Abstract
Microbes are ubiquitous on plant surfaces. However, interactions between epiphytic microbes and arthropods are rarely considered as a factor that affects arthropod behaviors. Here, volatile emissions from an epiphytic fungus were investigated as semiochemical attractants for two eusocial wasps. The fungus Aureobasidium pullulans was isolated from apples, and the volatile compounds emitted by fungal colonies were quantified. The attractiveness of fungal colonies and fungal volatiles to social wasps (Vespula spp.) were experimentally tested in the field. Three important findings emerged: (1) traps baited with A. pullulans caught 2750 % more wasps on average than unbaited control traps; (2) the major headspace volatiles emitted by A. pullulans were 2-methyl-1-butanol, 3-methyl-1-butanol, and 2-phenylethyl alcohol; and (3) a synthetic blend of fungal volatiles attracted 4,933 % more wasps on average than unbaited controls. Wasps were most attracted to 2-methyl-1-butanol. The primary wasp species attracted to fungal volatiles were the western yellowjacket (Vespula pensylvanica) and the German yellowjacket (V. germanica), and both species externally vectored A. pullulans. This is the first study to link microbial volatile emissions with eusocial wasp behaviors, and these experiments indicate that volatile compounds emitted by an epiphytic fungus can be responsible for wasp attraction. This work implicates epiphytic microbes as important components in the community ecology of some eusocial hymenopterans, and fungal emissions may signal suitable nutrient sources to foraging wasps. Our experiments are suggestive of a potential symbiosis, but additional studies are needed to determine if eusocial wasp–fungal associations are widespread, and whether these associations are incidental, facultative, or obligate.
Similar content being viewed by others
References
Altschul S, Madden T, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Ayres MP, Wilkens RT, Ruel JJ, Lombardero MJ, Vallery E (2000) Nitrogen budgets of phloem-feeding bark beetles with and without symbiotic fungi. Ecology 81:2198–2210
Börjesson T, Stöllman U, Schnürer J (1999) Volatile metabolites and other indicators of Penicillium aurantiogriseum growth on different substrates. Appl Env Microbiol 56:3705–3710
Bronstein JL (2001) Mutualisms. In: Fairbairn D, Roff D (eds) Evolutionary ecology: Perspectives and synthesis. Oxford University Press, New York
Brysch-Herzberg M (2004) Ecology of yeasts in plant-bumblebee mutualism in Central Europe. FEMS Microbiol Ecol 50:87–100
Davis TS, Hofstetter RW, Foster JT, Foote NE, Keim P (2011) Interactions between the yeast Ogataea pini and filamentous fungi associated with the western pine beetle. Microb Ecol 61:626–634
Durrell LW (1965) Fungi in nests of paper wasps. Am Midl Nat 71:501–503
de Jager ES, Wehner FC, Korston L (2001) Microbial ecology of the mango phylloplane. Microb Ecol 42:201–207
Fonseca Á, Inácio J (2006) Phylloplane yeasts. In: Rosa C, Péter G (eds) Biodiversity and ecophysiology of yeasts. Springer-Verlag, Berlin, pp 263–301
Ganter PF (2006) Yeast and invertebrate associations. In: Rosa C, Péter G (eds) Biodiversity and ecophysiology of yeasts. Springer-Verlag, Berlin, pp 303–370
Gildemacher PR, Heijne B, Houbraken J, Vromans T, Hoekstra ES, Boekhout T (2004) Can phyllosphere yeasts explain the effect of scab fungicides on russeting of Elstar apples? Eur J Plant Pathol 110:929–937
Giuci P, Zambonelli C, Kunkee RE (1993) Increased production of n-propanol in wine by yeast strains having an impaired ability to form hydrogen sulfide. Am J Enol Vitic 44:17–21
Gregg PC, Del Socorro AP, Henderson GS (2010) Development of a synthetic plant volatile-based attracticide for female noctuid moths: II. Bioassays of synthetic plant volatiles as attractants for the adults of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Aust J Entomol 49:21–30
Heath RR, Manukian A (1992) Development and evaluation of systems to collect volatile semiochemicals from insects and plants using charcoal-infused medium for air purification. J Chem Ecol 18:1209–1226
Honda K, Omura H, Hayashi N (1998) Identification of floral volatiles from Ligustrum japonicum that stimulate flower visiting by cabbage butterfly, Pieris rapae. J Chem Ecol 24:2167–2180
Kukor JJ, Martin MM (1983) Acquisition of digestive enzymes by the siricid woodwasps from their fungal symbiont. Science 220:1161–1163
Kurtzman CP, Robnett CJ (1998) Identification and phylogeny of ascomycetous yeasts from analysis on nuclear large-subunit (26 S) ribosomal DNA partial sequences. Anton van Lee 73:331–371
