elemental ratios. Insects 7(2):13CrossRefPubMedCentralGoogle Scholar
  61. Fisher RC (1940) Studies on the biology of the death-watch beetle, Xestobium rufovillosum De G. III. Fungal decay in timber in relation to the occurrence and rate of developmemt of the insect. Ann Appl Biol 27(4):12CrossRefGoogle Scholar
  62. Fisher RC (1941) Studies of the biology of the death-watch beetle, Xestobium rufovillosum De G. IV. The effect of type and extent of fungal decay in timber upon the rate of development of the insect. Ann Appl Biol 28(13):16Google Scholar
  63. Florez LV, Biedermann PH, Engl T, Kaltenpoth M (2015) Defensive symbioses of animals with prokaryotic and eukaryotic microorganisms. Nat Prod Rep 32(7):904–936.  https://doi.org/10.1039/c5np00010fCrossRefPubMedPubMedCentralGoogle Scholar
  64. Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, Martínez AT, Otillar R, Spatafora JW, Yadav JS, Aerts A, Benoit I, Boyd A, Carlson A, Copeland A, Coutinho PM, de Vries RP, Ferreira P, Findley K, Foster B, Gaskell J, Glotzer D, Górecki P, Heitman J, Hesse C, Hori C, Igarashi K, Jurgens JA, Kallen N, Kersten P, Kohler A, Kües U, Kumar TKA, Kuo A, LaButti K, Larrondo LF, Lindquist E, Ling A, Lombard V, Lucas S, Lundell T, Martin R, McLaughlin DJ, Morgenstern I, Morin E, Murat C, Nagy LG, Nolan M, Ohm RA, Patyshakuliyeva A, Rokas A, Ruiz-Dueñas FJ, Sabat G, Salamov A, Samejima M, Schmutz J, Slot JC, St. John F, Stenlid J, Sun H, Sun S, Syed K, Tsang A, Wiebenga A, Young D, Pisabarro A, Eastwood DC, Martin F, Cullen D, Grigoriev IV, Hibbett DS (2012) The paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336(6089):1715–1719.  https://doi.org/10.1126/science.1221748CrossRefPubMedPubMedCentralGoogle Scholar
  65. Francke-Grosmann H (1956) Hautdrüsen als Träger der Pilzsymbiose bei Ambrosiakäfern. ZMorphuÖkolTiere 45:275–308Google Scholar
  66. Francke-Grosmann H (1967) Ectosymbiosis in wood-inhabiting beetles. In: Henry SM (ed) Symbiosis. Academic Press, New York, pp 141–205CrossRefGoogle Scholar
  67. French JRJ, Roeper RA (1972) Interactions of ambrosia beetle, Xyleborus dispar (Coleoptera-Scolytidae), with its symbiotic fungus Ambrosiella hartigii (Fungi Imperfecti). Can Entomol 104(10):1635CrossRefGoogle Scholar
  68. Geib SM, Filley TR, Hatcher PG, Hoover K, Carlson JE, Jimenez-Gasco MD, Nakagawa-Izumi A, Sleighter RL, Tien M (2008) Lignin degradation in wood-feeding insects. Proc Natl Acad Sci Biol 105(35):12932–12937CrossRefGoogle Scholar
  69. Gibb H, Pettersson RB, Hjälten J, Hilszczanski J, Ball JP, Johansson T, Atlegrim O, Danell K (2006) Conservation-oriented forestry and early successional saproxylic beetles: responses of functional groups to manipulated dead wood substrates. Biol Conserv 129(4):437–450CrossRefGoogle Scholar
  70. Gilbertson RL (1984) Relationships between insects and wood-rotting basidiomycetes. In: Wheeler Q, Blackwell M (eds) Fungus-insect relationships. Perspectives in ecology and evolution. Columbia University Press, New York, pp 130–165Google Scholar
  71. Gilbertson RL, Ryvarden L (1986) North American polypores, vol 1. Fungiflora AS, OsloGoogle Scholar
  72. Gimmel ML, Ferro ML (2018) General overview of saproxylic Coleoptera. In: Ulyshen MD (ed) Saproxylic insects: diversity, ecology and conservation. Springer, Heidelberg, pp 51–128Google Scholar
  73. Graves RC (1965) Observations on the ecology, behavior and life cycle of the fungus-feeding beetle, Cypherotylus californicus, with a description of the pupa (Coleoptera: Erotylidae). Coleopter Bull 19(4):117–122Google Scholar
  74. Grebennikov VV, Leschen RA (2010) External exoskeletal cavities in Coleoptera and their possible mycangial functions. Entomol Sci 13(1):81–98CrossRefGoogle Scholar
  75. Greif MD, Currah RS (2003) A functional interpretation of the role of the reticuloperidium in whole-ascoma dispersal by arthropods. Mycol Res 107:77–81PubMedCrossRefPubMedCentralGoogle Scholar
  76. Greif MD, Currah RS (2007) Patterns in the occurrence of saprophytic fungi carried by arthropods caught in traps baited with rotted wood and dung. Mycologia 99(1):7–19PubMedCrossRefPubMedCentralGoogle Scholar
  77. Guevara R, Rayner ADM, Reynolds SE (2000) Effects of fungivory by two specialist ciid beetles (Octotemnus glabriculus and Cis boleti) on the reproductive fitness of their host fungus, Coriolus versicolor. New Phytol 145(1):137–144.  https://doi.org/10.1046/j.1469-8137.2000.00552.xCrossRefGoogle Scholar
  78. Hackman W, Meinander M (1979) Diptera feeding as larvae on macrofungi in Finland. Ann Zool Fenn 16:50–83Google Scholar
  79. Hågvar S (1999) Saproxylic beetles visiting living sporocarps of Fomitopsis pinicola and Fomes fomentarius. Norw J Entomol 46:25–32Google Scholar
  80. Hågvar S, Økland B (1997) Saproxylic beetle fauna associated with living sporocarps of Fomitopsis pinicola (Fr.) Karst. in four spruce forests with different management histories. Norw J Entomol 44(2):95–105Google Scholar
  81. Halbwachs H, Bâssler C (2015) Gone with the wind – a review on basidiospores of lamellate agarics. Mycosphere 6(1):78CrossRefGoogle Scholar
  82. Hall WE (1999) Generic revision of the tribe Nanosellini (Coleoptera: Ptiliidae: Ptiliinae). Trans Am Entomol Soc (1890–) 125(1/2):39–126Google Scholar
