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Chemical Signals That Mediate Insect-Fungal Interactions

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Biocommunication of Fungi

Abstract

This chapter reviews the diverse types of chemical communication that mediate interactions between fungi and insects. Both life forms utilize complex chemosensory systems to process environmental cues. As they coexist in terrestrial and aquatic habitats, the consequences of their interactions range from beneficial effects for both partners to adverse ones or even death for one partner. Plants, as an additional life form, also can be involved in these multifaceted relationships. Depending on the volatility of the produced compound(s), chemical cues generally are perceived either by contact or from a distance. Responses of insects to such cues may operate on various levels, including metabolism, immune defense, and behavior. Furthermore, insects may perceive compounds as attractive, repellent, deterrent, or neutral. Fungi, on the other hand, show various metabolic responses to insect-borne chemicals that come into contact with their cell wall. While numerous published reviews and textbooks cover insect-fungal symbiosis, we here present examples of communication systems in which one or more components regulating the signaling events have been identified. These examples include fungal pathogens of insects and plants, mycophagous and fungivorous insects, mutualistic symbioses between fungi and insects, fungal kairomones utilized by insects, and floral and other scent mimicry exploited by fungi.

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References

  • Adams AS, Jordan MS, Adams SM, Suen G, Goodwin LA, Davenport KW, Currie CR, Raffa KF (2011) Cellulose-degrading bacteria associated with the invasive woodwasp Sirex noctilio. ISME J 5:1323–1331

    Article  PubMed  CAS  Google Scholar 

  • Altizer SM, Thrall PH, Antonovics J (1998) Vector behavior and the transmission of anther-smut infection in Silene alba. Am Midl Nat 139:147–163

    Article  Google Scholar 

  • Andersen SB, Gerritsma S, Yusah KM, Mayntz D, Hywel-Jones NL, Billen J, Boomsma JJ, Hughes DP (2009) The life of a dead ant: the expression of an adaptive extended phenotype. Am Nat 174:424–433

    Article  PubMed  Google Scholar 

  • Atkinson W, Shorrocks B (1977) Breeding site specificity in domestic species of Drosophila. Oecologia 29:223–232

    Article  Google Scholar 

  • Bacon CW, Lyons PC, Porter JK, Robbins JD (1986) Ergot toxicity from endophyte-infected grasses – a review. Agron J 78:106–116

    Article  CAS  Google Scholar 

  • Barbosa P, Krischik VA, Jones CG (1991) Microbial mediation of plant-herbivore interactions. Wiley, New York/Chichester

    Google Scholar 

  • Batra LR (1991) World species of Monilinia (Fungi): their ecology, biosystematics and control (Mycological Memoir). J. Cramer, Berlin

    Google Scholar 

  • Batra LR, Batra SWT (1985) Floral mimicry induced by mummy-berry fungus exploits hosts pollinators as vectors. Science 228:1011–1013

    Article  PubMed  CAS  Google Scholar 

  • Beauvais A, Latge JP, Vey A, Prevost MC (1989) The role of surface components of the entomopathogenic fungus Entomophaga aulicae in the cellular immune response of Galleria mellonella (Lepidoptera). J Gen Microbiol 135:489–498

    Google Scholar 

  • Benda ND, Boucias D, Torto B, Teal P (2008) Detection and characterization of Kodamaea ohmeri associated with small hive beetle Aethina tumida infesting honey bee hives. J Apic Res 47:194–201

    Article  CAS  Google Scholar 

  • Berg A, Ehnstrom B, Gustafsson L, Hallingback T, Jonsell M, Weslien J (1994) Threatened plant, animal, and fungus species in Swedish forests: distribution and habitat associations. Conserv Biol 8:718–731

    Article  Google Scholar 

  • Boddy L, Jones TH (2008) Interactions between basidiomycota and invertebrates. Br Mycol Soc Symp Ser 28:155–179

    Article  Google Scholar 

  • Bogus MI, Kedra E, Bania J, Szczepanik M, Czygier M, Jablonski P, Pasztaleniec A, Samborski J, Mazgajska J, Polanowski A (2007) Different defense strategies of Dendrolimus pini, Galleria mellonella, and Calliphora vicina against fungal infection. J Insect Physiol 53:909–922

    Article  PubMed  CAS  Google Scholar 

  • Bogus MI, Czygier M, Golebiowski M, Kedra E, Kucinska J, Mazgajska J, Samborski J, Wieloch W, Wloka E (2010) Effects of insect cuticular fatty acids on in vitro growth and pathogenicity of the entomopathogenic fungus Conidiobolus coronatus. Exp Parasitol 125:400–408

    Article  PubMed  CAS  Google Scholar 

  • Boone CK, Six DL, Zheng YB, Raffa KF (2008) Parasitoids and dipteran predators exploit volatiles from microbial symbionts to locate bark beetles. Environ Entomol 37:150–161

    Article  PubMed  Google Scholar 

  • Bot ANM, Ortius-Lechner D, Finster K, Maile R, Boomsma JJ (2002) Variable sensitivity of fungi and bacteria to compounds produced by the metapleural glands of leaf-cutting ants. Insect Soc 49:363–370

