Journal of Chemical Ecology

, Volume 39, Issue 7, pp 840–859 | Cite as

Microbial Volatile Emissions as Insect Semiochemicals

  • Thomas Seth Davis
  • Tawni L. Crippen
  • Richard W. Hofstetter
  • Jeffery K. Tomberlin
Article

Abstract

We provide a synthesis of the literature describing biochemical interactions between microorganisms and insects by way of microbial volatile organic compound (MVOC) production. We evaluated the functionality and ecological context of MVOC signals, and explored important metabolic pathways involved in MVOC production. The cosmopolitan distribution of microorganisms creates a context for frequent, and frequently overlooked, insect responses to microbial emissions. There are numerous instances of MVOCs being closely associated with insect feeding behaviors, but some MVOCs are also powerful repellants. Emissions from microorganisms in situ may signal aspects of habitat suitability or potential exposure to entomopathogens. In some ecosystems, bacterial or fungal volatiles can also incite insect aggregations, or MVOCs can resemble sexual pheromones that elicit mating and oviposition behaviors from responding insects. A single microorganism or MVOC can have different effects on insect behaviors, especially across species, ontogenies, and habitats. There appears to be a multipartite basis for insect responses to MVOCs, and complex tritrophic interactions can result from the production of MVOCs. Many biochemical pathways for behaviorally active volatile production by microbial species are conserved across large taxonomic groupings of microorganisms. In addition, there is substantial functional redundancy in MVOCs: fungal tissues commonly produce polyketides and short-chain alcohols, whereas bacterial tissues tend to be more commonly associated with amines and pyrazines. We hypothesize that insect olfactory responses to emissions from microorganisms inhabiting their sensory environment are much more common than currently recognized, and that these signals represent evolutionarily reliable infochemicals. Insect chemoreception of microbial volatiles may contribute to the formation of neutral, beneficial, or even harmful symbioses and provide considerable insight into the evolution of insect behavioral responses to volatile compounds.

Keywords

Attraction Microbes Yeast Fungi Bacteria Insect behavior Signaling Orientation Pheromones Volatile organic compounds Tritrophic interaction 

Notes

Acknowledgements

The authors are indebted to numerous sources. Financial support was provided to T.S.D. under the REACCH Project, with funds from U.S.D.A. NIFA Award #2011-68002-30191. Financial support for T.L.C and J.K.T were provided by the National Institute of Justice, Office of Justice Programs, U.S. Department of Justice through Grant 2010-DN-BX-K243. Points of view in this document are those of the authors and do not necessarily represent the official position or policies of the U.S. Department of Justice. Mention of trade names, companies, or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement of the products by the U.S. Department of Agriculture. Financial support for R.W.H was partially provided by U.S.D.A. Forest Service Rocky Mountain Station on U.S.D.A. Grant 08-JV-11221633-250. We are also grateful to Peter Witzgall for encouraging our contribution. Finally, we thank three anonymous referees for contributing their time and effort to review and improve this manuscript.

References

  1. Adams AS, Six DL (2008) Detection of host habitat by parasitoids using cues associated with mycangial fungi of the mountain pine beetle, Dendroctonus ponderosae. Can Entomol 140:124–127Google Scholar
  2. Ahmad F, Daglish GJ, Ridley AW, Walter GH (2012) Responses of Tribolium castaneum to olfactory cues from cotton seeds, the fungi associated with cotton seeds, and cereals. Entomol Exp Appl 145:272–281Google Scholar
  3. Alper H, Moxley J, Nevoigt E, Fink G, Stephanopoulos G (2006) Engineering yeast transcription machinery for improved ethanol tolerance and production. Science 314:1565–1568PubMedGoogle Scholar
  4. Azeem M, Rajarao GK, Nordenhem H, Nordlander G, Borg-karlson AK (2013) Penicillium expansum volatiles reduce pine weevil attraction to host plants. J Chem Ecol 39:120–128PubMedGoogle Scholar
  5. Barker JSF, Parker GJ, Toll GL, Widders PR (1981a) Attraction of Drosophila buzzatii and D. aldrichi to species of yeasts isolated for their natural environment. Aust J Biol Sci 34:593–612Google Scholar
  6. Barker JSF, Toll GL, East PD, Widders PR (1981b) Attraction of Drosophila buzzatii and D. aldrichi to species of yeasts isolated from the natural environment. II. Field experiments. Aust J Biol Sci 34:613–624Google Scholar
  7. Bartelt RJ, Schaner AM, Jackson LL (1985) cis -Vaccenyl acetate as an aggregation pheromone in Drosophila melanogaster. J Chem Ecol 11:1747–1756Google Scholar
  8. Becher PG, Flick G, Rozpedowska E, Schmidt A, Hagman A, Lebreton S, Larsson MC, Hansson BS, Piskur J, Witzgall P, Bengtsson M (2012) Yeast, not fruit volatiles mediate Drosophila melanogaster attraction, oviposition and development. Funct Ecol 26:822–828Google Scholar
  9. Begon M (1986) Yeasts and Drosophila. In: Ashburner M, Carson H, Thompson JN (eds) The genetics and biology of Drosophila, vol 3b. Academic, London, pp 345–383Google Scholar
  10. Bekatorou A, Psarianos C, Koutinas AA (2006) Production of food grade yeasts. Food Tech Biotech 44:407–415Google Scholar