  83. Halme P, Vartija N, Salmela J, Penttinen J, Norros V (2013) High within- and between-trunk variation in the nematoceran (Diptera) community and its physical environment in decaying aspen trunks. Insect Conserv Divers 6(4):502–512CrossRefGoogle Scholar
  84. Hansen LO, Akre RD (1985) Biology of carpenter ants in Washington state (Hymenoptera: Formicidae: Camponotus). Melanderia 43:1–61Google Scholar
  85. Hanski I (1989) Fungivory: fungi, insects and ecology. In: Wilding N, Collins NM, Hammond PM, Webber JF (eds) Insect-fungus interactions. Academic Press, London, pp 25–86CrossRefGoogle Scholar
  86. Harrington TC (2005) Ecology and evolution of mycophagous bark beetles and their fungal partners. In: Vega FE, Blacwell M (eds) Insect-fungal associations: ecology and evolution. Oxford University Press, Oxford, pp 257–291Google Scholar
  87. Harrington T, Furniss M, Shaw C (1981) Dissemination of hymenomycetes by Dendroctonus pseudotsugae (Coleoptera: Scolytidae). Phytopathology 71(5):551–554CrossRefGoogle Scholar
  88. Hayslett M, Juzwik J, Moltzan B (2008) Three Colopterus beetle species carry the oak wilt fungus to fresh wounds on red oak in Missouri. Plant Dis 92(2):270–275CrossRefGoogle Scholar
  89. Hedlund K, Öhrn MS (2000) Tritrophic interactions in a soil community enhance decomposition rates. Oikos 88(3):585–591CrossRefGoogle Scholar
  90. Hofstetter RW, Moser JC (2014) The role of mites in insect-fungus associations. Annu Rev Entomol 59:537–557.  https://doi.org/10.1146/annurev-ento-011613-162039CrossRefPubMedPubMedCentralGoogle Scholar
  91. Holmer L, Renvall P, Stenlid J (1997) Selective replacement between species of wood-rotting basidiomycetes, a laboratory study. Mycol Res 101(6):714–720.  https://doi.org/10.1017/S0953756296003243CrossRefGoogle Scholar
  92. Hulcr J, Stelinski LL (2017) The ambrosia symbiosis: from evolutionary ecology to practical management. Annu Rev Entomol 62(62):285–303.  https://doi.org/10.1146/annurev-ento-031616-035105CrossRefPubMedPubMedCentralGoogle Scholar
  93. Ingold CT, Hudson HJ (1993) Dispersal in fungi. In: The biology of fungi. Springer Netherlands, Dordrecht, pp 119–131.  https://doi.org/10.1007/978-94-011-1496-7_7CrossRefGoogle Scholar
  94. Jacobs JM, Work TT (2012) Linking deadwood-associated beetles and fungi with wood decomposition rates in managed black spruce forests. Can J For Res 42(8):1477–1490.  https://doi.org/10.1139/x2012-075CrossRefGoogle Scholar
  95. Jacobsen RM, Birkemoe T, Sverdrup-Thygeson A (2015) Priority effects of early successional insects influence late successional fungi in dead wood. Ecol Evol 5(21):4896–4905.  https://doi.org/10.1002/ece3.1751CrossRefPubMedPubMedCentralGoogle Scholar
  96. Jacobsen RM, Kauserud H, Sverdrup-Thygeson A, Bjorbækmo MM, Birkemoe T (2017) Wood-inhabiting insects can function as targeted vectors for decomposer fungi. Fungal Ecol 29:76–84.  https://doi.org/10.1016/j.funeco.2017.06.006CrossRefGoogle Scholar
  97. Jacobsen RM, Sverdrup-Thygeson A, Kauserud H, Birkemoe T (2018a) Revealing hidden insect-fungus interactions; moderately specialized, modular and anti-nested detritivore networks. Proc R Soc B 285:20172833PubMedCrossRefPubMedCentralGoogle Scholar
  98. Jacobsen RM, Sverdrup-Thygeson A, Kauserud H, Mundra S, Birkemoe T (2018b) Exclusion of invertebrates influences saprotrophic fungal community and wood decay rate in an experimental field study. (submitted)Google Scholar
  99. Jakovlev J (2011) Fungus gnats (Diptera: Sciaroidea) associated with dead wood and wood growing fungi: new rearing data from Finland and Russian Karelia and general analysis of known larval microhabitats in Europe. Entomol Fenn 22:157–189Google Scholar
  100. Jaworski T (2018) Diversity of saproxylic Lepidoptera. In: Ulyshen MD (ed) Saproxylic insects: diversity, ecology and conservation. Springer, Heidelberg, pp 319–338Google Scholar
  101. Johansson T, Olsson J, Hjältén J, Jonsson BG, Ericson L (2006) Beetle attraction to sporocarps and wood infected with mycelia of decay fungi in old-growth spruce forests of northern Sweden. For Ecol Manage 237(1):335–341CrossRefGoogle Scholar
  102. Johansson T, Hjälten J, Hilszczanski J, Stenlid J, Ball JP, Alinvi O, Danell K (2007) Variable response of different functional groups of saproxylic beetles to substrate manipulation and forest management: implications for conservation strategies. For Ecol Manage 242(2–3):496–510CrossRefGoogle Scholar
  103. Jonsell M, Nordlander G (1995) Field attraction of Coleoptera to odours of the wood-decaying polypores Fomitopsis pinicola and Fomes fomentarius. In: Ann Zool Fenn, 1995. vol 4. Suomen Biologian Seura Vanamo, Helsinki, 1964–, pp 391–402Google Scholar
  104. Jonsell M, Nordlander G (2004) Host selection patterns in insects breeding in bracket fungi. Ecol Entomol 29(6):697–705CrossRefGoogle Scholar
  105. Jonsell M, Schroeder M, Weslien J (2005) Saproxylic beetles in high stumps of spruce: fungal flora important for determining the species composition. Scand J For Res 20(1):54–62CrossRefGoogle Scholar
  106. Jönsson MT, Edman M, Jonsson BG (2008) Colonization and extinction patterns of wood-decaying fungi in a boreal old-growth Picea abies forest. J Ecol 96(5):1065–1075CrossRefGoogle Scholar
  107. Jordal B, Cognato A (2012) Molecular phylogeny of bark and ambrosia beetles reveals multiple origins of fungus farming during periods of global warming. BMC Evol Biol 12(1):133PubMedPubMedCentralCrossRefGoogle Scholar