    Article  Google Scholar 

  • Boucias DG, Pendland JC (1987) Detection of protease inhibitors in the hemolymph of resistant Anticarsia gemmatalis which are inhibitory to the entomopathogenic fungus, Nomuraea rileyi. Experientia 43:336–339

    Article  CAS  Google Scholar 

  • Boucias DG, Pendland JC (1993) The galactose binding lectin from the beet armyworm, Spodoptera exigua: distribution and site of synthesis. Insect Biochem Mol Biol 23:233–242

    Article  PubMed  CAS  Google Scholar 

  • Boucias DG, Pendland JC (1998) Principles of insect pathology. Kluwer Academic, Boston

    Google Scholar 

  • Boucias DG, Pendland JC, Latge JP (1988) Nonspecific factors involved in attachment of entomopathogenic deuteromycetes to host insect cuticle. Appl Environ Microbiol 54:1795–1805

    PubMed  CAS  Google Scholar 

  • Boucias DG, Stokes C, Storey G, Pendland JC (1996) The effects of imidacloprid on the termite Reticulitermes flavipes and its interaction with the mycopathogen Beauveria bassiana. Pflanzenschutz-Nachrichten Bayer 49:103–144

    Google Scholar 

  • Bulmer MS, Bachelet I, Raman R, Rosengaus RB, Sasisekharan R (2009) Targeting an antimicrobial effector function in insect immunity as a pest control strategy. Proc Natl Acad Sci USA 106:12652–12657

    Article  PubMed  CAS  Google Scholar 

  • Bultman TL, White JF (1988) “Pollination” of a fungus by a fly. Oecologia 75:317–319

    Article  Google Scholar 

  • Bultman TL, White JF, Bowdish TI, Welch AM (1998) A new kind of mutualism between fungi and insects. Mycol Res 102:235–238

    Article  Google Scholar 

  • Bultman TL, Welch AM, Boning RA, Bowdish TI (2000) The cost of mutualism in a fly-fungus interaction. Oecologia 124:85–90

    Article  Google Scholar 

  • Chandra A, Huff DR (2008) Salmacisia, a new genus of Tilletiales: reclassification of Tilletia buchloeana causing induced hermaphroditism in buffalograss. Mycologia 100:81–93

    Article  PubMed  CAS  Google Scholar 

  • Chang VCS, Jensen L (1974) Transmission of pineapple disease organism of sugarcane by nitidulid beetles in Hawaii. J Econ Entomol 67:190–192

    Google Scholar 

  • Charnley AK (2003) Fungal pathogens of insects: cuticle degrading enzymes and toxins. Adv Bot Res 40:241–321

    Article  CAS  Google Scholar 

  • Choe DH, Millar JG, Rust MK (2009) Chemical signals associated with life inhibit necrophoresis in Argentine ants. Proc Natl Acad Sci USA 106:8251–8255

    Article  PubMed  CAS  Google Scholar 

  • Connick WJ, French RC (1991) Volatiles emitted during the sexual stage of the Canada thistle rust fungus and by thistle flowers. J Agric Food Chem 39:185–188

    Article  CAS  Google Scholar 

  • Crespo R, Juarez MP, Cafferata LFR (2000) Biochemical interaction between entomopathogenous fungi and their insect-host-like hydrocarbons. Mycologia 92:528–536

    Article  CAS  Google Scholar 

  • Crespo R, Pedrini N, Juarez MP, Dal Bello GM (2008) Volatile organic compounds released by the entomopathogenic fungus Beauveria bassiana. Microbiol Res 163:148–151

    Article  PubMed  CAS  Google Scholar 

  • Dobson HEM (1993) Floral volatiles in insect biology. In: Bernays EA (ed) Insect-plant interactions. CRC Press, Boca Raton, pp 47–81

    Google Scholar 

  • Douglas AE (2009) The microbial dimension in insect nutritional ecology. Funct Ecol 23:38–47

    Article  Google Scholar 

  • Faldt 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

    Article  CAS  Google Scholar 

  • Fargues J (1984) Adhesion of the fungal spore to the insect cuticle in relation to pathogenicity. In: Roberts DW, Aist JR (eds) Infection processes of fungi, Foundation conference reports. Rockefeller, New York, pp 90–110

    Google Scholar 

  • Febvay G, Decharme M, Kermarrec A (1984) Digestion of chitin by the labial glands of Acromyrmex octospinosus Reich (Hymenoptera: Formicidae). Can J Zool 62:229–234

    Article  CAS  Google Scholar 

  • Fransen JJ, Vanlenteren JC (1993) Host selection and survival of the parasitoid Encarsia formosa on greenhouse-whitefly, Trialeurodes vaporariorum, in the presence of hosts infected with the fungus Aschersonia aleyrodis. Entomol Exp Appl 69:239–249