  11. Belmain SR, Simmonds MJ, Blaney WM (2002) Influence of odor from wood-decaying fungi on host selection behavior of deathwatch beetle, Xestobium rufovillosum. J Chem Ecol 28:741–754PubMedGoogle Scholar
  12. Bengtsson G, Erlandsson A, Rundgren S (1988) Fungal odour attracts soil Collembola. Soil Biol Biochem 20:25–30Google Scholar
  13. Bengtsson G, Hedlund K, Rundgren S (1991) Selective odor perception in the soil collembolan Onychius armatus. J Chem Ecol 17:2113–2125Google Scholar
  14. Bentz BJ, Six DL (2006) Ergosterol content of fungi associated with Dendroctonus ponderosae and Dendroctonus rufipennis (Coleoptera: Curculionidae, Scolytinae). Ann Ent Soc Am 99:189–194Google Scholar
  15. Bestmann HJ, Vostrowsky O, Platz H (1977) Male sex pheromones of noctuids. Experientia 33:874–875PubMedGoogle Scholar
  16. Blackmer JL, Phelan PL (1991) Effect of physiological state and fungal inoculation on chemically modulated host-plant finding by Carpophilus hemipterus and Carpophilus lugubris. Entomol Exp Appl 61:33–43Google Scholar
  17. Blomquist GJ, Figueroa-teran R, Aw M, Song M, Gorzalski A, Abbott NL, Chang E, Tittiger C (2010) Pheromone production in bark beetles. Insect Biochem Mol Biol 40:699–712PubMedGoogle Scholar
  18. Boone CK, Six DL, Zheng Y, Raffa KF (2008) Parasitoids and dipteran predators exploit volatiles from microbial symbionts to locate bark beetles. Environ Entomol 37:150–161PubMedGoogle Scholar
  19. Brand JM, Bracke JW, Markovetz AJ, Wood DL, Browne LE (1975) Production of verbenol pheromone by a bacterium isolated from bark beetles. Nature 254:136–137PubMedGoogle Scholar
  20. Brand JM, Bracke JW, Britton LN, Markovetz J, Barras SJ (1976) Bark beetle pheromones: production of verbenone by a mycangial fungus of Dendroctonus frontalis. J Chem Ecol 11:1747–1756Google Scholar
  21. Brand JM, Schultz J, Barras SJ, Edson LJ, Payne TL, Hedden RL (1977) Bark beetle pheromones: enhancement of Dendroctonus frontalis (Coleoptera: Scolytidae) aggregation pheromone by yeast metabolites in laboratory bioassays. J Chem Ecol 3:657–666Google Scholar
  22. Braun SE, Sanderson JP, Daughtrey ML, Wraight SP (2012) Attraction and oviposition responses of the fungus gnat Bradysia impatiens to microbes and microbe-inoculated seedlings in laboratory bioassays. Entomol Exp Appl 145:89–101Google Scholar
  23. Brossut R, Dubois P, Rigaud J (1974) Legrégarisme ChezBlaberus Craniifer: isolement et identification de la Phéromone. J Insect Physiol 20:529–543Google Scholar
  24. Burkepile DE, Parker JD, Woodson CB, Mills HJ, Kubanek J, Sobecky PA, Hay ME (2006) Chemically mediated competition between microbes and animals: microbes as consumers in food webs. Ecology 87:2821–2831PubMedGoogle Scholar
  25. Cardoza YJ, Teal PE, Tumlinson JH (2003) Effect of peanut plant fungal infection on oviposition preference by Spodoptera exigua and on host-searching behavior by Cotesia marginiventris. Environ Entomol 32:970–976Google Scholar
  26. Chaudhury M, Skoda S, Sagel A, Welch J (2010) Volatiles emitted from eight would-isolated bacteria differentially attracted gravid screwworms (Diptera: Cliporidae) to oviposit. J Med Entomol 47:349–354PubMedGoogle Scholar
  27. Cheng L, Booker FL, Tu C, Burkey KO, Zhou L, Shew HD, Rufty TW, Hu S (2012) Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2. Science 337:1084–1087PubMedGoogle Scholar
  28. Cory J, Hoover K (2006) Plant-mediated effects in insect–pathogen interactions. Trends Ecol Evol 21:278–286PubMedGoogle Scholar
  29. Crawford JM, Korman TP, Labonte JW, Vagstad AL, Hill EA, Kamari-Bidkorpeh O, Tsai S-C, Townsend A (2009) Structural basis for biosynthetic programming of fungal aromatic polyketide cyclization. Nature 461:1139–1143PubMedGoogle Scholar
  30. Daisy BH, Strobel GA, Castillo U, Ezra D, Sears J, Weaver DK, Runyon JB (2002) Napthalene, an insect repellant, is produced by Muscodor vitigenus, a novel endophytic fungus. Microbiology 148:3737–3741PubMedGoogle Scholar
  31. Davis TS, Landolt PJ (2013) A survey of insect assemblages responding to volatiles from a ubiquitous fungus in an agricultural landscape. J Chem Ecol. doi:10.1007/s10886-013-0278-z Google Scholar
  32. 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 61:626–634PubMedGoogle Scholar
  33. Davis TS, BoundY-Mills K, Landolt PJ (2012a) Volatile emissions from an epiphytic fungus are semiochemicals for eusocial wasps. Microb Ecol 64:1056–1063PubMedGoogle Scholar
  34. Davis TS, Horton DR, Munyaneza JE, Landolt PJ (2012b) Experimental infection of plants with an herbivore associated bacterial endosymbiont influences herbivore host selection behavior. PLoS One 7:e49330. doi:10.1371/journal.pone.0049330 PubMedGoogle Scholar
  35. De Bruyne M, Baker TC (2008) Odor detection in insects: volatile codes. J Chem Ecol 34:882–897PubMedGoogle Scholar
  36. De Moraes CM, Mescher MC (1999) Interactions of entomology: plant-parasitoid interaction in tritrophic systems. J Entomol Sci 34:31–39Google Scholar
  37. De Moraes CM, Lewis WJ, Paré PW, Alborn HT, Tumlinson JH (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573Google Scholar
  38. Devries PJ (1987) The butterflies of Costa Rica and their natural history. I: papilionidae, pieridae and nymphalidae. Princeton University Press, PrincetonGoogle Scholar
  39. Dicke M (1988) Microbial allelochemicals affecting the behavior of insects, mites, nematodes, and protozoa in different tropic levels. In: Barbosa P, Letourneau DK (Eds) Novel aspects of insect-plant interactions, pp. 125–163Google Scholar