  108. Jordal BH, Beaver RA, Kirkendall LR (2001) Breaking taboos in the tropics: incest promotes colonization by wood-boring beetles. Global Ecol Biogeogr 10:345–357CrossRefGoogle Scholar
  109. Jordal BH, Sequeira AS, Cognato AI (2011) The age and phylogeny of wood boring weevils and the origin of subsociality. Mol Phylogenet Evo 59(3):708–724CrossRefGoogle Scholar
  110. Jørgensen HB, Elmholt S, Petersen H (2003) Collembolan dietary specialisation on soil grown fungi. Biol Fertil Soils 39(1):9–15.  https://doi.org/10.1007/s00374-003-0674-6CrossRefGoogle Scholar
  111. Jouquet P, Traoré S, Choosai C, Hartmann C, Bignell D (2011) Influence of termites on ecosystem functioning. Ecosystem services provided by termites. Eur J Soil Biol 47(4):215–222.  https://doi.org/10.1016/j.ejsobi.2011.05.005CrossRefGoogle Scholar
  112. Junninen K, Komonen A (2011) Conservation ecology of boreal polypores: a review. Biol Conserv 144(1):11–20CrossRefGoogle Scholar
  113. Jusino MA, Lindner DL, Banik MT, Rose KR, Walters JR (2016) Experimental evidence of a symbiosis between red-cockaded woodpeckers and fungi. Proc R Soc B Biol Sci 283(1827).  https://doi.org/10.1098/rspb.2016.0106PubMedPubMedCentralCrossRefGoogle Scholar
  114. Kadowaki K, Leschen RA, Beggs JR (2011a) No evidence for a Ganoderma spore dispersal mutualism in an obligate spore-feeding beetle Zearagytodes maculifer. Fungal Biol-UK 115(8):768–774CrossRefGoogle Scholar
  115. Kadowaki K, Leschen RAB, Beggs JR (2011b) Competition–colonization dynamics of spore-feeding beetles on the long-lived bracket fungi Ganoderma in New Zealand native forest. Oikos 120(5):776–786.  https://doi.org/10.1111/j.1600-0706.2011.19302.xCrossRefGoogle Scholar
  116. Kaila L, Martikainen P, Punttila P, Yakovlev E (1994) Saproxylic beetles (Coleoptera) on dead birch trunks decayed by different polypore species. Ann Zool Fenn 31:97–107Google Scholar
  117. Kaneko T, Takagi K (1966) Biology of some scolytid ambrosia beetles attacking tea plants: VI. A comparative study of two ambrosia fungi associated with Xyleborus compactus EICHHOFF and Xyleborus germanus BLANFORD (Coleoptera: Scolytidae). Appl Entomol Zool 1(4):173–176.  https://doi.org/10.1303/aez.1.173CrossRefGoogle Scholar
  118. Kasson MT, Wickert KL, Stauder CM, Macias AM, Berger MC, Simmons DR, Short DPG, DeVallance DB, Hulcr J (2016) Mutualism with aggressive wood-degrading Flavodon ambrosius (Polyporales) facilitates niche expansion and communal social structure in Ambrosiophilus ambrosia beetles. Fungal Ecol 23:86–96.  https://doi.org/10.1016/j.funeco.2016.07.002CrossRefGoogle Scholar
  119. Keeling CI, Yuen MM, Liao NY, Roderick Docking T, Chan SK, Taylor GA, Palmquist DL, Jackman SD, Nguyen A, Li M, Henderson H, Janes JK, Zhao Y, Pandoh P, Moore R, Sperling FA, W Huber DP, Birol I, Jones SJ, Bohlmann J (2013) Draft genome of the mountain pine beetle, Dendroctonus ponderosae Hopkins, a major forest pest. Genome Biol 14(3):R27.  https://doi.org/10.1186/gb-2013-14-3-r27CrossRefPubMedPubMedCentralGoogle Scholar
  120. Kirisits T (2004) Fungal associates of European bark beetles with special emphasis on the ophiostomatoid fungi. In: Lieutier F, Day KR, Battisti A, Grégoire J-C, Evans HF (eds) Bark and wood boring insects in living trees in Europe, a synthesis. Springer Netherlands, Dordrecht, pp 181–236.  https://doi.org/10.1007/978-1-4020-2241-8_10CrossRefGoogle Scholar
  121. Kirkendall LR, Biedermann PHW, Jordal BH (2015) Evolution and diversity of bark and ambrosia beetles. In: Vega FE, Hofstetter RW (eds) Bark beetles: biology and ecology of native and invasive species. Academic Press, London, pp 85–156CrossRefGoogle Scholar
  122. Klepzig KD, Adams AS, Handelsman J, Raffa KF (2009) Symbioses: a key driver of insect physiological processes, ecological interactions, evolutionary diversification, and impacts on humans. Environ Entomol 38(1):67–77.  https://doi.org/10.1603/022.038.0109CrossRefPubMedPubMedCentralGoogle Scholar
  123. Klironomos JN, Hart MM (2001) Food-web dynamics: animal nitrogen swap for plant carbon. Nature 410(6829):651–652PubMedPubMedCentralCrossRefGoogle Scholar
  124. Koehler F (2000) Saproxylic beetles in nature forests of the northern Rhineland. Comparative studies on the saproxylic beetles of Germany and contributions to German nature forest research. Schrr LÖBF/LAfAO NRW (Recklinghausen) 18:1–351Google Scholar
  125. Komonen A, Jonsell M, Okland B, Sverdrup-Thygeson A, Thunes K (2004) Insect assemblage associated with the polypore Fomitopsis pinicola: a comparison across Fennoscandia. Entomol Fenn 15(2):102–112Google Scholar
  126. Krasutskii B (2006) Beetles (Coleoptera) associated with the birch fungus Piptoporus betulinus (Bull.: Fr.) P. Karst.(Basidiomycetes, Aphyllophorales) in forests of the Urals and Transurals. Entomol Rev 86(8):889–900CrossRefGoogle Scholar
  127. Krasutskii B (2007a) Coleoptera associated with Fomitopsis pinicola (Sw.: Fr.) Karst. (Basidiomycetes, Aphyllophorales) in the forests of the Urals and Transurals. Entomol Rev 87(7):848–858CrossRefGoogle Scholar
  128. Krasutskii BV (2007b) Beetles (Coleoptera) associated with the polypore Daedaleopsis confragosa (Bolton: Fr.) J. Schrot (Basidiomycetes, Aphyllophorales) in forests of the Urals and Transurals. Entomol Rev 87(5):512–523.  https://doi.org/10.1134/s0013873807050028CrossRefGoogle Scholar