    Article  Google Scholar 

  • Gao QA, Jin K, Ying SH, Zhang YJ, Xiao GH, Shang YF, Duan ZB, Hu XA, Xie XQ, Zhou G, Peng GX, Luo ZB, Huang W, Wang B, Fang WG, Wang SB, Zhong Y, Ma LJ, St Leger RJ, Zhao GP, Pei Y, Feng MG, Xia YX, Wang CS (2011) Genome sequencing and comparative transcriptomics of the model entomopathogenic fungi Metarhizium anisopliae and M. acridum. PLoS Genet 7(1):e1001264

    Article  PubMed  CAS  Google Scholar 

  • Gibson CM, Hunter MS (2010) Extraordinarily widespread and fantastically complex: comparative biology of endosymbiotic bacterial and fungal mutualists of insects. Ecol Lett 13:223–234

    Article  PubMed  Google Scholar 

  • Gillespie JP, Bailey AM, Cobb B, Vilcinskas A (2000) Fungi as elicitors of insect immune responses. Arch Insect Biochem Physiol 44:49–68

    Article  PubMed  CAS  Google Scholar 

  • Golebiowski M, Malinski E, Bogus MI, Kumirska J, Stepnowski P (2008) The cuticular fatty acids of Calliphora vicina, Dendrolimus pini and Galleria mellonella larvae and their role in resistance to fungal infection. Insect Biochem Mol Biol 38:619–627

    Article  PubMed  CAS  Google Scholar 

  • Gorzynska K, Lembicz M, Olszanowski Z, Leuchtmann A (2011) Botanophila-Epichloe interaction in a wild grass, Puccinellia distans, lacks dependence on the fly vector. Ann Entomol Soc Am 104:841–846

    Article  Google Scholar 

  • Gottar M, Gobert V, Matskevich AA, Reichhart JM, Wang CS, Butt TM, BeIvin M, Hoffmann JA, Ferrandon D (2006) Dual detection of fungal infections in Drosophila via recognition of glucans and sensing of virulence factors. Cell 127:1425–1437

    Article  PubMed  CAS  Google Scholar 

  • Gross J, Muller C, Vilcinskas A, Hilker M (1998) Antimicrobial activity of exocrine glandular secretions, hemolymph, and larval regurgitate of the mustard leaf beetle Phaedon cochleariae. J Invertebr Pathol 72:296–303

    Article  PubMed  Google Scholar 

  • Grove JF, Blight MM (1983) The oviposition attractant for the mushroom phorid Megaselia halterata – the identification of volatiles present in mushroom house air. J Sci Food Agric 34:181–185

    Article  CAS  Google Scholar 

  • Guevara R, Rayner ADM, Reynolds SE (2000) Orientation of specialist and generalist fungivorous ciid beetles to host and non-host odours. Physiol Entomol 25:288–295

    Article  Google Scholar 

  • Hanski I (1989) Fungivory: fungi, insects and ecology. In: Wilding N, Collins NM, Hammond PM, Webber JF (eds) Insect-fungus interactions. Academic, London, pp 25–68

    Google Scholar 

  • Hinds TE (1972) Insect transmission of Ceratocystis species associated with aspen cankers. Phytopathology 62:221–226

    Article  Google Scholar 

  • Holder DJ, Keyhani NO (2005) Adhesion of the entomopathogenic fungus Beauveria (Cordyceps) bassiana to substrata. Appl Environ Microbiol 71:5260–5266

    Article  PubMed  CAS  Google Scholar 

  • Honda H, Ishiwatari T, Matsumoto Y (1988) Fungal volatiles as oviposition attractants for the yellow peach moth, Conogethes punctiferalis (Guenee) (Lepidoptera: Pyralidae). J Insect Physiol 34:205–211

    Article  Google Scholar 

  • Howard RW, Lord JC (2003) Cuticular lipids of the booklouse, Liposcelis bostrychophila: hydrocarbons, aldehydes, fatty acids, and fatty acid amides. J Chem Ecol 29:615–627

    Article  PubMed  CAS  Google Scholar 

  • Howard DF, Tschinkel WR (1976) Aspects of necrophoric behavior in the red imported fire ant, Solenopsis invicta. Behaviour 56:157–180

    Article  Google Scholar 

  • Hung S-Y, Boucias DG (1992) Influence of Beauveria bassiana on the cellular defense response of the beet armyworm, Spodoptera exigua. J Invertebr Pathol 60:152–158

    Article  Google Scholar 

  • Huxham IM, Lackie AM, McCorkindale NJ (1989) Inhibitory effects of cyclodepsipeptides, destruxins, from the fungus Metarhizium anisopliae on cellular immunity in insects. J Insect Physiol 35:97–105

    Article  CAS  Google Scholar 

  • Jennersten O (1988) Insect dispersal of fungal disease: effects of Ustilago infection on pollinator attraction in Viscaria vulgaris. Oikos 51:163–170

    Article  Google Scholar 

  • Jennersten O, Kwak MM (1991) Competition for bumblebee visitation between Melampyrum pratense and Viscaria vulgaris with healthy and Ustilago-infected flowers. Oecologia 86:88–98