  40. Dicke M (1999) Are herbivore-induced plant volatiles reliable indicators of herbivore identity to foraging carnivorous arthropods? Entomol Exp Appl 91:131–142Google Scholar
  41. Dillon RJ, Dillon VM (2004) The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49:71–92PubMedGoogle Scholar
  42. Dillon RJ, Vennard CT, Charnley AK (2000) Exploitation of gut bacteria in the locust. Nature 403:851PubMedGoogle Scholar
  43. Dillon RJ, Vennard CT, Charnley AK (2002) A note: Gut bacteria produce compounds of a locust cohesion pheromone. J Appl Microbiol 92:759–763PubMedGoogle Scholar
  44. Dindonis LL, Miller JR (1981) Onion fly and little house fly host finding selectively mediated by decomposing onion and microbial volatiles. J Chem Ecol 7:419–426Google Scholar
  45. Dolinski MG, Loschiavo SR (1973) The effect of fungi and moisture on the locometry of the rusty grain beetle, Cryptolestes ferrugineus (Coleoptera: Cucujidae). Can Entomol 105:485–490Google Scholar
  46. Douglas AE (2009) The microbial dimension in insect nutritional ecology. Funct Ecol 23:38–47Google Scholar
  47. Duffey SS, Blum MS, Fales HM, Evans SL, Roncadori RW, Tiemann DL, Nakagawa Y (1977) Benzoyl cyanide and mandelonitrile benzoate in defensive secretions of millipedes. J Chem Ecol 3:101–113Google Scholar
  48. Elena SF, Lenski RE (2003) Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat Rev Genet 4:457–469PubMedGoogle Scholar
  49. Elliot S, Sabelis M, Janssen A, van der Geest L, Beerling E, Fransen J (2000) Can plants use entomopathogens as bodyguards? Ecol Lett 3:228–235Google Scholar
  50. El-Sayed AM, Heppelthwaite BJ, Manning LM, Gibb AR, Suckling DM (2005) Volatile constituents of fermented sugar baits and their attractiveness to lepidopteran species. J Agric Food Chem 53:953–958PubMedGoogle Scholar
  51. Emmens RL, Murray MD (1983) Bacterial odours as oviposition stimulants for Lucilia cuprina (Wiedemann) (Diptera: Calliphoridae), the Australian sheep blow fly. Bull Entomol Res 73:411–415Google Scholar
  52. Endler JA (1993) Some general comments on the evolution and design of animal communication systems. Philos Trans R Soc B Biol Sci 340:215–225Google Scholar
  53. Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH (2004) Airborne signals prime plants against insect herbivore attack. Proc Natl Acad Sci U S A 101:1781–1785PubMedGoogle Scholar
  54. Epsky ND, Heath RR, Dueben BD, Lauzon CR, Proveaux AT, Maccollum GB (1998) Attraction of 3-methyl-1-butanol and ammonia identified from Enterobacter agglomerans to Anastrepha suspensa. J Chem Ecol 24:1867–1880Google Scholar
  55. Ezenwa VO, Gerardo NM, Inouye DW, Medina M, Xavier JB (2012) Animal behavior and the microbiome. Science 338:198–199PubMedGoogle Scholar
  56. Fäldt J, Jonsell M, Nordlander G, Borg-Karlson A (1999) Volatiles of bracket fungi Fomitopsis pinicola and Fomes fomentarius and their functions as insect attractants. J Chem Ecol 25:567–688Google Scholar
  57. Filipiak W, Sponring A, Baur MM, Filipiak A, Ager C, Wiesenhofer H, Nagl M, Troppmair J, Amann A (2012) Molecular analysis of volatile metabolites released specifically by Staphylococcus aureus and Pseudomonas aeruginosa. BMC Microbiol 12:113–129PubMedGoogle Scholar
  58. Finch S, Eckenrode CJ (1985) Influence of unharvested, cull-pile, and volunteer onions on populations of onion maggot (Diptera: Anthomyiidae). J Econ Entomol 78:542–546Google Scholar
  59. Foltan P, Puza V (2009) To complete their life cycle, pathogenic nematode-bacteria complexes deter scavengers from feeding on their host cadaver. Behav Proc 80:76–79Google Scholar
  60. Fontana A, Reichelt M, Hempel S, Gershenzon J, Unsicker SB (2009) The effect of arbuscular mycorrhizal fungi on direct and indirect defense metabolites of Plantago lanceolata L. J Chem Ecol 35:833–843PubMedGoogle Scholar
  61. Frago E, Dicke M, Godfray HCJ (2012) Insect symbionts as hidden players in insect plant interactions. Trends Ecol Evol 27:705–711PubMedGoogle Scholar
  62. Frederickx C, Dekeirsschieter J, Brostaux Y, Wathelet J-P, Verheggen FJ, Haubruge E (2012a) Volatile organic compounds released by blow fly larvae and pupae: new perspectives in forensic entomology. Forensic Sci Int 219:215–220PubMedGoogle Scholar
  63. Frederickx C, Dekeirsschieter J, Verheggen FJ, Haubruge E (2012b) Responses of Lucilia sericata Meigen (Diptera: Calliphoridae) to cadaveric volatile organic compounds. J Forensic Sci 57:386–390PubMedGoogle Scholar
  64. Fujiyuki T, Takeuchi H, Ono M, Ohka S, Sasaki T, Nomoto A, Kubo T (2004) Novel insect picorna-like virus identified in the brains of aggressive worker honeybees. J Virol 78:1093–1100PubMedGoogle Scholar
  65. George J, Jenkins NE, Blanford S, Baker TC (2013) Malaria mosquitoes attracted by fatal fungus. PLoS One 8:e62632. doi:10.1371/journal.pone.0062632 PubMedGoogle Scholar
  66. Gillespie JP, Bailey AM, Cobb B, Vilcinskas A (2000) Fungi as elicitors of insect immune responses. Arch Insect Biochem Physiol 44:49–68PubMedGoogle Scholar
  67. Gottschalk G (1986a) Bacterial fermentations. In: Bacterial metabolism. Springer-Verlag, New York. pp. 208–282Google Scholar
  68. Gottschalk G (1986b) How escherichia coli synthesizes ATP during aerobic growth on glucose. In: Bacterial metabolism. Springer-Verlag, New York. pp. 13–37Google Scholar