  129. Krasutskii B (2010) Coleoptera associated with the tree fungus Trichaptum biforme (Fr. in Klotzsch) (Basidiomycetes, Aphyllophorales) in the forests of the Urals and the Trans-Ural area. Entomol Rev 90(6):679–688CrossRefGoogle Scholar
  130. Krokene P (2015) Conifer defense and resistance to bark beetles. In: Hofstetter RW, Vega FE (eds) Bark beetles. Academic Press, San Diego, pp 177–207.  https://doi.org/10.1016/B978-0-12-417156-5.00005-8CrossRefGoogle Scholar
  131. Kubartova A, Ottosson E, Dahlberg A, Stenlid J (2012) Patterns of fungal communities among and within decaying logs, revealed by 454 sequencing. Mol Ecol 21(18):4514–4532PubMedCrossRefGoogle Scholar
  132. Kubartová A, Ottosson E, Stenlid J (2015) Linking fungal communities to wood density loss after 12 years of log decay. FEMS Microbiol Ecol 91(5)Google Scholar
  133. Kukor JJ, Martin MM (1983) Acquisition of digestive enzymes by siricid woodwasps from their fungal symbiont. Science 220(4602):1161–1163PubMedCrossRefGoogle Scholar
  134. Lawrence JF (1973) Host preference in ciid beetles (Coleoptera: ciidae) inhabiting the fruiting bodies of Basidiomycetes in North America. Bull Mus Comp Zool Harv Univ 138(2):29–51Google Scholar
  135. Lawrence JF (1989) Mycophagy in the Coleoptera: feeding strategies and morphological adaptations. In: Wilding N, Collins NM, Hammond PM, Webber JF (eds) Insect-fungus interactions. Academic Press, London, pp 1–23Google Scholar
  136. Lawrence JF, Powell JA (1969) Host relationships in North American fungus-feeding moths (Oecophoridae, Oinophilidae, Tineidae). Bull Mus Comp Zool Harv Univ 138(2):29–51Google Scholar
  137. Leach JG, Orr L, Christensen C (1937) Further studies on the interrelationship of insects and fungi in the deterioration of felled Norway pine logs. J Agric Res 55(2)Google Scholar
  138. Leather SR, Baumgart EA, Evans HF, Quicke DLJ (2014) Seeing the trees for the wood-beech (Fagus sylvatica) decay fungal volatiles influence the structure of saproxylic beetle communities. Insect Conserv Divers 7(4):314–326.  https://doi.org/10.1111/icad.12055CrossRefGoogle Scholar
  139. Lilleskov EA, Bruns TD (2005) Spore dispersal of a resupinate ectomycorrhizal fungus, Tomentella sublilacina, via soil food webs. Mycologia 97(4):762–769PubMedCrossRefGoogle Scholar
  140. Lim T (1977) Production, germination and dispersal of basidiospores of Ganoderma pseudoferreum on Hevea. J Rubber Res I Malay 25(2):93–99Google Scholar
  141. Lindblad I (1998) Wood-inhabiting fungi on fallen logs of Norway spruce: relations to forest management and substrate quality. Nord J Bot 18(2):243–255CrossRefGoogle Scholar
  142. Makipaa R, Rajala T, Schigel D, Rinne KT, Pennanen T, Abrego N, Ovaskainen O (2017) Interactions between soil- and dead wood-inhabiting fungal communities during the decay of Norway spruce logs. ISME J.  https://doi.org/10.1038/ismej.2017.57
  143. Malloch D, Blackwell M (1992) Dispersal of fungal diaspores. In: Carroll G, Wicklow D (eds) The fungal community: its organization and role in the ecosystem, vol 9. Mycology. Marcel Dekker, New York, pp 147–171Google Scholar
  144. 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(2):85–95CrossRefGoogle Scholar
  145. Marini L, Bruun HH, Heikkinen RK, Helm A, Honnay O, Krauss J, Kuhn I, Lindborg R, Partel M, Bommarco R (2012) Traits related to species persistence and dispersal explain changes in plant communities subjected to habitat loss. Divers Distrib 18(9):898–908CrossRefGoogle Scholar
  146. Martin MM (1979) Biochemical implications of insect mycophagy. Biol Rev Camb Philos 54(1):1–21CrossRefGoogle Scholar
  147. Martin MM (1983) Cellulose digestion in insects. Comp Biochem Phys A 75(3):313–324.  https://doi.org/10.1016/0300-9629(83)90088-9CrossRefGoogle Scholar
  148. Martin MM (1992) The evolution of insect-fungus associations - from contact to stable symbiosis. Am Zool 32(4):593–605CrossRefGoogle Scholar
  149. Mayers CG, Mcnew DL, Harrington TC, Roeper RA, Fraedrich SW, Biedermann PHW, Castrillo LA, Reed SE (2015) Three genera in the Ceratocystidaceae are the respective symbionts of three independent lineages of ambrosia beetles with large, complex mycangia. Fungal Biol-UK 119(11):1075–1092.  https://doi.org/10.1016/j.funbio.2015.08.002CrossRefGoogle Scholar
  150. McKenna DD, Scully ED, Pauchet Y, Hoover K, Kirsch R, Geib SM, Mitchell RF, Waterhouse RM, Ahn S-J, Arsala D, Benoit JB, Blackmon H, Bledsoe T, Bowsher JH, Busch A, Calla B, Chao H, Childers AK, Childers C, Clarke DJ, Cohen L, Demuth JP, Dinh H, Doddapaneni H, Dolan A, Duan JJ, Dugan S, Friedrich M, Glastad KM, Goodisman MAD, Haddad S, Han Y, Hughes DST, Ioannidis P, Johnston JS, Jones JW, Kuhn LA, Lance DR, Lee C-Y, Lee SL, Lin H, Lynch JA, Moczek AP, Murali SC, Muzny DM, Nelson DR, Palli SR, Panfilio KA, Pers D, Poelchau MF, Quan H, Qu J, Ray AM, Rinehart JP, Robertson HM, Roehrdanz R, Rosendale AJ, Shin S, Silva C, Torson AS, Jentzsch IMV, Werren JH, Worley KC, Yocum G, Zdobnov EM, Gibbs RA, Richards S (2016) Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle–plant interface. Genome Biol 17(1):227.  https://doi.org/10.1186/s13059-016-1088-8CrossRefPubMedPubMedCentralGoogle Scholar
  151. Micó E (2018) Saproxylic insects in tree hollows. In: Ulyshen MD (ed) Saproxylic insects: diversity, ecology and conservation. Springer, Heidelberg, pp 693–727Google Scholar
