Insect-killing fungi such as Beauveria bassiana are being evaluated as possible active ingredients for use in novel biopesticides against mosquito vectors that transmit malaria. Fungal pathogens infect through contact and so applications of spores to surfaces such as walls, nets, or other resting sites provide possible routes to infect mosquitoes in and around domestic dwellings. However, some insects can detect and actively avoid fungal spores to reduce infection risk. If true for mosquitoes, such behavior could render the biopesticide approach ineffective. Here we find that the spores of B. bassiana are highly attractive to females of Anopheles stephensi, a major anopheline mosquito vector of human malaria in Asia. We further find that An. stephensi females are preferentially attracted to dead and dying caterpillars infected with B. bassiana, landing on them and subsequently becoming infected with the fungus. Females are also preferentially attracted to cloth sprayed with oil-formulated B. bassiana spores, with 95% of the attracted females becoming infected after a one-minute visit on the cloth. This is the first report of an insect being attracted to a lethal fungal pathogen. The exact mechanisms involved in this behavior remain unclear. Nonetheless, our results indicate that biopesticidal formulations comprising B. bassiana spores will be conducive to attraction and on-source visitation by malaria vectors.
References
[1]
WHO World Malaria Report (2011) Geneva: World Health Organization.
Scholte EJ, Ng’habi K, Kihonda J, Takken W, Paaijmans K, et al. (2005) An entomopathogenic fungus for control of adult African malaria mosquitoes. Science 308: 1641–1642.
[4]
Farenhorst M, Hilhorst A, Thomas MB, Knols BGJ (2011) Development of fungal applications on netting substrates for malaria vector control. J Med Entomol 48(2): 305–313.
[5]
Blanford S, Shi W, Christian R, Marden JH, Koekemoer LL, et al. (2011) Lethal and pre-lethal effects of a fungal biopesticide contribute to substantial and rapid control of malaria vectors. PLoS One 6(8): e23591.
[6]
Fernandes EKK, Angelo IC, Rangel DEN, Bahiense TC, Moraes AML, et al. (2011) An intensive search for promising fungal biological control agents of ticks, particularly Rhipicephalus microplus. Vet Parasitol 182: 307–318.
[7]
Maniania NK, Odulaja A (1998) Effect of species, age and sex of tsetse on respons to infection by Metarhizium anisopliae. Biocontrol 43: 311–383.
[8]
Pedrini N, Mijailovsky SJ, Girott JR, Stariolo R, Cardozo RM, et al. (2009) Control of pyrethroid-resistant Chagas disease vectors with entomopathogenic fungi. PLoS Negl Trop Dis 3 (2): 1–11.
[9]
Barbarin AM, Jenkins NE, Rajotte EG, Thomas MB (2012) A preliminary evaluation of the potential of Beauveria bassiana for bedbug control. J Invert Pathol 111: 82–85.
[10]
Thomas MB, Read AF (2007) Can fungal biopesticides control malaria? Nat Rev Microbiol 5: 377–383.
[11]
Read AF, Lynch PA, Thomas MB (2009) How to make evolution-proof insecticides for malaria control. PLoS Biol 7: 4.
[12]
Lynch PA, Grimm U, Thomas MB, Read AF (2012) Prospective malaria control using entomopathogenic fungi: comparative evaluation of impact on transmission and selection for resistance. Malaria J 11: 383.
[13]
Maehara N, He HY, Shimazu M (2007) Maturation feeding and transmission of Bursaphelenchus xylophilus (Nematoda: Parasitaphelenchidae) by Monochamus alternatus (Coleoptera: Cerambycidae) inoculated with Beauveria bassiana (Deuteromycotina: Hyphomycetes). J Econ Entomol 100: 49–53.
[14]
Seyoum E, Bateman RP, Charnley AK (2002) The effect of Metarhizium anisopliae var acridum on haemolymph energy reserves and flight capability in the desert locust, Shistocerca greagaria. J Appl Entomol 126: 119–124.
[15]
Arthurs SA, Thomas MB (2001) Investigation into behavioral changes in Schistocerca gregaria following infection with a mycoinsecticide: implications for susceptibility to predation. Ecol Entomol 26: 227–234.
[16]
Pedrini N, Villaverde ML, Fuse CB, Dal Bello GM, Juarez MP (2010) Beauveria bassiana Infection Alters Colony Development and Defensive Secretions of the Beetles Tribolium castaneum and Ulomoides dermestoides (Coleoptera: Tenebrionidae). J Econ Entomol 103(4): 1094–1099.
[17]
Howard AFV, N’Guessan R, Koendraadt CJM, Asidi A, Farenhorst M, et al. (2010) The entomopathogenic fungi Beauveria bassiana reduces instantaneous blood feeding in wild multi–insecticide-resistant Culex quinquefasciatus mosquitoes un Benin, West Africa Parasit Vectors. 3: 87.
[18]
George J, Blanford S, Domingue MJ, Thomas MB, Read AF, et al. (2011) Reduction in host-finding behavior in fungus-infected mosquitoes is correlated with reduction in olfactory neuron responsiveness. Malar J 10: 219.
[19]
Scholte EJ, Knols BGJ, Takken W (2006) Infection of the malaria mosquito Anopheles gambiae with the entomopathogenic fungus Metarhizium anisopliae reduces blood feeding and fecundity. J Invertebr Pathol 91: 43–49.
