Abstract
An enormous variety of volatile substances are released in distinctive blends by fungal substrates that should be recognisable for fungivores. Certain compounds dominate in most of the fungal species. Fungal oxylipins as the eight-carbon volatiles are the most prominent. This raises the question whether such are specific enough to qualify as appropriate host cues for a fungivore. We could demonstrate differentiated responses of the fungivorous beetle Bolitophagus reticulatus to eight-carbon volatiles: Nine eight-carbon volatiles were identified with GC–MS from its host fungus Fomes fomentarius. 1-Octen-3-ol, 3-octanone and 3-octanol induced contrasting behaviour of beetles in olfactometer bioassays. Electroantennographic experiments investigating the beetle olfactory sense revealed distinguishable antennal responses. Moreover, their individual release from F. fomentarius fruiting bodies changes not only considerably, but also independently over successive stages of beetle colonisation. Concentrations of attractive and repellent eight-carbon volatiles correlate to frequency of beetles in the field and further substantiate their relevance as host cues. Our results show that a specialist fungivore is able to differentiate the most common eight-carbon volatiles of fungi to assess host quality. Key roles and marked similarities of fungal to plant oxylipins suggest a comparable importance of eight-carbon volatiles to fungivores as green leaf volatiles have to herbivores.
Similar content being viewed by others
References
Allison JD, Borden JH, Seybold SJ (2004) A review of the chemical ecology of the Cerambycidae (Coleoptera). Chemoecology 14:123–150. doi:10.1007/s00049-004-0277-1
Bouget C, Brustel H, Brin A, Valladres L (2009) Evaluation of window flight traps for effectiveness at monitoring dead wood-associated beetles: the effect of ethanol lure under contrasting environmental conditions. Agric For Entomol 11:143–152. doi:10.1111/j.1461-9563.2008.00400.x
Brodhun F, Feussner I (2011) Oxylipins in fungi. FEBS J 278:1047–1063. doi:10.1111/j.1742-4658.2011.08027.x
Brodhun F, Schneider S, Göbel C, Hornung E, Feussner I (2010) PpoC from Aspergillus nidulans is a fusion protein with only one active haem. Biochem J 425:553–565. doi:10.1042/BJ20091096
Bruce TJA, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends Plant Sci 10:269–274. doi:10.1016/j.tplants.2005.04.003
Byers JA, Zhang QH, Birgersson G (2000) Strategies of a bark beetle, Pityogenes bidentatus, in an olfactory landscape. Naturwissenschaften 87:503–507. doi:10.1007/s001140050768
Chen CC, Wu CM (1984) Studies on the enzymic reduction of 1-octen-3-one in mushroom (Agaricus bisporus). J Agr Food Chem 32:1342–1344. doi:10.1021/jf00126a030
Chiron N, Michelot D (2005) Odeurs des champignons: chimie et rôle dans les interactions biotiques—une revue (in French). Cryptogam, Mycol 26:299–364
Christensen SA, Kolomiets MV (2011) The lipid language of plant–fungal interactions. Fungal Genet Biol 48:4–14. doi:10.1016/j.fgb.2010.05.005
Combet E, Henderson J, Daniel CE, Burton KS (2006) Eight-carbon volatiles in mushrooms and fungi: properties, analysis, and biosynthesis. Mycoscience 47:317–326. doi:10.1007/s10267-006-0318-4
Combet E, Henderson J, Eastwood DC, Burton KS (2009) Influence of sporophore development, damage, storage, and tissue specificity on the enzymic formation of volatiles in mushrooms (Agaricus bisporus). J Agr Food Chem 57:3709–3717. doi:10.1021/jf8036209