  152. Misof B, Liu S, Meusemann K, Peters RS, Donath A, Mayer C, Frandsen PB, Ware J, Flouri T, Beutel RG, Niehuis O, Petersen M, Izquierdo-Carrasco F, Wappler T, Rust J, Aberer AJ, Aspöck U, Aspöck H, Bartel D, Blanke A, Berger S, Böhm A, Buckley TR, Calcott B, Chen J, Friedrich F, Fukui M, Fujita M, Greve C, Grobe P, Gu S, Huang Y, Jermiin LS, Kawahara AY, Krogmann L, Kubiak M, Lanfear R, Letsch H, Li Y, Li Z, Li J, Lu H, Machida R, Mashimo Y, Kapli P, McKenna DD, Meng G, Nakagaki Y, Navarrete-Heredia JL, Ott M, Ou Y, Pass G, Podsiadlowski L, Pohl H, von Reumont BM, Schütte K, Sekiya K, Shimizu S, Slipinski A, Stamatakis A, Song W, Su X, Szucsich NU, Tan M, Tan X, Tang M, Tang J, Timelthaler G, Tomizuka S, Trautwein M, Tong X, Uchifune T, Walzl MG, Wiegmann BM, Wilbrandt J, Wipfler B, Wong TKF, Wu Q, Wu G, Xie Y, Yang S, Yang Q, Yeates DK, Yoshizawa K, Zhang Q, Zhang R, Zhang W, Zhang Y, Zhao J, Zhou C, Zhou L, Ziesmann T, Zou S, Li Y, Xu X, Zhang Y, Yang H, Wang J, Wang J, Kjer KM, Zhou X (2014) Phylogenomics resolves the timing and pattern of insect evolution. Science 346(6210):763–767.  https://doi.org/10.1126/science.1257570CrossRefPubMedPubMedCentralGoogle Scholar
  153. Montoya D, Zavala MA, Rodriguez MA, Purves DW (2008) Animal versus wind dispersal and the robustness of tree species to deforestation. Science 320(5882):1502–1504PubMedCrossRefGoogle Scholar
  154. Mound L (1974) Spore-feeding thrips (Phlaeothripidae) from leaf litter and dead wood in Australia. Aust J Zool Suppl Ser 22(27):1–106.  https://doi.org/10.1071/AJZS027CrossRefGoogle Scholar
  155. Mueller UG, Gerardo NM, Aanen DK, Six DL, Schultz TR (2005) The evolution of agriculture in insects. Annu Rev Ecol Evol S 36:563–595.  https://doi.org/10.1146/annurev.ecolsys.36.102003.152626CrossRefGoogle Scholar
  156. Müller MM, Varama M, Heinonen J, Hallaksela A-M (2002) Influence of insects on the diversity of fungi in decaying spruce wood in managed and natural forests. For Ecol Manag 166(1):165–181CrossRefGoogle Scholar
  157. Müller DWH, Codron D, Meloro C, Munn A, Schwarm A, Hummel J, Clauss M (2013) Assessing the Jarman–Bell principle: scaling of intake, digestibility, retention time and gut fill with body mass in mammalian herbivores. Comp Biochem Phys A 164(1):129–140.  https://doi.org/10.1016/j.cbpa.2012.09.018CrossRefGoogle Scholar
  158. Nakashima T, Iizuka T, Ogura K, Maeda M, Tanaka T (1972) Isolation of some microorganisms associated with five species of ambrosia beetles and two kinds of antibiotics produced by Xv-3 strain in this isolates. J Fac Agric Hokkaido Univ 61:60–72Google Scholar
  159. N'Dri AB, Gignoux J, Konaté S, Dembélé A, Aïdara D (2011) Origin of trunk damage in West African savanna trees: the interaction of fire and termites. J Trop Ecol 27(3):269–278CrossRefGoogle Scholar
  160. Neger FW (1909) Ambrosiapilze. ii. Die Ambrosia der Holzbohrkafer. Berlin Ber D bot Ges 27(372-389)Google Scholar
  161. Newell K (1984) Interaction between two decomposer basidiomycetes and a collembolan under Sitka spruce: grazing and its potential effects on fungal distribution and litter decomposition. Soil Biol Biochem 16(3):235–239.  https://doi.org/10.1016/0038-0717(84)90007-5CrossRefGoogle Scholar
  162. Nielsen MT, Klejnstrup ML, Rohlfs M, Anyaogu DC, Nielsen JB, Gotfredsen CH, Andersen MR, Hansen BG, Mortensen UH, Larsen TO (2013) Aspergillus nidulans synthesize insect juvenile hormones upon expression of a heterologous regulatory protein and in response to grazing by Drosophila melanogaster larvae. PLoS One 8(8):e73369.  https://doi.org/10.1371/journal.pone.0073369CrossRefPubMedPubMedCentralGoogle Scholar
  163. Nikitsky NB, Schigel DS (2004) Beetles in polypores of the Moscow region: checklist and ecological notes. Entomol Fenn 15(1):6–22Google Scholar
  164. Nilsson T (1976) Soft-rot fungi - decay patterns and enzyme production. In: Becker G, Liese W (eds) Organismen und Holz. Duncker und Humblot, Berlin, pp 103–112Google Scholar
  165. Nobre T, Rouland-Lefèvre C, Aanen DK (2011) Comparative biology of fungus cultivation in termites and ants. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer Netherlands, Dordrecht, pp 193–210.  https://doi.org/10.1007/978-90-481-3977-4_8CrossRefGoogle Scholar
  166. Norros V (2013) Measuring and modelling airborne dispersal in wood decay fungi. University of HelsinkiGoogle Scholar
  167. Norros V, Penttila R, Suominen M, Ovaskainen O (2012) Dispersal may limit the occurrence of specialist wood decay fungi already at small spatial scales. Oikos 121(6):961–974CrossRefGoogle Scholar
  168. Nuss I (1982) Die Bedeutung der Proterosporen: Schlußfolgerungen aus Untersuchungen anGanoderma (Basidiomycetes). Plant Syst Evol 141(1):53–79CrossRefGoogle Scholar
  169. Økland B (1995) Insect fauna compared between six polypore species in a southern Norwegian spruce forest. Fauna Norv Ser B 42:21–26Google Scholar
  170. Økland B (1996) Unlogged forests: important sites for preserving the diversity of mycetophilids (Diptera: Sciaroidea). Biol Conserv 76(3):297–310.  https://doi.org/10.1016/0006-3207(95)00129-8CrossRefGoogle Scholar
  171. Orledge GM, Reynolds SE (2005) Fungivore host-use groups from cluster analysis: patterns of utilisation of fungal fruiting bodies by ciid beetles. Ecol Entomol 30(6):620–641.  https://doi.org/10.1111/j.0307-6946.2005.00727.xCrossRefGoogle Scholar