    Article  Google Scholar 

  • Jin K, Zhang YJ, Fang WG, Luo ZB, Zhou YH, Pei Y (2010) Carboxylate transporter gene JEN1 from the entomopathogenic fungus Beauveria bassiana is involved in conidiation and virulence. Appl Environ Microbiol 76:254–263

    Article  PubMed  CAS  Google Scholar 

  • Johnson SD, Jurgens A (2010) Convergent evolution of carrion and faecal scent mimicry in fly-pollinated angiosperm flowers and a stinkhorn fungus. S Afr J Bot 76:796–807

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Jonsell M, Nordlander G (2004) Host selection patterns in insects breeding in bracket fungi. Ecol Entomol 29:697–705

    Article  Google Scholar 

  • Julian GE, Cahan S (1999) Undertaking specialization in the desert leaf-cutter ant Acromyrmex versicolor. Anim Behav 58:437–442

    Article  PubMed  Google Scholar 

  • Kaiser R (2006) Flowers and fungi use scents to mimic each other. Science 311:806–807

    Article  PubMed  CAS  Google Scholar 

  • Kerwin JL (1982) Biological aspects of the interaction between two entomogenous fungi, Coelomomyces psorophorae and Entomophthora culicis, and their dipteran hosts. Dissert Abstr Int B Phys Sci Eng 42:1291

    Google Scholar 

  • Kerwin JL (1984) Fatty acid regulation of the germination of Erynia variabilis conidia on adults and puparia of the lesser housefly, Fannia canicularis. Can J Microbiol 30:158–161

    Article  CAS  Google Scholar 

  • Kilaru A, Bailey BA, Hasenstein KH (2007) Moniliophthora perniciosa produces hormones and alters endogenous auxin and salicylic acid in infected cocoa leaves. FEMS Microbiol Lett 274:238–244

    Article  PubMed  CAS  Google Scholar 

  • Kohlmeyer J, Kohlmeyer E (1974) Distribution of Epichloe typhina (Ascomycetes) and its parasitic fly. Mycologia 66:77–86

    Article  Google Scholar 

  • Komonen A, Penttila R, Lindgren M, Hanski I (2000) Forest fragmentation truncates a food chain based on an old-growth forest bracket fungus. Oikos 90:119–126

    Article  Google Scholar 

  • Kukor JJ, Martin MM (1983) Acquisition of digestive enzymes by siricid woodwasps from their fungal symbiont. Science 220:1161–1163

    Article  PubMed  CAS  Google Scholar 

  • Lamberty M, Zachary D, Lanot R, Bordereau C, Robert A, Hoffmann JA, Bulet P (2001) Insect immunity – constitutive expression of a cysteine-rich antifungal and a linear antibacterial peptide in a termite insect. J Biol Chem 276:4085–4092

    Article  PubMed  CAS  Google Scholar 

  • Latgé J-P, Boucias DG, Fournet B (1988) Structure of the exocellular polysaccharide produced by the fungus, Nomuraea rileyi. Carbohydr Res 181:282–286

    Article  Google Scholar 

  • Lecuona R, Riba G, Cassier P, Clement JL (1991) Alterations of insect epicuticular hydrocarbons during infection with Beauveria bassiana or B. brongniartii. J Invertebr Pathol 58:10–18

    Article  CAS  Google Scholar 

  • Lee JC, Hamud SM, Negron JF, Witcosky JJ, Seybold SJ (2010) Semiochemical-mediated flight strategies of two invasive elm bark beetles: a potential factor in competitive displacement. Environ Entomol 39:642–652

    Article  PubMed  Google Scholar 

  • Lin HC, Phelan PL (1992) Comparison of volatiles from beetle-transmitted Ceratocystis fagacearum and four non-insect-dependent fungi. J Chem Ecol 18:1623–1632

    Article  CAS  Google Scholar 

  • Lord JC (2001) Response of the wasp Cephalonomia tarsalis (Hymenoptera: Bethylidae) to Beauveria bassiana (Hyphomycetes: Moniliales) as free conidia or infection in its host, the sawtoothed grain beetle, Oryzaephilus surinamensis (Coleoptera: Silvanidae). Biol Control 21:300–304

    Article  Google Scholar 

  • Mackichan J, Thomsen L, Kerwin J, Latge JP, Beauvais A (1995) Unsaturated fatty acids are the active molecules of a glucan-synthase-inhibitory fraction isolated from entomophthoralean protoplasts. Microbiology 141:2757–2762

    Article  PubMed  CAS  Google Scholar 

  • Madden JL (1968) Behavioural responses of parasites to the symbiotic fungus associated with Sirex noctilio F. Nature 218:189–190

    Article  Google Scholar 

  • Maitland DP (1994) A parasitic fungus infecting yellow dungflies manipulates host perching behavior. Proc R Soc Lond Ser B Biol Sci 258:187–193

    Article  Google Scholar 

  • Martin MM (1979) Biochemical Implications of insect mycophagy. Biol Rev Cambridge Philos Soc 54:1–21