  69. Green EM (2011) Fermentative production of butanol—the industrial perspective. Curr Opin Biotech 22:337–343PubMedGoogle Scholar
  70. Guerenstein PG, Lorenzo MG, Nunez JA, Lazzari CR (1995) Baker’s yeast, an attractant for baiting traps for Chagas’ disease vectors. Cell Mol Life Sci 51:834–837Google Scholar
  71. Guevara R, Hutcheson KA, Mee AC, Rayner ADM, Reynolds SE (2000) Resource partitioning of the host fungus Coriolus versicolor by two ciid beetles: the role of odour compounds and host ageing. Oikos 91:184–194Google Scholar
  72. Gulcu B, Hazir S, Kaya HK (2012) Scavenger deterrent factor (SDF) from symbiotic bacteria of entomopathogenic nematodes. J Invert Pathol 110:326–333Google Scholar
  73. Haine ER, Moret Y, Siva-Jothy MT, Rolff J (2008) Antimicrobial defense and persistent infection in insects. Science 322:1257–1259PubMedGoogle Scholar
  74. Hajek AE, Mcmanus ML, Delalibera I Jr (2007) A review of introductions of pathogens and nematodes for classical biological control of insects and mites. Biol Control 41:1–13Google Scholar
  75. Harrington TC (2005) Biology and taxonomy of fungi associated with bark beetles. In: Vega FE, Blackwell M (eds) Insect-fungal associations: ecology and evolution. Oxford University Press, Inc., New York, pp 257–292Google Scholar
  76. Hatcher PE, Paul ND, Ayers PG, Whittaker JB (1994) Interactions between Rumex spp., herbivores and a rust fungus: Gastrophysa viridula grazing reduces subsequent infection by Uromyces rumicus. Funct Ecol 8:265–272Google Scholar
  77. Hatcher PE, Paul ND, Ayers PG, Whittaker JB (1995) Interactions between Rumex spp., herbivores and a rust fungus: the effect of Uromyces rumicus infection on leaf nutritional quality. Funct Ecol 9:97–105Google Scholar
  78. Hausmann SM, Miller JR (1989) Ovipositional preference and larval survival of the onion maggot (Diptera: Anthomyiidae) as influenced by previous maggot feeding. J Econ Entomol 82:426–429Google Scholar
  79. Hedlund K, Bengtsson G, Rundgren S (1995) Fungal odor discrimination in two sympatric species of fungivorous collembolans. Funct Ecol 9:869–875Google Scholar
  80. Herrera CM, García IM, Pérez R (2008) Invisible floral larcenies: microbial communities degrade floral nectar of bumble bee-pollinated plants. Ecology 89:2369–2376PubMedGoogle Scholar
  81. 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 34:205–211Google Scholar
  82. 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 24:2167–2180Google Scholar
  83. Hoyt CP, Osborne GO, Mulcock AP (1971) Production of an insect sex attractant by a symbiotic bacteria. Nature 230:472–473PubMedGoogle Scholar
  84. Huang J, Miller J, Chen S, Vulule J, Walker E (2004) Anopheles gambiae (Diptera: Culicidae) oviposition in response to agarose media and cultured bacterial volatiles. J Med Entomol 43:498–504Google Scholar
  85. Hugenholtz P, Goebel BM, Pace NR (1998) Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180:4765–4774PubMedGoogle Scholar
  86. Hughes DP, Anderson S, Hywel-Jones NL, Himaman W, Bilen J, Boomsma JJ (2011) Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection. BMC Ecol 11:13. doi:10.1186/1472-6785-11-1 PubMedGoogle Scholar
  87. Hulcr J, Pollet M, Ubik K, Vrkoc J (2005) Exploitation of kairomones and synomones by Medetera spp., (Diptera: Dolichopodidae) predators of the spruce bark beetles. Eur J Entomol 102:655–662Google Scholar
  88. Hulcr J, Mann R, Stelinski LL (2011) The scent of a partner: ambrosia beetles are attracted to volatiles from their fungal symbionts. J Chem Ecol 37:1374–1377PubMedGoogle Scholar
  89. Hunt DW, Borden JH (1990) Conversion of verbenols to verbenone by yeast isolated from Dendroctonus ponderosae (Coleoptera: Scolytidae). J Chem Ecol 16:1385–1397Google Scholar
  90. Hussain A, Tian M-Y, He Y-R, Bland JM, Gu W-X (2010) Behavioral and electrophysiological responses of Coptotermes formosanus Shiraki towards entomopathogenic fungal volatiles. Biol Control 55:166–173Google Scholar
  91. Hutchison SA (1973) Biological activities of volatile fungal metabolites. Ann Rev Phytopathol 11:223–246Google Scholar
  92. Hwang Y-S, Kramer W, Mulla M (1980) Oviposition attractants and repellents of mosquitoes. J Chem Ecol 6:71–80Google Scholar
  93. Ingwell LL, Eigenbrode SD, Bosque-Perez NA (2012) Plant viruses alter insect behavior to enhance their spread. Sci Rep 2:578PubMedGoogle Scholar
  94. Jang EB, Light DM, Binder RG, Flath RA, Carvalho LA (1994) Attraction of female Mediterranean fruit flies to the five major components of male-produced pheromone in a laboratory flight tunnel. J Chem Ecol 20:9–20Google Scholar
  95. Janzen DH (1977) Why fruits rot, seeds mold, and meat spoils. Am Nat 111:691–713Google Scholar
  96. Johnstone RA (2002) From parasitism to mutualism: partner control in asymmetric interactions. Ecol Lett 5:634–639Google Scholar
  97. Jonsell M, Nordlander G (1995) Field attraction to odors of the wood-decaying polypores Fomitopsis pinicola and Fomes fomentarius. Ann Zool Fenn 32:391–402Google Scholar
  98. Judd GJR, Borden JH (1992) Aggregated oviposition in Delia antiqua (Meigen): a case for mediation by semiochemicals. J Chem Ecol 18:621–635Google Scholar
  99. Kai M, Haustein M, Molina F, Petri A, Scholtz B, Piechulla B (2009) Bacterial volatiles and their action potential. Appl Microbiol Biotechnol 81:1001–1012PubMedGoogle Scholar
  100. Kalinová B, Podskalská H, Růžička J, Hoskovec M (2009) Irresistible bouquet of death—how are burying beetles (Coleoptera: Silphidae: Nicrophorus) attracted by carcasses. Naturwissenschaften 96:889–899PubMedGoogle Scholar