  172. Ottosson E (2013) Succession of wood-inhabiting fungal communities, PhD thesis. Swedish University of Agricultural Sciences, UppsalaGoogle Scholar
  173. Ottosson E, Kubartová A, Edman M, Jönsson M, Lindhe A, Stenlid J, Dahlberg A (2015) Diverse ecological roles within fungal communities in decomposing logs of Picea abies. FEMS Microbiol Ecol 91(3):fiv012Google Scholar
  174. Ovaskainen O, Schigel D, Ali-Kovero H, Auvinen P, Paulin L, Norden B, Norden J (2013) Combining high-throughput sequencing with fruit body surveys reveals contrasting life-history strategies in fungi. ISME J 7(9):1696–1709PubMedPubMedCentralCrossRefGoogle Scholar
  175. Owen-Smith RN (1988) Megaherbivores. The influence of very large body size on ecology, Cambridge studies in ecology. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  176. Parfitt D, Hunt J, Dockrell D, Rogers HJ, Boddy L (2010) Do all trees carry the seeds of their own destruction? PCR reveals numerous wood decay fungi latently present in sapwood of a wide range of angiosperm trees. Fungal Ecol 3(4):338–346CrossRefGoogle Scholar
  177. Park MS, Fong JJ, Lee H, Shin S, Lee S, Lee N, Lim YW (2014) Determination of coleopteran insects associated with spore dispersal of Cryptoporus volvatus (Polyporaceae: Basidiomycota) in Korea. J Asia-Pac Entomol 17(4):647–651CrossRefGoogle Scholar
  178. Paviour-Smith K (1960) The fruiting-bodies of macrofungi as habitats for beetles of the family Clidae (Coleoptera). Oikos 11 (1):43–71.  https://doi.org/10.2307/3564883CrossRefGoogle Scholar
  179. Persiani AM, Audisio P, Lunghini D, Maggi O, Granito VM, Biscaccianti AB, Chiavetta U, Marchetti M (2010) Linking taxonomical and functional biodiversity of saproxylic fungi and beetles in broad-leaved forests in southern Italy with varying management histories. Plant Biosyst 144(1):250–261.  https://doi.org/10.1080/11263500903561114CrossRefGoogle Scholar
  180. Persson Y, Ihrmark K, Stenlid J (2011) Do bark beetles facilitate the establishment of rot fungi in Norway spruce? Fungal Ecol 4(4):262–269CrossRefGoogle Scholar
  181. Pettey TM, Shaw CG (1986) Isolation of Fomitopsis pinicola from in-flight bark beetles (Coleoptera: Scolytidae). Can J Bot 64(7):1507–1509CrossRefGoogle Scholar
  182. Poldmaa K, Kaasik A, Tammaru T, Kurina O, Jurgenstein S, Teder T (2016) Polyphagy on unpredictable resources does not exclude host specialization: insects feeding on mushrooms. Ecology 97(10):2824–2833PubMedCrossRefPubMedCentralGoogle Scholar
  183. Pollierer MM, Langel R, Scheu S, Maraun M (2009) Compartmentalization of the soil animal food web as indicated by dual analysis of stable isotope ratios (N-15/N-14 and C-13/C-12). Soil Biol Biochem 41(6):1221–1226CrossRefGoogle Scholar
  184. Rajala T, Peltoniemi M, Hantula J, Makipaa R, Pennanen T (2011) RNA reveals a succession of active fungi during the decay of Norway spruce logs. Fungal Ecol 4(6):437–448.  https://doi.org/10.1016/j.funeco.2011.05.005CrossRefGoogle Scholar
  185. Rajala T, Peltoniemi M, Pennanen T, Makipaa R (2012) Fungal community dynamics in relation to substrate quality of decaying Norway spruce (Picea abies [L.] Karst.) logs in boreal forests. FEMS Microbiol Ecol 81(2):494–505.  https://doi.org/10.1111/j.1574-6941.2012.01376.xCrossRefPubMedPubMedCentralGoogle Scholar
  186. Rajala T, Tuomivirta T, Pennanen T, Mäkipää R (2015) Habitat models of wood-inhabiting fungi along a decay gradient of Norway spruce logs. Fungal Ecol 18:48–55.  https://doi.org/10.1016/j.funeco.2015.08.007CrossRefGoogle Scholar
  187. Ranius T, Jansson N (2000) The influence of forest regrowth, original canopy cover and tree size on saproxylic beetles associated with old oaks. Biol Conserv 95(1):85–94.  https://doi.org/10.1016/S0006-3207(00)00007-0CrossRefGoogle Scholar
  188. Rawlins JE (1984) Mycophagy in Lepidoptera. In: Wheeler Q, Blackwell M (eds) Fungus-insect relationships: perspectives in ecology and evolution. Columbia University Press, New YorkGoogle Scholar
  189. Rayner A, Boddy L (1988) Fungal communities in the decay of wood. In: Advances in microbial ecology, vol 10. Springer, Berlin, pp 115–166CrossRefGoogle Scholar
  190. Riley R, Haridas S, Wolfe KH, Lopes MR, Hittinger CT, Göker M, Salamov AA, Wisecaver JH, Long TM, Calvey CH, Aerts AL, Barry KW, Choi C, Clum A, Coughlan AY, Deshpande S, Douglass AP, Hanson SJ, Klenk H-P, LaButti KM, Lapidus A, Lindquist EA, Lipzen AM, Meier-Kolthoff JP, Ohm RA, Otillar RP, Pangilinan JL, Peng Y, Rokas A, Rosa CA, Scheuner C, Sibirny AA, Slot JC, Stielow JB, Sun H, Kurtzman CP, Blackwell M, Grigoriev IV, Jeffries TW (2016) Comparative genomics of biotechnologically important yeasts. Proc Natl Acad Sci Biol 113(35):9882–9887.  https://doi.org/10.1073/pnas.1603941113CrossRefGoogle Scholar
  191. Rohlfs M (2015) Fungal secondary metabolite dynamics in fungus-grazer interactions: novel insights and unanswered questions. Front Microbiol 5Google Scholar
  192. Rösch R, Liese W (1971) Untersuchungen über die Enzyme von Bläuepilzen. Archiv für Mikrobiologie 76(3):212–218.  https://doi.org/10.1007/bf00409117CrossRefPubMedPubMedCentralGoogle Scholar
  193. Saucedo JR, Ploetz RC, Konkol JL, Ángel M, Mantilla J, Menocal O, Carrillo D (2017) Nutritional symbionts of a putative vector, Xyleborus bispinatus, of the laurel wilt pathogen of avocado, Raffaelea lauricola. Symbiosis.  https://doi.org/10.1007/s13199-017-0514-3