    Article  CAS  Google Scholar 

  • Martinez AS, Fernandez-Arhex V, Corley JC (2006) Chemical information from the fungus Amylostereum areolatum and host-foraging behaviour in the parasitoid Ibalia leucospoides. Physiol Entomol 31:336–340

    Article  Google Scholar 

  • Masterman R, Ross R, Mesce K, Spivak M (2001) Olfactory and behavioral response thresholds to odors of diseased brood differ between hygienic and non-hygienic honey bees (Apis mellifera L.). J Comp Physiol A Sens Neural Behav Physiol 187:441–452

    Article  CAS  Google Scholar 

  • Matsuura K (2006) Termite-egg mimicry by a sclerotium-forming fungus. Proc R Soc B Biol Sci 273:1203–1209

    Article  Google Scholar 

  • Matsuura K, Tanaka C, Nishida T (2000) Symbiosis of a termite and a sclerotium-forming fungus: sclerotia mimic termite eggs. Ecol Res 15:405–414

    Article  Google Scholar 

  • Matsuura K, Yashiro T, Shimizu K, Tatsumi S, Tamura T (2009) Cuckoo fungus mimics termite eggs by producing the cellulose-digesting enzyme beta-glucosidase. Curr Biol 19:30–36

    Article  PubMed  CAS  Google Scholar 

  • Mazet I, Pendland JC, Boucias DG (1994) Comparative analysis of phagocytosis of fungal cells by insect hemocytes versus horse neutrophils. Dev Comp Immunol 18:455–466

    Article  PubMed  CAS  Google Scholar 

  • McLeod G, Gries R, von Reuss SH, Rahe JE, McIntosh R, Konig WA, Gries G (2005) The pathogen causing Dutch elm disease makes host trees attract insect vectors. Proc R Soc Lond Ser B Biol Sci 272:2499–2503

    Article  Google Scholar 

  • Meyling NV, Pell JK (2006) Detection and avoidance of an entomopathogenic fungus by a generalist insect predator. Ecol Entomol 31:162–171

    Article  Google Scholar 

  • Moller AP (1993) A fungus infecting domestic flies manipulates sexual behavior of its host. Behav Ecol Sociobiol 33:403–407

    Google Scholar 

  • Moser JC, Konrad H, Blomquist SR, Kirisits T (2010) Do mites phoretic on elm bark beetles contribute to the transmission of Dutch elm disease? Naturwissenschaften 97:219–227

    Article  PubMed  CAS  Google Scholar 

  • Mueller UG, Schultz TR, Currie CR, Adams RMM, Malloch D (2001) The origin of the attine ant-fungus mutualism. Q Rev Biol 76:169–197

    Article  PubMed  CAS  Google Scholar 

  • Myles TG (2002) Alarm, aggregation, and defense by Reticulitermes flavipes in response to a naturally occurring isolate of Metarhizium anisopliae. Sociobiology 40:243–255

    Google Scholar 

  • Naef A, Roy BA, Kaiser R, Honegger R (2002) Insect-mediated reproduction of systemic infections by Puccinia arrhenatheri on Berberis vulgaris. New Phytol 154:717–730

    Article  Google Scholar 

  • Ngugi HK, Scherm H (2004) Pollen mimicry during infection of blueberry flowers by conidia of Monilinia vaccinii-corymbosi. Physiol Mol Plant Pathol 64:113–123

    Article  Google Scholar 

  • Ngugi HK, Scherm H, Lehman JS (2002) Relationships between blueberry flower age, pollination, and conidial infection by Monilinia vaccinii-corymbosi. Phytopathology 92:1104–1109

    Article  PubMed  CAS  Google Scholar 

  • Ochiai M, Ashida M (2000) A pattern-recognition protein for beta-1,3-glucan. The binding domain and the cDNA cloning of beta-1,3-glucan recognition protein from the silkworm, Bombyx mori. J Biol Chem 275:4995–5002

    Article  PubMed  CAS  Google Scholar 

  • Oi DH, Pereira RM (1993) Ant behavior and microbial pathogens (Hymenoptera: Formicidae). Florida Entomol 76:63–74

    Article  Google Scholar 

  • Ormond EL, Thomas APM, Pell JK, Freeman SN, Roy HE (2011) Avoidance of a generalist entomopathogenic fungus by the ladybird, Coccinella septempunctata. FEMS Microbiol Ecol 77:229–237

    Article  PubMed  CAS  Google Scholar 

  • Ortius-Lechner D, Maile R, Morgan ED, Boomsma JJ (2000) Metapleural gland secretion of the leaf-cutter ant Acromyrmex octospinosus: new compounds and their functional significance. J Chem Ecol 26:1667–1683

    Article  CAS  Google Scholar 

  • Pedrini N, Crespo R, Juarez MP (2007) Biochemistry of insect epicuticle degradation by entomopathogenic fungi. Comp Biochem Physiol C Toxicol Pharmacol 146:124–137

    Article  PubMed  CAS  Google Scholar 

  • Pendland JC, Boucias DG (1992) Ultrastructural localization of carbohydrate in cell walls of the entomogenous hyphomycete Nomuraea rileyi. Can J Microbiol 38:377–386