  101. Keller NP, Turner G, Bennett JW (2005) Fungal secondary metabolism - from biochemistry to genomics. Nat Rev Microbiol 3:927–947Google Scholar
  102. Kim BH, Gadd GM (2008a) Anaerobic fermentation. In: Bacterial physiology and metabolism. Cambridge University Press, Cambridge. pp. 253–297Google Scholar
  103. Kim BH, Gadd GM (2008b) Glycolysis. In; Bacterial physiology and metabolism. Cambridge University Press, Cambridge. pp. 60–84Google Scholar
  104. Konaté S, le Roux X, Verdier B, Lepage M (2003) Effect of underground fungus-growing termites on carbon dioxide emission at the point- and landscape-scales in an African Savanna. Funct Ecol 17:305–314Google Scholar
  105. Korpi A, Jarnberg J, Pasanen AL (2009) Microbial volatile organic compounds. CRC Cr Rev Toxicol 39:139–193Google Scholar
  106. Lam K, Babor D, Duthie B, Babor EM, Moore M, Gries G (2007) Proliferating bacterial symbionts on house fly eggs affect oviposition behaviour of adult flies. Anim Behav 74:81–92Google Scholar
  107. Lam K, Thu K, Tsang M, Moore M, Gries G (2009) Bacteria on housefly eggs, Musca domestica, suppress fungal growth in chicken manure through nutrient depletion or antifungal metabolites. Naturwissenschaften 9:1127–1132Google Scholar
  108. Lam K, Tsang M, Labrie A, Gries R, Gries G (2010) Semiochemical-mediated oviposition avoidance by female house flies, Musca domestica, on animal feces colonized with harmful fungi. J Chem Ecol 36:141–147PubMedGoogle Scholar
  109. Landolt PJ (1998) Chemical attractants for Trapping Yellow jackets Vespula germanica and Vespula pensylvanica (Hymenoptera: Vespidae). Physiol Chem Ecol 27:1229–1234Google Scholar
  110. Lauzon CR, Sjogren RE, Wright SE, Prokopy RJ (1998) Attraction of Rhagoletis pomonella (Diptera: Tephritidae) flies to odor of bacteria: apparent confinement to specialized members of Enterobacteriaceae. Environ Entomol 27:853–857Google Scholar
  111. Leitner M, Kaiser R, Hause B, Boland W, Mithöfer A (2010) Does mycorrhization influence herbivore-induced volatile emission in Medicago truncatula? Mycorrhiza 20:89–101PubMedGoogle Scholar
  112. Leroy PD, Sabri A, Verheggen FJ, Francis F, Thonart P, Haubruge E (2011a) The semiochemically mediated interactions between bacteria and insects. Chemoecology 21:113–122Google Scholar
  113. Leroy PD, Sabri A, Heuskin S, Thonart P, Lognay G, Verheggen FJ, Francis F, Brostaux Y, Felton GW, Haubruge E (2011b) Microorganisms from aphid honeydew attract and enhance the efficacy of natural enemies. Nat Commun. 2, doi:10.1038/ncomms1347
  114. Leufven A, Bergstrom G, Falsen E (1984) Interconversion of verbenols and verbenone by identified yeasts isolated from the spruce bark beetle, Ips typographus. J Chem Ecol 10:1349–1361Google Scholar
  115. Lieutier F, Yart A, Ye H, Sauvard D, Gallois V (2004) Variation in growth and virulence of Leptographium wingfeldii Morelet, a fungus associated with the bark beetle Tomicus piniperda L. Ann For Sci 61:45–53Google Scholar
  116. Lin H, Phelan PL (1991) Identification of food volatiles attractive dusky sap beetle, Carpophilus lugubris (Coleoptera: Nitidulidae). J Chem Ecol 17:1273–1286Google Scholar
  117. Lindh JM, Borg-Karlson A-K, Faye I (2008) Transstadial and horizontal transfer of bacteria within a colony of Anopheles gambiae (Diptera: Culicidae) and oviposition response to bacteria-containing water. Acta Trop 107:242–250PubMedGoogle Scholar
  118. Lorenzo MG, Manrique G, Pires HH, De Brito Sanchez MG, Diotaiuti L, Lazzari CR (1999) Yeast culture volatiles as attractants for Rhodnius prolixus: electroantennogram responses and captures in yeast-baited traps. Acta Trop 72:119–124PubMedGoogle Scholar
  119. Lowery CA, Dickerson TJ, Janda KD (2008) Interspecies and interkingdom communication mediated by bacterial quorum sensing. Chem Soc Rev 37:1337–1346PubMedGoogle Scholar
  120. Ma Q, Fonseca A, Liu W, Fields AT, Pimsler ML, Spindola AF, Tarone AM, Crippen TL, Tomberlin JK, Wood TK (2012) Proteus mirabilis interkingdom swarming signals attract blow flies. ISME J 6:1356–1366PubMedGoogle Scholar
  121. Maccollom GB, Lauzon CR, Sjogren RE, Meyer WL, Olday F (2009) Association and attraction of Blueberry maggot fly Curran (Diptera: Tephritidae) to Pantoea (Enterobacter) agglomerans. Environ Entomol 38:116–120PubMedGoogle Scholar
  122. Madden JL (1968) Behavioral responses of parasites to the symbiotic fungus associated with Sirex noctilio F. Nature 218:189–190Google Scholar
  123. Mann RS, Ali JG, Hermann SL, Tiwari S, Pelz-Stelinski K, Alborn HT, Stelinski LL (2012) Induced release of plant-defense volatile ‘deceptively’ attracts insect vectors to plants infected with a bacterial pathogen. PLOS Pathogens 8:e1002610. doi:10.1371/journal.ppat.1002610 PubMedGoogle Scholar
  124. Mauck KE, De Moraes CM, Mescher MC (2010) Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts. Proc Natl Acad Sci USA 107:3600–3605PubMedGoogle Scholar
  125. Mburu DM, Maniania NK, Hassanali A (2012) Comparison of volatile blends and nucleotide sequences of two Beauveria bassiana isolates of different virulence and repellency towards the termite Macrotermes michealseni. J Chem Ecol 39:101–108PubMedGoogle Scholar
  126. McCarthy A, Williams S (1992) Actinomycetes as agents of biodegradation in the environment–a review. Gene 115:189–192PubMedGoogle Scholar