Lachance M-A, Starmer WT, Rosa CA, Bowles JM, Janzen DH (2001) Biogeography of the yeasts of ephemeral flowers and their insects. FEMS Yeast Res 1:1–8
Landolt PJ (1998) Chemical attractants for trapping yellowjackets Vespula germanica and Vespula pensylvanica (Hymenoptera:Vespidae). Environ Entomol 27:1229–1234
Landolt PJ, Smithhisler CS, Reed HC, McDonough LM (2000) Trapping social wasps (Hymenoptera:Vespidae) with acetic acid and short-chain alcohols. J Econ Entomol 93:1613–1618
Landolt PJ, Pantoja A, Green D (2005) Yellowjacket wasps (Hymenoptera:Vespidae) trapped in Alaska with heptyl butyrate, acetic acid, and isobutanol. J Entomol Soc British Colombia 102:35–42
Landolt PJ, Tóth M, Jósvai J (2007) First European report of social wasps trapped in response to acetic acid, isobutanol, 2-methyl-2-propanol, and heptyl butyrate in tests conducted in Hungary. Bull Insectol 60:7–11
Little AE, Currie CR (2008) Black yeasts compromise the efficiency of antibiotic defenses in fungus-growing ants. Ecology 89:1216–1222
Lorenzo MG, Manrique G, Pires HH, de Brito Sánchez MG, Diotauiti L, Lazzari CR (1999) Yeast culture volatiles as attractants for Rhodnius prolixus: electroantennogram responses and captures in yeast-baited traps. Acta Trop 72:119–124
Nout MJ, Bartelt RJ (1998) Attraction of a flying Nitidulid (Carpophilus humeralis) to volatiles produced by yeasts grown on sweet corn and corn-based medium. J Chem Ecol 24:1217–1239
O'Donnell K (1993) Fusarium and its near relatives. In: Reynolds D, J Taylor (ed) The fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics. CAB International, Wallingford, UK, pp 225–233
Phaff HJ, Starmer WT (1987) Yeasts associated with plants, insects, and soil. In: Rose AH, Harrison JS (eds) The yeasts. Academic, New York, pp 123–180
Poulsen M, Oh DC, Clardy J, Currie CR (2011) Chemical analyses of wasp-associated Streptomyces bacteria reveal a prolific potential for natural products discovery. PLoS One 6:1–8
Rosa CA, Morais PB, Hagler AN, Mendonça-Hagler LC, Monteiro RF (1994) Yeast communities of the cactus Pilosocereus arrabidae and associated insects in the Sandy Coastal Plains of Southeastern Brazil. Anton van Lee 65:55–62
Scott JJ, Oh DC, Yuceer MC, Klepzig KD, Clardy J, Currie CR (2008) Bacterial protection of a beetle–fungus mutualism. Science 322:63
Slepecky RA, Starmer WT (2009) Phenotypic plasticity in fungi: a review with observations on Aureobasidium pullulans. Mycologia 101:823–832
Starmer WT, Heed WB, Miranda M, Miller MW, Phaff HJ (1976) The ecology of yeast flora associated with cactiphilic Drosophila and their host plants in the Sonoran desert. Microb Ecol 3:11–30
Starmer WT, Barker JS, Phaff HJ, Fogleman JC (1986) Adaptations of Drosophila and yeasts: their interactions with the volatile 2-propanol in the cactus–microorganism Drosophila model system. Austral J Biol Sci 39:67–77
Stratford M, Bond CJ, James SA, Roberts IN, Steels H (2002) Candida davenportii sp. nov, a potential soft-drinks spoilage yeast isolated from a wasp. Int J Syst Evol Micr 52:1369–1375
Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microb Mol Biol Rev 67:491–502
Sunesson AL, Vaes WHJ, Nilsson CA, Blomquist G, Andersson B, Carlson R (1995) Identification of volatile metabolites from five fungal species grown on two media. Appl Env Microbiol 61:2911–2918
Takeo K, de Hoog GS (1991) Karyology and hyphal characteristics as taxonomic criteria in Ascomycetous black yeasts and related fungi. Anton van Leeuwenhoek 60:35–42
Utrio P, Ericksson K (1977) Volatile fermentation products as attractants for macrolepidoptera. Ann Zool Fen 14:98–104
Van der Walt JP (1959) Pichia robertsii nov. spec. a new haploid homothallic yeast. Anton van Lee 25:337–343
Verginer M, Leitner E, Berg G (2010) Production of volatile metabolites by grape-associated microorganisms. J Agric Food Chem 58:8344–8350
Acknowledgements
The authors thank Camille Stevens-Rumann for assistance in sorting and identifying trap catches, and Laura Ignatia for assistance in identifying fungi. Karen London and Dong Cha provided pre-reviews and commentary for this manuscript. We are also grateful to three anonymous reviewers whose helpful comments improved the quality of this manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Davis, T.S., Boundy-Mills, K. & Landolt, P.J. Volatile Emissions from an Epiphytic Fungus are Semiochemicals for Eusocial Wasps. Microb Ecol 64, 1056–1063 (2012). https://doi.org/10.1007/s00248-012-0074-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-012-0074-2