Abstract
The two major aldehydes (E)-2-hexenal and (E)-2-octenal emitted as defensive secretions by bed bugs Cimex lectularius L. (Hemiptera: Cimicidae), inhibit the in vitro growth of an isolate of Metarhizium anisopliae sensu lato (s.l.) (Metsch.) Sokorin (Hypocreales: Clavicipitaceae) (ARSEF 1548). These chemicals inhibit fungal growth by direct contact and via indirect exposure (“fumigation”). Fumigation with (E)-2-octenal for as little as 0.5 h was sufficient to inhibit all fungal growth. Bed bugs placed on filter paper treated with an isolate of M. anisopliae s.l. conidia in the absence of (E)-2-octenal exhibited 99 % mortality after one week. However, bed bugs placed on fungal-treated filter paper and exposed to (E)-2-octenal at 1 h experienced 10 % mortality. The inhibition of fungal growth by bed bug aldehydes is discussed in the context of other biotic and abiotic barriers to infection.
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References
Aldrich JR (1988) Chemical ecology of the Heteroptera. Annu Rev Entomol 33:211–238
Barbarin AM, Jenkins NE, Rajotte EG, Thomas MB (2012) A preliminary evaluation of the potential of Beauveria bassiana for bed bug control. J Invertbr Pathol 111:82–85
Bates D, Maechler M, Bolker BM, Walker SC (2014) lme4: linear mixed effects models using Eigen and S4. R package version 1.1–7. Available via http://CRAN.R-project.org/package=lme4. Cited 20 Mar 2015
Battinelli L, Daniele C, Cristiani M, Bisignano G, Saija A, Mazzanti G (2006) In vitro antifungal and anti-elastase activity of some aliphatic aldehydes from Olea europaea L. fruit. Phytomedicine 13:558–563
Benoit JB, Phillips SA, Croxall TJ, Christensen BS, Yoder JA, Denlinger DL (2009) Addition of alarm pheromone components improves the effectiveness of desiccant dusts against Cimex lectularius. J Med Entomol 46:572–579
Bisignano G, Laganá MG, Trombetta D, Arena S, Nostro A, Uccella N, Mazzanti G, Saija A (2001) In vitro antibacterial activity of some aliphatic aldehydes from Olea eropaea L. FEMS Microbiol Lett 198:9–13
Blanford S, Chan BHK, Jenkins N, Sim D, Turner RJ, Read AF, Thomas MB (2005) Fungal pathogen reduces potential for malaria transmission. Science 308:1638–1641
Braga GUL, Flint SD, Messias CL, Anderson AJ (2001) Effect of UV-B on conidia and germlings of the entompathogenic hyphomycete Metarhizium anisopliae. Mycol Res 105:874–882
Bukhari T, Takken W, Koenraadt CJM (2011) Development of Metarhizium anisopliae and Beauveria bassiana formulations for control of malaria mosquito larvae. Parasites & Vector 4:23
Chouvenc T, Su N-Y (2010) Apparent synergy among defense mechanisms in subterranean termites (Rhinotermitidae) against epizootic events: limits and potential for biological control. J Econ Entomol 103:1327–1337
Cleveland TE, Carter-Wientjes CH, DeLucca AJ, Boué SM (2009) Effect of soybean volatile compounds on Aspergillus flavus growth and aflatoxin production. J Food Sci 74:84–87
Collins RP (1968) Carbonyl compounds produced by bed bug Cimex lectularius. Ann Entomol Soc Am 61:1338–1339
de Faria MR, Wraigt SP (2007) Mycoinsecticides and mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biol Control 43:237–256
Feldlaufer MF, Harlan HJ, Miller DM (2014) Laboratory rearing of bed bugs. In: Mamamorosch K, Mahmood F (eds) Rearinig animal and plant vectors, 1st edn. CRC Press, Boca Raton, pp 118–140
Fernandes S, Simoes M, Dias N, Santos C, Lima N (2012) Fungicidal activity of microbicides. In: Fraise A, Maillard J-Y, Sattar S (eds) Russell, Hugo and Ayliffe’s principles and practice of disinfection, preservation and sterilization, 5th edn. Wiley, UK, pp 142–154
Gołębiowski M, Maliński E, Boguś 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
Gross J, Schumacher K, Schmidtberg H, Vilcinskas A (2008) Protected by fumigants: beetle perfumes in antimicrobial defense. J Chem Ecol 34:179–188
Hajek AE, Delalibera I Jr (2010) Fungal pathogens as classical biological control agents against arthropods. BioControl 55:147–158
Hajek AE, St Leger RJ (1994) Interactions between fungal pathogens and insect hosts. Annu Rev Entomol 39:293–322
Hänel H (1982) The life cycle of the insect pathogenic fungus Metarhizium anisopliae in the termite Nasutitermes exitiosus. Mycopathol 80:137–145
Harraca V, Ryne C, Ignell R (2010) Nymphs of the common bed bug (Cimex lectularius) produce anti-aphrodisiac defense against conspecific males. BMC Biol 8:121
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363
Inglis GD, Enkerli J, Goettel MS (2012) Laboratory techniques for entomopathogenic fungi: Hypocreales. In: Lacey LA (ed) Manual of techniques in invertebrate pathology, 2nd edn. Elsevier Ltd., London, pp 189–251
Jaronski ST (2010) Ecological factors in the inundative use of entomopathogens. BioControl 55:159–185