  127. Meyling NV, Pell JK (2006) Detection and avoidance of an entomopathogenic fungus by a generalist insect predator. Ecol Entomol 31:162–171Google Scholar
  128. Michailides TJ, Morgan DP, Spotts RA, Beglinger C, Odiet P-A (1992) Role of nitidulid beetles and vinegar flies in the sexual cycle of Mucor piriformis in tree fruit orchards. Mycologia 84:488–496Google Scholar
  129. Mondy N, Corio-Costet M-F (2004) Feeding insects with a phytopathogenic fungus influences their diapause and population dynamics. Ecol Entomol 29:711–717Google Scholar
  130. Moore J, Gotelli NJ (1990) A phylogenetic perspective on the evolution of altered host behaviours: a critical look at the manipulation hypothesis. Taylor & Francis Ltd., London, pp 193–233Google Scholar
  131. Morath SU, Hung R, Bennett JW (2012) Fungal volatile organic compounds: a review with emphasis on their biotechnological potential. Fungal Biol Rev 26:73–83Google Scholar
  132. Mukabana W, Mweresa C, Otieno B, Omusula P, Smallegange R, Loon JA, TAKKEN W (2012) A novel synthetic odorant blend for trapping of malaria and other African mosquito species. J Chem Ecol 38(3):235–244PubMedGoogle Scholar
  133. Nisbet EG, Sleep NH (2001) The habitat and nature of early life. Nature 409:1083–1091PubMedGoogle Scholar
  134. Noda H, Koizumi Y (2003) Sterol biosynthesis by symbiotes: cytochrome P450 sterol C-22 desaturase genes from yeast-like symbiotes of rice planthoppers and anobiid beetles. Insect Biochem Mol Biol 33:649–658PubMedGoogle Scholar
  135. Nout MR, 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 24:1217–1239Google Scholar
  136. Obire O (2005) Activity of Zymomonas species in palm-sap obtained from three areas in Edo State, Nigeria. J Appl Sci Env Manag 9:25–30Google Scholar
  137. Pasanen A-L, Korpi A, Kasanen J-P, Pasanen P (1998) Critical aspects on the significance of microbial volatile metabolites as indoor air pollutants. Environ Int 24:703–712Google Scholar
  138. Pelaez F (2004) Biological activities of fungal metabolites. In: An Z (ed) Mycology series, vol. 22: handbook of industrial mycology. Marcel Dekker, Inc., New York, pp 49–92Google Scholar
  139. Pelosi P, Zhou JJ, Ban LP, Calvello M (2006) Soluble proteins in insect chemical communication. Cell Mol Life Sci 63:1658–1676PubMedGoogle Scholar
  140. Phelan PL, Lin H (1991) Chemical characterization of fruit and fungal volatiles attractive to dried-fruit beetle, Carphophilus hemipterus (Coleoptera: Nitidulidae). J Chem Ecol 17:1253–1272Google Scholar
  141. Pichersky E, Noel JP, Dudareva N (2006) Biosynthesis of plant volatiles: nature’s diversity and ingenuity. Science 311:808–811PubMedGoogle Scholar
  142. Pierce AM, Pierce HD, Borden JH, Oehlschlager AC (1991) Fungal volatiles: semiochemicals for stored-product beetles (Coleoptera: Cucujidae). J Chem Ecol 17:581–597Google Scholar
  143. Pineda A, Zheng S-J, van Loon JJA, Pieterse CMJ, Dicke M (2010) Helping plants to deal with insects: the role of beneficial soil-born microbes. Trends Plant Sci 15:507–514PubMedGoogle Scholar
  144. Ponnusamy L, Xu N, Wesson DM, Schal C, Apperson CS (2008) Identification of bacteria and bacteria-associated chemical cues that mediate oviposition site preferences by Aedes aegypti. Proc Natl Acad Sci USA 105:9262–9267PubMedGoogle Scholar
  145. Ponnusamy L, Wesson DM, Arellano C, Schal C, Apperson CS (2010) Species composition of bacterial communities influences attraction of mosquitoes to experimental plant infusions. Microb Ecol 59:158–173PubMedGoogle Scholar
  146. Ponnusamy L, Böröczky K, Wesson D, Schal C, Apperson C (2011) Bacteria stimulate hatching of yellow fever mosquito eggs. PLoS One 6:e24409PubMedGoogle Scholar
  147. Popoff MR (1984) Selective medium for isolation of Clostridium butyricum from human feces. Clin Microbiol 20:417–420Google Scholar
  148. Poulin R (2000) Manipulation of host behaviour by parasites: a weakening paradigm? Proc R Soc Lond B 267:787–792Google Scholar
  149. Price PW, Denno RF, Eubanks MD, Finke DL, Kaplan I (2011) Insect ecology: behavior, populations, and communities. Cambridge University Press, New YorkGoogle Scholar
  150. Raguso RA (2004) Flowers as sensory billboards: towards an integrated understanding of floral advertisement. Curr Opin Plant Biol 7:434–440PubMedGoogle Scholar
  151. Raguso RA (2008) Wake up and smell the roses: the ecology and evolution of floral scent. Annu Rev Ecol Evol Syst 39:549–569Google Scholar
  152. Raguso RA, Roy BA (1998) ‘Floral’ scent production by Puccinia rust fungi that mimic flowers. Mol Ecol 7(9):1127–1136PubMedGoogle Scholar
  153. Reinhard J (2004) Insect chemical communication. ChemosSense 6:1–6Google Scholar
  154. Robacker DC, Bartelt RJ (1997) Chemicals attractive to Mexican fruit fly from Klebsiella pneumonia and Citrobacter freundii cultures sampled by solid-phase microextraction. J Chem Ecol 23:2897–2915Google Scholar
  155. Robacker DC, Flath RA (1995) Attractants from Staphylococcus aureus cultures for Mexican fruit fly, Anastrepha ludens. J Chem Ecol 21:1861–1874Google Scholar
  156. Robacker DC, Lauzon CR (2002) Purine metabolizing capability of Enterobacter agglomerans affects volatiles production and attractiveness to Mexican fruit fly. J Chem Ecol 28:1549–1563PubMedGoogle Scholar
  157. Robacker DC, Moreno DS (1995) Protein feeding attenuates attraction of Mexican fruit flies (Diptera: Tephritidae) to volatile bacterial metabolites. Fla Entomol 78:62–69Google Scholar