Cometto-Muñiz JE, Abraham MH (2010) Odour detection by humans of lineal aliphatic aldehydes and helional as gauged by dose-response functions. Chem Senses 35:289–299. doi:10.1093/chemse/bjq018
Drilling K, Dettner K (2009) Electrophysiological responses of four fungivorous coleoptera to volatiles of Trametes versicolor: implications for host selection. Chemoecology 19:109–115. doi:10.1007/s00049-009-0015-9
Fäldt J, Jonsell M, Nordlander G, Borg-Karlson AK (1999) Volatiles of bracket fungi Fomitopsis pinicola and Fomes fomentarius and their functions as insect attractants. J Chem Ecol 25:567–590. doi:10.1023/A:1020958005023
Gara RI, Littke WR, Rhoades DF (1993) Emission of ethanol and monoterpenes by fungal infected lodgepole pine trees. Phytochemistry 34:987–990. doi:10.1016/S0031-9422(00)90699-X
Getz WM, Lánsky P (2001) Receptor dissociation constants and the information entropy of membranes coding ligand concentration. Chem Senses 26:95–104. doi:10.1093/chemse/26.2.95
Hågvar S (1999) Saproxylic beetles visiting living sporocarps of Fomitopsis pinicola and Fomes fomentarius. Nor J Entomol 46:25–32
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 25–68
Holighaus G, Schütz S (2006) Odors of wood decay as semiochemicals for Trypodendron domesticum L. (Col., Scolytidae). Mitt dtsch Ges allg angew Entomol 15:161–165
Inamdar AA, Masurekar P, Bennett JW (2010) Neurotoxicity of fungal volatile organic compounds in Drosophila melanogaster. Toxicol Sci 117:418–426. doi:10.1093/toxsci/kfq222
Jonsell M, Nordlander G (1995) Field attraction of Coleoptera to odours of the wood-decaying polypores Fomitopsis pinicola and Fomes fomentarius. Ann Zool Fenn 32:391–402
Jonsell M, Nordlander G (2004) Host selection patterns in insects breeding in bracket fungi. Ecol Entomol 29:697–705. doi:10.1111/j.0307-6946.2004.00654.x
Jonsell M, Nordlander G, Jonsson M (1999) Colonisation patterns of insects breeding in wood-decaying fungi. J Insect Conserv 3:145–161. doi:10.1023/A:1009665513184
Jonsell M, Nordlander G, Ehnström B (2001) Substrate associations of insects breeding in fruiting bodies of wood-decaying fungi. Ecol Bull 49:173–194
Jonsell M, Schroeder M, Larsson T (2003) The saproxylic beetle Bolitophagus reticulatus: its frequency in managed forests, attraction to volatiles and flight period. Ecography 26:421–428. doi:10.1034/j.1600-0587.2003.03449.x
Kachroo A, Kachroo P (2009) Fatty acid–derived signals in plant defense. Annu Rev Phytopathol 47:153–176. doi:10.1146/annurev-phyto-080508-081820
Knaden M, Strutz A, Ahsan J, Sachse S, Hansson BS (2012) Spatial representation of odorant valence in an insect brain. Cell Rep 1:392–399. doi:10.1016/j.celrep.2012.03.002
Knezevic SZ, Streibig JC, Ritz C (2007) Utilising R software package for dose-response studies: the concept and data analysis. Weed Technol 21:840–848. doi:10.1614/WT-06-161.1
Kües U, Navarro-González M (2009) Communication of fungi on individual, species, kingdom, and above kingdom levels. In: Anke T, Weber D (eds) The Mycota. Physiology and genetics. Selected basic and applied aspects, vol. 15. Springer, Berlin, pp 79–106. doi:10.1007/978-3-642-00286-1_5
Matthewman WG, Pielou DP (1971) Arthropods inhabiting the sporophores of Fomes fomentarius (Polyporaceae) in Gatineau Park, Quebec. Can Entomol 103:775–847. doi:10.4039/Ent103775-6
Mau JL, Chyau CC, Li JY, Tseng YH (1997) Flavor compounds in straw mushrooms Volvariella volvacea harvested at different stages of maturity. J Agr Food Chem 45:4726–4729. doi:10.1021/jf9703314