  194. Schigel DS (2011) Polypore-beetle associations in Finland. Ann Zool Fenn 48(6):319–348CrossRefGoogle Scholar
  195. Schigel D (2012) Fungivory of saproxylic Coleoptera: the mystery of rejected polypores. Stud For Slov 137:53–58Google Scholar
  196. Schigel D, Niemelä T, Kinnunen J (2006) Polypores of western Finnish Lapland and seasonal dynamics of polypore beetles. Karstenia 46:37–64CrossRefGoogle Scholar
  197. Schlick-Steiner BC, Steiner FM, Konrad H, Seifert B, Christian E, Moder K, Stauffer C, Crozier RH (2008) Specificity and transmission mosaic of ant nest-wall fungi. Proc Natl Acad Sci USA 105(3):940–943.  https://doi.org/10.1073/pnas.0708320105CrossRefPubMedPubMedCentralGoogle Scholar
  198. Schupp EW, Jordano P, Gomez JM (2010) Seed dispersal effectiveness revisited: a conceptual review. New Phytol 188(2):333–353PubMedCrossRefPubMedCentralGoogle Scholar
  199. Seibold S, Mueller J, Baldrian P, Cadotte MW, Stursova M, Biedermann PHW, Baessler C (2018) Vectoring of fungi by beetles dispersing from dead wood – Let’s take the beetle bus! Am Nat (submitted)Google Scholar
  200. Seifert B (2006) Social cleptogamy in the ant subgenus Chthonolasius - survival as a minority. Abhandlungen und Berichte des Naturkundemuseums Görlitz 77:251–276Google Scholar
  201. Sevcik J (2001) Diptera (excluding Mycetophilidae S. str.) associated with fungi in Czech and Slovak Republics: a survey of rearing records from 1998-2000. Acta Universitatis Carolinae Biologica 45:157–168Google Scholar
  202. Sevcik J (2003) Insects associated with wood-decaying fungi in the Czech and Slovak republics: a review of present knowledge. Biol Ecol:9Google Scholar
  203. Shaw PJA (1992) Fungi, fungivores and fungal food webs. In: Carroll G, Wicklow D (eds) The fungal community: its organisation and role in ecosystems. CRC Press, New York, pp 295–310Google Scholar
  204. Sherwood-Pike MA, Gray J (1985) Silurian fungal remains: probable records of the Class Ascomycetes. Lethaia 18(1):1–20.  https://doi.org/10.1111/j.1502-3931.1985.tb00680.xCrossRefGoogle Scholar
  205. Siitonen J, Ranius T (2015) The importance of veteran trees for saproxylic insects. In: Kirby KJ, Watkins C (eds) Europe’s changing woods and forests: from wildwood to managed landscapes. CABI, OxfordshireGoogle Scholar
  206. Six DL (2003) A comparison of mycangial and phoretic fungi of individual mountain pine beetles. Can J For Res 33(7):1331–1334.  https://doi.org/10.1139/X03-047CrossRefGoogle Scholar
  207. Six DL (2012) Ecological and evolutionary determinants of bark beetle-fungus symbioses. Insects 3(1):339–366PubMedPubMedCentralCrossRefGoogle Scholar
  208. Six D (2013) The bark beetle holobiont: why microbes matter. J Chem Ecol:1–14.  https://doi.org/10.1007/s10886-013-0318-8
  209. Stokland JN, Siitonen J, Jonsson BG (2012) Biodiversity in dead wood. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  210. Stötefeld L, Scheu S, Rohlfs M (2012) Fungal chemical defence alters density-dependent foraging behaviour and success in a fungivorous soil arthropod. Ecol Entomol 37(5):323–329.  https://doi.org/10.1111/j.1365-2311.2012.01373.xCrossRefGoogle Scholar
  211. Strid Y, Schroeder M, Lindahl B, Ihrmark K, Stenlid J (2014) Bark beetles have a decisive impact on fungal communities in Norway spruce stem sections. Fungal Ecol 7:47–58.  https://doi.org/10.1016/j.funeco.2013.09.003CrossRefGoogle Scholar
  212. Suh SO, Blackwell M (2005) Four new yeasts in the Candida mesenterica clade associated with basidiocarp-feeding beetles. Mycologia 97(1):167–177PubMedCrossRefPubMedCentralGoogle Scholar
  213. Suh SO, McHugh JV, Pollock DD, Blackwell M (2005) The beetle gut: a hyperdiverse source of novel yeasts. Mycol Res 109(Pt 3):261–265PubMedPubMedCentralCrossRefGoogle Scholar
  214. Sverdrup-Thygeson A, Skarpaas O, Odegaard F (2010) Hollow oaks and beetle conservation: the significance of the surroundings. Biodivers Conserv 19(3):837–852.  https://doi.org/10.1007/s10531-009-9739-7CrossRefGoogle Scholar
  215. Swift MJ, Boddy L (1984) Animal-microbial interactions during wood decomposition. In: Anderson JM, Rayner ADM, Walton DWH (eds) Invertebrate-microbe interactions. Cambridge University Press, Cambridge, pp 89–131Google Scholar
  216. Talbot P (1952) Dispersal of fungus spores by small animals inhabiting wood and bark. Trans Br Mycol Soc 35(2):123–128CrossRefGoogle Scholar
  217. Tanahashi M, Hawes CJ (2016) The presence of a mycangium in European Sinodendron cylindricum (Coleoptera: Lucanidae) and the associated yeast symbionts. J Insect Sci 16(1):76.  https://doi.org/10.1093/jisesa/iew054CrossRefPubMedPubMedCentralGoogle Scholar
  218. Tanahashi M, Matsushita N, Togashi K (2009) Are stag beetles fungivorous? J Insect Physiol 55(11):983–988.  https://doi.org/10.1016/j.jinsphys.2009.07.002CrossRefPubMedPubMedCentralGoogle Scholar
  219. Tanahashi M, Kubota K, Matsushita N, Togashi K (2010) Discovery of mycangia and the associated xylose-fermenting yeasts in stag beetles (Coleoptera: Lucanidae). Naturwissenschaften 97(3):311–317PubMedPubMedCentralCrossRefGoogle Scholar
  220. Thompson BM, Grebenok RJ, Behmer ST, Gruner DS (2013) Microbial symbionts Shape the sterol profile of the xylem-feeding woodwasp, Sirex noctilio. J Chem Ecol 39(1):129–139.  https://doi.org/10.1007/s10886-012-0222-7CrossRefPubMedPubMedCentralGoogle Scholar