[20]
Hall DR, Beevor PS, Cork A, Nesbitt BF, Vale GA (1984) 1-octen-3-ol, a potent olfactory stimulant and attractant for tsetse isolated from cattle odours. Insect Sci Appl 5: 335–339.
[21]
Cork A, Park KC (1996) Identification of electrophysiologically active compounds for the malaria mosquito, Anopheles gambiae, in human sweat extracts. Med Vet Entomol 10: 269–276.
[22]
Qiu YT, van Loon JJA, Takken W, Meijerink J, Smid HM (2006) Olfactory coding in antennal neurons of the malaria mosquito, Anopheles gambiae, Chem Sense. 31: 845–863.
[23]
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.
[24]
Lecuona RE, Turica M, Tarocco F, Crespo DC (2005) Microbial control of Musca domestica (Diptera: Muscidae) with selected strains of Beauveria bassiana. J Med Entomol 42: 332–336.
[25]
Liu HP, Bauer LS (2008) Microbial control of Agrilus planipennis (Coleoptera: Buprestidae) with Beauveria bassiana strain GHA: field applications. Biocontril Science and Technol 18: 565–579.
[26]
Jones WE, Grace JK, Tamashiro M (1996) Virulence of seven isolates of Beauveria bassiana and Metarhizium anisopliae to Coptotermes formosanus (Isoptera: Rhinotermitidae). Environ Entomol 25: 481–487.
[27]
Lomer CJ, Bateman RP, Johnson DL, Langewald J, Thomas M (2001) Biological control of locusts and grasshoppers. Annu Rev Entomol 46: 667–702.
[28]
Harris P, Riordan DF, Cooke D (1969) Mosquitoes feeding on insect larvae. Science, New Vol. 164, No. 3876: 184–185.
[29]
Martel V, Schlyter F, Ignell R, Hansson BS, Anderson P (2011) Mosquito feeding affects larval behavior and development in a moth. PLoS ONE 6(10): e25658.
[30]
Gillies MT (1980) The role of carbon dioxide in host-finding by mosquitoes (Diptera: Culicidae): a review. Bull Entomol Res 70: 525–32.
[31]
Dekker T, Geier M, Cardé RT (2005) Carbon dioxide instantly sensitizes female yellow fever mosquitoes to human skin odours. J Exp Biol 208: 2963–2972.
[32]
Mburu DM, Ochola L, Maniania NK, Njagi PGN, Gitonga LW, et al. (2009) Relationship between virulence and repellency of entomopathogenic isolates of Metarhizium anisopliae and Beauveria bassiana to the termite Macrotermes michaelseni. J Insect Physiol 55: 774–780.
[33]
Mburu DM, Ndung'u MW, Maniania NK, Hassanali A (2011) Comparison of volatile blends and gene sequences of two isolates of Metarhizium anisopliae of different virulence and repellency toward the termite Macrotermes michaelseni J Exp Bio. 214: 956–962.
[34]
Waage JK (1979) The evolution of insect/vertebrate associations. Biol J Linn Soc 12: 216.
[35]
Carruthers RI, Ramos ME, Larkin TS, Hostetter DL, Soper RS (1997) The Entomophaga grylli (Fresenius) Batko species complex: its biology, ecology, and use for biological control of pest grasshoppers. Memoirs of the Entomological Society of Canada 171: 329–353.
[36]
Andersen SB, Gerritsma S, Yusah KM, Mayntz D, Hywel-Jones NL, et al. (2009) "The life of a dead ant: The expression of an adaptive extended phenotype". The American Naturalist, volume 174 (3): 424–433.
[37]
Cator LJ, Lynch PA, Read AF, Thomas MB (2012) Do malaria parasites manipulate mosquitoes? Trends in Parasitol 28: 466–470.
[38]
Scholte E-J, Knols BGJ, Samson RA, Takken W (2004) Entomopathogenic fungi for mosquito control: A review. J Insect Science 4: 19.
[39]
Takken W, Knols BGJ (1999) Odor mediated behavior of Afrotropical malaria mosquitoes. Annu Rev Entomol 44: 131–157.
[40]
Mnyone LL, Lyimo IN, Lwetoijera DW, Mpingwa MW, Nchimbi N, et al. (2012) Exploiting the behaviour of wild malaria vectors to achieve high infection with fungal biocontrol agents. Malar J 11: 87.
[41]
Farenhorst M, Farina D, Scholte EJ, Takken W, Hunt RH, et al. (2008) African water storage pots for the delivery of the entomopathogenic fungus Metarhizium anisopliae to the malaria vectors Anopheles gambiae s.s. and Anopheles funestus. Am J Trop Med Hyg 78: 910–916.
[42]
Caputo B, Ienco A, Cianci D, Pombi M, Petrarca V, et al. (2012) The “Auto-Dissemination” Approach: A novel concept to fight Aedes albopictus in urban areas. PLoS Negl Trop Dis 6(8): e1793.
[43]
Müller GC, Junnila A, Qualls W, Revay EE, Kline DL, et al. (2010) Control of Culex quinquefasciatus in a storm drain system in Florida using attractive toxic sugar baits. Med Vet Entomol 24: 346–351.
[44]
Jenkins NE, Heviefo G, Langewald J, Cherry AJ, Lomer CJ (1998) Development of mass production technology for aerial conidia of mitosporic fungi for use as mycopesticides. Biocontrol News and Information 19: 21–31.