McLafferty FW (2009) Registry of mass spectral data combined with NIST/EPA/NIH database 2008. Wiley-Blackwell, Hoboken
Midtgaard F, Rukke BA, Sverdrup-Thygeson A (1998) Habitat use of the fungivorous beetle Bolitophagus reticulatus (Coleoptera: Tenebrionidae): Effects of basidiocarp size, humidity and competitors. Eur J Entomol 95:559–570
Müller-Using S, Bartsch N (2009) Decay dynamic of coarse and fine woody debris of a beech (Fagus sylvatica L.) forest in central Germany. Eur J Forest Res 128:287–296. doi:10.1007/s10342-009-0264-8
Mushobozy DK, Pierce HD, Borden JH (1993) Evaluation of 1-octen-3-o1 and nonanal as adjuvants for aggregation pheromones for three species of cucujid beetles (Coleoptera: Cucujidae). J Econ Entomol 86:1835–1845
Nadvornaya LS, Nadvornyy VG (1991) Biology of the beetles Bolitophagus reticulatus L. and Uloma culinaris L. (Coleoptera, Tenebrionidae) in the forest-steppe zone of Ukraine. Entomol Rev 70:35–40 (originally published in Ėntomologičeskoe Obozrenie 70:349–354, in Russian)
Nilsson T (1997) Survival and habitat preferences of adult Bolitophagus reticulatus. Ecol Entomol 22:82–89. doi:10.1046/j.1365-2311.1997.00035.x
Ômura H, Kuwahara Y, Tanabe T (2002) 1-Octen-3-ol together with geosmin: new secretion compounds from a polydesmid millipede, Niponia nodulosa. J Chem Ecol 28:2601–2612. doi:10.1023/A:1021400606217
Pfeil RM, Mumma RO (1993) Bioassay for evaluating attraction of the phorid fly, Megaselia halterata to compost colonised by the commercial mushroom, Agaricus bisporus and to 1-octen-3-ol and 3-octanone. Entomol Exp Appl 69:137–144. doi:10.1111/j.1570-7458.1993.tb01736.x
Pierce AM, Pierce HD, Oehlschlager AC, Borden JH (1991a) 1-Octen-3-ol, attractive semiochemical for foreign grain beetle, Ahasverus advena (Waltl) (Coleoptera: Cucujidae). J Chem Ecol 17:567–580. doi:10.1007/BF00982127
Pierce AM, Pierce HD, Borden JH, Oehlschlager AC (1991b) Fungal volatiles: semiochemicals for stored-product beetles (Coleoptera: Cucujidae). J Chem Ecol 17:581–597. doi:10.1007/BF00982128
Piveteau F, Le Guen S, Gandemer G, Baud JP, Prost C, Demaimay M (2000) Aroma of fresh oysters Crassostrea gigas: composition and aroma notes. J Agr Food Chem 48:4851–4857. doi:10.1021/jf991394k
Ranius T (2006) Measuring the dispersal of saproxylic insects: a key characteristic for their conservation. Popul Ecol 48:177–188. doi:10.1007/s10144-006-0262-3
Ritz C, Streibig JC (2008) Nonlinear regression with R. Springer Science + Business Media, New York
Rohlfs M, Churchill ACL (2011) Fungal secondary metabolites as modulators of interactions with insects and other arthropods. Fungal Genet Biol 48:23–34. doi:10.1016/j.fgb.2010.08.008
Rösecke J, Pietsch M, König WA (2000) Volatile constituents of wood-rotting basidiomycetes. Phytochemistry 54:747–750. doi:10.1016/S0031-9422(00)00138-2
Sawahata T, Shimano S, Suzuki M (2008) Tricholoma matsutake 1-octen-3-ol and methyl cinnamate repel mycophagous Proisotoma minuta (Collembola: Insecta). Mycorrhiza 18:111–114. doi:10.1007/s00572-007-0158-x
Schütz S, Weißbecker B, Koch UT, Hummel HE (1999) Detection of volatiles released by diseased potato tubers using a biosensor on the basis of intact insect antennae. Biosens Bioelectron 14:221–228. doi:10.1016/S0956-5663(98)00092-X
Sieber TN (2007) Endophytic fungi in forest trees: are they mutualists? Fungal Biol Rev 21:75–89. doi:10.1016/j.fbr.2007.05.004