  221. Thompson BM, Bodart J, McEwen C, Gruner DS (2014) Adaptations for symbiont-mediated external digestion in Sirex noctilio (Hymenoptera: Siricidae). Ann Entomol Soc Am 107(2):453–460.  https://doi.org/10.1603/An13128CrossRefGoogle Scholar
  222. Thorn S, Müller J, Bässler C, Gminder A, Brandl R, Heibl C (2015) Host abundance, durability, basidiome form and phylogenetic isolation determine fungivore species richness. Biol J Linn Soc 114(3):699–708.  https://doi.org/10.1111/bij.12447CrossRefGoogle Scholar
  223. Thunes KH, Midtgaard F, Gjerde I (2000) Diversity of coleoptera of the bracket fungus Fomitopsis pinicola in a Norwegian spruce forest. Biodivers Conserv 9(6):833–852CrossRefGoogle Scholar
  224. Toong YC, Schooley DA, Baker FC (1988) Isolation of insect juvenile hormone III from a plant. Nature 333(6169):170–171CrossRefGoogle Scholar
  225. Tordoff GM, Boddy L, Jones TH (2008) Species-specific impacts of collembola grazing on fungal foraging ecology. Soil Biol Biochem 40(2):434–442.  https://doi.org/10.1016/j.soilbio.2007.09.006CrossRefGoogle Scholar
  226. Tuno N (1999) Insect feeding on spores of a bracket fungus, Elfvingia applanata (Pers.) Karst. (Ganodermataceae, Aphyllophorales). Ecol Res 14(2):97–103CrossRefGoogle Scholar
  227. Ulyshen MD (2015) Insect-mediated nitrogen dynamics in decomposing wood. Ecol Entomol 40:97–112CrossRefGoogle Scholar
  228. Ulyshen MD (2018) Saproxylic Diptera. In: Ulyshen MD (ed) Saproxylic insects: diversity, ecology and conservation. Springer, Heidelberg, pp 167–192Google Scholar
  229. Ulyshen MD, Muller J, Seibold S (2016) Bark coverage and insects influence wood decomposition: direct and indirect effects. Appl Soil Ecol 105:25–30.  https://doi.org/10.1016/j.apsoil.2016.03.017CrossRefGoogle Scholar
  230. Urbina H, Blackwell M (2012) Multilocus phylogenetic study of the scheffersomyces yeast clade and characterization of the N-terminal region of xylose reductase gene. PLoS One 7(6).  https://doi.org/10.1371/journal.pone.0039128PubMedPubMedCentralCrossRefGoogle Scholar
  231. Urbina H, Schuster J, Blackwell M (2013) The gut of Guatemalan passalid beetles: a habitat colonized by cellobiose- and xylose-fermenting yeasts. Fungal Ecol 6(5):339–355.  https://doi.org/10.1016/j.funeco.2013.06.005CrossRefGoogle Scholar
  232. van der Wal A, Ottosson E, de Boer W (2015) Neglected role of fungal community composition in explaining variation in wood decay rates. Ecology 96(1):124–133PubMedCrossRefPubMedCentralGoogle Scholar
  233. Vega FE, Blacwell M (eds) (2005) Insect-fungal associations: ecology and evolution. Oxford University Press, OxfordGoogle Scholar
  234. Vega FE, Dowd PF (2005) The role of yeasts as insect endosymbionts. In: Vega FE, Blackwell M (eds) Insect-fungal assocations: ecology and evolution. Oxford University Press, New York, pp 211–243Google Scholar
  235. Walker LP, Wilson DB (1991) Enzymatic hydrolysis of cellulose: an overview. Bioresour Technol 36(1):3–14.  https://doi.org/10.1016/0960-8524(91)90095-2CrossRefGoogle Scholar
  236. Watkinson SC, Boddy L, Money N (2015) The fungi. Academic Press, LondonGoogle Scholar
  237. Werner PA, Prior LD (2007) Tree-piping termites and growth and survival of host trees in savanna woodland of north Australia. J Trop Ecol 23(06):611–622CrossRefGoogle Scholar
  238. Weslien J, Djupström LB, Schroeder M, Widenfalk O (2011) Long-term priority effects among insects and fungi colonizing decaying wood. J Anim Ecol 80(6):1155–1162PubMedPubMedCentralCrossRefGoogle Scholar
  239. Wheeler Q, Blackwell M (eds) (1984) Fungus-insect relationships. Columbia University Press, New YorkGoogle Scholar
  240. Whitman WB, Coleman DC, Wiebe WJ (1998) Prokaryotes: the unseen majority. Proc Natl Acad Sci Biol 95(12):6578–6583CrossRefGoogle Scholar
  241. Wilding N, Collins NM, Hammond PM, Webber JF (eds) (1989) Insect-fungus interactions. Academic Press, LondonGoogle Scholar
  242. Wood TG, Thomas JR (1989) The mutualistic association between Macrotermitinae and Termitomyces. In: Wilding N, Collins CD, Hammond PM, Webber JF (eds) Insect-fungus interactions. Academic Press, London, pp 69–92CrossRefGoogle Scholar
  243. Yamashita S, Ando K, Hoshina H, Ito N, Katayama Y, Kawanabe M, Maruyama M, Itioka T (2015) Food web structure of the fungivorous insect community on bracket fungi in a Bornean tropical rain forest. Ecol Entomol 40(4):390–400.  https://doi.org/10.1111/een.12200CrossRefGoogle Scholar
  244. Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32(5):723–735PubMedCrossRefPubMedCentralGoogle Scholar
  245. Zuo J, Fonck M, van Hal J, Cornelissen JHC, Berg MP (2014) Diversity of macro-detritivores in dead wood is influenced by tree species, decay stage and environment. Soil Biol Biochem 78:288–297CrossRefGoogle Scholar

Copyright information

© This is a U.S. government work and its text is not subject to copyright protection in the United States; however, its text may be subject to foreign copyright protection.  2018

Authors and Affiliations

  • Tone Birkemoe
    • 1
  • Rannveig M. Jacobsen
    • 1
  • Anne Sverdrup-Thygeson
    • 1
  • Peter H. W. Biedermann
    • 2
  1. 1.Faculty of Environmental Sciences and Natural Resource Management (MINA)Norwegian University of Life Sciences (NMBU)AasNorway
  2. 2.Research Group Insect-Fungus Symbiosis, Department of Animal Ecology and Tropical BiologyUniversity of WürzburgWürzburgGermany

Personalised recommendations