    Article  CAS  Google Scholar 

  • Pendland JC, Boucias DG (1993) Variations in the ability of galactose and mannose specific lectins to bind to cell wall surfaces during growth of the insect pathogenic fungus Paecilomyces farinosus. Eur J Cell Biol 60:322–330

    PubMed  CAS  Google Scholar 

  • Pendland JC, Boucias DG (1998) Characterization of monoclonal antibodies against cell wall epitopes of the insect pathogenic fungus, Nomuraea rileyi: differential binding to fungal surfaces and cross-reactivity with host hemocytes and basement membrane components. Eur J Cell Biol 75:118–127

    Article  PubMed  CAS  Google Scholar 

  • Pendland JC, Boucias DG (2000) Comparative analysis of the binding of antibodies prepared against the insect Spodoptera exigua and against the mycopathogen Nomuraea rileyi. J Invertebr Pathol 75:107–116

    Article  PubMed  CAS  Google Scholar 

  • Pfeil RM, Mumma RO (1992) Air sampling of volatiles from Agaricus bisporus in a mushroom facility and from mushroom compost. Hortscience 27:416–419

    CAS  Google Scholar 

  • Pfeil RM, Mumma RO (1993) Bioassay for evaluating attraction of the phorid fly, Megaselia halterata, to compost colonized by the commercial mushroom, Agaricus bisporus, and to 1-octen-3-ol and 3-octanone. Entomol Exp Appl 69:137–144

    Article  CAS  Google Scholar 

  • Phelan PL, Lin HC (1991) Chemical characterization of fruit and fungal volatiles attractive to dried-fruit beetle, Carpophilus hemipterus (L) (Coleoptera: Nitidulidae). J Chem Ecol 17:1253–1272

    Article  CAS  Google Scholar 

  • Pontoppidan MB, Himaman W, Hywel-Jones NL, Boomsma JJ, Hughes DP (2009) Graveyards on the move: the spatio-temporal distribution of dead Ophiocordyceps-infected ants. PLoS One 4:e4835

    Article  PubMed  CAS  Google Scholar 

  • Poulsen M, Bot ANM, Nielsen MG, Boomsma JJ (2002) Experimental evidence for the costs and hygienic significance of the antibiotic metapleural gland secretion in leaf-cutting ants. Behav Ecol Sociobiol 52:151–157

    Article  Google Scholar 

  • Raguso RA, Roy BA (1998) ‘Floral’ scent production by Puccinia rust fungi that mimic flowers. Mol Ecol 7:1127–1136

    Article  PubMed  CAS  Google Scholar 

  • Renucci M, Tirard A, Provost E (2011) Complex undertaking behavior in Temnothorax lichtensteini ant colonies: from corpse-burying behavior to necrophoric behavior. Insect Soc 58:9–16

    Article  Google Scholar 

  • Roh KB, Kim CH, Lee H, Kwon HM, Park JW, Ryu JH, Kurokawa K, Ha NC, Lee WJ, Lemaitre B, Soderhall K, Lee BL (2009) Proteolytic cascade for the activation of the insect toll pathway induced by the fungal cell wall component. J Biol Chem 284:19474–19481

    Article  PubMed  CAS  Google Scholar 

  • Rosengaus RB, Jordan C, Lefebvre ML, Traniello JFA (1999) Pathogen alarm behavior in a termite: a new form of communication in social insects. Naturwissenschaften 86:544–548

    Article  PubMed  CAS  Google Scholar 

  • Roy BA (1993) Floral mimicry by a plant pathogen. Nature 362:56–58

    Article  Google Scholar 

  • Roy BA (1994) The effects of pathogen-induced pseudoflowers and buttercups on each others insect visitation. Ecology 75:352–358

    Article  Google Scholar 

  • Roy BA, Raguso RA (1997) Olfactory versus visual cues in a floral mimicry system. Oecologia 109:414–426

    Article  Google Scholar 

  • Roy HE, Steinkraus DC, Eilenberg J, Hajek AE, Pell JK (2006) Bizarre interactions and endgames: entomopathogenic fungi and their arthropod hosts. Annu Rev Entomol 51:331–357

    Article  PubMed  CAS  Google Scholar 

  • Roy HE, Brown PMJ, Rothery P, Ware RL, Majerus MEN (2008) Interactions between the fungal pathogen Beauveria bassiana and three species of coccinellid: Harmonia axyridis, Coccinella septempunctata and Adalia bipunctata. Biocontrol 53:265–276

    Article  Google Scholar 

  • Schiestl FP, Steinebrunner F, Schulz C, von Reuss S, Francke W, Weymuth C, Leuchtmann A (2006) Evolution of ‘pollinator’-attracting signals in fungi. Biol Lett 2:401–404

    Article  PubMed  CAS  Google Scholar 

  • Schwemmler W, Gassner G (1989) Insect endocytobiosis: morphology, physiology, genetics, evolution. CRC Press, Boca Raton