  158. Robacker DC, Lauzon CR, He X (2004) Volatiles production and attractiveness to Mexican fruit fly of Enterobacter agglomerans isolated from apple maggot flies and Mexican fruit flies. J Chem Ecol 30:1329–1347PubMedGoogle Scholar
  159. Roder G, Rahier M, Naisbit RE (2007) Coping with an antagonist: the impact of a phytopathogenic fungus on the development and behavior of two species of alpine leaf beetle. Oikos 116:1514–1523Google Scholar
  160. Rohlfs M, Churchill ACL (2011) Fungal secondary metabolites as modulators of interactions with insects and other arthropods. Fungal Genet Biol 48:23–34PubMedGoogle Scholar
  161. Rohlfs M, Albert M, Keller NP, Kempken F (2007) Secondary chemicals protect mold from fungivory. Biol Lett 3:523–525PubMedGoogle Scholar
  162. Romano P, Suzzi G, Turbanti L, Polsinelli M (1994) Acetaldehyde production in Saccharomyces cerevisiae wine yeasts. FEMS Micro Lett 118:213–218Google Scholar
  163. Romero A, Broce A, Zurek L (2006) Role of bacteria in the oviposition behavior and larval development of stable flies. Med Vet Entomol 20:115–121PubMedGoogle Scholar
  164. Rozen DE, Engelmoer DJP, Smiseth PT (2008) Antimicrobial strategies in burying beetles breeding on carrion. Proc Natl Acad Sci USA 105:17890–17895PubMedGoogle Scholar
  165. Ryan K, de Groot P, Davis C, Smith SM (2012) Effect of two bark beetle-vectored fungi on the on-host search and oviposition behavior of the introduced woodwasp Sirex noctilio (Hymenoptera: Siricidae) on Pinus sylvestris trees and logs. J Insect Behav 25:453–466Google Scholar
  166. Ryu C-M, Faragt MA, Hu C-H, Reddy MS, Wei H-X, Paré PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci USA 1008:4927–4932Google Scholar
  167. Ryu C-M, Farag MA, Hu C-H, Reddy MS, Kloepper JW, Pare PW (2004) Bacterial volatiles induce systematic resistance in Arabidopsis. Plant Physiol 134:881–882Google Scholar
  168. Schiesti FP, Steinebrunner F, Schulz C, von Reub S, Francke W, Weymuth C, Leuchtmann A (2006) Evolution of ‘pollinator’-attracting signals in fungi. Biol Lett 2:401–404Google Scholar
  169. Schultz S, Dickschat J (2007) Bacterial volatiles: the smell of small organisms. Nat Prod Rep 24:814–842Google Scholar
  170. Segura DF, Viscarret MM, Ovruski SM, Cladera JL (2012) Response of the fruit fly parasitoid Diachasmimorpha longicaudata to host and host-habitat volatile cues. Entomol Exp Appl 153:164–176Google Scholar
  171. Shendure J, Ji H (2008) Next-generation DNA sequencing. Nat Biotechnol 26:1135–1145PubMedGoogle Scholar
  172. Six DL, Wingfield MJ (2011) The role of phytopathogenecity in bark beetle-fungus symbioses: a challenge to the classic paradigm. Annu Rev Entomol 56:255–272PubMedGoogle Scholar
  173. Solheim H (1992) The early stages of fungal invasion in Norway spruce infested by the bark beetle Ips typographus. Can J Bot 70:1–5Google Scholar
  174. St. Leger RJ (2008) Studies on adaptation of Metarhizium anisopliae to life in the soil. J Invert Pathol 98:271–276Google Scholar
  175. Stamps JA, Yang LH, Morales VM, Boundy-Mills KL (2012) Drosophila regulate yeast density and increase yeast community similarity in a natural substrate. PLoS One 7:e42238. doi:10.1371/journal.pone.0042238 PubMedGoogle Scholar
  176. Steinebrunner F, Schiestl F, Leuchtmann A (2008) Variation of insect attracting odor in endophytic Epichloë fungi: phylogenetic constrains versus host influence. J Chem Ecol 34:772–782PubMedGoogle Scholar
  177. Steiner S, Erdmann D, Steidle JLM, Ruther J (2007a) Host habitat assessment by a parasitoid using fungal volatiles. Frontiers Zool 4:3. doi:10.1186/1742-9994-4-3 Google Scholar
  178. Steiner S, Seidleb JLM, Ruther J (2007b) Host-associated kairomones used for habitat orientation in the parasitoid Lariophagus distinguendus (Hymenoptera: Pteromalidae). J Stored Prod Res 43:587–593Google Scholar
  179. Stensmyr MC, Urru I, Collu I, Celander M, Hansson BS, Angioy A-M (2002) Rotting smell of dead-horse arum florets. Nature 420:625–626PubMedGoogle Scholar
  180. Stensmyr MC, Dweck HKM, Farhan A, Ibba I, Strutz A, Mukunda L, Linz J, Grabe V, Steck K, Lavista-Llanos S, Wicher D, Sachse S, Knadsen M, Becher PG, Seki Y, Hansson BS (2012) A conserved dedicated olfactory circuit for detecting harmful microbes in Drosophila. Cell 151:1345–1357PubMedGoogle Scholar
  181. Stotzky G, Schenck S (1976) Volatile organic compounds and microorganisms. CRC Cr Rev Microbiol 4:333–382Google Scholar
  182. Sullivan BT, Berisford CW (2004) Semiochemicals from fungal associates of bark beetles may mediate host location behavior of parasitoids. J Chem Ecol 30:703–717PubMedGoogle Scholar
  183. Sun Y, Cheng J (2002) Hydrolysis of lignocellulosic materials for ethanol production: a review. Biores Tech 83:1–11Google Scholar
  184. Tasin M, Betta E, Carlin S, Gasperi F, Mattivi F, Pertot I (2011) Volatiles that encode host-plant quality in the grapevine moth. Phytochemistry 72:1999–2005PubMedGoogle Scholar
  185. Tasin M, Knudsen GK, Pertot I (2012) Smelling a diseased host: grapevine moths responses to healthy and fungus-infected grape. Anim Behav 83:555–562Google Scholar
  186. Thibout E, Guillot JF, Auger J (1993) Microorganisms are involved in the production of volatile kairomones affecting host seeking behavior of Diadromus pulchellus, a parasitoid of Acrolepiosis assectella. Physiolog Entomol 18:176–182Google Scholar
  187. Thibout E, Guillot JF, Ferary S, Limouzin P, Auger J (1995) Origin and identification of bacteria which produce kairomones in the frass of Acrolepiosis assectella (Lep., Hyponomeutoidea). Experientia 51:1073–1075PubMedGoogle Scholar