Thakeow P (2008) Development of a basic biosensor system for wood degradation using volatile organic compounds. Dissertation, Göttingen University, Göttingen, Germany
Thakeow P, Angeli S, Weißbecker B, Schütz S (2008) Antennal and behavioral responses of Cis boleti to fungal odour of Trametes gibbosa. Chem Senses 33:379–387. doi:10.1093/chemse/bjn005
Tressl R, Bahri D, Engel KH (1982) Formation of eight-carbon and ten-carbon components in mushrooms (Agaricus campestris). J Agr Food Chem 30:89–93. doi:10.1021/jf00109a019
Trienens M, Rohlfs M (2012) Insect–fungus interference competition—the potential role of global secondary metabolite regulation, pathway-specific mycotoxin expression and formation of oxylipins. Fungal Ecol 5:191–199. doi:10.1016/j.funeco.2011.07.009
Tsitsigiannis DI, Keller NP (2007) Oxylipins as developmental and host–fungal communication signals. Trends Microbiol 15:109–118. doi:10.1016/j.tim.2007.01.005
van Giessen WA, Fescemyer HW, Burrows PM, Peterson JK, Barnett OW (1994) Quantification of electroantennogram responses of the primary rhinaria of Acyrthosiphon pisum (Harris) to C4–C8 primary alcohols and aldehydes. J Chem Ecol 20:909–927. doi:10.1007/BF02059587
Visser JH (1986) Host odor perception in phytophagous insects. Annu Rev Entomol 31:121–144. doi:10.1146/annurev.ento.31.1.121
Weissbecker B, Holighaus G, Schütz S (2004) Gas chromatography with mass spectrometric and electroantennographic detection: analysis of wood odorants by direct coupling of insect olfaction and mass spectrometry. J Chromatogr A 1056:209–216. doi:10.1016/j.chroma.2004.06.120
Wood WF, Archer CL, Largent DL (2001) 1-Octen-3-ol, a banana slug antifeedant from mushrooms. Biochem Syst Ecol 29:531–533. doi:10.1016/S0305-1978(00)00076-4
Wurzenberger M, Grosch W (1983) Bestimmung von 1-Octen-3-ol in Pilzen und Pilzprodukten (in German). Z Lebensm Unters Forsch A 176:16–19
Wurzenberger M, Grosch W (1986) Enzymic oxidation of linolenic acid to 1, Z-5-octadien-3-ol, Z-2, Z-5-octadien-1-ol and 10-oxo-E-8-decenoic acid by a protein fraction from mushrooms (Psalliota bispora). Lipids 21:261–266. doi:10.1007/BF02536408
Yaws CL (2007) The Yaws handbook of vapour pressure, Antoine coefficients. Gulf Publishing Company, Houston
Zhang ZM, Wu WW, Li GK (2008) A GC–MS study of the volatile organic composition of straw and Oyster Mushrooms during maturity and its relation to antioxidant activity. J Chromatogr Sci 46:690–696. doi:10.1093/chromsci/46.8.690
Ziegenbein FC, Hanssen HP, König WA (2006) Chemical constituents of the essential oils of three wood-rotting fungi. Flavour Fragr J 21:813–816. doi:10.1002/ffj.1732
Acknowledgments
We would like to thank Marko Rohlfs for valuable comments on the manuscript and Johannes Steidle for its examination. Rüdiger Blohme performed preliminary experiments and provided the photographs. Norbert Bartsch granted access to the long term study site “B2” in the Solling mountains. Yann Clough and Christoph Scherber gave us essential advice on statistical analyses. Anna Plašil helped to improve the English.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Marko Rohlfs.
Rights and permissions
About this article
Cite this article
Holighaus, G., Weißbecker, B., von Fragstein, M. et al. Ubiquitous eight-carbon volatiles of fungi are infochemicals for a specialist fungivore. Chemoecology 24, 57–66 (2014). https://doi.org/10.1007/s00049-014-0151-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00049-014-0151-8