    Google Scholar 

  • Silbering AF, Benton R (2010) Ionotropic and metabotropic mechanisms in chemoreception: ‘chance or design’? EMBO Rep 11:173–179

    Article  PubMed  CAS  Google Scholar 

  • Sloman IS, Reynolds SE (1993) Inhibition of ecdysteroid secretion from Manduca prothoracic glands in vitro by destruxins – cyclic depsipeptide toxins from the insect pathogenic fungus Metarhizium anisopliae. Insect Biochem Mol Biol 23:43–46

    Article  CAS  Google Scholar 

  • Sosa-Gomez DR, Boucias DG, Nation JL (1997) Attachment of Metarhizium anisopliae to the southern green stinkbug Nezara viridula cuticle and fungistatic effect of cuticular lipids and aldehydes. J Invertebr Pathol 69:31–39

    Article  PubMed  CAS  Google Scholar 

  • Spradber JP (1974) Responses of Ibalia species (Hymenoptera: Ibaliidae) to fungal symbionts of siricid woodwasp hosts. J Entomol 48:217–222

    Google Scholar 

  • Staples JA, Milner RJ (2000) A laboratory evaluation of the repellency of Metarhizium anisopliae conidia to Coptotermes lacteus (Isoptera: Rhinotermitidae). Sociobiology 36:133–148

    Google Scholar 

  • Starratt AN, Loschiavo SR (1970) Chemical stimuli from fungus Nigrospora sphaerica that induce aggregation of confused flour beetle, Tribolium confusum Duval, pest. Abstr Pap Am Chem Soc 1970:21

    Google Scholar 

  • Steinebrunner F, Schiestl FP, Leuchtmann A (2008a) Ecological role of volatiles produced by Epichloe: differences in antifungal toxicity. FEMS Microbiol Ecol 64:307–316

    Article  PubMed  CAS  Google Scholar 

  • Steinebrunner F, Schiestl FP, Leuchtmann A (2008b) Variation of insect attracting odor in endophytic Epichloe fungi: phylogenetic constrains versus host influence. J Chem Ecol 34:772–782

    Article  PubMed  CAS  Google Scholar 

  • Steinebrunner F, Twele R, Francke W, Leuchtmann A, Schiestl FP (2008c) Role of odour compounds in the attraction of gamete vectors in endophytic Epichloe fungi. New Phytol 178:401–411

    Article  PubMed  CAS  Google Scholar 

  • Steiner S, Erdmann D, Steidle JLM, Ruther J (2007) Host habitat assessment by a parasitoid using fungal volatiles. Front Zool 4:3 (10 pp)

    Article  PubMed  CAS  Google Scholar 

  • St Leger RJ, Joshi L, Roberts D (1998) Ambient pH is a major determinant in the expression of cuticle-degrading enzymes and hydrophobin by Metarhizium anisopliae. Appl Environ Microbiol 64:709–713

    PubMed  CAS  Google Scholar 

  • St Leger RJ, Nelson JO, Screen SE (1999) The entomopathogenic fungus Metarhizium anisopliae alters ambient pH, allowing extracellular protease production and activity. Microbiology SGM 145:2691–2699

    CAS  Google Scholar 

  • Storey GK, Vandermeer RK, Boucias DG, McCoy CW (1991) Effect of fire ant (Solenopsis invicta) venom alkaloids on the in vitro germination and development of selected entomogenous fungi. J Invertebr Pathol 58:88–95

    Article  CAS  Google Scholar 

  • Sullivan BT, Berisford CW (2004) Semiochemicals from fungal associates of bark beetles may mediate host location behavior of parasitoids. J Chem Ecol 30:703–717

    Article  PubMed  CAS  Google Scholar 

  • Swanson JAI, Torto B, Kells SA, Mesce KA, Tumlinson JH, Spivak M (2009) Odorants that induce hygienic behavior in honeybees: identification of volatile compounds in chalkbrood-infected honeybee larvae. J Chem Ecol 35:1108–1116

    Article  PubMed  CAS  Google Scholar 

  • Tartar A, Shapiro AM, Scharf DW, Boucias DG (2005) Differential expression of chitin synthase (CHS) and glucan synthase (FKS) genes correlates with the formation of a modified, thinner cell wall in in vivo-produced Beauveria bassiana cells. Mycopathologia 160:303–314

    Article  PubMed  CAS  Google Scholar 

  • Thakeow P, Angeli S, Weissbecker B, Schutz S (2008) Antennal and behavioral responses of Cis boleti to fungal odor of Trametes gibbosa. Chem Senses 33:379–387

    Article  PubMed  CAS  Google Scholar 

  • Torto B, Arbogast RT, Van Engelsdorp D, Willms S, Purcell D, Boucias D, Tumlinson JH, Teal PEA (2007a) Trapping of Aethina tumida Murray (Coleoptera: Nitidulidae) from Apis mellifera L. (Hymenoptera: Apidae) colonies with an in-hive baited trap. Environ Entomol 36:1018–1024