Kilpinen O, Liu D, Adamsen APS (2012) Real-time measurement of volatile chemicals released by bed bugs during mating activities. PLoS ONE 7:e50981
Kubo A, Kubo I (1995) Antimicrobial agents from Tanacetum balsamita. J Nat Prod 58:1565–1569
Lacey LA, Solter LF (2012) Initial handling and diagnosis of diseased invertebrates. In: Lacey LA (ed) Manual of techniques in invertebrate pathology, 2nd edn. Academic Press, Amsterdam, pp 1–14
Levinson HZ, Bar Ilan AR (1971) Assembling and alerting scents produced by the bed bug Cimex lectularius L. Experientia 27:102–103
Levinson HZ, Levinson AR, Maschwitz U (1974) Action and composition of the alarm pheromone of the bedbug Cimex lectularius L. Naturwissenschaften 61:684–685
McCauley VJE, Zacharuk RY (1968) Histopathology of green muscardine in larvae of four species of elateridae (Coleoptera). J Invertbr Pathol 12:444–459
Moino A Jr, Alves SB, Lopes RB, Oliveira PM, Neves J, Pereira RM, Vieira A (2002) External development of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in the subterranean termite Heterotermes tenuis. Sci Agric 59:267–273
Myles TG (2002) Alarm, aggregation, and defense by Reticulitermes flavipes in response to a naturally occurring isolate of Metarhizium anisopliae. Sociobiol 40:243–255
Ortiz-Urquiza A, Keyhani NO (2013) Action on the surface: entomopathogenic fungi versus the insect cuticle. Insects 4:357–374
R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available at http://www.R-project.org/. Accessed 25 Aug 2014
Schildknecht H, Holoubek K, Weis KH, Krämer H (1964) Defensive substances of the arthropods, their isolation and identification. Agn Chem (international edition) 3:73–82
Shah PA, Pell JK (2003) Entomopathogenic fungi as biological control agents. Appl Microbiol Biotechnol 61:413–423
Siljander E, Gries R, Khaskin K, Gries G (2008) Identification of the airborne aggregation pheromone of the common bed bug, Cimex lectularius. J Chem Ecol 34:708–718
Sosa-Gomez DR, Boucias DG, Nation JL (1997) Attachment of Metarhizium anisopliae to the southern green stink bug Nezara viridula cuticle and fungistatic effect of cuticular lipids and aldehydes. J Invertbr Pathol 69:31–39
Trombetta D, Saija A, Bisignano G, Arena S, Caruso S, Mazzanti G, Uccella N, Castelli F (2002) Study on the mechanisms of antibacterial action of some plant α, β—unsaturated aldehydes. Lett Appl Microbiol 35:285–290
Ulrich KR, Feldlaufer MF, Kramer M, St. Leger RJ (2014) Exposure of bed bugs to Metarhizium anisopliae at different humidities. J Econ Entomol 107:2190–2195
Vega FE, Meyling NV, Luangsa-ard JJ, Blackwell M (2012) Fungal entomopathogens. In: Vega F, Kaya H (eds) Insect pathology, 2nd edn. Elsevier, London, pp 171–220
Vieira CR, Blassioli-Moraes MC, Borges M, Pires CSS, Sujii ER, Laumann RA (2014) Field evaluation of (E)-2-hexenal efficacy for behavioral manipulation of egg parasitoids in soybean. BioControl 59:525–537
Vilcinskas A, Götz P (1999) Parasitic fungi and their interactions with the insect immune system. Adv Parasitol 43:267–313
Wang C, St Leger RJ (2005) Developmental and transcriptional responses to host and nonhost cuticles by the specific locust pathogen Metarhizium anisopliae var. acridum. Eukaryot Cell 4:937–947
Wilson K, Cotter SC, Reeson AF, Pell JK (2001) Melanism and disease resistance in insects. Ecol Lett 4:637–649
Yeo H, Pell JK, Alderson PG, Clark SJ, Pye BJ (2003) Laboratory evaluation of temperature effects on the germination and growth of entomopathogenic fungi and on their pathogenicity to two aphid species. Pest Manag Sci 59:156–165
Zimmermann G (2007) Review on safety of the entomopathogenic fungus Metarhizium anisopliae. Biocontrol Sci Technol 17:879–920
Acknowledgments
We thank Barbara Thorne (University of Maryland, College Park, USA) for guidance and reviewing the manuscript. We also thank members of the Armed Forces Pest Management Board (Silver Spring MD, USA), and personnel at the Walter Reed National Military Medical Center (Bethesda MD, USA) for their help in obtaining the blood products used to maintain insect colonies. This project was funded in part by the University of Maryland’s Department of Entomology’s Gahan Fellowship. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture. USDA is an equal opportunity provider and employee.
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Ulrich, K.R., Feldlaufer, M.F., Kramer, M. et al. Inhibition of the entomopathogenic fungus Metarhizium anisopliae sensu lato in vitro by the bed bug defensive secretions (E)-2-hexenal and (E)-2-octenal. BioControl 60, 517–526 (2015). https://doi.org/10.1007/s10526-015-9667-2
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DOI: https://doi.org/10.1007/s10526-015-9667-2