  188. Tillman JA, Seybold SJ, Russell AJ, Blomquist GJ (1999) Insect pheromones — an overview of biosynthesis and endocrine regulation. Insect Biochem Mol Biol 29:481–514PubMedGoogle Scholar
  189. Todar K (2012) Todar’s online textbook of bacteriology. Todar K (Ed). Madison, WisconsinGoogle Scholar
  190. Tomberlin JK, Byrd JH, Wallace JR, Benbow ME (2012a) Assessment of decomposition studies indicates need for standardized and repeatable methods in forensic entomology. J Forensic Res. 3: doi:10.4172/2157-7145.1000147
  191. Tomberlin JK, Crippen TL, Tarone AM, Singh B, Adams K, Rezenom YH, Benbow E, Flores M, Longnecker M, Pechal JL, Russell DH, Beier RC, Wood TK (2012b) Interkingdom responses of flies to bacteria mediated by fly physiology and bacterial quorum sensing. Anim Behav 84:1449–1456Google Scholar
  192. Trexeler JD, Apperson CS, Zurek L, Gemmeno C, Schal C, Kaufman M, Walker E, Watson DW, Wallace L (2003) Role of bacteria in mediating the oviposition responses of Aedes albopictus (Diptera: Culicidae). J Med Entomol 40:841–848Google Scholar
  193. Turlings TC, Benrey B (1998) Effect of plant metabolites on the behavior and development of parasitic wasps. Ecoscience 5:321–333Google Scholar
  194. Turlings TCJ, Wackers F (2004) Recruitment of predators and parasitoids to herbivore-injured plants. In: Cardé RT, Millar JG (eds) Advances in insect chemical ecology. Cambridge University Press, Cambridge, pp 21–75Google Scholar
  195. Utrio P, Eriksson K (1977) Volatile fermentation products as attractants for Macrolepidoptera. Ann Zool Fenn 14:98–104Google Scholar
  196. Vanhaelen M, Vanhaelen-Fastre R, Geeraerts J (1980) Occurrence in mushroom (Homobasidiomycetes) of cis- and trans-octa-1,5-dien-3-ol, attractants to the cheese mite Tyrophagus putrescentiae (Schrank) (Acarina, Acaridae). Experientia 36:406–407Google Scholar
  197. Vega FE, Goettel MS, Blackwell M, Chandler D, Jackson MA, Keller S, Koike MS, Maniania NK, Monzón A, Ownley BH, Pell JK, Rangel DEN, Roy HE (2006) Fungal entomopathogens: new insights on their ecology. Fungal Ecol 2:149–159Google Scholar
  198. Verhulst NO, Beijleveld H, Knols BG, Takken W, Schraa G, Bouwmeester HJ, Smallegange RC (2009) Cultured skin microbiota attracts malaria mosquitoes. Malaria J 8:302Google Scholar
  199. Verhulst NO, Andriessen R, Groenhagen U, Bukovinszkiné-Kiss G, Schulz S, Takken W, van Loon JJA, Schraa G, Smallegange RC (2010a) Differential attraction of malaria mosquitoes to volatile blends produced by human skin bacteria. PLoS One 5:e15829PubMedGoogle Scholar
  200. Verhulst NO, Takken W, Dicke M, Schraa G, Smallegange RC (2010b) Chemical ecology of interactions between human skin microbiota and mosquitoes. FEMS Microbiol Ecol 74:1–9PubMedGoogle Scholar
  201. Verhulst NO, Mukabana WR, Takken W, Smallegange RC (2011) Human skin microbiota and their volatiles as odour baits for the malaria mosquito Anopheles gambiae. Entomol Exp Appl 139:170–179Google Scholar
  202. Vining LC (1990) Functions of secondary metabolites. Annu Rev Microbiol 44:395–425PubMedGoogle Scholar
  203. von Hoermann C, Ruther J, Reibe S, Madea B, Ayasse M (2011) The importance of carcass volatiles as attractants for the hide beetle Dermestes maculatus (De Geer). Forensic Sci Int 212:173–179Google Scholar
  204. Wertheim B, van Baalen E-JA, Dicke M, Vet LEM (2005) Pheromone-mediated aggregation in nonsocial arthropods. Annu Rev Entomol 50:321–346PubMedGoogle Scholar
  205. Wessen B, Schoeps K-O (1996) Microbial volatiles organic compounds–What substances can be found in sick buildings? Analyst 121:1203–1205PubMedGoogle Scholar
  206. Wildman JD (1933) Note on the use of microorganisms for the production of odors attractive to the dried fruit beetle. J Econ Entomol 26:516–517Google Scholar
  207. Witzgall P, Proffit M, Rozpedowska E, Becher PG, Andreadis S, Coracini M, Lindblom TU, Ream LJ, Hagman A, Bengtsson M, Kurtzmann CP, Piskur J, Knight A (2012) “This is not an apple” – yeast mutualism in codling moth. J Chem Ecol 38:949–957PubMedGoogle Scholar
  208. Xu J (2006) Invited review: microbial ecology in the age of genomics and metagenomics: concepts, tools, and recent advances. Mol Ecol 15:1713–1731PubMedGoogle Scholar
  209. Yanagawa A, Fujiwara-Tsuji N, Akino T, Yoshimura T, Yanagawa T, Shimizu S (2011) Musty odor of entomopathogens enhances disease-prevention behaviors in the termite Coptotermes formosanus. J Invert Pathol 108:1–6Google Scholar
  210. Zhang C, Yang H, Yang F, Ma Y (2009) Current progress on butyric acid production by fermentation. Curr Microbiol 59:656–663PubMedGoogle Scholar
  211. Zhu GH, Xu XH, Yu XJ, Zhang Y, Wang JF (2006) Puparial case hydrocarbons of Chrysomya megacephala as an indicator of the postmortem interval. Forensic Sci Int 169:1–5PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Thomas Seth Davis
    • 1
  • Tawni L. Crippen
    • 2
  • Richard W. Hofstetter
    • 3
  • Jeffery K. Tomberlin
    • 4
  1. 1.Plant, Soil, and Entomological SciencesUniversity of IdahoMoscowUSA
  2. 2.U.S.D.A. Agricultural Research ServiceSouthern Plains Agricultural Research CenterCollege StationUSA
  3. 3.College of Engineering, Forestry, and Natural SciencesNorthern Arizona UniversityFlagstaffUSA
  4. 4.Department of EntomologyTexas A&M UniversityCollege StationUSA

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