    Article  PubMed  Google Scholar 

  • Torto B, Boucias DG, Arbogast RT, Tumlinson JH, Teal PEA (2007b) Multitrophic interaction facilitates parasite-host relationship between an invasive beetle and the honey bee. Proc Natl Acad Sci USA 104:8374–8378

    Article  PubMed  CAS  Google Scholar 

  • Trumbo ST, Robinson GE (1997) Learning and task interference by corpse-removal specialists in honey bee colonies. Ethology 103:966–975

    Article  Google Scholar 

  • Tsitsigiannis DI, Keller NP (2007) Oxylipins as developmental and host-fungal communication signals. Trends Microbiol 15:109–118

    Article  PubMed  CAS  Google Scholar 

  • Uchida W, Matsunaga S, Sugiyama R, Kazama Y, Kawano S (2003) Morphological development of anthers induced by the dimorphic smut fungus Microbotryum violaceum in female flowers of the dioecious plant Silene latifolia. Planta 218:240–248

    Article  PubMed  CAS  Google Scholar 

  • Veal DA, Trimble JE, Beattie AJ (1992) Antimicrobial properties of secretions from the metapleural glands of Myrmecia gulosa (the Australian bull ant). J Appl Bacteriol 72:188–194

    Article  PubMed  CAS  Google Scholar 

  • Vega FE, Blackwell M (2005) Insect-fungal associations: ecology and evolution. Oxford University Press, Oxford

    Google Scholar 

  • Vet LEM, Janse C, Vanachterberg C, Vanalphen JJM (1984) Microhabitat location and niche segregation in two sibling species of drosophilid parasitoids: Asobara tabida (Nees) and A. rufescens (Foerster) (Braconidae: Alysiinae). Oecologia 61:182–188

    Article  Google Scholar 

  • Vey A (1985) Efficiency of the encapsulation reaction in insects: effect on the structure and the viability of the encapsulated fungus. Dev Comp Immunol 9:174–174

    Google Scholar 

  • Vilcinskas A, Matha V, Götz P (1997) Inhibition of phagocytic activity of plasmatocytes isolated from Galleria mellonella by entomopathogenous fungi and their secondary metabolites. J Insect Physiol 43:475–483

    Article  CAS  Google Scholar 

  • Visscher PK (1983) The honey bee way of death: necrophoric behavior in Apis mellifera colonies. Anim Behav 31:1070–1076

    Article  Google Scholar 

  • Wang C, Leger RJS (2006) A collagenous protective coat enables Metarhizium anisopliae to evade insect immune responses. Proc Natl Acad Sci USA 103:6647–6652

    Article  PubMed  CAS  Google Scholar 

  • Wang CS, Hu G, St Leger RJ (2005) Differential gene expression by Metarhizium anisopliae growing in root exudate and host (Manduca sexta) cuticle or hemolymph reveals mechanisms of physiological adaptation. Fungal Genet Biol 42:704–718

    Article  PubMed  CAS  Google Scholar 

  • Welch AM, Bultman TL (1993) Natural release of Epichloe typhina ascospores and its temporal relationship to fly parasitism. Mycologia 85:756–763

    Article  Google Scholar 

  • Wheeler Q, Blackwell M (1984) Fungus-insect relationships: perspectives in ecology and evolution. Columbia University Press, New York

    Google Scholar 

  • Wilson EO, Durlach NI, Roth LM (1958) Chemical releasers of necrophoric behavior in ants. Psyche 65:108–114

    Article  Google Scholar 

  • Yanagawa A, Yokohari F, Shimizu S (2009) The role of antennae in removing entomopathogenic fungi from cuticle of the termite, Coptotermes formosanus. J Insect Sci 9:9

    Article  Google Scholar 

  • Yoshida S, Yamashita M, Yonehara S, Eguchi M (1990) Properties of fungal protease inhibitors from the integument and hemolymph of the silkworm and effect of an inhibitor on the fungal growth. Comp Biochem Physiol B Biochem Mol Biol 95:559–564

    Google Scholar 

  • Zhang YJ, Zhang JQ, Jiang XD, Wang GJ, Luo ZB, Fan YH, Wu ZQ, Pei Y (2010) Requirement of a mitogen-activated protein kinase for appressorium formation and penetration of insect cuticle by the entomopathogenic fungus Beauveria bassiana. Appl Environ Microbiol 76:2262–2270

    Article  PubMed  CAS  Google Scholar 

  • Zurek L, Watson DW, Krasnoff SB, Schal C (2002) Effect of the entomopathogenic fungus, Entomophthora muscae (Zygomycetes: Entomophthoraceae), on sex pheromone and other cuticular hydrocarbons of the house fly, Musca domestica. J Invertebr Pathol 80:171–176

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

In part this work was supported by funding provided through a specific cooperative program between P. Teal (CMAVE, USDA/ARS) and D. Boucias (University of Florida, Gainesville).

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Correspondence to Drion G. Boucias .

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Boucias, D.G., Lietze, VU., Teal, P. (2012). Chemical Signals That Mediate Insect-Fungal Interactions. In: Witzany, G. (eds) Biocommunication of Fungi. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4264-2_20

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